Climate Change & Crop Production
Climate Change & Crop Production
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Table 4.1. Effect of climate and human-induced activities on disease cycle components in selected food crop pathosystems.
Disease cycle
component Pathogen/vectors Disease
Crop
affected Observation
Effect of climate and human-induced
activities References
Survival Fusarium graminearum,
Fusarium culmorum
Fusarium head
blight
Wheat Fusarium head blight
severity increase
Maize grown at higher latitudes; over-
wintering of inoculum on previous
crop residues (maize) under zero
tillage
Bateman et al.
(2007)
Puccinia triticina Leaf rust Wheat Yield losses increased in
some areas
Over-wintering of inoculum Eversmeyer and
Kramer (2000)
Rhopalosiphum padi,
Sitobion avenae,
Metopolophium
dirhodum
Aphid vectors of
barley yellow
dwarf virus
(BYDV)
Oats,
barley,
wheat
More BYDV Vector overwintering is favoured by mild
winters; CO
2
increases root biomass
and water-use effciency of infected
plants (virus reservoirs)
Malmstrm and Field
(1997), Fabre et al.
(2005), Chancellor
and Kubiriba (2006)
Infection Blumeria graminis Barley powdery
mildew
Barley Reduced penetration of
the fungus
Dry air environment; elevated CO
2
concentrations mobilize assimilates
and plant response
Hibberd et al. (1996),
Jahn et al. (1996)
Cochliobolus sativus Spot blotch Wheat More wheat areas
affected and increased
severity
Rising temperatures, particularly night
temperatures, increase host
susceptibility
Sharma and
Duveiller (2004),
Sharma et al.
(2007)
F. culmorum Fusarium head
blight
Wheat Incidence and severity Cool and humid environment favours
disease
Jennings et al.
(2004), Xu et al.
(2008)
F. graminearum Fusarium head
blight
Wheat Incidence and severity Warm and wet environment at anthesis
favours disease
Jennings et al.
(2004), Xu et al.
(2008)
Fusarium
pseudograminearum,
F. culmorum,
C. sativus and
nematodes
(Heterodera spp.,
Pratylenchus spp.)
Dryland root rots
and nematodes
Wheat Prevalence in dryland
areas
Drought-stress affected areas
increasing; optimum irrigation less
available
Duveiller et al. (2007)
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Mycosphaerella
graminicola
Septoria tritici
blotch
Wheat Prevalence and severity
increased in last
decades
Reduction in SO
2
in the air in last
decades; rainfall patterns
Jahn et al. (1996),
Bearchell et al.
(2005)
Phaeosphaeria nodorum Septoria nodorum
blotch
Wheat Prevalence decreased in
Western Europe
Reduction in SO
2
in the air in last
decades
Bearchell et al.
(2005)
Ramularia colo-cygni Ramularia leaf
spot
Barley Emerging disease Effect on host physiology infuencing
susceptibility to toxin
Schtzendbel et al.
(2008)
Latency Bemisia tabaci (whitefy) Vector of cassava
mosaic virus
Cassava Disease prevalence
associated with vector
multiplication
Reduction in generation time of the
vector
Chancellor and
Kubiriba (2006)
Vector of sweet
potato chlorotic
stunt virus
Sweet
potato
Disease prevalence
associated with vector
multiplication
Reduction in generation time of the
vector
Chancellor and
Kubiriba (2006)
Cicadulina mbila and
other leafhoppers
Vectors of maize
streak virus
Maize Disease prevalence
associated with vector
multiplication
Reduction in generation time of the
vector
Chancellor and
Kubiriba (2006)
Phytophtora infestans Potato late blight Potato Model predicts fungicide
needed for longer
period
13C temperature increase
accelerates pathogen multiplication;
longer epidemics
Kaukoranta (1996),
Boland et al.
(2004)
Increased disease
severity
Warmer and wetter growing seasons Baker et al. (2005)
Puccinia triticina Leaf rust Wheat Increasing incidence in
new areas
Reduction in generation time FAO (2008)
Dispersal B. graminis Powdery mildew Barley,
wheat
Spore dispersal favoured Dry air and warm temperature favouring
spore spread
Jahn et al. (1996),
Chancellor and
Kubiriba (2006)
M. graminicola Septoria leaf
blotch
Wheat Severity increased in rainy
years
Rain splashes and rainfall patterns
changed
Jahn et al. (1996)
P. infestans Potato leaf blight Wheat Severity increased in rainy
years
Rainfall patterns changing Baker et al. (2005)
Puccinia graminis f. sp.
tritici
Stem rust Wheat Ug99 dispersal
progressing to Iran
Wind; outstanding storms Hodson et al. (2009)
56 A. Legrve and E. Duveiller
colo-cygni, a pertotrophic fungus producing a
toxin that leads to leaf infection at a late
growth stage, has gained increasing import-
ance in Europe as the causal agent of a new
leaf spot disease in barley, Ramularia leaf
spot. Te physiological status of the host
appears to govern the susceptibility of winter
barley to this pathogen (Schtzendbel et al.,
2008). In southern Asia, spot blotch of wheat
caused by Cochliobolus sativus is more severe
under stress conditions, such as heat or poor
soil quality, and is therefore highly depend-
ent on plant physiology and growth stage
(Sharma and Duveiller, 2004). A 6-year study
at multiple sites has shown that disease
severity increased with rising temperatures,
particularly night temperatures, after anthe-
sis, suggesting that more wheat growing
areas will become afected by spot blotch,
along with heat stress afecting more regions
(Sharma et al., 2007; Ortiz et al., 2008).
Soilborne pathogens, including dryland
root rot and cereal nematodes, have a global
distribution and cause yield losses in rainfed
regions where cereals dominate the cropping
system and in irrigated areas where water
supply or rainfall might not always be
adequate, exposing the crops to water stress
and potential damage by these pathogens
(Duveiller et al., 2007). As climate change is
expected to increase the number of drought-
stress afected areas around the world, the
severity of root diseases such as common
root rot (C. sativus), foot rot induced by
several Fusarium pathogens, as well as nema-
tode problems, will increase when irrigation
becomes limited, as illustrated by the preva-
lence of these diseases in rainfed wheat-
based cropping systems in northern Africa
and western Asia.
Latency
Increasing temperatures reduce the latency
period or generation time, often measured
in degree days, and allow a higher number of
generations per season in terms of both
diseases and pests. Tis has a major efect on
polycyclic diseases and on diseases transmit-
ted by insect vectors. Generation time deter-
mines the amplifcation of plant diseases in
two ways: (i) it accelerates and increases the
inoculum load in a feld or agroecosystem;
and, more importantly, (ii) it afects patho-
gen evolution rates and a pathogens capac-
ity to adapt to a changing environment often
faster than a host can respond. Leaf rust of
wheat will be favoured by higher tempera-
tures and might therefore spread to areas
where it is not currently important, such as
the facultative and winter wheat growing
areas of China, parts of Europe, the Pacifc
north-west region of the USA and the winter
facultative wheat areas of Central Asia (FAO,
2008). In the case of potato late blight caused
by Phytophthora infestans, a model predict-
ing the date of outbreak in Finland based on
thermal time on rainy days suggests that
over a range of 13C warming, the period
during which the disease needs to be control-
led by fungicide applications would be 1020
days longer per 1C (Kaukoranta, 1996). In
the upper Great Lakes region of the USA,
the risk of late blight of potato is increasing
because the climatological trends here have
resulted in warmer and wetter growing
season conditions (Baker et al., 2005). In
Africa, higher temperatures and rainfall
have led to an increase in the abundance of
whitefy, Bemisia tabaci, the vector of cassava
mosaic virus and sweet potato chlorotic
stunt virus, and of leafhoppers transmitting
maize streak disease (Chancellor and
Kubiriba, 2006).
Dispersal
Te absence or scarcity of precipitation could
drastically limit the dispersal of splash-
dispersed propagules such as the Septoria
pycnidiospores produced by Mycosphaerella
graminicola in wheat or the sporanges and
spores of potato leaf blight. Rusts are well-
known examples of diseases dispersed by
wind over long distances. Te recent outbreak
and dispersal of Ug99 (a highly virulent race
of Puccinia graminis f. sp. tritici that causes
susceptibility in most wheat cultivars) that
has moved from eastern Africa to Yemen
and Iran, now threatens southern Asias
wheat growing areas. Although the exact
cause of dispersal was not pinpointed, it is
Preventing Potential Disease and Pest Epidemics 57
suspected that unusual wind and storm
events might have spread the inoculum to
Iran (Hodson et al., 2009).
Effects of Climate Change on
Evolutionary Forces,
Agroecosystems and Food Crops
Apart from the specifc changes in disease-
infection cycle components, climate change
is almost certain to be a strong driver of
evolutionary change in plant and pathogen
populations by interfering with hostpatho-
gen interactions, gene expression and popu-
lation dynamics (Harvell et al., 2002) (Table
4.2). Population genetic structure and
disease dynamics are very infuenced by
pathogenhostenvironment interactions
through the action of evolutionary forces.
McDonald and Linde (2002) identifed fve
forces afecting pathogen populations: (i)
mutation; (ii) genetic drift; (iii) gene fow;
(iv) asexual and sexual reproduction; and (v)
selection. Interspecifc hybridization and
gene expression or functionality also infu-
ence the composition of pathogen popula-
tions. Climate change could infuence
selection, an evolutionary force character-
ized by a directional process that leads to an
increase or decrease in the frequency of
genes or genotypes in a pathogen or pest
population. Tese forces afect biological
systems in various ways and infuence
epidemiological dynamics and pathosys-
tems, depending on environmental condi-
tions. Trough its impact on temperature or
humidity, climate change might select
stronger individuals. However, predicting
the potential responses of a pathosystem is
very complex because of the multivariate
nature of climate change and the multiple
efects of the biotic components of the
system, including the pathogen, its natural
hosts (crops or weeds) and its natural
enemies. Although most hostparasite
systems are predicted to experience more
frequent or severe disease occurrence with
warming, a subset of pathogens might
decline with warming, releasing hosts from
disease (Harvell et al., 2002). Some examples
of how climate change could infuence evolu-
tionary forces, and the resulting conse-
quences are given hereafter (and see Table
4.3).
Mutation and genetic drift
Mutation is the ultimate source of genetic
variation, leading directly to changes in the
DNA sequence of individual genes and thus
creating new alleles in populations
(McDonald and Linde, 2002). Te loss of
alleles over time, or genetic drift, can also
generate new diseases through the selection
of gene combinations that can adapt to a
new ecosystem. Te evolutionary potential
of a small population is limited, but its adap-
tation capability to a new environment
should not be underestimated. Yellow rust is
a wheat disease known to occur in cool envir-
onments. It is caused by Puccinia striiformis,
a biotrophic asexually reproducing fungal
species harbouring new virulence strains
resulting from mutation. A study on P. strii-
formis diversity at global level has demon-
strated the recent intercontinental spread of
yellow rust (Hovmller et al., 2008). New
epidemics in North America may be driven
by an increase in aggressiveness conferring
the ability to cause disease more quickly and
at temperatures once considered too warm
for the fungus (Milus et al., 2009). Particular
strains and their derivatives resulting from
mutation were found at multiple sites in
relatively warm or dry wheat growing areas
where severe yellow rust epidemics have
been observed in recent years. Te genera-
tion time (latent period) was approximately
2 days shorter for new strains compared
with isolates of representative strains
sampled before 2000 from multiple regions
in North America and Europe (Hovmller et
al., 2008; Milus et al., 2009). Te dramatic
increase in spore production potential
explains why a new and stronger strain can
spread rapidly at a global scale, for example,
by increasing the likelihood of rare events
occurring, such as long-range spore disper-
sal by wind or accidental spread (Wellings et
al., 1987; Brown and Hovmller, 2002;
Hovmller and Justesen, 2007; Hodson,
2009).
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Table 4.2. Effects of climate changes and human activities on evolutionary forces leading to a modifcation of pathogen populations resulting in new pest and
disease epidemics: examples from forestry, agroecosystems and food crops.
Evolutionary forces Pathogen Disease
Affected
crop/species
Effects of climate changes and human
activities References
Mutation and
genetic drift
Puccinia striiformis Yellow rust Wheat Intercontinental spread
Adaptation to higher temperatures;
reduction in generation time; increase in
spore production potential
Hovmller et al. (2008)
Milus et al. (2009)
Wind and accidental spread Wellings et al. (1987),
Brown and Hovmller
(2002), Hovmller and
Justesen (2007), Hodson
et al. (2009)
Gene fow Cryphonectria
parasitica
Asian chestnut tree
blight
American chestnut Introduction of pathogen into new
ecological niches
Anagnostakis (1987)
Ophiostoma novo-
ulmi
Dutch elm disease Elm Introduction of pathogen into new
ecological niches
Brasier (1991)
Puccinia graminis f.
sp. avenae,
Puccinia coronata
Stem and leaf rusts Oat Interactions at the agroecological
interfaces between wild host and
cultivated populations
Burdon and Thrall (2008)
Gene expression
or functionality
P. graminis f. sp.
avenae
Stem rust Oat Temperature sensitive resistance genes
deactivated
Maertens et al. (1967)
P. striiformis Yellow rust Triticum turgidum
ssp. dicoccoides
As a result of gene Yr36 HTAPR
a
is
effective
Uauy et al. (2005)
Xanthomonas
oryzae
Bacterial leaf blight Rice Xa7 resistance gene infuenced by
temperature
Garrett et al. (2006)
Blumeria graminis Powdery mildew Barley Mlo resistance gene disrupted by drought
stress
Newton and Young (1996)
Magnaporthe
oryzae
Blast Rice Elevated atmospheric CO
2
increases
lesions possibly due to a reduction in
leaf silicon content
Kobayashi et al. (2006)
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Barley yellow dwarf
virus (BYDV)
Barley yellow dwarf
(BYD)
Oats, barley and
wheat
Elevated atmospheric CO
2
increases root
biomass, photosynthesis and water-use
effciency, favouring the persistence of
infected plants and virus reservoirs
Malmstrm and Field
(1997)
Interspecifc
hybridization
New Phytophthora
species
Alder tree New aggressive species emerging naturally
from hybridization between Phytophthora
cambivora-like and Phytophthora
fragariae-like taxons
Brasier et al. (1999),
Brasier (2001)
New Phytophthora
species
Primula,
Spathiphyllum
New natural hybrids from Phytophthora
cactorum and Phytophthora nicotianae
Man int Veldt et al. (1998)
Pyrenophora tritici-
repentis
Tan spot Wheat Horizontal transfer of ToxA gene from
Phaeosphaeria nodorum into the
P. tritici-repentis genome
Friesen et al. (2006),
Stukenbrock and
McDonald (2008)
Sexual and
asexual
reproduction
Phytophthora
infestans
Late blight Potato Introduction of a second mating type to
new areas allowing sexual recombination
leading to more aggressive isolates with
high sporulation capacity and lower
generation time in the absence of host
resistance
Goodwin et al. (1994),
McDonald and Linde
(2002)
a
HTAPR, high temperature adult-plant resistance.
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Table 4.3. Synopsis of type of events and succession of effects resulting from the infuence of climate change on evolutionary forces modifying hostpathogen
interactions and leading to new disease and pest epidemics.
Evolutionary forces Type of change occurring Induced effect Impact on host and pathogen Outcome
Mutation and genetic drift Ultimate change at DNA
level
Adaptation to new
environmental
conditions
Reduction in generation time,
higher spore production
New epidemics resulting from
dispersal or introduction to new
areas including continents through
rare events and human activity
Gene fow Exchange between
populations of alleles or
individuals
Increased population
diversity
Variation in host resistance;
variation in pathogen virulence;
new specifc interactions
New disease or pathogen emergence
Interactions at the agroecological
interfaces between wild host
and cultivated populations
Introduction of pathogen into new
ecological niches
Gene expression or
functionality
Phenotypic changes Change in pathosystems Host physiology and resistance
modifed
Susceptibility or resistance to disease
increased
Interspecifc hybridization New species formed Change in pathosystems Shifts in the geographical
distribution of hosts and
pathogens
Dispersal of exotic pests or pathogens
Horizontal gene transfer Emergence of new diseases
Sexual and asexual
reproduction
New aggressive strains
formed with high ftness
Change in pathosystems Recombination leading to
emergence of more adapted
aggressive isolates with high
sporulation and shorter
generation time leading to
reduction of host resistance
capacity
Emergence of new outbreak and
chemical treatments; effcacy
reduced due to rapid fungicide
resistance selection
Preventing Potential Disease and Pest Epidemics 61
Gene fow
Te gene or genotype fow, or the process
through which particular alleles or individu-
als are exchanged among separate popula-
tions (McDonald and Linde, 2002), is another
evolutionary force. While considered as a
unifying force that usually prevents popula-
tions from diverging by breaking down the
geographical or other boundaries that could
otherwise isolate populations, this evolution-
ary force could lead to the increased incidence
or severity of a disease or even to a new
disease. It tends to modify pathosystems
involving pathogens that produce propagules
with the natural potential of long-distance
dispersal, such as powdery mildew and rust
fungi, but also applies to pathogens with the
potential of short-distance spreading because
of dispersal by anthropogenic movement.
Depending on the distribution of populations
and the environmental conditions, which are
infuenced by climate change, gene fow leads
to an increase in population diversity or to
the introduction of a new population in new
ecological niches, depending on the presence
or otherwise of another population of the
same species in the introduction area. Te
evolutionary potential resulting from gene
fow allows for a variation in host resistance
and pathogen virulence, as well as new disease
or pathogen emergence.
In the newly colonized area, specifc inter-
actions could lead to very diverse situations.
Te introduction of the Asian chestnut tree
blight fungus, Cryphonectria parasitica, led
to the extermination of the American chest-
nut, Castanea dentata, from eastern USA
forests (Anagnostakis, 1987). Similarly, the
introduction of the aggressive pathogen
Ophiostoma novo-ulmi sp. nov. in North
America caused the extermination of many
elms that had survived the original epidemic
by Ophiostoma ulmi. Dutch elm disease
epidemics that resulted from the movement
of Ophiostoma species between and across
continents illustrate the dangers of moving
plant material around the world (Brasier,
1991). Climate change was not the cause of
the gene fow or its consequence in this case,
but these examples illustrate the high risks
of introducing pathogen genotypes into new
ecological niches where favourable inter-
actions allow the development of new
epidemics. Te role played by wild oat popu-
lations in driving virulence evolution in the
pathogen populations of oat rusts (Puccinia
graminis f. sp. avenae and Puccinia coronata)
on oats in Australia also shows that inter-
actions at the agroecological interface
through gene fow between cultivated and
wild host plant populations could also alter
pathosystems (Burdon and Trall, 2008).
Gene expression or functionality
Apart from the evolutionary forces infuenc-
ing population diversity, climate change may
induce phenotypic change leading to difer-
ences in gene expression or functionality,
which also tend to modify pathosystems.
Increases in temperature can modify host
physiology and resistance by changing gene
expression and activity. For example, temper-
atures above 20C deactivate temperature-
sensitive resistance to stem rust in oat
cultivars with Pg3 and Pg4 genes (Maertens et
al., 1967). In tetraploid wheat, lines carrying
Yr36, a previously unidentifed stripe rust
resistance gene from Triticum turgidum ssp.
dicoccoides located on chromosome arm 6BS,
are susceptible to almost all stripe rust resist-
ance races of P. striiformis tested at the seed-
ling stage, but show adult-plant resistance to
the prevalent races in California at high diur-
nal temperatures (Uauy et al., 2005). Tis
high temperature adult-plant resistance
(HTAPR) is closely linked to the grain protein
content locus and has proven to be more
durable than seedling resistance due to its
non-race-specifc nature (Uauy et al., 2005).
Temperature was also shown to infuence the
resistance gene Xa7 in rice against bacterial
blight caused by Xanthomonas oryzae (Garrett
et al., 2006). Other environmental conditions
are also likely to alter the physiology and
functionality of resistance genes. In barley,
Newton and Young (1996) showed that the
mechanisms of Mlo-resistance, an important
powdery mildew resistance source, could be
disrupted following drought stress as cells
undergo expansion once water supply is
restored. Te positive efect of the elevation
62 A. Legrve and E. Duveiller
of the CO
2
concentration on plant growth is
now well recognized (Drake et al., 1997), but
the interference with pathogen development
will also infuence the evolution of pathosys-
tems. Kobayashi et al. (2006) observed that
rice plants grown in an elevated atmospheric
CO
2
concentration showed more leaf blast
(Magnaporthe oryzae) lesions than those in
ambient CO
2
. A relationship with leaf silicon
content, lower at high CO
2
concentration,
and plant susceptibility was suggested.
Malmstrm and Field (1997) showed that
barley yellow dwarf (BYD) infection on Avena
sativa infuenced plant response to CO
2
enrichment by increasing root biomass
response, photosynthesis and water-use ef-
ciency. A change in the epidemiology of BYD
could occur at high CO
2
content by increasing
the persistence of infected plants.
Interspecifc hybridization
Te most likely impact of climate change on
plant pathosystems would be shifts in the
geographical distribution of hosts and path-
ogens. Plant disease epidemics following the
dispersal of exotic pests or pathogens are
not rare (Brown and Hovmller, 2002), but
the simultaneous occurrence of introduced
and resident species in a given ecosystem
could lead to the development of new patho-
gens. Interspecifc hybridization between
Phytophthora cambivora-like species and an
unknown taxon similar to Phytophthora
fragariae has led to the emergence of a new
aggressive Phytophthora species pathogen
on alder trees in Europe (Brasier et al., 1999;
Brasier, 2001). Other natural hybrids of
Phytophthora nicotianae and Phytophthora
cactorum have demonstrated the evolution-
ary potential of this genus (Man int Veldt et
al., 1998).
Horizontal gene transfer due to nuclear or
somatic recombination is a further source of
new diseases and results from the simultane-
ous presence of diferent species in the same
environment. Te species Pyrenophora tritici-
repentis, originally described as a saprophyte,
became pathogenic by inducing a damaging
disease of wheat called yellow spot or tan
spot. Friesen et al. (2006) suggest that this
change in virulence occurred after the trans-
fer of the ToxA gene coding for a protein-
aceous toxin from Phaeosphaeria nodorum,
the causative agent of blotch disease, into
the P. tritici-repentis genome. Tis example is
evidence of a new disease emerging because
of the interspecifc transfer of a toxin gene
that changed a previously benign micro-
organism into an important pathogen
(Stukenbrock and McDonald, 2008).
Sexual and asexual reproduction
By afecting the distribution of gene diver-
sity among individuals in a population,
reproduction is a strong driver of evolution,
particularly for pathogens undergoing regu-
lar recombination, but also for asexually
reproducing pathogens because environ-
mental conditions promote the selection of
adapted individuals. Phytophthora infestans,
the causal agent of potato late blight, has
often caused major damage as the fungus
has moved into new countries. Te Irish
famine, from 1844 to 1849, is a well-known
example illustrating how the introduction of
a new pathogen can afect food security in
the absence of host resistance. Until the late
20th century, with the exception of Mexico,
little genetic variation was found within and
among pathogen populations dominated by
a single mating. In the 1980s, the migration
of a the second mating type from northern
Mexico allowed sexual recombination in
P. infestans populations and the appearance
of increased aggressive isolates with a high
sporulation rate capacity and lower genera-
tion time (Goodwin et al., 1994; McDonald
and Linde, 2002). As new strains of
P. infestans evolve, new outbreaks of the
disease occur, which afects not only host
resistance capacity but also chemical treat-
ment efcacy as fungicide-resistant strains
are selected more rapidly (Anderson et al.,
2004).
Strategies for Mitigating the Climate-
related Effects of Pests and Diseases
on Crop Yields
Overall, strategies to limit the efect of
climate change on pests and diseases follow
Preventing Potential Disease and Pest Epidemics 63
sound crop husbandry principles and do not
fundamentally difer from existing inte-
grated crop management practices, the basis
for sustainable agriculture (Oerke and
Dehne, 2004). More specifc interventions
relate to limiting the movement of trans-
boundary pathogens and pests, evolving
germplasm improvement priorities in given
geographical areas, optimizing control prac-
tices and encouraging modelling and fore-
casting systems. When the enemies and
drivers of changes to hostpathogen inter-
actions are known, preventing potential
epidemics requires working against evolu-
tionary forces and minimizing inoculum
sources while remaining environment
friendly. In this context, breeding for host
resistance will continue to have a pivotal role
among the diferent options.
Limiting transboundary diseases and
controlling quarantine pests
Transboundary diseases and pests refer to
organisms that can be dispersed over a long
distance beyond the national or geograph-
ical boundaries (e.g. mountains and deserts),
such as rusts or migratory pests (e.g. locusts).
Transboundary plant pests are also quaran-
tine organisms that are absent from one
region or reported under control in one
country and could cause a threat if intro-
duced. With the globalization of trade and
international travel, quarantine measures
and early intervention are essential to
protect agroecosystems from the introduc-
tion of exotic pests and diseases and to
prevent the establishment and spread of
new epidemics . Tis implies the develop-
ment and implementation of adequate poli-
cies, and the efective inspection and
certifcation of seed and plant materials free
from pathogens and pests (FAO, 2008).
Precautionary measures are also necessary
for endemic diseases characterized by the
existence of physiological races. Winds
disperse airborne pathogens such as soybean
and cereal rusts over a long distance. Soybean
rust caused by the Phakopsora pachyrhizi
fungus has been invasive in South America
since 2001 and was confrmed in the USA in
2004 (Oerke, 2006; Kumudini et al., 2008).
Recent examples show that wheat rust
epidemics have emerged from the introduc-
tion of a new virulent race following global
travel (Brown and Hovmller, 2002;
Hovmller et al., 2008), highlighting the
importance of public awareness of the need
to avoid introducing pathogens or pests. In
wheat, the rapid response of the scientifc
community and the support given to wheat
research in reaction to the dispersal of Ug99,
the aggressive race of stem rust caused by P.
graminis f. sp. tritici, also illustrated how
internationally coordinated breeding eforts,
backstopped by advanced research insti-
tutes, can mitigate the threat caused by the
migration of a race that is virulent against
90% of commercial wheat cultivars world-
wide (Singh et al., 2008). Te same principle
applies to preventing the introduction of the
vectors of viral diseases. Te monitoring of
emerging diseases and early diagnostic
capacity to identify new problems in the
feld are therefore essential. Wheat blast, an
emerging disease caused by Magnaporthe
grisea (Duveiller et al., 2007), presently
restricted to warmer growing areas in the
Southern Cone, deserves attention in
preventing the pathogen, or its wheat-
afecting pathotype, migrating or being
introduced into climatically comparable
wheat systems in other regions.
Improving plant resistance to biotic
stresses
Breeding for disease and pest resistance is
one of the primary objectives of breeding
programmes. It requires an understanding
of parasite biology and ecology, disease
cycles and drivers infuencing the evolution
of plantpathogen interactions because,
unlike other traits, pest resistance is infu-
enced by genetic variability in the pest popu-
lation, especially in diseases. With evolving
pathogen populations and changes in ftness
favouring new pathotypes, as a result of
climate change or not, the continuous
improvement of resistance to biotic stresses
is paramount in maintaining yield potential
and genetic gains. Resistance is essential for
food security in economies where farmers
cannot aford to use chemical control, and
64 A. Legrve and E. Duveiller
increasingly in advanced countries where
the reduction in authorized active ingredi-
ents on the market, due to environmental
concerns of the public and policy makers,
has meant that farmers have to rely more on
host resistance. Tere are numerous exam-
ples documenting the progress in host resist-
ance in many crops. Sayre et al. (1998)
demonstrated the impact of breeding for
leaf rust resistance over time using a set of
Mexican wheat cultivars released between
1966 and 1988. Data showed that while yield
potential (yield with fungicide applied) had
increased signifcantly (0.52%/year), pro gress
protecting the yield potential due to incorp-
oration of leaf rust resistance genes (yield
without fungicide) was higher (2.1%/year).
Progress in biotechnology, particularly
marker assisted selection, will contribute to
making breeding for resistance against dif-
cult traits more efcient. Tactics and meth-
ods might change, depending on the
pathosystems, but breeding for durable
resistance is perhaps the major objective of
plant breeders. Although durable resistance
can be confrmed only after a cultivar has
been grown on a large scale for a relatively
long time, it is generally accepted that it is
more likely to be achieved by breeding for
non-race-specifc resistance and the accu-
mulation of minor genes conferring partial
resistance. Tere has been a major genetics
and breeding emphasis in recent decades on
slow-rusting, minor-resistance genes with
additive efects against leaf and yellow rust
pathogens in wheat. Te use of Sr2 and Lr34
and minor genes in controlling stem rust
and leaf rust in wheat illustrates this
approach (Singh et al., 2000). A study with
Lr34 isolines showed yield losses of approxi-
mately 15% associated with leaf rust infec-
tion in the presence of the genes, while when
Lr34 was absent losses were 4085%,
depending on planting date (Singh and
Huerta-Espino, 1997). Gene pyramiding and
the deployment of major genes could ofer
an option for a rapid response against a new
threat. However, these remain controversial
because although the selection of new
complex races is possible, the efect might
not last in the case of a rapid race evolution.
Te development of resistant material
against the Sr24 virulent variant of Ug99
confrms the value of breeding strategies
based on minor genes, as demonstrated by
the development of new genotypes (Singh et
al., 2009).
In the context of climate change, breed-
ing for resistance against several pathogens
should not be disconnected from improving
resistance to abiotic stresses, particularly for
water-use efciency and heat tolerance,
because abiotic stress factors could enhance
the disease efect. Spot blotch of wheat is
more severe under heat stress, and therefore
improving yield potential and heat toler-
ance, particularly to night heat during grain
flling, should contribute to lower disease
losses (Sharma et al., 2007). It is also likely
that improving root systems and drought
tolerance could increase resistance to soil-
borne foot rot diseases. Breeding priorities
in a given geographical region might be
evolving as new crops and systems are intro-
duced. Stubble-borne diseases such as tan
spot (P. tritici-repentis), Fusarium ear rot or
Septoria leaf blotch in wheat receive more
attention in areas where reduced tillage is
being adopted.
Agricultural practices: rotation, time of
planting and avoidance
In many regions, intensifcation has replaced
diverse agroecosystems and increased the
vulnerability to pest attacks. Monoculture
and growing megacultivars (varieties occu-
pying millions of hectares, such as the wheat
cultivars PBW343 and Inqualab in India
and Pakistan) increase the likelihood of
pathogen recombination or mutation by
selection pressure. Changes in seasonal
weather patterns could also contribute to
the displacement of land use and crop-
producing areas (Kiritani, 2007). While
temperate cereal-based systems will expand
to higher latitudes, reduced water availabil-
ity in Africa could reduce the areas under
maize and force farmers to grow sorghum
instead, which will bring new requirements
for pest and disease control (Chancellor and
Kubiriba, 2006). Te package of technolo-
gies available, including resistant cultivars,
Preventing Potential Disease and Pest Epidemics 65
might not always be readily available when a
new crop is cultivated. Growing soybean in
the summer in Yaqui Valley in Sonora,
Mexico, has stopped because of the lack of
resistance against whitefy, Bemisia argenti-
folii (= B. tabaci B biotype). In Brazil, wheat
blast has been a major constraint to expand-
ing wheat cultivation in the Cerrados.
Traditional crop management approaches
such as rotation, intercropping, crop diversi-
fcation and switching cultivars are import-
ant adaptive strategies for minimizing the
amount of inoculum. Earlier or later plant-
ing may help prevent the window of climatic
conditions (e.g. rainfall) favouring a patho-
gen outbreak or reduce the exposure to a
critical abiotic stress (e.g. heat) that predis-
poses a crop to diseases such as spot blotch
in wheat in southern Asia (Sharma and
Duveiller, 2004). Te management of rice
tungro bacilliform virus transmitted by
Cicadellidae can be improved by the synchro-
nized planting of partially resistant geno-
types (Cabunagan et al., 2001). Conservation
agriculture practices are being adopted in
many areas, partly to reduce production
costs but more importantly to address envir-
onmental concerns such as soil degradation
and declining water resources. Reduced till-
age and residue retention will shift the
breeding emphasis towards resistance
against stubble-borne diseases such as tan
spot and Septoria diseases of wheat.
However, conservation agriculture has the
advantage of stimulating microorganisms
and arthropod diversity, bacterial antago-
nisms and biocontrol. Mazzola (Chapter 11,
this volume) illustrates the efects of
suppressive soils in controlling some soil-
borne diseases. With population growth and
global warming leading to soil degradation
and declining water resources, cereal systems
will evolve in various regions, such as south-
ern Asia, to cope with the increasing demand
for food. New agronomic practices such as
direct-seeded rice, alternate water supply
(dry/wet), reduced tillage or the use of
permanent raised beds will require monitor-
ing to observe the potential efect on pests
and diseases. Te study of pest and disease
injury profles (Savary et al., 2006) under
current and new agronomic practices will
determine future needs in breeding and crop
protection strategies.
Chemical control
Chemical control is among the options avail-
able for limiting yield losses (Oerke, 2006).
Intrinsic pest/pathogen characteristics (e.g.
diapause, life cycle, generation time, mini-
mum, maximum and optimum growth
temperatures, and host interaction) and
intrinsic ecosystem characteristics (e.g.
monoculture and biodiversity) lead to
changes in microorganism populations. An
increase in pest infestation might lead to
greater use of chemical pesticides to control
them. It has been estimated that the use of
fungicides for controlling late blight in
potato will increase by 1520% in the coming
decades (Fry and Goodwin, 1997). Climate
change could change the efcacy of crop
protection because precipitation patterns
and increased CO
2
may afect the residual
efect of active ingredients on the leaf or
their uptake in the case of systemic
compounds, respectively (Coakley et al.,
1999). Pesticide use could also have detri-
mental efects on benefcial organisms, as in
the case of the brown plant hopper
(Nilaparvata lugens) on rice (Savary et al.,
2006). Te reduction in the number of
authorized active ingredients on the market
for ecological reasons could reduce chemical
control options and lead to a situation that
will require a better knowledge of the target
populations and their resistance levels, the
further development and application of
integrated pest management (IPM) tech-
niques, and the use of prediction systems in
precision agriculture.
Forecasting models
Modelling is a tool for developing early warn-
ing systems and reducing the application of
chemicals. Forecasting models need to be
valid and to predict actual feld observations
adequately. With climate change, the chal-
lenge is to take account of the variability in
disease epidemiology. Disease forecasting
66 A. Legrve and E. Duveiller
systems using non-linear responses to
temperature and leaf wetness ofer more
potential for representing these efects
(Bourgeois et al., 2004). However, although
modelling is becoming more sophisticated,
the main concern for these studies on the
impact of climate change on crop production
is to include the changed pest dynamics and
intensity (insects, plant pathogens and
weeds) that are generally ignored under
climate change (Scherm, 2004). Savary et al.
(2006) have reviewed the types of crop loss
knowledge and various models integrating
environment, disease and losses. Te ulti-
mate objective is to contribute to decisions
on whether or not to apply a pesticide and
minimize economic losses. With the devel-
opment of new tools such as geographic
information systems (GIS) and remote sens-
ing, access through the Internet to site-
specifc weather information without
sensors could ofer new possibilities for fore-
casting conditions that favour a disease or
pest (Magarey et al., 2001). Te Integrated
Pest Management Pest Information
Platform for Extension and Education
(IpmPIPE) site illustrates the efectiveness
of Internet-based tools to monitor and
manage new disease outbreaks such as that
of soybean rust in the USA (USDA, 2009).
Research on the relationship between leaf
area and relative yield is expected to lead to
the development of a yield-loss prediction
model specifc to the impact of soybean rust
(Kumudini et al., 2008; University of
Kentucky, 2009). Te Rustmapper system
is another example using the Internet that
allows the risk of dispersal of the wheat stem
rust pathogen by tracking unusual climatic
events (winds, rainfall) to be assessed
(Hodson et al., 2009). Similarly the Desert
Locust Information Service (DLIS) based at
the Food and Agriculture Organization of
the United Nations (FAO) headquarters in
Rome sends early alerts and forecasts for
each country on desert locust plagues; it
generates maps showing where solitary and
gregarious hoppers and adults are observed
(FAO, 2009). Te locust forecasting system
is based on a network of surveillance, remote
sensing, meteorological information and
GIS analysis. Te impact of climate change is
also under investigation.
Conclusions
Climate change, with its multiple efects on
ecosystems, is likely to change the inter-
actions between an infectious propagule, a
susceptible host and favourable environ-
mental conditions, leading to the develop-
ment of new epidemics. Te efect of plant
diseases and insect pests on crop damage is
recognized because agriculture is highly
infuenced by climatic factors. Tis review
highlights the difculty of separating normal
seasonal variations from global climate
change efects, due either to subtle changes
in temperature or humidity or to extraordin-
ary events. Te lack of long-term data is also
hampering the ability to document with
certainty changes in pest and disease
profles. Crop intensifcation and economic
forces have a strong and direct impact on
pests and diseases because changing crop-
ping systems drive changes in pathogen and
pest populations in a relatively short time.
Climate change is expected to have major
efects on population thresholds of micro-
organisms and disease vectors. Te dynam-
ics afecting hostpathogen interactions
lead to the selection of new pathotypes or
pathogens. Tey also determine the emer-
gence of new diseases and pests. Options to
prevent these efects have been discussed.
Among these strategies, breeding for pest
and disease resistance is critical and will
remain an essential part of germplasm
improvement. Increases in yield per unit of
area will continue to depend largely on more
efcient control of (biotic) stresses rather
than on an increase in yield potential
(Cassman, 1999). Integrated crop manage-
ment is therefore the basis for sustainable
agriculture. Te range of options for adapt-
ing to the changes increases with technolog-
ical advances. It is anticipated that modelling,
remote sensing and spatial integration of
critical climatic information and its access in
near real time through the Internet will also
contribute to precision agriculture.
Preventing Potential Disease and Pest Epidemics 67
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CAB International 2010. Climate Change and Crop Production (ed. M.P. Reynolds) 71
5
Introduction
Te Intergovernmental Panel on Climate
Change (IPCC) predicts that by 2050, mean
temperatures around the planet may rise by
between 2 and 5C or more and atmospheric
CO
2
concentration are likely to be > 550 ppm
(cf. 380 ppm at present). Tropical and semi-
tropical climates in particular are expected
to experience dramatic increases in temper-
atures, as well as more variable rainfall
(Jarvis et al., Chapter 2, this volume). Of
serious concern is the fact that most of the
worlds low-income families dependent on
agriculture live in vulnerable areas, namely
in Africa and Asia. Not surprisingly, climate
change has been acknowledged as a major
challenge to future food security (Lobell and
Burke, Chapter 3, this volume).
Among the major cereal crops, rice,
sorghum and maize are relatively well
adapted to high temperatures, given their
sites of origin and the fact that they have
been grown extensively in tropical regions
during the modern agricultural era. It can be
argued that extant breeding programmes
are already geared up to delivering germ-
plasm that will be productive in warmer
than average years (Braun et al., Chapter 7,
this volume). For these cropping systems, a
substantial challenge associated with climate
change will be to stabilize their performance
in drier than average years. Ongoing eforts
to genetically improve maize (Bnziger et al.,
2006; Campos et al., 2006), rice (Wassmann
et al., 2009) and sorghum (e.g. Mason et al.,
2008) under water defcit will need to be
intensifed to maintain and increase
Breeding for Adaptation to
Heat and Drought Stress
Matthew P. Reynolds, Dirk Hays and Scott Chapman
Abstract
Crops respond similarly to drought and heat stress: life cycle is accelerated reducing photosynthetic
capacity via restricted leaf area and duration. Metabolism is inhibited at temperature and water
potential ranges outside those optimal for growth. Reproductive processes are impaired when stress
occurs at critical developmental stages reducing seed set. Both stresses can be exacerbated by nutrient
defciencies and biotic factors while elevated CO
2
levels may partially ameliorate stress in C
3
species.
Although stress adaptive traits and consistent quantitative trait loci associated with them are used
to design new cultivars, the physiological and genetic bases of adaptation are only partially understood.
Terefore, plant selection requires empirical approaches such as multi-location testing across
representative environments, while detailed characterization of target sites permits genotype
environment interaction to be dissected, providing feedback into breeding and research. Precision
phenotyping approaches assist by dissecting yield into its physiological components and have
application in breeding and gene discovery. Examples of stress-adaptive traits which have been
selected for in several species include deeper roots enabling plants to remain hydrated under drought
and permitting canopy cooling under heat stress, transpiration efciency, delayed senescence in
sorghum, and synchronous fowering in maize. New traits and genes must be identifed perhaps
among crop wild relatives or in model species that permit cultivars to be bufered against temporal
variation in water supply, adapt to higher temperatures without loss of water-use efciency, and
tolerate sudden extreme climatic events or combinations of stress factors. Examples of past successes
and promising new approaches are discussed.
72 M.P. Reynolds et al.
productivity . Temperate cereals such as
wheat and barley, on the other hand, are
relatively well adapted to drier environ-
ments, being grown widely throughout the
world in semi-arid regions such as North
Africa, Central Asia and Australia. Ongoing
breeding work has made steady progress in
improving performance (e.g. Trethowan et
al., 2002; Ammar et al., 2008). However,
performance of cereals shows substantial
loss at high temperature (Wardlaw et al.,
1989; Reynolds et al., 1994) and signifcant
breeding efort will be required to maintain
their productivity under warmer conditions.
For C
3
cereals (wheat, barley, rice), there is
some evidence that increased CO
2
will
partially ofset the efects of higher tempera-
ture and drought through improvements in
the water-use efciency, however, the extent
of its impact on productivity is still in doubt
(Leakey et al., 2006).
Already, a large portion of global varia-
tion in crop yield is explained by rainfall and
temperature fuctuation and this will
increase as climate changes (Jarvis et al.,
Chapter 2, this volume). Specifc scenarios
in which their detrimental efects are likely
to be most devastating include situations
where irrigation water is not available to
compensate for decreased rainfall or to miti-
gate the efects of higher temperature via
evaporative cooling of leaves, and in agro-
ecosystems where soils have been degraded
to a point where they no longer provide
sufcient bufer (e.g. adequate water-hold-
ing capacity) against drought and heat stress.
Tese problems cannot be addressed by
improving genetic adaptation to heat or
drought stress alone and readers are referred
to the chapter on conservation agriculture
(Hobbs and Govaerts, Chapter 10, this
volume); investment in genetic improve-
ment will be best realized if crops are grown
in well-managed soils that maximize expres-
sion of genetic potential, bufer the crop
against weather fuctuations, and guarantee
long-term returns by stabilizing the natural
resource base.
Te remainder of this chapter will outline
the challenges of genetically improving
major food crops to adaptation to warmer
and drier conditions. We frst consider that
research focused on genetic improvement
should be conducted with adequate know-
ledge of the environmental factors that
interact with trait expression to ensure that
genetic gains achieved in breeding environ-
ments are realized at target locations and
across years (Salekdeh et al., 2009). Tis
section is followed by an overview of the
genetic and physiological basis of adaptation
to drought and heat stress in the context of
traits having known or probable economic
signifcance. Several case studies of success-
ful genetic improvement strategies are
presented in a range of cereal crops. Lastly
there is a discussion on promising future
approaches to raise the genetic yield thresh-
old of crops under heat and drought stress,
and on strategies to accelerate genetic gain.
Characteristics of Heat and Drought-
stressed Environments
Drought
Productivity gains in water-limited environ-
ments involve many traits (Fig. 5.1a) that
tend to show a complex interaction with a
number of environmental factors. Patterns
of rainfall distribution across target regions
as well as between seasons are unpredictable
and their variance is expected to increase as
climate changes (Jarvis et al., Chapter 2, this
volume).
Drought-prone environments also exhibit
wide variation in other climatic characteris-
tics, biotic stresses and edaphic factors
including micronutrient defciency (like
zinc) and mineral toxicity (such as boron,
salinity and sodicity). With a few exceptions,
combination efects have received scant
attention, despite the fact that crop product-
ivity is especially vulnerable when more than
one abiotic stress is experienced (Mittler,
2006). Te main implication for breeding
will be a need to develop genetic combina-
tions of traits that are robust to inter- and
intra-seasonal variation in drought intensity
as well as the other exacerbating factors
mentioned while ensuring that such culti-
vars remain responsive to favourable years.
Because understanding of the physiological
Breeding for Adaptation to Heat and Drought Stress 73
YIELD = WU WUE HI (drought stress)
Photoprotection (WUE)
Leaf
morphology
wax
posture/rolling
Partitioning (HI)
Floret fertility
flowering synchrony (maize)
panicle extrusion (rice)
Stem carbohydrate storage
and remobilization
Grain harvest index
Rht alleles
Water uptake (WU)
Ground cover protects soil
moisture
early vigour
Access to water by roots
cool canopy
osmotic adjustment
Pigments
chlorophyll a:b
carotenoids
Antioxidants
stay-green)
(a)
YIELD = LI RUE HI (heat stress)
Photoprotection (RUE)
Leaf
morphology
wax
posture/rolling
Efficient metabolism (RUE)
Starch synthase
Dark respiration rate
CO2 fixation
CO2 concentrating mechanism
Rubisco activase
Rubisco specificity
Partitioning (HI)
Floret fertility
Stem carbohydrate storage
and remobilization
Grain harvest index
Rht alleles
Light interception (LI)
Rapid ground cover
Stay-green
Water uptake (RUE)
Access to water by roots
vascular system to match
evaporative demand
Pigments
chlorophyll a:b
carotenoids
Antioxidants
(b)
Fig. 5.1. Conceptual models for traits associated with adaptation to: (a) moisture-stressed environments
grouped according to main drivers of yield under drought (yield = water uptake (WU) water-use
effciency (WUE) harvest index (HI) as defned by Passioura, 1977); (b) hot-irrigated environments
grouped according to main drivers of yield without water limitation (yield = light interception (LI)
radiation-use effciency (RUE) harvest index (HI)). Spike photosynthsis may have higher WUE
associated with recycling of respiratory CO
2
. Other traits presented are discussed in the text (and
references therein); however, the list is not exhaustive, and while some of the traits have been
successfully combined to achieve cumulative gene action for drought adaptation in wheat (Reynolds et
al., 2009), traits cannot be assumed to be additive, or necessarily of equal value across a range of target
environments because trait environment interaction can be expected.
74 M.P. Reynolds et al.
and genetic basis of adaptation to water-
limited environments is incomplete, breed-
ing progress will require empirical approaches
such as multi-location testing (Braun et al.,
Chapter 7, this volume).
However, detailed characterization of
target environments can help with the inter-
pretation of adaptive responses, as well as
germplasm deployment. Recent develop-
ments in the area of geographical informa-
tion systems (GIS) make it more feasible
than in the past to characterize target envir-
onments. For example, with GIS software,
weather data can be interpolated across
regions that may encompass relatively few
weather stations, while databases permit
additional information on soil properties
and cropping systems to be entered and read-
ily accessed (Hodson and White, Chapter 13,
this volume). Such a database can be further
enhanced by the calculation of stress indices
(via crop simulation models) and summaries
of weather variables coinciding with difer-
ent stages of growth. When combined with
phenotypic data from feld trials, such indi-
ces and summaries of stress patterns can be
applied in advanced statistical analyses to
indicate the traits and genetic backgrounds
associated with adaptation to specifc envir-
onmental factors (see Crossa et al., Chapter
14, this volume). Molecular information can
also be used to help explain genetic bases of
genotype environment interactions (Boer
et al., 2007).
Heat
High temperature stress is relatively predict-
able in some regions (e.g. parts of South Asia
and sub-Saharan Africa) increasing slowly in
a way that permits plants to acclimate. In
other regions, however, stress can occur quite
suddenly and may be accompanied by desic-
cating winds (e.g. the Great Plains in the USA
or North Africa). An additional dimension to
heat stress is relative humidity (RH). In moist
tropical regions, high RH further ex acerbates
heat stress in two ways. Saturated air:
(i) reduces the potential for evaporative cool-
ing of plant organs; and (ii) is accompanied
by higher night temperatures.
While optimum mean temperatures for
diferent crop species are reasonably well
defned, ranging from the mid-teens (degrees
Celsius, C) for wheat, to the twenties for rice,
maize, sorghum and soybean (CCSP, 2009),
air temperature is not necessarily an indica-
tor of the stress experienced by plants.
Specifcally in low RH environments, plant
temperature may be several degrees below
ambient air temperature, assuming sufcient
water is available to match evaporative
demand (Amani et al., 1996). Terefore, the
actual heat stress experienced by a plant will
be a function not only of air temperature but
also of agronomic and genetic factors deter-
mining the potential for evaporative cooling
(Table 5.1).
Interaction of heat and drought with
elevated CO
2
By 2050 atmospheric CO
2
levels are expected
to be around 550 ppm. In C
3
species such as
wheat and rice, the elevated CO
2
level is
expected to increase productivity due to the
improvement of CO
2
difusion through
stomata and a consequent efect on photo-
synthesis. However, a complex of interactions
can arise among plant development, growth
and environment variables. Plants that have
acclimated to high CO
2
and grown new leaves
over time (with typically fewer and smaller
stomata) do not show the same high photo-
synthesis rates as a normal CO
2
plant will
under short periods of exposure (Leakey et
al., 2009; Parry and Hawkesford, Chapter 8,
this volume). Consequently, the observed
increases in yield have been only in the order
of 1020% for crops like wheat, when grown
in open-top chambers with elevated CO
2
.
Recent open-air experiments for maize have
demonstrated no increase in yield in feld-
level experiments under well-watered condi-
tions and CO
2
levels of 550 ppm, although
there was substantial reduction in water use
(Leakey et al., 2009). Tese types of fndings
have implications for irrigation needs in C
3
versus C
4
crops under elevated CO
2
: that is, if
growth is stimulated in C
3
crops, then more
water may be required to maintain additional
leaf area, and in dry areas, there may be an
B
r
e
e
d
i
n
g
f
o
r
A
d
a
p
t
a
t
i
o
n
t
o
H
e
a
t
a
n
d
D
r
o
u
g
h
t
S
t
r
e
s
s
7
5
Table 5.1. Factors affecting plant canopy temperature (CT) in crops.
Factors Mechanism
Estimated range
of effect (C) Reference
a
Environmental Ambient air temperature Equilibrium with air ~50
Radiation load Plant organs absorb energy directly ~10 Loomis and Connor (1992)
Rainfall Potential for evapotranspirative cooling ~10 Ehrler (1973)
Relative humidity Potential for evapotranspirative cooling ~10 Ehrler (1973)
Soil depth and water capacity Potential for evapotranspirative cooling ~10 Kirkegaard et al. (2007)
CO
2
level High CO
2
can interact with cooling capability via stomatal
development and regulation
~2 Leakey et al. (2009)
Agronomic Planting time Realized impact of ambient temperatures on development
and growth patterns
~10 McMaster et al. (2005)
Planting method (e.g. row
spacing)
Affects boundary layers and energy balance ~2 Loomis and Connor (1992)
Irrigation Potential for evapotranspirative cooling ~10 Ehrler (1973)
Tillage system Affects water infltration into soil ~10 Hobbs and Govaerts (Chapter
10, this volume)
Residue management Residues impact on water fuxes at soil surface ~10 Hobbs and Govaerts (Chapter
10, this volume)
Weed control Weeds compete for water ~5 Oerke (2006)
Pests and diseases Can affect stomatal behaviour ~2 Rosyara et al. (2008)
Genetic Ground cover and establishment Bare soil heats quickly affecting crown temperature ~20 Ross et al. (1985)
Canopy architecture Area and structure affects energy absorbed and water
demand to balance exchange of CO
2
~2 Araus et al. (1993)
Stomatal conductance Determines rate of evaporative cooling ~2 Amani et al. (1996)
Root growth Area and pattern affects water supply ~5 Reynolds et al. (2007)
Root signalling Affects rate of evaporative cooling ~2 Davies et al. (2005)
Pigment composition Affects energy absorbed ~2 Tardy et al. (1998)
Epicuticular wax Affects energy absorbed ~2 Richards (2006)
Phenological pattern E.g. foral structures have lower evapotranspiration rate
than leaves
~2 Ayeneh et al. (2002)
a
Refers to mechanism rather than actual temperature differences, which are estimated by authors.
76 M.P. Reynolds et al.
increased risk of drought impact through the
exhaustion of stored soil water compared
with slower growing crops.
However, as temperatures increase CO
2
solubility declines relative to O
2
. Tus, for C
3
crops the compensation of elevated CO
2
can
be confounded by photorespiration. Also,
elevated temperatures are known to impair
Rubisco activase, the enzyme responsible for
removing the inhibitory ribulose 1,5-bis-
phosphate from a deactivated Rubisco (Parry
and Hawkesford, Chapter 8, this volume). As
such, some of the apparent benefts of
elevated CO
2
may be ofset by higher
tempera tures, causing photosynthesis to be
energetically more expensive.
Biotic stress
Although beyond the scope of this chapter,
changing patterns of drought and heat, as
well as elevated CO
2
, are likely to be accom-
panied by a change in the spectrum of biotic
stresses. For most cereals, more tropical
environments are also associated with
greater numbers of foliar pests and diseases;
therefore climate change would be likely to
result in increased risk of epidemics (Legrve
and Duveiller, Chapter 4, this volume). In
dry regions, root diseases such as nematode
infestation are also problematic since they
further reduce the plants ability to extract
scarce water (Nicol and Rivoal, 2007).
Physiological Basis of Stress
Adaptation in Major Crops
Physiological effects of water stress
Water defcit leads directly to stomatal
closure and reduces the potential for CO
2
fxation relative to well-watered plants.
Closure is caused both by hydraulic efects
and by chemical signalling, the latter being
an adaptive function that increases transpir-
ation efciency (Davies et al., 2005) and is
the basis of the common practice of defcit
irrigation in water-scarce environments
(Fereres and Soriano, 2007). A consequence
of reduced transpiration rate may be that
plant organs experience heat stress (see next
section). Increasing water defcit leads to
changes in tissue water potentials that may
be suboptimal for expansive growth and
metabolism (Hsiao, 2003). Osmotic adjust-
ment is commonly observed under water
defcit to resist further dehydration and to
maintain favourable gradients of water
potential that permit growth to continue
(Morgan, 2000). If these drought-adaptive
strategies are insufcient to maintain
growth and development, reproductive
behaviour will be impaired leading to foret
sterility and/or inadequate levels of assimi-
lation to sustain seed growth (see Barnabas
et al., 2008). Cessation of growth may be
followed by tissue dehydration if water stress
is not relieved, potentially resulting in
damage to the photosynthetic apparatus
and other metabolic processes (Ghannoum,
2009). A more recently observed phenom-
enon under drought is that of micronutrient
defciency caused by reduced transpiration
rates under water defcit. Zinc is involved in
detoxifcation of reactive oxygen species
(ROS) so low rates of passive uptake coupled
with increased production of ROS under
moisture stress combine to exacerbate
drought-stress symptoms in soils that are
zinc defcient (Bagci et al., 2007).
Physiological effects of heat stress
A principal efect of heat is to accelerate
growth and development, shortening the
window of opportunity to intercept radia-
tion. As a result of accelerated growth rate,
total leaf area available for photosynthesis is
frequently reduced also, further reducing
yield potential. For example, wheat has been
shown to lose 34% of yield/C above the
optimum daytime temperature of 15C
(Wardlaw et al., 1989). However, the actual
degree of heat stress experienced by a crop
depends on the interaction of many environ-
mental and genetic efects (Table 5.1),
including evaporative cooling which may
vary considerably throughout the crops life
cycle and at a local level. When evaporative
cooling is insufcient to maintain plant
organs at close to optimal temperatures, the
Breeding for Adaptation to Heat and Drought Stress 77
plants will experience metabolic inefcien-
cies associated with functioning outside
optimal temperature ranges (Burke et al.,
1988). For example, starch synthase may be
rate limiting to grain flling at warmer
temperatures (Hurkman et al., 2003) and
elevated temperatures also increase wasteful
photorespiration in C
3
species (Parry and
Hawksworth, Chapter 8, this volume).
Increased rates of dark respiration are
another source of lost productivity at high
temperature and remain an important chal-
lenge to stabilizing crop productivity in the
advent of climate change; even a tropical
crop such as rice loses yield potential at
warmer night temperatures (Mohammed
and Tarpley, 2009). As under water defcit,
high temperature stress can also lead directly
to sterility by impairing meiosis, gametogen-
esis and fertilization (Barnabas et al., 2008;
Hedhly et al., 2009). In an agronomic
context, heat stress can lead to macronutri-
ent defciency associated with the inability
of transport processes to match accelerated
growth rates (Rawson, 1986).
Short-term extreme increases in tempera-
ture of 510C can have quite catastrophic
efects on yield especially if they occur at
critical stages of development. Tis sensitiv-
ity is not exclusive to cool season crops but is
also observed in relatively heat-adapted
crops, such as rice (Wassmann et al., 2009).
Adaptive strategies
Tere are a number of strategies to amelior-
ate the efects of drought and heat stress.
Agronomic strategies
Agronomic strategies include: (i) modifying
planting time such that critical growth
stages do not coincide with stressful condi-
tions (McMaster et al., 2005); (ii) resource
conserving technologies that help available
growth inputs, especially water, to be
supplied as optimally as possible to the crop
(Hobbs and Govaerts, Chapter 10, this
volume); and (iii) good husbandry to avoid
weeds, pests and diseases from further
exacerbating stress.
Trait-based strategies
Te most efective genetic strategy has been
to change the phenological pattern of the
crop so that critical growth stages do not
coincide with stressful conditions or simply
to fnish the life cycle early before severe
stress conditions occur (Ludlow and
Muchow, 1990). Another is to minimize the
occurrence of stress through development
of a good root system, which in the case of
drought permits water to be accessed deeper
in the soil (Lopes and Reynolds, 2010) and
in the case of heat permits transpiration
rates that better match evaporative demand
(Amani et al., 1996), thereby permitting
maximal carbon fxation with the benefts of
canopy cooling. In environments where
extra water is not available to mitigate
stress, other stress-adaptive strategies
include a range of leaf canopy traits such as
epicuticular wax, pigment composition, leaf
angle and rolling, etc. that infuence radia-
tion load and photosynthetic response,
while increased transpiration efciency
permits available water to be used more
efectively (Richards, 2006). Maintaining
foliar and root health through genetic resist-
ance to pest and diseases is usually consid-
ered prerequisite. Such efects can be
cumulatively signifcant and will interact
with other environmental and agronomic
efects such as irrigation and tillage systems
(Table 5.1). Examples of their application
are discussed subsequently in the context of
specifc breeding eforts, as well as in various
books (see Ribaut, 2006; Jenks et al., 2007).
Cellular and molecular strategies
It is expected that the growing understand-
ing of the cellular and molecular basis of
adaption to heat and drought stress will
have signifcant impact in breeding for
climate change in future decades. For exam-
ple, it is established that plant response to
drought involves multiple mechanisms asso-
ciated with water relations, chemical signals
and membranes (Chaves et al., 2003). In
maize, part of the efect of drought on foret
abortion a trait which has a disproportion-
ate efect on harvest index compared with
78 M.P. Reynolds et al.
its efect on water-use efciency has been
traced to several genes involved in sucrose
metabolism (Boyer and McLaughlin, 2007).
Gene expression studies have confrmed
that soluble starch synthase is a rate-
limiting step for grain flling in wheat when
exposed to high temperature (Hurkman et
al., 2003), while surprisingly no clear role for
heat shock proteins has been identifed in
cereals despite a well-established role in
acclimation to heat stress in Arabidopsis
(Barnabas et al., 2008). Favourable water
relations are a crucial aspect of adaptation
to both drought and heat stress so further
understanding of the role of aquaporins,
which show a high degree of diversity, in
maintaining plant function under stress may
lead to useful genetic modifcations
(Kaldenhof et al., 2008). When combining
heat and drought stress, novel metabolic
responses have been demonstrated compared
to when stresses are experienced in isolation
(Mittler, 2006). Readers are referred to
comprehensive reviews of genomic
approaches to determine the mechanistic
basis of adaptation to heat and drought
stresses, which shed light on candidate genes
for crop improvement, by Chaves et al.
(2003), Shinozaki and Yamaguchi-Shinozaki
(2007) and Barnabas et al. (2008) and refer-
ences therein.
Part of the molecular basis for heat
susceptibility in wheat seems to be related
to ethylene levels. In a comparison of heat-
susceptible versus -tolerant winter wheat
cultivars, an increase in ethylene was shown
to be directly responsible for regulating the
heat-induced grain abortion and reduction
in kernel weight (Hays et al., 2007a).
Ethylene may be playing a fundamental role
in stress signalling, given that the ethylene
receptors share signifcant homology with
two-component histidine kinase receptors
in prokaryotes that have been shown to act
as heat sensors. However, ethylene-induced
kernel abortion and premature maturation
in response to heat stress, while possibly
being a useful survival trait (to temper prog-
eny load in warm, dry climates), is clearly
detrimental to productivity, and these stud-
ies have led to markers for selection against
its expression.
However, the general current under-
standing of the complex interaction of cellu-
lar/molecular mechanisms with whole-plant
adaptation to contrasting environments
does not yet permit its reliable application
in cultivar selection. Nevertheless, a few
ambitious projects exist, such as the C
4
rice
initiative which aims to identify all of the
genes necessary to introduce Kranz anat-
omy and CO
2
-concentrating mechanisms
into C
3
species (Hibberd et al., 2008), and
genetic modifcations associated with
increasing CO
2
fxation rate by Rubisco
(Parry and Hawkesford, Chapter 8, this
volume). If successful, these would lead the
way to substantial increases in heat adapta-
tion in C
3
crops, as well as adaptation to
moderate levels of moisture stress, though
C
4
photosynthesis is possibly more sensi-
tive to dehydration stress than is C
3
photo-
synthesis (Ghannoum, 2009). On the other
hand, empirical studies involving geneti-
cally mapped populations have identifed
quantitative trait loci (QTLs) associated
with adaptation to drought and heat; the
potential of these QTLs to achieve genetic
gains in yield is discussed later.
Breeding Approaches for Heat and
Drought Adaptation
Conventional breeding approaches have had
considerable impact in marginal environ-
ments as well as favourable ones. For exam-
ple, economic analysis shows that in the late
1990s, around 25% of global wheat produc-
tion increase came from improved produc-
tion in marginal environments (Lantican et
al., 2003). Much of this impact was achieved
by combining genes of major efect associ-
ated with agronomic type, phenology and
disease resistance into good yielding back-
grounds. However, impacts have also been
achieved more recently through targeting
specifc heat- and drought-adaptive traits in
cereals. Tese have typically occurred for
integrative traits, such as transpiration ef-
ciency and canopy temperature (CT), which
are composite measures of numerous physio-
logical and morphological processes.
Breeding for Adaptation to Heat and Drought Stress 79
Wheat breeding
Over 200 million ha of wheat are cultivated
worldwide in environments ranging from
very favourable in Western Europe to
severely stressed in parts of Asia, Africa and
Australia.
Breeding for dry environments in Australia
In Australia, trait-based breeding has
resulted in the adoption of a number of
useful traits afecting water-use efciency.
Tese include intrinsic transpiration ef-
ciency of leaves as well as longer coleoptiles
and tillering traits that improve early season
canopy coverage and, therefore, decrease
surface water losses in environments with
early season moisture followed by post-
anthesis stress (Richards, 2006; Rebetzke et
al., 2009). A recent review of this research
(Rebetzke et al., 2009) emphasized the
opportunities to employ multi-disciplinary
approaches to develop improved wheat culti-
vars that have characteristics that modify
their water demands over the season (modi-
fcations in vigour, tillering and canopy
structure) and their capability to maintain
water supply. For wheat, which is subject to
a large range of root stresses due to both
biotic (nematodes, Fusarium spp.) and
abiotic (salinity, B toxicity, Zn defciency)
constraints, breeding for tolerance to such
conditions has resulted in favourable returns
in marginal environments even where aver-
age yields may be < 1.5 t/ha.
Breeding for dry environments internationally
Te semi-dwarf habit associated with Rht
genes increased yield potential in all wheat
growing environments (Lantican et al.,
2003), sparking of the Green Revolution led
by Norman Borlaug, and led to the establish-
ment of international crop breeding insti-
tutes such as the International Maize and
Wheat Improvement Center (CIMMYT) and
the International Rice Research Institute
(IRRI), with IRRI leading the Green Revolu-
tion in rice. To this day, CIMMYT coordi-
nates an international collaborative wheat
improvement network that distributes
approximately 1000 new genotypes annu-
ally to collaborators worldwide (Braun et al.,
Chapter 7, this volume). Tese genotypes
are specifcally targeted to the range of
mega-environments (MEs) found in wheat-
producing developing countries, including
MEs designated as experiencing substantial
periods of drought and heat. Analyses of
CIMMYT international yield trial data for
germplasm distributed to semi-arid envir-
onments between 1979 and 1998 (namely
of the Semi-Arid Wheat Yield Trial, SAWYT)
indicate highly signifcant genetic gains for
yield (Trethowan et al., 2002). Economic
analysis of the impact in drought- and heat-
afected environments showed annual yield
gains of 23% in the same period, in part
because it coincided with the frst introduc-
tions of disease-resistant, semi-dwarf culti-
vars for many farmers in these more marginal
environments (Lantican et al., 2003).
However, the upward trend (~1%/year)
continues to the present for bread wheat
(Y. Mannes, Mexico City, 2009, personal
communication), while durum wheat culti-
vars show still larger genetic gains of
1.21.4%/year (average increase for the
period 19832004) across hundreds of
environments worldwide (Fig 5.2). Although
the greatest progress is observed in the
drought-stressed sites, the data of Ammar et
al. (2008) clearly show that breeding for
broad adaptation has substantial impact
across a wide range of environments.
Te CIMMYT approach focused initially
on delivering broadly adapted germplasm
that performed relatively well in dry years
but aimed to retain yield potential in above-
average rainfall years and where irrigation
was available. Subsequently, broader genetic
bases were utilized, including wild wheat
ancestors through wide crossing techniques,
generating re-synthesized hexaploid wheats
(Trethowan and Mujeeb-Kazi, 2008). Tis
provides genetic sources that can, for exam-
ple, confer more drought-adaptive root
growth to permit access to water from
deeper soil profles (Reynolds et al., 2007).
Marker assisted selection (MAS) has also
been incorporated into conventional breed-
ing to screen for a number of genetically
simple traits mainly associated with disease
80 M.P. Reynolds et al.
resistance (William et al., 2007). For exam-
ple, use of molecular markers for resistance
to cereal cyst nematode improved the devel-
opment of healthy roots in the many low
rainfall areas where this pest is most prob-
lematic (Nicol and Rivoal, 2007).
Physiological breeding approaches have
also been recently adopted by CIMMYT and
are used in several phases of breeding
(Reynolds et al., 2009). Specifcally: (i) physi-
ologically characterized parents are used to
design crosses more strategically, thereby
resulting in cumulative gene action in
selected progeny; (ii) early generation selec-
tion using high-throughput screening tools
such as infrared thermometry enrich the
gene frequency for desirable traits before
yield testing is feasible; (iii) evaluation of
non-adapted genetic resources such as
landraces or even wild species help deter-
mine genotypes that show promising expres-
sion of stress-adaptive traits for subsequent
use in hybridization; and (iv) design and
precision phenotyping of experimental
populations have facilitated gene discovery
for potential applications in molecular
breeding.
Breeding for hot, dry environments
Considerably more efort has gone into
breeding crops for drought than for heat
adaptation. None the less, work in a few
heat-stressed environments has revealed
valuable traits. Te Southern Great Plains of
the USA are among the most challenging
environments for wheat cultivation and it
has been estimated that wheat loses 3050%
of its yield potential due to high tempera-
tures alone based on a yearly average
temperature of 28C during reproductive
development (Hays et al., 2007b). Te
response of wheat to both chronic heat
stress (Wardlaw et al., 1989) and short-term
heat shock (Hays et al., 2007a) is well docu-
mented and many of the current hard red
winter wheat varieties grown in the Great
Plains region have shown susceptibility in
Fig. 5.2. Relative performance of the fve top lines of the 14th35th International Durum Yield Nursery
expressed as percentage yield of the widely adapted check cultivar Yavaros 79, grown at 827
environments in 48 countries between 1983 and 2004. Performance is expressed for three main
environments based on average nursery yield: < 2.5 t/ha, representing water-stressed sites ();
2.55.0 t/ha, (); and > 5.0 t/ha, representing well-watered sites () (fgure drawn by Karim Ammar
using data from Ammar et al., 2008).
Y
i
e
l
d
(
%
)
o
f
a
d
a
p
t
e
d
c
h
e
c
k
14th35th International Durum Yield Nursery (year)
160
150
140
130
120
110
100
90
1980 1985 1990 1995 2000 2005
<2.5 t/ha (Drought environments) Y = 1.40x 2663. R
2
= 0.42
2.55.0 t/ha (Intermediate envs) Y = 1.32x 2517. R
2
= 0.65
>5.0 t/ha (High yield envs) Y = 1.24x 2369. R
2
= 0.75
Breeding for Adaptation to Heat and Drought Stress 81
terms of their inability to maintain yield and
quality under high temperatures (Hays et al.,
2007b). While varieties that show improved
yield stability under heat stress have been
identifed (Hays et al., 2007a, b), the quanti-
tative nature of heat tolerance and unpre-
dictability of heat stress in the feld make it
particularly difcult for breeders to efec-
tively select for the trait. Furthermore, in a
rainfed environment, heat is often exacer-
bated by drought stress (Mittler, 2006).
One trait that is showing promise in this
complex and unpredictable environment is
leaf glaucousness. As the primary interface
between the plant and the environment, the
plant wax cuticle is one plant adaptation
that can ameliorate both water loss from
epidermal transpiration and excess radia-
tion load. Te cuticle reduces transpirational
cooling needs by acting as an adaxial and
abaxial refective surface to excess light
energy. A reduced absorption at visible and
near-infrared wavelengths due to enhanced
refectance can reduce internal tissue
temperatures and the vapour pressure difer-
ences between the tissues and the outside
air, which reduces transpirational water loss
(Sheppard and Grifths, 2006). It has been
postulated that plants adapted to hotter,
dryer climates have thicker cuticles and
lower rates of transpiration through the
cuticle. In structurally similar leaves, when
stomates are closed, water loss has been
shown to be inversely proportional to the
cuticle thickness (Jenks et al., 1994). Despite
the apparent diversity in leaf wax layers and
the variation in wax composition, little criti-
cal information exists relating this variation
to improve adaptation under heat- or
drought-stress conditions. In wheat and
other cereals, epicuticular wax imparts a
bluish-green cast, and is a useful marker for
selecting for heat and drought adaptation.
Using pairs of near-isogenic lines of wheat,
Johnson et al. (1983) reported that leaf
waxiness reduced transpiration and
increased yield and water-use efciency in
dryland conditions. Others have reported
similar efects, for example in rice
(Wassmann et al., 2009). Stem and leaf
cuticular wax is genetically simple. In wheat,
the gene for waxiness W1 has been mapped
to chromosome 2BS while a gene for heavy
wax is located on chromosome 2A
(Tsunewaki and Ebana, 1999).
Breeding for hot, irrigated environments
Considering germplasm targeted for warmer,
irrigated environments, analysis shows
signifcant progress in CIMMYT inter-
national nurseries, with many of the lines
that perform well at the hottest sites also
expressing good yield potential under more
temperate conditions (Lillemo et al., 2005),
an important consideration given typical
year-to-year variation in temperature. In hot
low RH environments, CT measured at the
breeding location was shown to be a good
predictor of performance across a range of
heat-stressed target environments (Reynolds
et al., 1994). More recent eforts have
focused on breeding for earlier maturing
cultivars that escape terminal heat stress
and encompass resistance to diseases associ-
ated with warm humid environments (Joshi
et al., 2007) as well as the highly virulent
Ug99 stem rust strain.
Selecting for root characteristics using
canopy temperature (CT)
Capacity for more extensive roots is an adap-
tive trait with good potential to increase
productivity in drought- and heat-prone
environments where water is available at
deeper soil profles. For example, subsoil
water accessed during grain flling is used
especially efciently since it contributes
entirely to grain growth (Kirkegaard et al.,
2007). While estimating root characteristics
of cultivars is not practical on a breeding
scale, measuring CT of crops permits rela-
tive water-uptake capacity by roots to be
estimated very easily. A repeatable value of
CT can be measured in about 10 s per plot
using an inexpensive infrared thermometer.
Validation studies using genetic resources
have shown that CT measured during peak
stress periods is associated with approxi-
mately 50% of the variation in soil water
extraction in soil profles below 60 cm
82 M.P. Reynolds et al.
(Reynolds et al., 2007) and is directly associ-
ated with root depth (Lopes and Reynolds,
2010). CT measurements in a wheat popula-
tion of 167 recombinant inbred lines
confrmed the potential for achieving signif-
icant genetic gains when using CT as an
in direct selection criterion; it typically
explains 50% or more of yield variation
under drought (Olivares-Villegas et al., 2007)
and heat stress (Amani et al., 1996; Pinto et
al., 2010). Economic analysis has confrmed
the value of CT as an indirect selection tool
to increase breeding efciency (Brennan et
al., 2007) and several QTLs for CT have been
recently identifed (Pinto et al., 2010).
Maize breeding
Maize is grown on approximately 150 million
ha worldwide, of which ~100 million ha is in
developing countries, though the latter
account for less than half of total produc-
tion. Over the last 100 years, maize has been
the major commercial success of cereals.
Adaptation of the crop in the main produc-
tion areas of the USA is now expanding
further into the more marginal western
areas (Mason et al., 2008), while production
and adoption of hybrids has also begun to
increase more rapidly in tropical regions,
particularly in Brazil, Argentina, India,
Tailand, Vietnam and parts of China.
Campos et al. (2006) demonstrated that the
major gains in productivity since the mid-
1950s have been in an increased tolerance to
stress. At low plant densities (< 20,000
plants/ha), modern hybrids have little
advantage over mid-20th century hybrids.
However, at higher commercial densities
and under conditions of drought (Campos et
al., 2006) and heat (Mason et al., 2008)
modern hybrids are better able to initiate
and establish productive ears and grains. Lee
and Tollenaar (2007) concluded that the
success of maize breeding was realized
through continuous and simultaneous
improvements in the maintenance of the
source of assimilate supply, mainly through
increased stay-green (under conditions
including stress), and in the sink as
described below.
Maize is relatively well adapted to high
temperature and also shows good transpir-
ation efciency because of the C
4
character-
istic of concentrating CO
2
to bypass the
oxygenase activity of Rubisco. However,
maize shows large genetic variation in the
relative timing of male and female fower-
ing, commonly referred to as the anthesis
silking interval (ASI). Since expression of
longer ASI is associated with signifcantly
larger relative investment in tassel biomass
over ear biomass (and under extreme stress
may result in total ear barrenness while not
preventing pollen dissemination), delayed
ASI leads to reduced kernel set under
drought and a number of other stresses
(Edmeades et al., 2000). Based on this, ASI
was used as the main physiological selection
criterion to make genetic gains under
drought in CIMMYTs maize stress breeding
programme (Edmeades et al., 2000). Building
on ASI-improved germplasm and the concept
of selection under well-managed stress
environments, Bnziger and colleagues
(2006) began a maize breeding programme
in CIMMYTs sub-Saharan Africa operation
in 1997 that has resulted in dozens of new
hybrids which, on average, outperformed
standard checks (checks are well-adapted
elite cultivars) across a broad range of envir-
onments at over 40 locations across eastern
and southern Africa and by as much as
100% under severe stress.
Sorghum breeding
Sorghum, which is grown on approximately
40 million ha worldwide, is an especially
important crop for resource-poor farmers in
rainfed regions of the developing world as a
result of its excellent level of adaptation to
drought and heat stress (again related to its
C
4
metabolism) and its dual-purpose nature,
it being used both in cooking and, as the
stover, for animal feed.
Maintenance of stay-green under termi-
nal drought conditions is used as a visual
Breeding for Adaptation to Heat and Drought Stress 83
selection criterion for sorghum breeding
under drought in the USA and Australia
(Borrel et al., 2000 and references therein).
Stay-green is valuable not only as a selection
criterion for yield under drought but also
because non-senescent genotypes accumu-
late more soluble sugars in stems during and
after grain flling to improve nutritional and
commercial value (McBee et al., 1983).
Research has suggested that greater green
leaf area duration in sorghum is the product
of diferent combinations of three factors:
green leaf area at fowering, time of onset of
senescence and rate of senescence, all of
which appear to be inherited independently
(Borrell et al., 2000; Borrell and Hammer,
2000).
Despite the ease with which stay-green
can be selected, a number of doubts have
existed among breeders with respect to its
merits, including: (i) whether the trait might
be associated with smaller panicle size; (ii)
that its selection under drought might result
in a yield penalty under irrigated conditions;
(iii) the magnitude of genetic gains associ-
ated with its selection; and (iv) whether it is
also involved in lodging resistance. Tese
issues were comprehensively addressed by
Borrell and colleagues (2000) in a study of
nine closely related hybrids that varied in
rate of leaf senescence under contrasting
water regimes in north-eastern Australia.
While diferences in yield among hybrids
under well-watered conditions were negligi-
ble, under terminal water stress stay-green
hybrids produced almost 50% more post-
anthesis biomass than senescent lines, and
green leaf area at maturity was strongly
correlated with grain yield (Borrell et al.,
2000). Mechanisms related to supply and
demand for N during grain flling contribute
to stay-green expression in sorghum and
include: (i) a higher initial level of leaf N at
fowering; (ii) more N uptake during grain
flling; (iii) less remobilization of N from
leaves; and (iv) larger retention of chloro-
plast proteins until late senescence (Borrel
and Hammer, 2000). Genetic studies have
identifed QTLs associated with stay-green
(Harris et al., 2007).
Rice breeding
Rice, which is grown on ~150 million ha
worldwide, is the major staple food in Asia,
where 90% of the crop is produced. IRRI
leads an Asia-based rice research and breed-
ing programme which tackles all aspects of
adaptation including to drought and heat
stress. While most rice is grown under
monsoonal rains, a substantial area is also
grown under dryland conditions with the
possibility of water defcit. Evolving from a
semi-aquatic ancestor, rice is generally more
susceptible to water-limited conditions
compared to other cereals crops (Wassmann
et al., 2009). None the less genetic variation
has been exploited and under upland feld
conditions, increased root diameter, and
depth and/or branching of root systems
have been associated with decreased plant
water stress and increased grain yield under
severe stress (Laftte and Courtois, 2002).
QTLs associated with constitutive and adap-
tive root growth under drought have been
identifed (Khowaja et al., 2009). As proof of
concept, near-isogenic lines (NILs) were
developed by introgressing four root QTLs
on chromosomes 2, 7, 9 and 11 from the
variety Azucena into the Indian upland vari-
ety Kalinga III, and evaluated in the feld and
on-farm trials; NILs with root QTLs out-
performed Kalinga III for grain and straw
yield (Steele et al., 2007).
Under drought stress, decreased pedun-
cle elongation reduces panicle extrusion and
forets that remain in the fag leaf sheaf are
usually completely sterile, severely reducing
grain yield in cultivars that are prone to
reduced extrusion (OToole and Namuco,
1983). Selection for continued peduncle
elongation under reproductive stage drought
stress in rice is being used to increase grain
yield under feld drought stress. Rice pedun-
cle elongation is partially controlled by local
gibberellin levels (Kaneko et al., 2004).
Repression of cell-wall invertase genes and
the cell-wall loosening genes for xyloglucan
endotransglycosylase/hydrolase (XTH) have
also been linked to reduced peduncle elong-
ation (Ji et al., 2005).
84 M.P. Reynolds et al.
Comparatively less research has been
conducted on heat tolerance in rice
(Wassman et al., 2009). Genetic variation
for high temperature tolerance per se has
been observed in rice, with fowering being
the most sensitive stage. Variation for the
time of day of fowering is an important
mechanism of heat avoidance (Jagadish et
al., 2008). Oryza glaberrima fowers earlier in
the day than Oryza sativa and crosses
between them have shown that earlier fow-
ering can be easily selected for (Prasad et al.,
2006).
For further details on breeding of cereals
for adaptation to low-yielding stress envir-
onments, readers are referred to chapters in
Drought Adaptation in Cereals (Ribaut,
2006).
Strategies to Accelerate Genetic
Gains
Outputs from the above examples, while
providing stress-adapted genetic stocks, also
serve as good models for breeders and
researchers worldwide tackling drought and
heat stress. Te following section will focus
on other promising approaches that are
likely to have additional impacts in the near
future.
Exploration of genetic resources to boost
physiological and molecular breeding
While conventional plant breeding has
already achieved signifcant progress in
stress breeding as outlined, three main
approaches can be employed to widen gene
pools: (i) introgression of traits from genetic
resources with compatible genomes, such as
landraces; (ii) wide crosses involving inter-
specifc or intergeneric hybridization; and
(iii) genetic transformation. To date genetic
resources have been used mainly to intro-
duce resistance to biotic stresses (Dwivedi et
al., 2008), while relatively few wild crop rela-
tives have been exploited for adaptation to
abiotic stress (Hajjar and Hodgkin, 2007). In
fact, the majority of accessions in germ-
plasm collections remain uncharacterized in
terms of their potential to improve yield
under abiotic stress; current challenges are
to identify elite sources of traits among
genetic resources, estimate potential yield
gains associated with trait expression in
good agronomic backgrounds, and defne
potentially complementary traits that if
introgressed into a common genetic back-
ground are likely to result in cumulative gene
action for yield (Reynolds et al., 2009).
Hexaploid wheat has been a useful model for
alien introgressions and impacts include
increased yield in a range of environments
including drought (Trethowan and Mujeeb-
Kazi, 2008). Another avenue currently being
explored is the use of Leymus racemosus to
introgress genes for root exudation of nitri-
fcation inhibitors (Subbarao et al., 2007);
the potential impact on reducing potent
greenhouse gas emissions is enormous and
could signifcantly mitigate global warming
if successfully adopted on a global scale. A
vast reserve of genetic potential in closely
related crop species has yet to be evaluated,
and as understanding of the physiological
and genetic basis of stress adaptation
improves, it will become easier to apply
molecular marker technology to mine
genetic resource collections for potentially
useful alleles.
Transgenic technology efectively
re moves taxonomic barriers altogether but
although much data has been collected under
controlled environments for candidate genes
that improve survival of both model and
crop species under abiotic stress (Umezawa
et al., 2006), more candidate genes need to
be tested in a range of relevant feld environ-
ments (Nelson et al., 2007) if impacts are to
be achieved. Candidate genes, such as those
associated with functional proteins and
especially upstream regulation, could afect
any of the drivers of yield under stress (see
Fig. 5.1 for examples) depending on at what
stage of development and in which tissue
they are expressed. One well-studied candi-
date gene is DREB1A; stress-regulated
expression of this gene with the rd29A
promoter produced plants with increased
tolerance to freezing, salt and drought
Breeding for Adaptation to Heat and Drought Stress 85
stresses, without producing changes in the
normal phenotype of the transformed plants
(Chandler and Robertson, 1994). Te gene
has been associated with improved root
growth under water stress in well-controlled
phenotyping studies in groundnut (Vadez et
al., 2007). Another approach that may be
useful in tackling climate change is to replace
genes that are especially heat susceptible in
temperate crops with their analogues from
tropical species like rice or maize; a good
example would be soluble starch synthase
which is a rate limiting step to grain flling in
wheat at high temperature (Hurkman et al.,
2003).
Molecular breeding for drought and heat
In breeding applications, molecular markers
may be either diagnostic (i.e. perfect mark-
ers of a specifc allele within a specifc gene
sequence) or putative (e.g. markers associ-
ated with or fanking a QTL that has been
discovered via mapping in biparental crosses
or in association panels of related or unre-
lated lines). Diagnostic markers are prefer-
able as they can be used to select desired
alleles in any parental or progeny line of a
species under any crossing strategy.
Alternatively, such markers can be used to
prepare a gene for transgene (genetic modif-
cation, GM) approaches within or across
crop species. QTL markers from mapping
studies are not perfectly linked to genes (i.e.
they are nearby) and are frequently difcult
to transfer between crosses, unless there is
substantial research investment in crossing
and mapping to fne map the QTL to locate
markers that are within a gene. Te identif-
cation of QTLs for complex traits is further
confounded by substantial genotype envir-
onment interaction efects that occur for
traits like heat and drought adaptation.
Crossa et al. (Chapter 14, this volume) high-
light the new capabilities in statistical
methods , such as modelling of QTL envir-
onment efects (Boer et al., 2007) that enable
the more robust detection of useful genomic
regions for selection.
MAS is routinely applied for traits such as
disease resistance and grain quality
characters when diagnostic gene-based
markers have been identifed (William et al.,
2007; Whitford et al., Chapter 12, this
volume). Such markers, located within a
gene sequence, are discovered through either
fne mapping around QTLs of large efect, or
by looking for gene candidates that are part
of known pathways (e.g. functional disease
resistance genes). Only few QTLs of large
efect have been documented for perform-
ance-related traits under heat or drought
and no candidate genes in known biochem-
ical pathways of response to heat or drought
have been shown to have large efects on
performance traits such as yield. Using fne-
mapping approaches, genes have been iden-
tifed and cloned for a number of abiotic
stresses, including salinity, fooding, Al
tolerance and B tolerance (Collins et al.,
2008), but none has been cloned from QTLs
associated with drought or heat stress. In
part, the low success rate for these stresses
relates partly to the genetic and environ-
mental complexity of adaptation. Mapping
populations have frequently been made by
crossing highly contrasting parents to maxi-
mize genetic polymorphisms in the progeny.
Terefore, performance QTLs identifed in
random lines or in deliberately contrasting
lines are likely to be associated with traits
that have already been optimized by breed-
ing. Furthermore, in crops like wheat and
barley, it has been demonstrated that segre-
gation for genes of major agronomic efect
(height and maturity) within experimental
populations makes it more difcult to iden-
tify QTLs of minor efect that may be associ-
ated with more direct mechanisms of
adaptation (Reynolds et al., 2009). Using
mapping populations with more uniform
fowering time (Olivares-Villegas et al.,
2007) both trait and yield QTLs were readily
detected independent of loci associated with
phenology (Pinto et al., 2010).
Discovery and utilization of QTLs for
drought and heat tolerance requires further
investment in development of genetic
resources and in more detailed phenotypic
dissection of complex performance traits.
86 M.P. Reynolds et al.
To assist with gene discovery, several preci-
sion phenotyping protocols based on remote
sensing can be applied, including spectral
refectance indices for a range of growth-
related parameters (Montes et al., 2007) and
infrared thermometry as mentioned earlier.
Application of these principles in wheat has
led to the identifcation of a number of QTLs
that are associated with both drought and
heat adaptation, which suggests some
common genetic basis for adaptation to
these two stresses (Pinto et al., 2010). Te
usefulness of such traits in selection requires
the development of a comprehensive under-
standing of the genetic and environmental
infuences that determine their efect on
yield and other performance characteristics
(see Crossa et al., Chapter 14, this volume).
Molecular breeding is benefting from the
rapidly decreasing cost of genotyping, and
points to a more pragmatic future in which
phenotyping is again highly valued.
Commercial breeding programmes (espe-
cially in maize and soybean) are now begin-
ning to release germplasm that has been
developed for yield through the application
of marker-assisted recurrent selection
(MARS) (Eathington et al., 2007). Tis
approach relies on cheap abundant marker
systems being applied to a large number of
accurately phenotyped biparental popula-
tions, followed by rigorous statistical meth-
ods. Breeders either estimate QTLs using
the types of methods described by Boer et al.
(2007) or apply techniques such as genome-
wide selection (GWS) to assign predictive
values to every marker used in the analysis
(e.g. Hefner et al., 2009). Favourable QTLs
and/or markers are then used in several
cycles of glasshouse selection to quickly
assemble new inbred lines as complexes of
useful genomic regions, although without
direct knowledge of the genes or their mech-
anisms (i.e. fne mapping and gene discovery
is not utilized at all in the breeding, although
these may follow at a later date to locate
genes for future use as diagnostic markers or
in gene transformation). Hefner et al.
(2009) have argued that the typical lack of
success in breeding with QTLs means that
genome-selection methods, where every
marker has a value (positive or negative),
will probably take over from QTL approaches.
MARS molecular breeding methods acceler-
ate the traditional phenotyping approach of
breeding and are being deployed in many
breeding programmes as an adjunct to
phenotypic methods. Readers are referred to
the chapter by Whitford et al. (Chapter 12,
this volume) for further examples of applica-
tions of biotechnology in breeding.
Conclusions
In terms of genetic improvement of crops, a
number of research approaches can be
adopted to help ofset the negative efects of
climate change. Multi-disciplinary breeding
with a special focus on adaptation to warmer
and drier environments should be the base-
line. New genetic variation can be introduced
into such programmes, for example, through
interspecifc hybridization with crop rela-
tives, or by introducing genes of proven value
from model species. Torough characteriza-
tion of target agroecosystems is essential
such that diferent models of genetic adapta-
tion can be systematically evaluated, taking
into account climatic and edaphic factors as
well as management practices. A more
complete understanding of the environment
will also help with gene discovery and deploy-
ment of QTLs for complex adaptive traits.
Application of appropriate tools molecular
techniques, remote sensing for precision
phenotyping, networks of feld operations,
etc. will permit rapid genome analysis to be
coupled to the adaptive response of crops.
Determination of the theoretical limits to
yield under water-limited and temperature-
stressed environments will help to establish
realistic research targets, while new research
must consider how crops can maintain
productivity in warmer climates without
substantial sacrifces in water-use efciency,
as well as adapt to extreme climatic events
such as sudden temperature spikes and
combinations of stresses. Given that climate
is in a state of fux, more extreme weather
variation can be expected in the future,
therefore new ideotypes should be evaluated
for their relative yield stability, using realistic
farmer conditions, under a full range of
Breeding for Adaptation to Heat and Drought Stress 87
potential scenario s from optimal, well-
managed en vir on ments to those with
extreme climatic stresses.
Acknowledgements
MPR acknowledges Jill Cairns for providing
information on rice breeding and the
Australian Grains Research and Develop-
ment Corporation (GRDC) for its fnancial
support. SC leads the project A national
research programme for climate-ready
cereals funded by the Department of
Agriculture, Fisheries and Forestry under
Australias Farming Future: Climate Change
Research Program.
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6
Introduction
Climate change is expected to have a variety
of efects on global temperatures, sea levels
and the availability of water in agricultural
landscapes. According to the Intergovernmen
tal Panel on Climate Change (IPCC), since
1950 average global surface temperatures
have risen by ~0.7C and the sea level has
risen by ~10 cm. Tere has also been decreased
precipitation in the Sahel, the Mediterranean,
southern Africa and parts of southern Asia,
and an increased risk of heavy precipitation
events over most areas (IPCC, 2007).
Over the next century, average global
surface temperatures are expected to rise by
1.83.5C. As a consequence, the thermal
expansion of the oceans will lift sea levels by
up to 0.6 m, annual precipitation will increase
in high latitudes and decrease in most
subtropical land regions, and future tropical
storms will become more intense (IPCC,
2007). One of the large unknowns is the
extent to which the melting of the Greenland
and Antarctic ice sheets will impact on sea
level rise. Te 2007 IPCC report notes that
the expected future temperatures in
Greenland are comparable to those inferred
for the last interglacial period 125,000 years
ago, when palaeological data suggest that the
loss of polar land ice was associated with a
46 m rise in sea level (IPCC, 2007). Global
climate change is likely to invoke substantial
changes to the worlds agricultural regions
and the severity with which abiotic stress
will afect crop production.
Salinity is widespread, particularly in arid
regions (Ghassemi et al., 1995), and it can
coincide with the additional stresses of
waterlogging and periodic inundation
1
Breeding Crops for Tolerance to
Salinity, Waterlogging and
Inundation
Daniel J. Mullan and Edward G. Barrett-Lennard
Abstract
During the next century, global climate change is likely to cause substantial increases in the severity
with which salinity, waterlogging and inundation afect crop production in many of the worlds
agricultural regions. In this chapter we address the efects of climate change on these three
environmental stresses in terms of their threat to sustainable crop production. Te efects of salinity,
waterlogging and inundation on crop plants are examined, with a focus also directed towards the
exacerbating efects of the complex interactions between these stresses. We identify key plant
physiological traits as targets for breeding initiatives. Tree possible approaches to the development
of crops for saline, waterlogged and inundated soils are considered: (i) selection within crop species;
(ii) the development of hybrids between adapted wild species and crop plants; and (iii) the domestication
of halophytes. Finally, we detail some of the complex research, development and agricultural issues
that need to be addressed by a broad research and development community in order to increase crop
production during the foreseeable period of global climate change.
1
We prefer these separate terms to fooding, which is used ambiguously in the literature to refer to both
saturation of the soil (waterlogging), which affects roots (e.g. Barrett-Lennard, 2003; Colmer and Flowers,
2008), and the covering of shoots with water (inundation), which affects both shoots and roots (e.g.
Pedersen et al., 2006).
Breeding for Tolerance to Salinity, Waterlogging and Inundation 93
(BarrettLennard, 2003). In these cases the
combination of salinity, waterlogging and
inundation may be of natural origin, linked
with proximity to waterways, lakes and food
plains (primary salinity), or it may have an
anthropomorphic origin (secondary salin
ity). In the latter cases, the agricultural vege
tation uses less than the incident rainfall (or
irrigation water), excess water percolates
into the soil profle, the water table rises
towards the soil surface, and where the
groundwater comes to within ~2 m, salt rises
to the soil surface through capillarity
(Ghassemi et al., 1995). Te total area of
secondary salinity around the world has
been estimated at ~76.6 million ha (Table
6.1), though this is almost certainly an
underestimate, being based on data acces
sible in 1991.
Although it has been long recognized that
salinity can occur in landscapes associated
with a shallow water table (e.g. Wood, 1924),
understanding the implications that the
coincidence of salinity, waterlogging and
inundation have for plant growth is rela
tively recent. Initial studies in the area
focused on the need to obtain useful produc
tion on salinized irrigated land (see papers
by West and colleagues cited by Barrett
Lennard, 1986) and subsequent studies
focused more on the interaction between
salinity and moisture excess as a physio
logical curiosity (reviewed by Barrett
Lennard, 2003). More recent research has
examined the efects of the combined
constraints on the growth of saltland
pastures (reviewed by Bennett et al., 2009)
and the physiology of halophytic vegetation
(reviewed by Colmer and Flowers, 2008).
Climate change can be expected to have
varying efects (both negative and positive)
on the expression of salinity, waterlogging
and inundation in landscapes.
First, there will be increased irrigation
with hazardous water. Hydrological basins
are defned as being water stressed if they
either have a per capita water availability of
less than 1000 m
3
/year or they have a ratio
of withdrawals to longterm average annual
runof above 0.4. Using these criteria, water
stressed basins occur in northern Africa, the
Mediterranean region, the Middle East, the
Near East, southern Asia, northern China,
Australia, the USA, Mexico, northeast Brazil
and the southwest of South America. Tese
areas have a population of 1.42.1 billion
people (Bates et al., 2008). As areas at risk
become hotter and drier, good quality water
will increasingly be reserved for drinking
and urban use, and irrigators will turn to the
use of brackish water and water of high
sodium hazard. Irrigation with water of high
sodium hazard on fne textured soils leads to
soil sodicity (i.e. the decline of soil structure
associated with the substitution of Na
+
for
Ca
2+
in the soils cation exchange complex).
Under these conditions, there is a decreased
rate of infltration, a lack of salt leaching and
the development of saline/waterlogging
stresses (reviewed by Qureshi and Barrett
Lennard, 1998).
Secondly, there will be increased inunda
tion in valley foors and lowlying landscapes
associated with increased runof from
Table 6.1. Global extent of human-induced salinization (reproduced from Ghassemi et al., 1995, p. 19
with permission from University of New South Wales; data from Oldeman et al., 1991).
Continent
Level of salinization (million ha)
Light Moderate Strong Extreme Total
Africa 4.7 7.7 2.4 14.8
Asia 26.8 8.5 17.0 0.4 52.7
South America 1.8 0.3 2.1
North and Central
America
0.3 1.5 0.5 2.3
Europe 1.0 2.3 0.5 3.8
Australasia 0.5 0.4 0.9
Total 34.6 20.8 20.4 0.8 76.6
94 D.J. Mullan and E.G. Barrett-Lennard
tropical storms. Te IPCC rates the probabil
ity of a link between increased tropical storm
activity and global warming as more likely
than not. In the North Atlantic the 10year
running average number of named tropical
storms has increased from ~10/year (1930
1990) to ~15/year (19982007) (Pew Centre
on Global Climate Change, 2009). Te efects
of climate change are likely to be especially
severe for regions in South Asia. Te
frequency and severity of inundation are
expected to increase due to increased rain
fall and temperatures. Monsoon rainfall is
expected to increase in magnitude and raise
the frequency and severity of inundation in
the Ganges, Brahmaputra and Meghna
basins (Douglas, 2009). Furthermore, higher
tem pera tures will increase the melting of
Himalayan snowfelds and glacial ice, signif
cantly increasing the occurrence of inunda
tion through greater river fows and extreme
weather events (Jagtap and Nagle, 2007;
Douglas, 2009). Inundation in landscapes at
risk of salinity will cause substantial
increases in recharge to the groundwater, a
rise in the water table and increased expres
sion of salinity as the groundwater evap
orates at the soil surface. Te most acute
consequences of inundation can presently
be seen in Bangladesh, where nearly 85% of
the rainfall occurs during the monsoon
(JuneOctober). Highintensity foods occur
when any two of the three major rivers reach
peak fow conditions simultaneously, and
over half of the country has an elevation
within 10 m of average sea level (Ahmad and
Ahmed, 2003). In this landscape, the return
period of severe foods is every 7 years
(Ahmad and Ahmed, 2003), and during the
1998 food, about 70% of the countrys area
was inundated (compared to an average
value of 2025%; Bates et al., 2008). Soil
salinity in the feld is commonly measured
as the electrical conductivity of the satura
tion extract (EC
e
). Te coastal ricelands of
Bangladesh generally have a shallow water
table (~1.01.5 m below the soil surface) and
in the dry season soil salinity in the upper
15 cm of the soil profle varies from between
moderately (EC
e
= 48 dS/m) to highly saline
(EC
e
= 816 dS/m) (Mondal et al., 2001).
Tirdly, there will be adverse efects on
agricultural production and natural ecosys
tems in landscapes at low elevations above
sea level. Coastal areas exposed to the future
rising sea level will be subject to an increased
risk of inundation from high tides and storm
surges, and from increased subsoil seawater
intrusion. Such areas include the worlds
river deltas, especially the Asian mega deltas
of the GangesBrahmaputra in Bangladesh
and West Bengal (Bates et al., 2008). Nicholls
(1995) predicts that an increase of 1 m will
inundate over 17% of Bangladesh. Clearly,
sea level rise will have major implications for
the severity of salinity, waterlogging and
inundation, future land use and the develop
ment of more tolerant crops for the region.
However, not all the efects of climate
change on salinity, waterlogging and inun
dation will be negative. In semiarid envir
onments there may be decreases in dryland
salinity associated with a decline in depth to
water table. In the southwest of Australia,
dryland salinity is caused by the replace
ment of native vegetation with annual crops
and pastures; this has resulted in a general
rise in water table over the last 150 years,
and about 2.32 million ha have been
regarded as being at risk from dryland salin
ity (Sparks et al., 2006). However, since
2000 the region has experienced a decline
in winter rainfall of about 20% (Bureau of
Meteorology, 2009), which has caused an
increase in depth to water table, decreasing
the area at risk of salinity, particularly in
the northern (drier) areas of the wheatbelt
(George et al., 2008).
Tis chapter has three main sections.
First, we examine the efects that salinity,
waterlogging, inundation and their inter
actions have on crop plants and the traits
that plants need to withstand these efects.
Secondly, we consider three diferent
approaches for the selection of plants for
afected landscapes: (i) selection within crop
species; (ii) the development of hybrids
between adapted wild species and crop
plants; and (iii) the domestication of halo
phytes. Finally, we conclude with some
thoughts about priorities for future
research.
Breeding for Tolerance to Salinity, Waterlogging and Inundation 95
Stresses and the Key Plant
Physiological Adaptations
Salinity
Soil salinity afects plant growth and survival
because ions (mainly Na
+
and Cl
, but also
Ca
2+
, Mg
2+
and SO
4
2
; Richards, 1954)
increase in the soil solution to concentra
tions that adversely decrease the availability
of water to the plant (the osmotic efect).
Te accumulation of these ions in the plant
tissues also impairs plant metabolism and
growth (the toxic efect) (Greenway and
Munns, 1980). Te efects difer in their
timing: the osmotic efects are immediate,
but the ion toxicity efects take time (days or
weeks) to decrease growth (Munns, 2002).
Figure 6.1 shows typical vegetative growth
responses for three species: river saltbush
(Atriplex amnicola; a typical halophyte),
barley (a salt tolerant crop) and beans (a salt
sensitive crop). Most crop species would
have economic yields only at soil EC
e
values
less than 10 dS/m.
Te key physiological traits associated
with salt tolerance in crops centre around
factors that: (i) enable plants to withstand
the adverse water relations caused by salin
ity; (ii) decrease the movement of toxic ions
to the shoots; and (iii) complete the life cycle
in the least saline part of the growing season
(Greenway and Munns, 1980; Munns, 2002;
Colmer et al., 2005). In relatively saline soils,
the traits of importance are:
High Na
+
(and Cl
into cell
vacuoles where they have a lower chance
of interfering with the activities of the
enzymes involved in metabolism in the
cytosol and cellular organelles.
Ability to adjust osmotically: this refers to
the accumulation of solutes in cells to
maintain cell turgor, and is achieved
through the compartmentation of ions
(particularly Na
+
and Cl
) into vacuoles,
and the synthesis of organic solutes (e.g.
glycinebetaine and proline) that are
compatible with enzyme function, which
are located in the cytosol.
Enhanced ability to accumulate Na
+
and Cl
in older rather than younger leaves.
Enhanced vigour, and early fowering and
grain flling: this refers to the ability of
the plant to grow rapidly when condi
tions are cool and soil water is more avail
able, and the ability of the plant to
complete its life cycle before the salinity
of the soil solution increases at the end of
the growing season.
In addition to these traits, it is also neces
sary for seeds to remain viable and germin
ate in saline soils, and although genotypic
variation exists in the tolerance of seeds to
salinity (Ungar, 1978; Nichols et al., 2009),
the physiological traits associated with this
capacity are not known.
Some of the above traits are relatively
easy to assess. For example, Na
+
and Cl
exclusion and the discrimination between
K
+
and Na
+
can be assessed by measuring the
concentrations of ions in specifc tissues
such as the youngest fully expanded leaf (as
recommended by Greenway and Munns,
1980). However, other traits can be harder
to assess. Tese include the ability to adjust
osmotically (which requires accurate meas
urements of the change in relative growth
rate in the immediate few days after salinity
is applied) and the ability of plants to toler
ate ions in the leaves (which requires meas
urements of the degree of leaf senescence
specifcally caused by salinity). Te use of
nondestructive imaging systems to assess
plant growth over short time frames, and to
separate natural from saltinduced senes
cence in leaves may lead to greater progress
in the latter two areas (cf. Rajendran et al.,
2009).
Given the wide range of physiological
traits associated with tolerance to salinity, it
is not surprising that reviewers have
suggested that this tolerance requires the
involvement of a number (unknown) of
genes (Flowers and Yeo, 1995), and attempts
to improve the salt tolerance of crop plants
have only occasionally been efective (Colmer
et al., 2005; discussed further in the Breeding
for Tolerance section).
Waterlogging
Waterlogging refers to saturation of soils by
water. Tis leads to the displacement of air
from the soil pores and an approximate
10,000fold decrease in the rate at which O
2
difuses into the soil (Grable, 1966). As a
result, soils typically become hypoxic (O
2
defcient) within a few days. Although soil
hypoxia has a range of moderate to long
term impacts on the chemistry and biology
of soils, the efects on plant roots are quite
rapid (see reviews by Ponnamperuma, 1972;
Drew and Lynch, 1980). Plants require O
2
to
provide the energy for root growth and func
tion; with O
2
available, plants are able to
produce 2436 moles of the energy storage
compound adenosine triphosphate (ATP)
per mole of glucose; without O
2
, plants are
only able to produce 2 moles of ATP per mole
of glucose through alcoholic fermentation.
Rootzone hypoxia has a variety of efects
on plant roots. Decreases in the elongation
of roots and the death of nonadapted apices
are observable within a few hours to a day
(Tomson et al., 1990), and this can lead to
substantial decreases in total root relative to
shoot biomass within 1 week. For example,
exposure of barley seedlings to 6 days of
hypoxia (O
2
concentrations ~10% of satur
ated) decreased the root:shoot ratio from
~0.37 (well aerated) to 0.23 (hypoxic) (calcu
lated from data of Benjamin and Greenway,
1979). Hypoxia can decrease the uptake of
nutrients by crop plants (Trought and Drew,
Breeding for Tolerance to Salinity, Waterlogging and Inundation 97
1980; Buwalda et al., 1988) and, therefore,
transient waterlogging can decrease yields if
crops are not subsequently refertilized
(Robertson et al., 2009).
In addition to these efects, in water
logged saline land, rootzone hypoxia can
lead to increased Na
+
and/or Cl
uptake to
the shoots, which decreases plant growth
and survival (reviewed by BarrettLennard,
1986, 2003). In a wideranging review of the
literature, hypoxia under saline conditions
caused at least 30% increases in either Na
+
or Cl
NO
2
NO
N
2
O
N
2
Any management practice that creates
anaerobic conditions including fooding,
especially in heavy textured soils, when
nitrate is present will lead to increased N
2
O
emissions (Ball et al., 1999). Tese emissions
can be reduced by aerating the soil, espe-
cially in coarse textured soils, as evidenced
by reduced emissions in permanent raised-
bed planted crops (Patio-Ziga et al.,
2009).
Te other N cycle process that generates
N
2
O is nitrifcation. Tis occurs under
aerobic conditions with the oxidation of
ammonia to NO
2
and fnally NO
3
. If this
soil is then fooded, denitrifcation can occur.
N
2
O is also released from soils to the atmos-
phere during
nitrifcation of ammonium and
ammonium-producing fertilizers
under
aerobic conditions. Tis can be signifcant
during fertilizer applications. Such emis-
sions can be greatly
reduced through the use
Conservation Agriculture Buffering Climate Change 191
of nitrapyrin, which inhibits nitrifcation
of
ammonium by soil microorganisms.
Tese two N-cycle processes are mainly
infuenced by factors such as soil tempera-
ture, soil moisture content, pH, supply of C
and N compounds (Skiba et al., 1998; Lee et
al., 2006) and soil electrical conductivity
(Adviento-Borbe et al., 2006). Tese factors
can be manipulated by tillage (Venterea et
al., 2005), residue management, irrigation
(Qian et al., 1997) and the application of N
fertilizer (Smith et al., 1997). Increased soil
organic matter can also result in increased
N
2
O emission through the increase in N
cycling in the soil as nitrifcation is stimu-
lated (Butterbach-Bahl et al., 2004). However,
zero tillage combined with residue retention
results in a better soil structure, facilitating
O
2
difusion and reducing the amount of
anaerobic sites in the soil, and stimulating
oxidation of CH
4
, but it remains to be seen
how emissions of NO and N
2
O are really
afected.
GHG emissions were studied in water-
saving experiments with rice in China
(Dittert et al., 2002). Te results showed a
signifcant drop in CH
4
emissions with a
more aerobic rice production system
compared to a fooded rice system, but N
2
O
emissions increased, especially after N fertil-
izer application. Te researchers concluded
that N fertilizer applications needed to be
optimized to minimize N
2
O emissions, espe-
cially since this gas has a much greater heat-
ing potential than CH
4
or CO
2
. Patio-Ziga
et al. (2009) observed in a laboratory incuba-
tion experiment that the N
2
O emission from
conventional tillage with residue retention
was 2.3 times larger compared to no tillage
with residue retention. Jacinthe and Dick
(1997) observed that the seasonal N
2
O emis-
sion from zero tillage was signifcantly lower
than from conventional tillage (chisel till-
age) under continuous maize, maize
soybean rotation and maizesoybean/
wheathairy vetch rotation in Ohio, USA.
Kessavalou et al. (1998) demonstrated that
the application of tillage during fallow
increased the N
2
O fux by almost 100% rela-
tive to the no-tillage treatment. Robertson
et al. (2000) reported that N
2
O emissions
from zero tillage were similar to or slightly
higher than from conventional tillage under
maizewheatsoybean rotations in the
Midwest USA. Rochette et al. (2008) demon-
strated in a 3-year study in East Canada that
the average N
2
O emissions from zero tillage
were more than double those from conven-
tional tillage in a heavy clay soil. In a loam
soil, the average emissions during the 3 years
were similar in the two treatments. Rochette
(2008) concluded that N
2
O emissions only
increased in poorly drained, fnely textured
agricultural soils under zero tillage located
in regions with a humid climate, but not in
well-drained aerated soils. Six et al. (2004)
compiled all available data of soil-derived
GHG emission comparisons between
conventional tilled and no-tillage systems
for humid and dry temperate climates. Tey
concluded that in both humid and dry
climates, diferences in N
2
O emissions
between the two tillage systems changed
over time. In the frst 10 years, N
2
O fuxes
were higher in zero tillage compared to
conventional tillage, regardless of climate.
After 20 years, however, N
2
O emissions in
humid climates were lower in zero tillage
than conventional tillage and were similar
between tillage systems in the dry climate.
Te key for the implementation of CA as
a GHG mitigation strategy is the under-
standing of the integrated efect of the prac-
tice on all GHGs and developing the
necessary component technologies and
fertilization practices to reduce the emis-
sions of N
2
O, since any gains in reduction of
CO
2
and CH
4
emissions could be lost if these
practices resulted in increased N
2
O emis-
sions. Part of the conficting results with
zero-tillage and CA practices is related to
development of the optimal implementation
of the system. Years of research and develop-
ment have been spent to optimize conven-
tional tillage systems but a knowledge base
for CA on all production-related components
in diferent locations has yet to be devel-
oped. For example land levelling is a compo-
nent technology that drastically increases
the efciency of zero tillage and CA in food
irrigated systems. In this case farmers level
their felds using equipment on their farms.
However, the use of laser land levelling
results in an even better feld level.
192 P.R. Hobbs and B. Govaerts
Well-levelled felds give much better results
with CA whether they are planted on the fat
or on beds; in particular, water productivity
can be signifcantly improved.
Accelerating the adoption of conservation
agriculture
CA adoption statistics are hard to quantify,
since statistics are not collected on this
specifc management practice. Instead, the
acreage of zero tillage is used as a proxy for
CA. Tis tends to overestimate the area since
many farmers do not adopt all three prin-
ciples of CA. For example farmers in South
Asia will adopt zero tillage for wheat planted
after rice, but the rice crop is still planted
with full tillage and puddling of soils (Hobbs
et al., 2005). In dryland areas with low
biomass yields and competing uses for crop
residues, farmers may not be able to spare
needed amounts of residues for optimal CA
management. Te latest statistics on adop-
tion of zero tillage worldwide is 105 million
ha (Derpsch and Friedrich, 2009). Although
this is only 7.5% of the 1.4 billion ha of total
arable land (FAO, 2003) it does provide
benefts in terms of reducing GHG emissions
and does provide the potential for mitigat-
ing global climate change if adoption is
increased.
Tere are several factors that need to be
addressed to accelerate the adoption of CA.
Probably the most important factor in adop-
tion of CA is overcoming the bias or mindset
about tillage. Changing the mindset of farm-
ers from a system that has promoted tillage
for centuries to one where tillage is reduced
or even avoided is a major obstacle to adop-
tion. Tere are many examples of where
farmers were ridiculed by their neighbours
when they frst tried this technology. In
some cases, farmers actually ploughed up
their felds rather than be subjected to this
criticism. But once the crop emerged and the
farmer and his or her neighbours could see
that tillage was not necessary for a good
plant stand they gained confdence and in
fact became the best extension agents for
this technology. Te next step after identify-
ing a willing farmer was to expose other
farmers to the performance of CA in the
feld. Tis was done by word-of-mouth from
farmer to farmer but also by visits of farm-
ers from other villages and discussion with
the innovative farmer and what he or she
had done. Once farmers were convinced that
they could grow a successful crop without
tillage they began to think of the many other
benefts that CA would give them.
Another critical factor for adoption of CA
is the availability of suitable equipment to
enable farmers to successfully plant their
crops without tillage. Tis is a factor for any
new technology; the adoption of conserva-
tion tillage following the dust bowl of the
1930s was dependent on the development
of seed drills that could plant into soil with
minimum tillage and with loose residue on
the surface. Tis led to the development of
disk-based seed drills that could cut the resi-
due and place the seed in the soil at the
correct depth for good germination. Today
there is a whole array of diferent equipment
for planting into minimally disturbed soil.
Tese drills also place fertilizer in the soil at
the time of planting which improves the ef-
ciency of nutrient application. Tis equip-
ment is efcient at planting seed and getting
good plant stands; however, these expensive
and power-thirsty zero-tillage drills are not
well adapted to some developing countries
with smaller powered tractors and in some
cases no tractors at all. In these cases,
researchers and engineers have developed
equipment that is lower in cost, lighter and
can be powered by smaller tractors. Tere is
also manual and animal-powered equipment
that can be used to plant seed into any zero-
tillage feld. Once the equipment is made
available to farmers for experimentation,
they see for themselves the benefts of
reduced costs and time, improved produc-
tion and improved soil health. However, it is
clear that in order to spread the CA technol-
ogy a dynamic of innovation of equipment
has to be catalysed with close interaction
between farmer, technician, machine build-
ers, local private enterprises, craftsman,
scientists, engineers, etc.
CA can be scale neutral. Te key is to fnd
mechanisms that allow even resource-poor
farmers to practise and experiment with this
Conservation Agriculture Buffering Climate Change 193
technology, making sure they have access to
the equipment and also the knowledge about
the benefts. In some cases in developing
countries farmers do not own tractors.
Gaining access to equipment, however, can
be found through service providers. A farmer
who owns a tractor and has purchased CA
equipment provides a service to his poorer
neighbour on rent. Te resource-poor farmer
can beneft from the technology by getting
his or her felds planted on time and with
the minimal amount of time, leaving the
farmer to fnd other productive employ-
ment. In this way he or she gets better yields
at less cost and time, leading to better
returns from agriculture. If training is
imparted to the service provider then the
quality of planting is also maintained. Te
service provider can also be linked to local
manufacturers so that the farmer can get a
good supply of spare parts but also provide
feedback to the manufacturer about ways to
improve the efciency of the equipment. In
fact, farmers who did not own tractors were
able to plough their felds by the same rental
service system prior to the introduction of
zero tillage.
Te old linear top-down approach to
extension is not very efcient in the case of
CA. Farmers have to see for themselves and
overcome their apprehensions before they
are willing to adopt this new technology. In
this case it is important that equipment is
made available to farmers, that they are
trained in its proper use and that the equip-
ment is left with the farmers to experiment
on their own farm. If scientists or extension
agents only conduct demonstrations in farm-
ers felds and then take the equipment back
to their experiment stations, adoption rates
are much lower. An example of this can be
found in India where in the state of Haryana,
farmers were given the seed drills and
sufcient training and left to experiment.
Adoption rates were very rapid (Malik et al.,
2002). In Punjab and Uttar Pradesh states in
India, researchers and extension agents used
the equipment for demonstrations and then
carried the equipment back to their stations.
In this case adoption was very slow.
A network of stakeholders has to be
developed in order to address various issues
that arise during adoption. Researchers and
extension agents need to interact with farm-
ers to address issues and problems that arise
during the initial phases of CA adoption.
Local manufacturers need to be actively
involved with farmers to identify improve-
ments to machinery that lead to better
performance. Banks and credit agencies are
needed to provide funds for farmers to buy
equipment. Input agencies are needed to
supply fertilizers and other inputs needed
for good yields. Tese can be coordinated
through public institutions or through
publicprivate collaborations. However, it is
clear that rather than a linear line of adop-
tion an inter-actor innovation process has to
be promoted. Terefore, a network of decen-
tralized learning hubs within diferent farm-
ing systems and agroecological zones should
be developed (Sayre and Govaerts, 2009). In
those hubs, an intense contact and exchange
of information is organized between the
diferent partners in the research and exten-
sion process. Multiple actors within the
production system (farmers, scientists,
machine builders, decision makers, input
suppliers, etc.) come together in the hubs,
work together and learn together in order to
multiply this efort in an intense extension
and out-scaling process. Because of the
multifaceted nature of CA technology devel-
opment and extension, activities should be
concentrated in a few defned locations
representative of certain farming systems
rather than having lower intensity eforts on
a wide scale. Trough the research and train-
ing, regional CA networks are established to
facilitate and foment research and the exten-
sion of innovation systems and technolo-
gies. Research at the hubs also provides an
example of the functionality of CA systems,
helping to break down the culture of the
plough. Te hubs are linked to the strategic
science platforms operated by international
centres and national research institutes to
synthesize a global understanding of CA and
its adaptability to diferent environments,
cropping systems and farmers circum-
stances. Innovative farmers are intensively
involved and are the key factor for the build-
up and extension of a successful CA network
that leads to a sustainable impact.
194 P.R. Hobbs and B. Govaerts
Conclusions
Global climate change caused by anthropo-
genic GHG emissions is already afecting
weather patterns including temperatures
and rainfall. CA that consists of minimal soil
disturbance, permanent ground cover and
crop rotations is a management system that
can alleviate some of the efects of climate
change. CA results in healthier soils, both
physically and biologically, and this in turn
improves nutrient cycling and crop growth.
Water infltration and soil penetration by
roots is increased allowing crops to better
adapt to lower rainfall and make better use
of irrigation water. Water and wind erosion
is also reduced by CA since the soil surface is
protected from erosion and water runof is
lowered as more water enters the soil profle.
CA creates soils and production systems
more resilient to climate variation and risk.
Agricultural production is one contributor
to GHG emissions including CO
2
, CH
4
and
N
2
O, the three main gases infuencing global
warming. In fact, agriculture is a major
contributor to CH
4
and N
2
O emissions, two
gases with greater warming potential than
CO
2
, although emitted at lower concentra-
tions. CA can mitigate these GHG emissions.
CH
4
is a by-product of rice cultivation under
fooded conditions. Growing rice with less
water and adopting CA practices can reduce
CH
4
emissions. However, care has to be
taken with fertilizer management to mini-
mize N
2
O emissions that can increase under
the resulting aerobic conditions. CA can also
substantially reduce CO
2
emissions through
reduced diesel use and potentially increase
the sequestration of C in the soil. Terefore,
CA not only helps crops adjust to changes in
climate but also helps reduce GHG emis-
sions. At present just over 105 million ha of
land worldwide uses zero tillage in agricul-
ture. Not all of it is CA but it still impacts
positively in the global climate change
scenario. In order for this acreage to increase
attempts are needed to expand adoption
through better extension systems, farmer
knowledge and making suitable equipment
available to farmers. Much more integrated
research and development is needed to
develop the fundamental knowledge base
for CA as well as to fne tune CA to specifc
locations and identify suitable germplasm,
fertility management, weed control and
control of other biotic factors to move this
technology onwards. Because of the multi-
faceted nature of CA technology develop-
ment and extension, activities should be
concentrated in a few defned locations
representative of specifc farming systems
rather than having lower intensity eforts on
a wide scale. Scaling up can then occur from
these hubs or focal points by using the farm-
ers and felds as demonstrations to other
farmers in surrounding areas.
Acknowledgements
Te authors wish to thank Nele Verhulst and
Adrian Carrillo Garcia for their valuable help
with this chapter.
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200 CAB International 2010. Climate Change and Crop Production (ed. M.P. Reynolds)
11
Introduction
Soilborne diseases present signifcant
constraints to continued utilization of arable
land in both intensive and low-input agricul-
tural production systems. Diseases incited
by fungi and bacteria were reported to
account for yield losses ranging on average
from 7 to 15% during the period 20012003
for the major world crops (Oerke, 2005).
Among the 2000 major plant diseases afect-
ing the principle crops produced in the USA,
approximately 90% are caused by soilborne
pathogens (Lewis and Papavizas, 1991).
Economic losses due to plant parasitic nema-
todes have been estimated at US$100 billion/
year worldwide (Bird and Kaloshian, 2003),
while in the USA soilborne diseases are esti-
mated to produce crop losses that exceed
US$4 billion/year (Lumsden et al., 1995).
Relative to those employed against diseases
afecting aerial surfaces of plants (see
Legrve and Duveiller, Chapter 4, this
volume), methods for the management of
soilborne diseases tend to yield less compre-
hensive disease control and there are few
efective disease control options applicable
in a post-plant or perennial crop production
setting. Certain practices currently employed
for the control of soilborne diseases can
confer signifcant impact on society and the
environment that far exceeds the direct
Management of Resident Soil
Microbial Community Structure
and Function to Suppress
Soilborne Disease Development
Mark Mazzola
Abstract
Climate change is likely to alter the distribution and severity of soilborne diseases afecting both
intensive and low-input agricultural production systems. Naturally occurring disease suppressive soils
have been documented in a variety of cropping systems, and in many instances the biological attributes
contributing to suppressiveness have been identifed. While these studies have often yielded an
understanding of operative mechanisms leading to the suppressive state, signifcant difculty has
been realized in the transfer of this knowledge into the development of efective feld-level disease
control practices. Early eforts focused on the inundative application of individual or mixtures of
microbial strains recovered from these systems, and known to function in specifc soil suppressiveness.
However, the introduction of biological agents into non-native soil ecosystems typically fails to yield
commercially viable or consistent levels of disease control. Of late, greater emphasis has been placed
on manipulation of the cropping system to manage resident benefcial rhizosphere microorganisms as
a means to suppress soilborne plant pathogens. One such strategy is the cropping of specifc plant
species or genotypes, or the application of soil amendments with the goal of selectively enhancing
disease suppressive microbial communities. Tis chapter will briefy review the existence of biologically
functional disease suppressive soils, document the research history supporting the potential in
managing microbial communities for disease control, describe methods available for the efective
manipulation of bioactive populations, and describe specifc examples demonstrating the efective
application of the approach.
Soil Microbial Community Management 201
costs to the grower and consumers. For
example, in the case of soil fumigation,
although efective disease control may be
achieved, such a practice results in major
ecological disturbances to the production
system as a whole. In the instance of certain
chemicals such as methyl bromide, a fumi-
gant once widely used for the control of soil-
borne plant pathogens, disease control
activities not only directly impact the treated
biological system but can also adversely
impact air quality and may contribute
broadly to environmental degradation.
Disease management strategies that are
considered to impart a more ecologically
sustainable footprint, such as host resist-
ance or the application of microbial
biological control agents, are generally efec-
tive towards a more limited and targeted
pathogen population than chemical control
alternatives (Table 11.1). With few excep-
tions, biological controls have not attained
the level of performance in terms of both
efcacy and consistency required to achieve
widespread adoption for use in commercial
feld-level agricultural production systems.
Host resistance is a proven and efective
strategy for the management of numerous
economically important foliar plant diseases
such as those incited by biotrophic rust fungi
(McIntosh et al., 1995). Fewer examples
exist for soilborne pathogens or parasites,
however efective host resistance has been
obtained for the control of particular agents
such as the ubiquitous and specialized
fungus Fusarium oxysporum (El Mohtar et al.,
2007; Herman and Perl-Treves, 2007).
Likewise, a multitude of resistance sources
in cereals to the cereal cyst nematode have
been documented with resistance conferred
by a single host gene (Nicol and Rivoal,
2008). Climate change will be likely to have
signifcant impacts on both of these disease
control options, which may further limit
their potential for the management of soil-
borne plant diseases. A dominant impedi-
ment to the broad-scale efective use of
microbial biological control agents is their
failure to persist at required threshold popu-
lations in non-native or environmentally
extreme environments. Tus, several micro-
bial groups currently viewed as an efective
source of biological control agents (e.g.
Pseudomonas spp.) may exhibit impaired
performance under the predicted climate
change models. Likewise, temperature and
drought stress associated with climate
change has the potential to modulate the
efectiveness of host gene resistance, and
not necessarily in a predictable fashion
(Garrett et al., 2006).
As climate is undergoing a period of rapid
change, the underlying functional biology
indigenous to any ecosystem will itself
undergo transformations allowing for adap-
tation of the resident biology to the altered
environment (Jarvis et al., Chapter 2; Legrve
and Duveiller, Chapter 4, this volume). In
Table 11.1. Successful non-chemical approaches for control of soilborne diseases.
Method References
Host resistance Fazio et al. (2006), El Mohtar et al. (2007), Herman and
Perl-Treves (2007), Nicol and Rivoal (2008)
Soil solarization Katan (1987)
Crop rotation Larkin and Honeycutt (2006), Subbarao et al. (2007), Kirkegaard
et al. (2008)
Tillage Cook et al. (1990), Roget et al. (1996)
Biological control Kerr (1980), Fravel (2005)
Disease suppressive soils (native) Stotzky and Martin (1963), Rouxel et al. (1979)
Disease suppressive soils induced
via:
Plant residue amendments Cohen et al. (2005), Wiggins and Kinkel (2005a)
Tillage Peters et al. (2003)
Cropping sequence Shipton et al. (1973)
Specifc plant genotype Larkin et al. (1993), Mazzola and Gu (2002), Mazzola et al.
(2004)
202 M. Mazzola
some instances this will yield changes in
distribution or incidence of specifc plant
pests, with parasites of previously restricted
distribution perhaps becoming more cosmo-
politan. Nevertheless, within the context of
this biological community many elements
exist that function to enhance plant growth,
development and survival. Tese include
such entities as natural enemies, many of
which have been efectively utilized in pest
management systems for the biological
control of plant parasitic insects. Te utiliza-
tion of natural enemies often relies upon the
inundative release of one or a few native or
non-native predators or parasitoids, a model
commonly employed in the application of
microbial biological control (Myers et al.,
1989). Within the entomological discipline,
an alternative model has been utilized at
times to promote native biological control.
Such a strategy relies upon the establishment
of systems designed to enhance the abun-
dance and diversity of naturally occurring
insect predators, ranging from insectivorous
birds to the more commonly considered
insect predators. Such systems may involve
the establishment of mixed cropping systems,
internal or external refugia which provide
habitats for benefcial organisms to enable
pesticide avoidance, an alternative food
source or appropriate habitat needs external
to the crop production season (Bianchi et al.,
2006).
Within the context of soilborne plant
disease management, attempts to employ
microbial biological control have typically
involved the inundative release of non-
native microorganisms into soil systems.
Such an approach assumes that the intro-
duced microbial agent or mixture will efec-
tively compete with the resident microbial
community, efciently colonize the rhizo-
sphere of the targeted plant and persist in
the rhizosphere at the threshold population
required for activity during the period of
plant susceptibility, and also that the active
mechanism is operative in the environment
into which it has been applied. Soil dwelling
microbial antagonists of plant pests and
pathogens have been studied extensively as
to their role in the development of soil
suppressiveness (Weller et al., 2002). Tese
same entities have served as a primary
source of microorganisms that have subse-
quently been evaluated for their capacity to
function as agents for the biological control
of soilborne plant diseases. Despite the
extensive study of these microbial biocon-
trol agents, there continue to exist extensive
gaps in our knowledge of the factors that
infuence microbial survival and the
attributes of the system that will modulate
expression of mechanisms directly contrib-
uting to disease suppression. As such, in
general, attempts to utilize biological control
for the suppression of soilborne plant
diseases in commercial feld-level produc-
tion systems have failed to yield the predicted
disease control potential of these microbial
resources. Perhaps this outcome should have
been expected as the persistence and activ-
ity of any organism in an alien environment,
while in competition with the myriad of
organisms adapted to that same soil, is
rather improbable. In addition, the func-
tional biotic milieu responsible for disease
suppression may involve a complexity of
interactions well beyond a single microbe or
microbial mixture, and may not necessarily
function outside its native abiotic matrix.
Suppressive Soils
A signifcant body of research has focused on
the description and function of soils possess-
ing the capacity to suppress soilborne plant
diseases. Disease suppressive soils have been
defned as those in which disease develop-
ment is minimal even in the presence of a
virulent pathogen and a susceptible host.
Te concept of disease suppressive soil has
been described in terms of both general
suppression and specifc suppression. Every
natural soil possesses some ability to suppress
the activity of plant pathogens due to the
presence and activity of its complement of
resident soil microorganisms (Cook and
Baker, 1983). Tis can readily be observed
when one compares disease progression and
severity after artifcial introduction of a plant
pathogen into a natural soil relative to that
achieved in the same soil that has been
pasteurized prior to pathogen introduction.
Soil Microbial Community Management 203
Te phenomenon is termed general suppres-
sion and is thought to be directly related to
the total amount of microbial activity in a
given soil rather than operating through the
action of a specifc microorganism or specifc
group of microorganisms.
While general suppression is a compo-
nent of disease suppressive soils, manipula-
tion or exploitation of the biological
components contributing to the phenom-
enon termed specifc suppression has
perhaps more commonly been the desire of
researchers and crop producers when formu-
lating a disease management strategy.
Certain disease suppressive soils are natur-
ally occurring and suppressiveness is attrib-
uted in part to physical or chemical attributes
of the soil (Stotzky and Martin, 1963; Stutz
et al., 1989), or may be modulated by such
properties (Amir and Alabouvette, 1993). In
other systems it is accepted that suppres-
siveness is fundamentally a function of
microbiological activity resident to a given
soil. Te microbial contribution to disease
suppression is confrmed by demonstrating
that the disease suppressive factor can be
transferred to a conducive soil through the
introduction of very small amounts of the
suppressive soil. Likewise, the observation
that the suppressive factor could be elimi-
nated through soil pasteurization afrmed
the role of soil microorganisms in disease
suppression. Te attributes of biologically
mediated disease suppression are diverse
and the specifc qualities or components of
the functional biology difer widely with the
disease of interest. For example, elevated
bacterial population diversity has been asso-
ciated with a higher degree of soil suppres-
siveness towards the fungal pathogen
Fusarium graminearum, and selective attenu-
ation of this diversity resulted in a reduction
in soil fungistasis (Wu et al., 2008). However,
in many instances specifc disease suppres-
sion is attributed to the activity of an indi-
vidual or select group of microorganisms
that are antagonistic towards the target
pathogen (Weller et al., 2002). Tose
instances in which soils derive disease
suppressive potential through a biologically
mediated process will be the focus of this
discussion.
Functional Biology of Disease
Suppressive Soils
Disease suppressive soils have been identi-
fed for a number of plant pathogens, with a
few of the more prominent examples includ-
ing those soils suppressive to Fusarium wilt
(Rouxel et al., 1979; Scher and Baker, 1980),
potato scab (Menzies, 1959), cyst nematode
(Westphal and Becker, 1999), Rhizoctonia
root rot (Henis et al., 1979; Barnett et al.,
2006; Garbeva et al., 2006), Pythium root
rot (Adiobo et al., 2007) and take-all of wheat
(Cook and Rovira, 1976). Harnessing the
potential of these soils as a practical means
to manage diseases in agroecosystems has
long been a goal; however, there have been
limited attempts to actively manage these
resources in the context of an overall plant
production system.
Clearly, the efective implementation of
strategies to manage resident soil microbial
communities for the suppression of soilborne
plant pathogens requires the capacity to
initially identify the biological components
involved in disease suppression. As noted
above, the biotic factors that contribute to
specifc soil suppressiveness have been eluci-
dated for a number of plant-pathogen systems
(Weller et al., 2002). In certain systems, the
capacity of a soil to limit disease is elevated
over time in response to the application of
specifc plant management systems. One of
the more notable examples has been docu-
mented in soils that are suppressive to the
disease take-all of wheat which is incited by
the fungal pathogen Gaeumannomyces
graminis var. tritici. In systems where wheat is
grown under continuous monoculture,
disease incidence commonly increases during
the initial few years of production but at some
point thereafter a spontaneous decline in
disease severity is realized, termed take-all
decline, and the soil remains suppressive to
the disease as long as wheat monoculture is
not interrupted (Gerlagh, 1968; Shipton et
al., 1973). Take-all decline has been observed
across geographic regions, and in multiple
instances 2,4-diacetylphloroglucinol (2,4-
DAPG)-producing fuorescent pseudomonads
have been shown to play a prominent role in
the development of take-all suppressive soils
204 M. Mazzola
(Weller et al., 2002; de Souza et al., 2003).
Fusarium wilt suppressive soils may also
develop in response to crop cultivation
(Larkin et al., 1993), and non-pathogenic
Fusarium spp. have repeatedly been impli-
cated as a factor functioning in disease
suppression (Alabouvette et al., 1996), at
times in concert with resident siderophore or
phenazine-producing fuorescent Pseudo
monas spp. (Duijf et al., 1999; Mazurier et al.,
2009). Te commonality of functional biol-
ogy and inducing agronomic practices leading
to specifc suppression of a disease across
geographic regions supports the premise that
managing these phenomena is a credible
strategy to pursue for soilborne disease
management.
Management of Biologically Mediated
Soil Suppressiveness
Various attributes of a cropping system
including plant species (Garbeva et al.,
2006), input system (organic versus conven-
tional) (Workneh et al., 1993; van Bruggen,
1995; Liu et al., 2007), tillage (Peters et al.,
2003) and fertilization (Smiley, 1978),
among others, will infuence ecological
processes that determine microbial commu-
nity structure and function, including its
capacity to induce suppression of soilborne
plant pathogens. Tese observations imply
that, given knowledge of the operative
biological mechanisms, there exists the abil-
ity to enhance or diminish the suppressive
nature of a resident microbial community
through timely application of the appropri-
ate agronomic practices (Workneh and van
Bruggen, 1994; Hoeper and Alabouvette,
1996; Pankhurst et al., 2002). As the induc-
tion of soil suppressiveness is often medi-
ated through transformations in soil
microbial communities over time (Liu and
Baker, 1980; Larkin et al., 1993; Raaijmakers
et al., 1997; Mazzola and Gu, 2002; Weller et
al., 2002), there may be a signifcant oppor-
tunity to manage the phenomenon, and
perhaps accelerate the onset of the disease-
suppressive state, a notable prerequisite to
the economic viability and adoption of such
a disease control strategy.
In the management of soil suppressive-
ness, it may be argued that enhancement of
overall general suppression would be the
easier course to pursue as this can be achieved
simply through elevation of general micro-
bial activity in a soil. In certain instances
such a tactic may be a viable means to achieve
disease suppression. However, as is true for
all but the most drastic control methods (e.g.
soil fumigation), it is unlikely to be a univer-
sal solution to the management of soilborne
diseases. For example, the general suppres-
sion phenomenon is reported to function in
certain soils suppressive to Pythium root rot
(Adiobo et al., 2007). In addition, control of
diseases incited by Pythium spp. in response
to addition of organic residues to soils is
often attributed to and dependent upon an
overall elevation in general soil microbial
activity (Hoitink and Boehm, 1999). While
the level of disease control attained will be
dependent upon substrate composition and
state at the time of soil incorporation
(Mandelbaum and Hadar, 1990), pursuing
this strategy for control of diseases incited
by Pythium would appear to possess signif-
cant potential. In contrast, suppression of
other soilborne diseases, such as Rhizoctonia
root rot (Henis et al., 1979; Mazzola and Gu,
2002), may function through specifc
suppression and rely upon the activity of a
defned subset of the total soil microbial
community. Substrate-induced generation of
soil suppressiveness to Rhizoctonia root rot
was dependent upon specifc microorganisms
or communities resident in the organic
substrate (Kuter et al., 1983; Kwok et al.,
1987) or the capacity of the amendment to
selectively amplify the functional popula-
tions resident to the soil (Cohen et al., 2005;
Wiggins and Kinkel, 2005a). Tus, in patho-
systems where specifc suppression is the
primary determinant of disease control, even
where overall enhancement of microbial
activity realized in response to a manage-
ment practice, in the absence of the specifc
functional microbial population disease
control may not be realized (Aryantha et al.,
2000; Cohen et al., 2005).
Eforts to direct development of specifc
soil suppressiveness as a management tool
requires knowledge of the biological
Soil Microbial Community Management 205
consortia conferring disease suppression as
well as an understanding of how any partic-
ular strategy will infuence the activity of the
functional population. Many biologically
based alternative practices have failed to
live up to their potential owing to an inabil-
ity to identify the functional population(s)
leading to pest suppression. When such
information is available, functional groups
can be monitored enabling the prediction of
pest control efcacy. For instance, the
natural development of soils suppressive
towards take-all of wheat in response to
wheat monoculture was shown to be depend-
ent upon native 2,4-DAPG-producing fuor-
escent pseudomonads attaining a threshold
population of 10
5
colony forming units
(cfu)/g root or greater in order to achieve
efective disease control (Raaijmakers and
Weller, 1998; de Souza et al., 2003). Tis
functional population can now serve as a
biological indicator to predict the efcacy of
practices (e.g. continuous wheat monocul-
ture) that lead to take-all suppressive soils.
Within the scope of a functional micro-
bial population exists an extraordinary level
of complexity that may not be apparent nor
routinely considered in the application of
such a disease management strategy.
For instance, populations of 2,4-DAPG-
producing fuorescent pseudomonads are
genetically diverse and difer in capacity to
suppress take-all of wheat (Raaijmakers and
Weller, 2001). Wheat cultivars also difer in
both relative density and genetic compos-
ition of the 2,4-DAPG population selected
from indigenous soil populations of these
bacteria (Mazzola et al., 2004). Te capacity
of the plant host to seize the beneft from a
particular functional group, and diversity in
susceptibility of the universal pathogen
population to the mode(s) of action contrib-
uting to disease suppression will also infu-
ence disease development. For instance, a
particular plant growth promoting rhizo-
bacteria that elicits defence responses in one
plant species (Tran et al., 2007) may yield no
such response in a diferent plant species
(Mazzola et al., 2007b). Although cyclic
lipopeptide-producing rhizobacteria func-
tion to provide control of diseases incited by
certain Pythium spp. through the zoosporo-
cidal activity of these metabolites (de Souza
et al., 2003), this mechanism obviously will
not contribute to suppression of diseases
incited by Pythium spp. for which zoospore
production is not a functional or important
component of the disease cycle (Mazzola et
al., 2007b). Tus, various attributes of an
agricultural ecosystem are likely to modulate
the development and efcacy of a disease
suppressive soil.
Strategies to Induce Specifc Soil
Suppressiveness
Organic residue amendment-induced
biological soil suppressiveness
A diversity of soil amendments has been
explored for the potential to yield a disease
suppressive soil. Composts have been the
most commonly used substrate in this
context and extensive literature exists
concerning development and utilization of
plant-based composts for control of soil-
borne plant diseases (Hoitink and Boehm,
1999; van der Gaag et al., 2007). Tese
organic substrates have demonstrated signif-
cant capacity to induce disease suppression
in defned environment or growth media
conditions (Mandelbaum and Hadar, 1990;
Widmer et al., 1998). However, while it may
be arguable, there has been minimal efective
use of such materials in feld-level produc-
tion agriculture for this intended purpose.
Tere is no doubt that composts are utilized
in a multitude of plant production systems,
but consistently and predictably realizing the
intended goal, that being the development of
soil suppressiveness, has been elusive due to
an inability to predict efects on soil biological
composition and function. Tis in part can
be attributed to variability in consistency of
compost activity, which is a function of
multiple factors including substrate compos-
ition (Termorshuizen et al., 2006), storage
conditions (van Rijn et al., 2007) and curing
duration (Danon et al., 2007). Disease control
achieved with any given compost may also be
a consequence of host-mediated efects (van
Rijn, 2007). In addition, there exists the
potential that organic amendments including
206 M. Mazzola
composts will yield not only increases in the
microbial consortia responsible for potential
disease suppression, but may also enhance
disease development due to an increase in
populations or activity of non-target or
target plant pathogens (Cohen et al., 2005;
Termorshuizen et al., 2006; Mazzola et al.,
2009).
Tat being said, there are signifcant
opportunities to utilize more clearly defned
bio-based products to enhance specifc
processes including soilborne disease
suppression. By clearly defned, reference is
being made to the consistency of product
composition which will enable reproducibil-
ity of function, and a capacity to determine
functional mechanism(s) involved in such
processes. Certain of these amendments,
such as fsh emulsion or bone meal, operate
primarily, though perhaps not exclusively,
through chemical mechanisms (Tenuta and
Lazarovits, 2004; Abbasi, et al., 2009).
However, there are other examples in which
the use of residues from specifc sources,
such as an individual plant species, act to
selectively modulate the resident biology in a
manner that yields a suppressive soil.
Residues from plants belonging to the family
Brassicaceae have been studied extensively
for their potential to yield suppression of
various plant pests including pathogens,
insects and weeds (Brown and Morra, 1997).
Active interest in these plant residues as a
soil amendment emanated from the fact that
members of this plant family produce
glucosinolates which, upon hydrolysis, yield
several biologically active compounds, includ-
ing isothiocyanates. Chemical mechanisms
have long been viewed as the dominant mode
leading to pest suppression as a result of
brassicaceous amendments (Matthiessen
and Kirkegaard, 2006). However, several
studies have revealed that other functional
mechanisms operate to yield pest control. In
some instances soilborne disease and weed
suppression obtained in response to specifc
brassicaceous amendments is not chemically
mediated but rather functions at least in part
through the resident soil biology (Mazzola et
al., 2001; Hoagland et al., 2008).
Brassicaceous seed meal amendments
efectively control a number of soilborne
diseases (Smolinska et al., 1997; Mazzola et
al., 2001; Chung et al., 2002). Te operative
mechanism(s) difers according to the target
pathogen and seed meal plant source
(Mazzola et al., 2007a), and in certain
instances disease control requires specifc
changes in microbial community compos-
ition that yield soil suppressiveness (Cohen
and Mazzola, 2006; Mazzola et al., 2007a).
Another level of complexity is realized when
the temporal nature of disease suppression is
examined and changes in functional
mechanism(s) are revealed. Tis phenom-
enon has been most apparent in seed meal-
induced control of Rhizoctonia root rot of
apple where several lines of support impli-
cated the need for a functional microbial
community to attain seed meal-induced
disease suppression. Such evidence includes
the fact that Brassica napus seed meal (BnSM)
provided disease control irrespective of
glucosinolate content; the capacity of BnSM
amendment to suppress Rhizoctonia root rot
was abolished if soil was pasteurized prior to
introduction of the pathogen, and only seed
meals such as BnSM, but not soybean meal,
which signifcantly elevated densities of resi-
dent Streptomyces spp. provided efective
disease suppression (Mazzola et al., 2001;
Cohen et al., 2005). Introduction of individ-
ual Streptomyces sp. isolates from seed meal
amended soils provided a level of disease
control that was equivalent to BnSM amend-
ment, and the majority of Streptomyces
isolates provided control of Rhizoctonia solani
through the induction of host defence
responses (Cohen and Mazzola, 2006).
In Brassica juncea seed meal (BjSM)
amended soil, the temporal dynamics in
elevation of resident Streptomyces popula-
tions corresponded with the induction of
soil suppressiveness, providing further
support for this phenomenon as a functional
mechanism. Disease control in response to
BjSM amendment was attained even in
pasteurized soil, but only if the amendment
was made at the time of pathogen infest-
ation. When addition of R. solani inoculum
was delayed until 24 h post-seed meal
amendment, pathogen suppression in native
(Fig. 11.1) or pasteurized soil was not
observed. Te pattern of observed disease
Soil Microbial Community Management 207
suppression corresponded with the pattern
of allyl isothiocyanate (AITC) generation, a
process that was completed within 24 h of
seed meal amendment (Mazzola et al.,
2007a). Soil suppressiveness to Rhizoctonia
root rot was restored to native soils when
incubated for a period of 4 weeks, and the
re-establishment of disease suppression was
associated with the elevation of resident
Streptomyces spp. populations (Mazzola et
al., 2007a). Seed meal-induced soil suppres-
siveness towards Rhizoctonia root rot of
apple was also obtained in feld trials through
the use of various brassicaceous seed meals
including that of B. napus (Mazzola and
Mullinix, 2005; Fig. 11.2).
Accumulating data demonstrate that soil
biology may also contribute to seed meal-
0 1 2 3 4 5 6 7 8
Control
Bj SM 0 h
Bj SM 24 h
Bj SM 4 wk
Streptomyces population (log cfu/g soil)
0 20 40 60 80 100
Rhizoctonia solani root infection (%)
0
2
4
6
8
10
12
14
16
18
a
a
b
b
b
b
Control 1,3-D:C17 BnSM
(
%
)
R
h
i
z
o
c
t
o
n
i
a
s
o
l
a
n
i
r
o
o
t
i
n
f
e
c
t
i
o
n
Fig. 11.1. Duration of Brassica juncea seed meal (Bj SM) incubation period in soil prior to pathogen
infestation affects native Streptomyces densities, level of Rhizoctonia solani AG-5 infection of apple seedling
roots and mode of disease suppression induced by the seed meal amendment. Relative to a non-treated
control, disease was suppressed when the pathogen was introduced into soil at the time of seed meal
amendment (Bj SM 0h) or at 4 weeks after amendment (Bj SM 4 wk) but not when the pathogen was
introduced at 24 h after application of the amendment (Bj SM 24 h) (left panel). Populations (colony forming
units, cfu) of resident Streptomyces spp. in the corresponding soils, and their proliferation at 4 weeks post-
seed meal amendment are evident (right panel). Disease suppression attained when the pathogen was
introduced at the time of seed meal amendment (0 h) was attributed to the generation of allyl
isothiocyanate, but this chemical was evacuated from the system by 24 h post-seed meal amendment
(Mazzola et al., 2007a). Disease suppression attained when the pathogen was introduced at 4 weeks post-
seed meal amendment was attributed to the elevated populations and activity of resident Streptomyces.
Fig. 11.2. Effect of soil treatment on Rhizoctonia solani infection of Gala/M26 and Golden Delicious/M7
roots in two apple orchards in Washington state: CV (black bars) and WVC (grey bars), respectively
(Mazzola and Mullinix, 2005). Soil fumigation and seed meal amendment signifcantly reduced root
infection relative to the non-treated control at both orchard sites (treatments with different letters differ
signifcantly P < 0.05), and there was no signifcant difference between seed meal and fumigation
treatments. BnSM, Brassica napus seed meal soil amendment; 1,3-D:C17, 1,3-dichloropropene-
chloropicrin soil fumigation.
208 M. Mazzola
induced suppression of root disease incited
by Pythium spp. BjSM efectively controls
Pythium root rot through the release of AITC
(Mazzola et al., 2009). However, other mech-
anisms of disease suppression must function
in a time-dependent manner as at least partial
disease control was attained in response to
seed meal amendment even when inoculum
of Pythium irregulare was introduced into soils
16 weeks post-seed meal amendment (Fig.
11.3.). Analysis of fungal communities using
a taxonomic macroarray indicated that
Trichoderma spp. were preferentially domin-
ant in amended soils suppressive to Pythium
whereas the fungal community was more
evenly distributed in soils conducive to
Pythium spp. (Izzo and Mazzola, 2007). It is
plausible that these fungi, which possess a
well-known capacity to provide biological
control of Pythium spp. (Howell, 1982;
Wolfhechel and Jensen, 1992), contributed
to the observed disease suppression.
Green manure systems to induce
biological soil suppressiveness
Green manures have been examined exten-
sively as a means to improve soil quality, but
although long studied (Millard and Taylor,
1927; Rouatt and Atkinson, 1950) this prac-
tice has been less efective or consistent
when applied to a system for the control of
soilborne diseases. As with certain organic
residue amendments, green manuring may
exacerbate disease development if used in
concert with an inappropriate pathosystem
(Manici et al., 2004). Te lack of consistency
can be attributed to various factors, most
being similar to those limiting the efcacy of
organic residue soil amendments detailed
above, including an absence of knowledge
concerning the underlying mechanisms of
the organic-matter-mediated disease sup pres-
sion. As a result, incorporation of green
manure crops into soil with the intended goal
of specifcally managing disease suppressive
elements of the resident soil microbial
community has received minimal study.
Te incorporation of green manures has
been shown to increase the diversity and
density of certain microbes known to have
pathogen inhibitory activity, including fuor-
escent Pseudomonas spp., non-pathogenic
Fusarium spp. and Streptomyces spp. However,
within resident populations of each of these
microbial communities numerous members
will inherently lack one or more of the func-
tional attributes that confer capacity to limit
disease incited by any given pathogen
(Larkin and Fravel, 1999; Gu and Mazzola,
2003; Zhao et al., 2009). Tus, as in the use
of bio-based soil amendments, identifcation
of operative mechanisms and the ability to
0
10
20
30
40
50
60
70
80
90
Control BjSM fine BjSM coarse
Soil treatment
P
y
t
h
i
u
m
i
r
r
e
g
u
l
a
r
e
r
o
o
t
i
n
f
e
c
t
i
o
n
(
%
)
Fig. 11.3. Effect of Brassica juncea seed meal (BjSM) on apple root infection incited by Pythium
irregulare when oospore inoculum of the pathogen (~2000 propagules/g soil) was introduced into the soil
system 16 weeks post-seed meal amendment. Coarse (24 mm diameter) and fne (< 1 mm diameter)
seed meal particles were used in the assay.
Soil Microbial Community Management 209
monitor the relative presence of the attribute
in native soil microbial populations will be
intrinsic to the successful application of
green manuring as a means to induce biolog-
ically based disease suppressive soils.
Kinkel and colleagues have been at the
forefront in attempts to discern the mech-
anisms of biologically mediated disease
suppressive soils developing in response to
green manuring. In particular, studies have
focused on the contribution of the resident
Streptomyces community towards the induc-
tion of soil suppressiveness in response to
green manures. A green manure crop of
buckwheat or canola increased the propor-
tion of streptomycetes in the resident popu-
lation that were antagonistic towards the
potato pathogens Streptomyces scabies,
Verticillium dahliae and R. solani (Wiggins
and Kinkel, 2005a). Te relative increase in
inhibitory activity of the streptomycete
community was frequently associated with a
decrease in disease development and an
increase in potato yields. Similar increases
in the proportion of antagonistic strepto-
mycetes and reduction in lucerne root rot
were observed in buckwheat or sorghum
sudan grass-treated soils (Wiggins and
Kinkel, 2005b). Buckwheat and sorghum
sudan grass green manures also increased
the density and inhibitory activity of resi-
dent bacterial populations and Streptomyces
spp. expressing antagonistic action towards
the causal pathogen of Fusarium head blight
of wheat, F. graminearum (Perez et al., 2008).
As an initial step in the process towards
developing a protocol for selection of appro-
priate green manure crops (or other resource
amendments) for the generation of a highly
inhibitory soil microbial community, studies
were conducted to explore the efects of
specifc types and quantities of C compounds
on resident populations of Streptomyces spp.,
and their antagonistic potential (Schlatter et
al., 2009). Addition of complex C sources
tended to yield greater Streptomyces densi-
ties than the simple sugar glucose. Higher
inputs in the form of these C sources resulted
in a Streptomyces community with greater
antibiotic inhibitory activity than when soil
was treated at a lower input level. In this
system, further characterization of the
means by which specifc nutrient inputs
infuence Streptomyces inhibitory activity
may enhance the ability to actively manage
disease suppressive soils through the green
manure management programmes.
Cropping systems to mediate biologically
based soil suppressiveness
Several modifcations to crop production
systems have been employed as a means to
control soilborne plant diseases. Te most
common and efective scheme has been the
use of crop rotations, with disease control
believed to be achieved as the absence of a
suitable plant host results in diminished
viability of the pathogen. Attempts to develop
specifc cropping models to manage the resi-
dent soil microbiota for disease suppression
have been few. It has been reasoned that as
increased plant diversity can enhance micro-
bial community biomass (Zak et al., 2003)
mixed cropping systems will generate a more
diverse microbial community and thus should
be more resilient to pathogen invasion
(Workneh and van Bruggen, 1994; Hiddink et
al., 2005). However, the preponderance of
examples of induced suppressive soils come
from crop monoculture systems (Chet and
Baker, 1980; Cook and Weller, 1987), and
limited attempts to compare mixed crop
systems with single crop systems indicate
that mixed systems may not enhance micro-
bial diversity or disease suppressiveness
(Hiddink et al., 2005).
Plant root systems and their release of a
complement of root exudates serve as a
dominant driving force in determining soil
microbial community diversity and density
(Lemanceau et al., 1995; Dalmastri et al.,
1999; Miethling et al., 2000; Marschner et
al., 2001; Berg et al., 2002; Mazzola and Gu,
2002), particularly in conventional crop
production systems where organic matter
and substrate availability is typically
nominal. As noted above, certain crop mono-
culture systems express the ability to select
for microbial communities that over time
lead to the development of soils suppressive
to specifc soilborne pathogens (Larkin et al.,
1993; Weller et al., 2002). Alternatively,
210 M. Mazzola
previous cropping systems may inadvert-
ently yield a soil suppressive to a pathosys-
tem of a subsequent unrelated crop. For
example a soil cropped to a continuous
wheat monoculture was shown to be
bio logically suppressive to Rhizoctonia root
rot of apple incited by R. solani AG-5
(Mazzola, 1999). Once planted to apple, soil
suppressiveness towards this pathogen
diminished over time and loss of disease
suppression corresponded with specifc
changes in composition of the fuorescent
Pseudomonas spp. population and reduced
densities of Burkholderia cepacia recovered
from orchard soils. Interestingly, soil
suppressiveness towards Rhizoctonia root
rot of both apple and wheat could be restored
in greenhouse trials through repeated culti-
vation of these soils with wheat (Mazzola
and Gu, 2000, 2002). Restoration of soil
suppressiveness was associated with a trans-
formation of the fuorescent pseudomonad
community to one that more closely resem-
bled that initially recovered from the feld
suppressive soil.
Although extended cultivation of apple
selected for a microbial community lacking
apparent inhibitory activity towards soil-
borne fungal pathogens (Mazzola, 1999),
this does not appear to be a universal
response in perennial plant production
systems. Long-term grapevine monoculture
enriched the soil with fuorescent
pseudomonad genotypes that produce
2,4-DAPG and hydrogen cyanide (HCN)
(Svercel et al., 2009), bacterial characteris-
tics which have been repeatedly associated
with disease suppressive soils (Haas and
Dfago, 2005). While the duration of grape-
vine monoculture examined in this study
was excessive, with certain sites planted
since the frst millennium without interrup-
tion, this example does demonstrate again
the capacity of crop monoculture to selec-
tively enhance microbial communities func-
tional in the development of disease
suppressive soils.
In an evaluation of organic cropping
systems, Postma et al. (2008) reported
signifcant diferences in soil suppressive-
ness towards multiple pathogens, including
R. solani AG 2.2IIIB, which is an important
pathogen of sugarbeet. Disease suppression
was elevated in systems that employed a
grassclover sequence within the rotation
cycle, and suppressiveness lasted 2 years
beyond this sequence but disappeared after
3 years. Te development of soil suppres-
siveness in this system was correlated with a
signifcant increase in Lysobacter spp. popu-
lations. Lysobacter spp. produce a number of
lytic enzymes and antibiotics that account
for their capacity to provide biological
control of various fungi and oomycetes
(Kobayashi et al., 2005). Te association of
Rhizoctonia suppressiveness and Lysobacter
was re stricted to clay soils and was not
detected in sandy soils (Postma et al., 2008).
Multiple aspects of a production system
have the capacity to limit or enhance the
adoption of plant-mediated induction of soil
suppressiveness as a viable practice for the
management of soilborne plant diseases.
Foremost among these is the time frame,
perceived or actual, required to bring about
the disease suppressive state. Diferent plant
species or genotypes have inherently difer-
ential abilities to select for microbial commu-
nities with the capacity to yield disease
suppression (Smith et al., 1999; Mazzola and
Gu, 2002; Mazzola et al., 2004; Berg et al.,
2005). Tus, plant species or genotype evalu-
ation will be instrumental to optimizing
densities of the functional microbial popula-
tion and reducing the time necessary to yield
a disease suppressive soil. 2,4-DAPG-
producing fuorescent pseudomonads have a
demonstrable role in the development of
soils suppressive to take-all of wheat (Weller
et al., 2002) and also have been isolated from
soils that naturally suppress black root rot of
tobacco (Keel et al., 1996; Ramette et al.,
2003) or Fusarium wilt disease (Landa et al.,
2002). Development of a take-all suppres-
sive soil requires a threshold population of
these bacteria (Raaijmakers et al., 1997) and
certain bacterial genotypes possess a
superior capacity to limit disease develop-
ment (Raaijmakers and Weller, 2001).
Plant genotypes were shown to difer in
both the ability to enrich for populations of
indigenous 2,4-DAPG-producing fuorescent
pseudomonads and the dominant bacterial
genotype that was supported in the
Soil Microbial Community Management 211
rhizosphere (Mazzola et al., 2004; Picard et
al., 2008). In addition, expression of
2,4-DAPG biosynthetic genes in the rhizo-
sphere is infuenced by plant genotype (Notz
et al., 2001; Jamali et al., 2009). Tus, efort
to select for plant genotypes that possess a
greater capacity to stimulate resident popu-
lations of efective 2,4-DAPG-producing
fuorescent pseudomonad genotypes, or
other functional genotypes, should be of
beneft in systems that seek to utilize crop-
ping systems as a means to induce disease
suppressive soils.
Te importance of plant genotype in deter-
mining the development of a biologically
suppressive soil has been demonstrated in
multiple systems. Te capacity of continuous
cropping of watermelon to induce soil
suppressiveness to Fusarium wilt was cultivar
dependent (Larkin et al., 1993). Furthermore,
plant genotype was shown to be a signifcant
factor in the capacity of wheat cultivation to
yield a soil microbial community suppressive
towards Rhizoctonia root rot of wheat and
apple (Mazzola and Gu, 2002). Among fve
genotypes evaluated, only two were shown to
consistently generate a soil biologically
suppressive towards Rhizoctonia root rot in
response to successive wheat growth cycles
(Mazzola and Gu, 2002). Te two efective
wheat cultivars, Lewjain and Penawawa,
altered the genetic and species composition
of the fuorescent pseudomonad community
resident in the wheat-cropped orchard soils
(Mazzola and Gu, 2002; Gu and Mazzola,
2003). Te fuorescent Pseudomonas spp.
population from the resulting suppressive
soils demonstrated a signifcantly greater
degree of antagonism towards R. solani than
did the population from non-treated control
soil or soils cultivated with wheat genotypes
that were inefective in the induction of soil
sup pressive ness.
In subsequent studies, the capacity of
continuous wheat cropping as a means to
efectively control Rhizoctonia root rot of
apple was demonstrated in feld trials
(Mazzola and Mullinix, 2005). In this
system, a three-cultivar seed mixture was
used in the cropping of wheat on a replant
apple orchard site with three successive
10-week growth cycles. At the end of each
growth cycle plant biomass was removed
prior to replanting the site, and at the end of
the third wheat cycle the orchard was planted
to Gala/M26 apple. Under this practice,
Rhizoctonia root infection was signifcantly
reduced (Fig. 11.4) and the wheat cropping
0
5
10
15
20
25
Control MeBr Fallow
(3 years)
Wheat
(1 year)
Cgm
(1 year)
Cgm
(2 years)
Cgm
(2 years)
wheat
(1 year)
Cgm
(3 years)
Soil treatment
(
%
)
R
h
i
z
o
c
t
o
n
i
a
s
o
l
a
n
i
r
o
o
t
i
n
f
e
c
t
i
o
n a
c
a
c
a
ab
bc
c
Fig. 11.4. Effect of soil treatments on incidence of Rhizoctonia solani infection of Gala/M26 apple roots
at CV orchard, Orondo, Washington state (Mazzola and Mullinix, 2005). Bars designated with the same
letter do not differ signifcantly (P > 0.05). MeBr, pre-plant methyl bromide soil fumigation; Wheat (1 year),
mixed cultivar cover crop grown for three successive 10-week plantings followed by removal of plant
biomass; Cgm, canola green manure with soil incorporation of plant biomass.
212 M. Mazzola
procedure was more efective than a 1- or
2-year canola green manure in suppressing
this root disease. Te 3-year canola green
manure was as efective as the wheat-
cropping scheme in limiting apple root infec-
tion by Rhizoctonia spp.
Conclusions
Active management of the biological
resources native to agricultural soil ecosys-
tems is a logical progression in our studies of
the basis for the function of disease suppres-
sive soils. While studies of disease suppres-
sive soils have provided a wealth of
information concerning the source of
biological activity there has been relatively
little progress in our capacity to manage the
efective microbial resources indigenous to
agricultural ecosystems. Rather, focus has
remained on isolation and identifcation of
the numerous biologically active microbial
agents resident in such soils, and subse-
quently resorting to the inundative release of
these microorganisms into non-native soils
or crop production systems. Climate change
undoubtedly will have an efect on many
biological processes leading to altered ecosys-
tem function. Such changes are predicted to
modulate the efcacy of certain strategies
that are commonly utilized for the manage-
ment of soilborne diseases. In concert with
the loss or impending restricted use of
numerous chemicals (e.g. methyl bromide)
previously used for soilborne disease control,
it seems an appropriate time to further
examine the prospect for managing ecosys-
tem microbial resources as a viable soilborne
disease control strategy. While climate
change is bound to have impacts on the soil
biology that is functional in disease suppres-
sive soils, pathogen populations will acclima-
tize to these changes concurrently with the
resident microbial milieu and thus efective
adaptive traits are likely to reside across
these broad communities.
In the development of protocols for the
management of disease suppressive soil
biology, it may be useful to consider the
similar eforts pursued within the feld of
bioremediation and the comparable
impediments to efective use of specifc
plant-mediated strategies. Specifc plant
systems are designed not only for phyto-
extraction of pollutants but also as a means
to secure the value of microbial partners
that possess the ability to degrade organic
pollutants. Much as is the case in phytore-
mediation eforts, little emphasis has been
placed on breeding eforts towards the devel-
opment of crop genotypes with an elevated
capacity to select for specifc microbial geno-
types functional in disease suppression.
Reluctance to pursue plant breeding
programmes focused on such attributes was
limited until recently by a lack of acceptance
or understanding of this phenomenon as a
valuable parameter to crop improvement.
Molecular plant breeding programmes
are at the head in the development of plants
with enhanced capacity to select for plant
benefcial microbial communities, including
those involved in disease suppression.
Multiple recent examples demonstrate the
potential of this approach. A transgenic
tobacco overexpressing ferritin imposed
reduced iron availability in the rhizosphere
resulting in a fuorescent pseudomonad
community with a greater ability to grow
under iron stress conditions. Tis resulting
bacterial population possessed a greater
capacity to inhibit growth of the plant path-
ogen Pythium aphanidermatum (Robin et al.,
2007). Genetic modifcation of the wheat
cultivar Bobwhite by insertion of the
powdery mildew resistance gene Pm3b
resulted in multiple transgenic lines with an
enhanced capacity, relative to the parental
line, to select for 2,4-DAPG-producing fuor-
escent pseudomonads (Meyer et al., 2009).
Tus, evidence indicates that eforts to
develop crop cultivars with an elevated
potential to exploit the resident disease
suppressive microbial community are not
futile, and in fact will be worthwhile for the
development of more sustainable crop
production systems.
Strategies other than those discussed
here have received a modicum of research
investigation but may efectively serve to
manage microbial resources resident in agro-
ecosystems in a manner to suppress soil-
borne plant diseases. In addition to the use
Soil Microbial Community Management 213
of organic amendments or the design of
specifc cropping sequences, further meth-
ods such as fertility management, crop resi-
due management and soil tillage (Peters et
al., 2003) may function to enhance soil
suppressiveness. While adaptation of these
cultural practices to increase the level of soil
suppressiveness is receiving increased atten-
tion as a potential soilborne disease control
practice, there has been only minimal consid-
eration of the efect of such treatments on
overall soil biology composition and func-
tion.
It is a daunting task to envision develop-
ment of management systems to yield
biologically suppressive soils for diseases in
which such soils have not previously been
characterized. Such an undertaking requires
initial focus on identifcation of the micro-
bial attributes that function to elicit disease
suppression. Although such investigations
continue to be a complex and protracted
process, emerging tools in molecular micro-
bial ecology, including metagenomics and
pyrosequencing will enable more rapid evalu-
ation of microbial community structure, and
ultimately function (van Elsas et al., 2008).
Such analytical tools will enable more
complete examination of resident soil biol-
ogy, changes to such populations in response
to specifc practices, and comparative micro-
bial community analysis among soils allow-
ing one to more reliably predict microbial
efectors of disease suppression. Tese same
methods will enable more efcient analysis
of microbial community structure in response
to agroecosystem management practices and
enable prediction of the resulting benefts to
plant growth through disease suppression. A
greater understanding of the consequence of
such treatments on food webs that modulate
the density and activity of microbial popula-
tions functional in disease control will be
instrumental to the development and even-
tual adoption of tools for the management of
disease suppressive soil biology.
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microbial communities and ecosystem function:
are there any links? Ecology 84, 20422050.
Zhao, X., Tewoldemedhin, Y., Mcleod, A. and
Mazzola, M. (2009) Multiple personalities of
Streptomyces spp. from the rhizosphere of
apple cultivated in Brassica seed meal amended
soils. Phytopathology 99, S150.
CAB International 2010. Climate Change and Crop Production (ed. M.P. Reynolds) 219
12
What is Biotechnology?
Biotechnology is the targeted modifcation
of living organisms and is used widely in
agriculture. It includes tools used to under-
stand and manipulate the genetic make-up
of organisms used for producing or process-
ing agricultural products.
Increasingly, extreme climatic events will
impact on food production in many areas of
the world. A +1C local temperature change
may threaten rainfed cereal production while
changes of over +3C will lead to major crop
losses (Easterling et al., 2007). Adaptation in
management may partially mitigate against
these efects but biotechnology may also be
used to improve resistance to pests and
diseases, improve yield stability, reduce reli-
ance on fertilizer and enhance the nutri-
tional value of staple crops.
A rapidly changing climate will require
rapid development of new plant varieties;
biotechnology can enhance the speed, fexi-
bility and efciency of plant breeding (Fig.
12.1).
Nature of adaptive change
Biological organisms undergo adaptive
change as they acclimatize to new environ-
ments. Many adaptive characteristics result
from the prevailing environment infuenc-
ing expression of genes related to adapta-
tion. Genes are also subject to constant
change; random changes or mutations can
occur through internal errors in DNA repair
Biotechnology in Agriculture
Ryan Whitford, Michael Gilbert and
Peter Langridge
Abstract
Climate change is predicted to result in disruption of many farming systems. Te Food and Agriculture
Organization (FAO) predicts a 1520% fall in global agricultural production by 2080. Consequently,
adaptation of major crop species to climate change will be the biggest challenge for plant breeders this
century. Biotechnology will be important when adapting crops to better tolerate changing stresses. It
includes using advanced genetic mapping technologies, like molecular markers, in the breeding and
development of new varieties. Molecular markers are used to provide greater focus, accuracy and
speed in crop breeding programmes with further advances coming. Genetic modifcation (GM)
techniques are providing access to a diversity of genes, used to develop plant varieties more tolerant
to the negative impacts of climate change.
R
a
t
e
o
f
c
h
a
n
g
e
E
f
f
e
c
t
s
o
f
c
l
i
m
a
t
e
c
h
a
n
g
e
Technology gap
Time
C
o
n
v
e
n
t
io
n
a
l
b
r
e
e
d
in
g
s
o
lu
t
io
n
s
Fig. 12.1. Keeping pace with climate change.
220 R. Whitford et al.
and replication or when subjected to external
infuences such as ultraviolet irradiation.
Tese mutations can alter expression or
activity of encoded proteins.
Within any population of plants there is
genetic variation: natural or induced. Over
many centuries, farmers have generated
heterogeneous plant populations adapted to
local climates and cultivation conditions.
More recently, plant breeders have selected
superior variants to generate genetically
homogenous, highly adapted, elite cultivars.
Intense cereal breeding has resulted in
spectacular improvements in yield and qual-
ity but has narrowed genetic diversity.
Continued genetic gain is becoming increas-
ingly difcult (Feuillet et al., 2008). Using
biotechnology, plant breeders have sought
to identify and deploy new sources of vari-
ation by understanding the available genetic
variation, the genetic control of adaptation,
and the gene-by-environment interactions.
Plant responses to diferent environ-
ments are not thoroughly understood nor
are their genetic bases. Studies of funda-
mental adaptation mechanisms have focused
on single, rather than multiple, genotype
stress relationships. Many have also exam-
ined plant survival under extreme stress
rather than more realistic, agronomically
relevant, stress scenarios (Cushman and
Bohnert, 2000; Bartels and Salamini, 2001;
Araus et al., 2003).
Adapting to drought stress is a huge chal-
lenge in plant breeding because drought
means many diferent things. Stresses may
be caused during grain flling, pre-fowering
or may be continuous throughout a growing
season. In Mediterranean-type dryland
areas, grain-flling stress is common, in South
America pre-fowering stress is more likely
and continuous stress is frequent in non-
irrigated parts of southern Asia where plants
are often dependent upon water stored in
the soil (Reynolds et al., 2005). Plants often
face multiple stresses concurrently; under
water-limiting conditions, there may also be
high temperatures, increased irradiance and
less permeable soil. Tese factors make the
plant breeders task very complex, and
breeders must grapple with drought-related
stresses most relevant to them.
Variation
Natural genetic variation
Introgression
Genetic variation can be exploited by intro-
gression; genes are moved into the cultivated
gene pool by continuously backcrossing with
the cultivated parent. While this takes many
generations, it is the most widely adopted
method for expanding available variation in
a breeding programme. However, it can be a
slow process.
Example 1: Improved resistance of cultivated
European spring barley to mildew has been
achieved by introgressing an Ethiopian landrace
mlo-11 (Jrgensen, 1992). Norman Borlaug
successfully introgressed Rht semi-dwarfng
genes from the Japanese variety Norin-10 into
elite wheat varieties resulting in the 1960s
Green Revolution (Ellis et al., 2007).
Linkage drag is the simultaneous introgres-
sion of deleterious alleles. Introgression of
chromosome regions from landraces or wild
relatives can be a slow and complex process
because just the minimal region needs to be
introduced. Biotechnology, particularly
through the use of molecular markers, plays
a key role in accelerating this process.
Example 2: Rye chromosome fragment 1RS
contains genes responsible for improved grain
yield, race-specifc rust resistance, improved
adaptation and stress tolerance (Zarco-
Hernandez et al., 2005). When introgressed into
wheat, the 1RS/1BL translocation in wheat
negatively impacts gluten strength: it makes
bread dough sticky.
Amphiploids
Entire chromosomes or even entire genomes
can be added as an alternative to introgres-
sion. Genetic diversity in intensively bred
species, such as wheat, can be exploited.
Biotechnology in Agriculture 221
Example 3: In 1938, the frst fertile Triticale
(Triticosecale) exhibited improved yield and
adaptability to regions not suitable for wheat
production (Feuillet et al., 2008). This repro-
duced a naturally occurring process exploited
by early farmers to develop many modern crop
species such as hexaploid wheat, tetraploid
potatoes and tetraploid cotton. Genome analy-
sis has shown that even maize and rice are
ancient tetraploids. Synthetic hexaploid wheats
can be generated by hybridizing durum wheat
(AABB) with Aegilops tauschii (DD). Breeding
programmes have produced more than 1000
synthetic wheats and are an important source
of genetic diversity (CIMMYT, 2009b).
Induced genetic variation
Sexual reproduction has many barriers, such
as hybrid infertility, that prevent the use of
wild germplasm in plant breeding.
Mutagenesis can be used to induce, or create,
new genetic variability.
Mutagenesis
Radiation, such as gamma-rays, or chemicals
such as alkylalkanesulfonates, can be used
to generate variation from which plants with
desirable characteristics can be selected.
Example 4: The frst successful mutant barley
with stiff straw (cultivar Pallas, 1958) was
generated because of a new process: combine
harvesting (Lundqvist, 1986). A gamma-irradi-
ated malting-cultivar mutant was selected for its
semi-dwarf growth habit and cultivar Golden
Promise became the dominant malting quality
barley in Scotland throughout the 1970s and
1980s (Forster et al., 1997).
In vitro culture
In vitro culture of totipotent plant cells and
tissues has increased the importance of the
laboratory in plant breeding. In vitro culture
of haploid microspores, or androgenesis, is
used to produce doubled haploids for genetic
mapping; this is important when decipher-
ing the relationship between genetic vari-
ation and agronomic traits. Doubled haploidy
enables complete homozygosis in one gener-
ation rather than recurrent backcrossing for
six or more generations, as is usually
required; many breeding programmes use
this technique to accelerate the delivery of
homozygous lines for release.
In vitro culture can be used to induce soma-
clonal variation such as changes in chromo-
some number (polyploidy, aneuploidy),
chromosome structure (translocations, dele-
tions, insertions and duplications) and DNA
sequence (base mutations). Tis has been
useful for introgressing alien genes.
Example 5: A cereal cyst nematode resistance
was transferred from rye into wheat by the in
vitro culture of wheatrye monosomic addition
lines (Larkin et al., 1989; Banks et al., 1995).
Insertional mutagenesis
Insertional mutagenesis uses foreign DNA
fragments to disrupt gene function.
Agrobacterium-mediated gene transfer has
been widely applied for generating such
mutations and has been used to support
gene discovery programmes.
Role of Biotechnology
Advances in molecular biology have resulted
in rapid identifcation and quantifcation of
genetic variation as well as identifcation of
genes or genomic regions associated with
the expression of qualitative and quantita-
tive traits (Fig. 12.2).
Building knowledge and understanding
An explosion in plant genetics and genom-
ics research as well as the quantity of infor-
mation about plant genome structure, has
resulted in a technology gap. Resource
development has exceeded the ability to
solve practical plant breeding problems
using those resources. Tis gap is being
closed by providing tools and methods to
breeders to help them identify, and select,
traits and underlying genes.
222 R. Whitford et al.
Understanding mechanisms and processes
Biotechnology helps us understand the
efects of simultaneous multiple, complex
stresses, such as drought, where multiple
signalling pathways are activated and specifc
responses cannot always be assigned to an
individual stress. Transcript profling can be
used to classify stress responses: for exam-
ple osmotic stress responses can be initiated
via either an abscisic acid (ABA)-dependent
or an independent signalling pathway (Gosti
et al., 1995; Ishitani et al., 1997).
Example 6: A reduction in leaf water causes a
passive loss in guard cell turgor, reducing photo-
synthetic activity, and, with increased irradiance,
an excess of reactive oxygen species (ROS).
These are toxic to cellular metabolism. Plants
produce chemical antioxidants such as ascorbic
acid, glutathione and -tocopherol as well as
enzymes such as peroxidases and superoxide
dismutases capable of detoxifying ROS. Turgor
is managed by subcellular sequestration of ions
such as Na
+
and K
+
into the vacuole and by
synthesizing osmolytes (reviewed by Langridge
et al., 2006).
It is unclear which physiological or molecu-
lar processes need to be modifed, or selected
for, to improve crop productivity under
drought stress. Tere is controversy about
the value of selection for osmotic adjust-
ment and ABA response; a systematic trait
orientated breeding approach is required in
order to fully exploit these genetic mech-
anisms (Reynolds et al., 2005).
Example 7: Identifcation of the disaccharide,
trehalose, from desert resurrection species has
helped to classify non-reducing disaccharides
as osmoprotectants functionally important for
drought tolerance. Understanding the physiol-
ogy of trehalose accumulation has led to an
improvement in drought tolerance of species
such as rice, potato and tomato. These fndings
show that novel physiological traits can be used
for selection (Almeida et al., 2007).
Biotechnologies are tools used to identify,
classify and select these traits.
Plant modelling
Plant breeding predicts phenotypes, based
on genotypes, by measuring phenotypic
performance in large segregating popula-
tions and then applying statistical pro cedures
based on quantitative genetic theory.
Plant modelling can link phenotypic and
physiological/molecular knowledge.
Example 8: Modelling of osmotic adjustment in
sorghum identifed the functional mode of
action, and estimated yield advantages of up to
5% across multiple stress environments
(Hammer et al., 1999). Plant modelling can be
also used to develop alternative breeding strat-
egies (Chapman et al., 2003). Kuchel et al.
(2005) used computer simulation to design a
genetically effective, economically effcient
marker-assisted wheat breeding strategy.
Signifcant genetic gains in yield, end-use qual-
ity and disease resistance resulted.
Gene network models, while less common,
may predict the consequences of altering
specifc gene sequences and protein modif-
cations.
Example 9: Flowering-time transition models in
Arabidopsis (Koornneef et al., 1998; Welch et
al., 2003) laid the foundation for gene-sequence-
based predictive modelling, which is now
applied to predict sorghum fowering time. The
simulation model predicted grain yield, from two
allelic variants of sorghum, for a number of
specifc environments (Hammer et al., 2008).
Improving
diversity and
population
dynamics
Generating
genetically
modified
plants
Developing
new crop
breeding
strategies
Better
understanding
of adaptive
change
mechanisms
Fig. 12.2. How biotechnology helps breeding.
Biotechnology in Agriculture 223
Yield potential and stability
Molecular processes underlying yield poten-
tial and stability have primarily targeted
increasing source and sink strengths and the
modifcations of assimilate partitioning,
plant architecture and development (Van
Camp, 2005). Little progress has been made
in quantitatively identifying genetic compo-
nents that defne yield.
Strategies to enhance yield per se may
include:
1. Introducing more efcient C
4
-like photo-
synthesis from maize into C
3
rice. So far,
these approaches have not resulted in full C
4
photosynthesis despite maize having a close
evolutionary relatedness to rice. Combining
the expression of two C
4
enzymes (phos-
phoenolpyruvate carboxylase and pyruvate
orthophosphate dikinase) has, however,
resulted in increases of 35% in photosyn-
thetic capacity and 22% in yield (Ku et al.,
2001).
2. Introducing variants of Rubisco, a key
enzyme for carbon fxation, with a higher
catalytic rate and/or better discrimination
between gaseous substrates. Manipulating
Rubisco activase by targeting the synthesis
or degradation of inhibitors may modulate
Rubisco activity and control its stability
under stress. Some chimeric and mutant
versions of Rubisco activase are less heat
labile and, when reintroduced back into
Arabidopsis, have improved photosynthesis
and leaf growth under heat stress (Kurek et
al., 2007; Portis et al., 2007).
3. Increased endosperm ADP-glucose pyro-
phosphorylase activity. Yield enhancement
of more than 20% occurred when wheat and
rice were modifed for this rate-limiting
enzyme in endosperm starch synthesis, an
important determinant of sink strength.
Supporting conventional breeding
Screening
Breeding programmes often grow thou-
sands, or millions, of individual plants to
increase the probability of identifying indi-
vidual plants with specifc gene combina-
tions; this requires new tools, some
biotechnological, for plant selection.
Isozyme markers were used in the 1980s
to hasten the introgression of monogenic
traits from wild germplasm into a cultivated
background, a process now known as marker
assisted selection (MAS) and now based
around the direct detection of variation in
DNA sequences (Table 12.1). Tis can be
used to indirectly select traits by detecting
genetic variation closely linked to underly-
ing genes.
MARKER-ASSSTED BACKCROSSNG Te use of
molecular markers is justifed when conven-
tional phenotypic trait selection is difcult,
or is dependent on specifc environments or
developmental stages that infuence the
expression of the target phenotype (Xu and
Crouch, 2008). MAS can hasten backcross-
ing and is useful in maintaining recessive
alleles.
Example 10: Marker-assisted backcrossing
(MABC) of Sub1, a major quantitative trait locus
(QTL) on chromosome 9 of rice, has improved
submergence tolerance of Swarna, a cultivar
widely grown in food-prone regions of Asia
(Neeraja et al., 2007). Simple sequence repeat
(SSR) markers aided both the introgression of
Sub1 and the subsequent recovery of the recur-
rent parental background. Introgression of Sub1
converted Swarna to a submergence-tolerant
variety within three backcross generations (23
years).
Table 12.1. Recent marker systems developed and applied to marker
assisted selection (MAS).
Acronym Description
RFLPs Restriction fragment length polymorphisms
RAPDs Random amplifed length polymorphisms
STS Sequence tagged site
AFLPs Amplifed fragment length polymorphisms
SSRs Simple sequence repeats or microsatellites
SNPs Single nucleotide polymorphisms
224 R. Whitford et al.
MARKER-ASSSTED PYRAMDNG MAS may be
used to pyramid multiple monogenic traits,
or several QTLs for a single target trait, with
complex inheritance such as drought toler-
ance. Root architecture is a secondary trait
intrinsically linked to drought tolerance.
Example 11: The effect of QTLs for root archi-
tecture on yield has been reported under vary-
ing moisture regimes in rice and maize (reviewed
by Collins et al., 2008). After the identifcation of
four major root architecture QTLs in rice, MAS
aided the introgression of all alleles for increased
root length from Azucena into Kalinga III, an
upland variety (Steele et al., 2006, 2007).
EARLY-GENERATON MAS MAS is often simpler
than phenotypic screening selection and can
be carried out at early stages of development
and on single plants, rather than plant fami-
lies or plots. Using MAS to select in of-
season nurseries enables cost-efective
production of more generations per year.
DNA extraction is the largest cost in MAS
and is often the primary rate-limiting factor
for scaling up the whole process (Xu and
Crouch, 2008).
Recent development of non-destructive
single seed-based DNA extraction and geno-
typing systems is enhancing MAS efciency
signifcantly and is being applied to the
International Maize and Wheat
Improvement Centers (CIMMYT) maize
molecular breeding programmes (Gao et al.,
2008).
METABOLTE-ASSSTED BREEDNG Genomic-
based technologies such as metabolic profl-
ing are now used in addition to MAS. Te
rapid development of high-throughput tools
for metabolite profling makes DNA
sequence-based profling cost competitive
(Kopka et al., 2004). Metabolite profling
will assist in the selection of components of
yield and stress tolerance (Fernie and
Schauer, 2009).
Example 12: Important metabolic traits include
carotenoid content of tomato, protein content of
maize and starch content of both potato and
rice (Fernie and Schauer, 2009). High-
throughput metabolomic screening of large
tomato breeding populations for carotenoid
metabolites has used matrix-assisted laser
desorption ionization time-of-fight mass spec-
trometry (MALDI-TOF-MS). Profling of lines
from two tomato populations (Solanum pennellii
introgression lines and saturated mutants) iden-
tifed germplasm likely to assist breeding of fruit
containing high levels of nutriceuticals (Fraser
et al., 2007).
Combined MAS
Genetic gain can be improved when pheno-
typic selection is combined with MAS. Even
where relationships between gene informa-
tion and phenotypic variation are well
defned, a lack of appropriate computational
tools has hampered incorporation into
breeding programmes (Xu and Crouch,
2008). However, new simulation and deci-
sion-support software are enabling the inte-
gration of genomics into breeding
programmes, increasing the scale, efciency
and impact of MAS. Combining screening
technologies and computational modelling
should shorten the introduction of new
varieties by between 3 and 5 years.
Example 13: The genetics and breeding simu-
lation tool, QULNE/QUCM, has been used by
wheat breeders to predict cross performance
and compare selection strategies (Wang et al.,
2003, 2007; Kuchel et al., 2005).
Analysis of diversity and population
dynamics
Applying molecular marker technologies to
large breeding programmes has advanced
genetic mapping; many QTLs controlling a
range of abiotic stresses have been identi-
fed.
Biotechnology in Agriculture 225
SSRs, amplifed fragment length poly-
morphisms (AFLPs) and random amplifed
length polymorphisms (RAPDs) have been
used to assess genetic diversity in synthetic
wheat derivatives (Zhang et al., 2005) and
landraces (Strelchenko et al., 2004), import-
ant sources of abiotic stress tolerance.
Genotypic variation is used to improve
stress tolerance in elite germplasm. Superior
genotypes can be developed by the molecular
measurement of genetic similarity or genetic
distance between parents (Korzun, 2003).
Example 14: In common bean (Phaseolus
vulgaris L.), ultrametric genetic distances
between progeny and a target parent were used
in combination with nine indexed QTL-linked
markers, weighted according to the amount of
phenotypic variance they explained, to select
high-yielding lines that retained important QTLs
in a desirable genetic background (Taran et al.,
2003). Critical for this methodology was a
bio informatic platform capable of compiling and
comparing complex molecular fngerprints and
delivering predictions of genetic distance and
variance.
Rapidly identifying genotypes using DNA-
based molecular marker technologies is help-
ing breeders to select elite genotypes without
extensive feld-based testing (Reynolds et al.,
2009).
Abiotic stress tolerance diversity in wild
relatives and breeding populations is also
used to validate candidate genes.
Example 15: Collaboration between CIMMYT,
Cornell University and the Chinese, Kenyan,
Thai and Zimbabwean governments is identify-
ing key regulators in drought response pheno-
types from 350 tropical maize lines. Metabolites
such as sucrose, glucose, starch, ABA and the
ABA glucose ester of leaves and reproductive
organs are being assessed under both water-
stressed and well-watered conditions, alongside
yield components and secondary traits. The
genotypic component of the association test
involves haplotyping about 130 ABA and carbo-
hydrate synthesis pathway candidate genes
and drought-tolerance response genes involved
from maize and other plant species (Ribaut et
al., 2009). One- and two-dimensional gas chro-
matography/mass spectrometry (GC-MS) has
been used to survey 70 rice cultivars for import-
ant nutritional metabolites (Kusano et al., 2007;
Oryzabase, 2009).
Management of germplasm resources is a
major problem for many crop improvement
programmes. Diversity surveys help with
the compilation of smaller genotype-based
reference sets refecting the allelic diversity
present in the larger germplasm reserves.
Example 16: The analysis of 3000 chickpea
accessions with 48 SSR markers revealed
extensive allelic diversity: 78% of all alleles were
captured in a reference set of 300 accessions
(Upadhyaya et al., 2008).
High-throughput technologies
(genotyping, phenotyping)
It typically takes 12 years to release a
commercial cereal variety from the time of
the initial cross, and perennials may take
longer. Te increasing rate of climate change
requires accelerated breeding, now being
assisted by high-throughput genotyping and
phenotyping technologies.
Phenotyping
For many traits, phenotyping is the limiting
component. Extensive studies of the genetic
control of drought tolerance have not yet
resulted in the deployment of markers for
specifc loci and alleles in breeding
programmes. It is difcult to reproduce
seasonal diferences in combination with
diferent genetic backgrounds, and validat-
ing markertrait associations has been prob-
lematic. However, phenotyping is often
more reliable for some factors afecting root
health, notably tolerance to root disease,
pests and nutrient defciencies. Reliable
phenotyping leads to more reliable mapping,
usually linked to higher heritability, from
which markers can be readily developed and
deployed.
High-throughput phenotyping facilities
using robotics and image analysis are being
constructed at many research sites (APPF,
2009) but it will be several years before their
impact can be measured. Similar facilities are
already widely used by industry (CropDesign,
2009) to accurately and objectively measure
plant characteristics under a range of
stresses.
226 R. Whitford et al.
Phenotyping systems focusing on clusters
of mega-environments and high-throughput
feld-based phenotyping criteria have been
used by CIMMYT and the International Rice
Research Institute (IRRI). When combined
with sampling and data acquisition systems,
phenomics-based protocols for breeding
programmes can be developed. In natural or
controlled environments, drought-tolerance
breeding programmes (CIMMYT, 2009a;
IRRI, 2009) are incorporating techniques
such as remote sensing of plant water status,
canopy chlorophyll content and canopy
temperature.
Genotyping
PCR-based assays have allowed extensive
automation of genotyping, but high marker
development costs and low levels of poly-
morphisms in breeding material have inhib-
ited the use of MAS in many breeding
programmes. Cheap, fast-screening using
single nucleotide polymorphisms (SNPs) has
led to the development of a large SNP detec-
tion industry largely servicing medical geno-
typing but also applicable to crop plants.
Next Generation Sequencing Technologies,
such as Solexa and 454/FLX, have dramati-
cally reduced sequencing costs and SNP
discovery is now possible in species where
other marker systems are poorly developed
such as cowpea, chickpea, pigeonpea and
groundnut (Varshney et al., 2009).
Private companies are using high-
throughput technologies for transgene test-
ing in several model systems.
Example 17: Mendel Biotechnology has over-
expressed 1700 transcription factors in
Arabidopsis and identifed transcription factors
related to biomass production, seed yield and a
stay-green phenotype under drought stress
(Gutterson, 2005). With Monsanto, these genes
have been introduced into important cereal
crops (Monsanto, 2009a). CropDesign has
tested 1400 constructs in rice and identifed
genes that enhance seed yield and biomass
(e.g. SYT1 and STZ) (CropDesign, 2009).
Genetic Modifcation or Transgenic
Technologies
Genetic modifcation (GM) involves alter-
ation of an organisms genetic material (DNA
or RNA) involving:
1. Transferring genes between organisms.
2. Moving, deleting, modifying or multiply-
ing genes within an organism.
3. Modifying existing genes.
4. Te incorporation of newly constructed
genes into a new organism.
Example 18: GM techniques have been used to
develop male sterility for use in hybrid breeding,
cereals enriched in commercially valuable oils,
proteins and starches as well as resistance to
herbicides such as glyphosate (Roundup
) and
phosphinothricin (Liberty
, Basta
).
Transformation
Transformation of cereal crops such as rice
and barley is possible because of hyperviru-
lent Agrobacterium strains and technical
breakthroughs in the use of cell and plant
selectable markers. It was previously only
successful in dicotyledonous plants.
Example 19: The frst, but unsuccessful, trans-
formation of a major crop species was by direct
DNA injection into the shoot apical meristem of
maize seedlings (Coe and Sarkar, 1966). In
1984, the frst transgenic tobacco plants (Horsch
et al., 1984) used a natural gene vector system,
the Ti plasmid, of the crown gall-causing bac -
terium Agrobacterium tumefaciens (Zambryski,
1988).
Another transformation method, biolistics,
involves fring high-velocity DNA-coated
microprojectiles into plant cells and tissues.
Its disadvantages include higher copy
numbers of unstable transgenes and more
DNA rearrangements.
Both methods have generated commer-
cially grown transgenic plants.
Biotechnology in Agriculture 227
Plant viral vectors can also be used for
transformation or naked DNA can be directly
taken into protoplasts by treating with poly-
ethylene glycol, divalent cations (either Ca
2+
or Mg
2+
) or electroporation (Holzberg et al.,
2002).
The components of transformation vectors
Transgenes typically contain a gene sequence
encoding a marker used for transgenic plant
cell/tissue selection, a gene of interest and
promoters that drive expression in tissues
or cell layers of interest.
SELECTABLE MARKERS Antibiotic or herbi-
cide-resistant selectable marker genes are
used to identify successful vector incorpor-
ation into transformed cells. Most antibiotic
and herbicide selectable markers inactivate
metabolites (Table 12.2).
TRAT GENES Trait genes can include novel
gene(s) sequences, which may synthesize a
protein(s) responsible for metabolite
synthesis or inactivation.
Example 20: Transgenic Golden Rice is an
example of modifed metabolite biosynthesis.
-carotene (a pro-vitamin A carotenoid) is
increased using a phytoene synthase from
either daffodil (Narcissus pseudonarcissus) or
maize and a carotene desaturase (CrtI) from
the soil bacterium Erwinia uredovora (Paine et
al., 2005).
Te trait gene(s) of interest may be from an
unrelated species or may be a natural or
synthetic allelic variant of an endogenous
gene.
Example 21: Superior naturally occurring
HMW-GS alleles (Altpeter et al., 1996) and
synthetic hybrids (Blechl and Anderson, 1996)
have been used to generate transgenic wheat
lines, some of which also possess superior
bread-making qualities (Alvarez et al., 2001;
Barro et al., 2003; Blechl et al., 2007).
Portions of a trait gene can also be used to
induce post-transcriptional gene silencing
(PTGS). PTGS or RNA interference (RNAi) is
the sequence specifc degradation of RNA.
Both microRNAs (miRNAs) and small inter-
fering RNAs (siRNAs) are central to RNAi
and have been used to create transgenes
that, upon expression, generate double-
stranded RNA molecules, which are cleaved
by the enzyme Dicer and yield short frag-
ments of about 20 nucleotides. Te guide
strand can then base pair with the comple-
mentary mRNA sequence of the trait gene.
Trait gene mRNAs are then cleaved by the
RNAi-induced silencing complex (RISC)
rendering them inactive. Hairpin-induced
RNAi silencing has been demonstrated as an
efcient tool for functional gene character-
ization in several crop species (for example:
Wang et al., 2000; Travella et al., 2006).
For the purpose of PTGS, transgenes can
be constructed to express antisense RNAs
(aRNA), hairpin RNAs (hpRNA) and artif-
cial precursor miRNAs (amiRNA).
PROMOTERS Promoters are regions of DNA
that facilitate transcription of selectable
marker and trait genes. Te most commonly
used promoters in crop transformation
include Ubiquitin (Ubi), Actin (Act1) or a dual
enhanced caulifower mosaic virus (CaMV)
35S (35Sx2) promoter.
Table 12.2. Common selectable markers.
Marker Resistance conferred
Neomycin phosphotransferase II (nptII) Kanamycin
Hygromycin phosphotransferase (hpt) Hygromycin
5-Enolpyruvylshikimate-3-phosphate (EPSP) synthase Glyphosate
Phosphinothricin acetyltransferase (pat, bar) Phosphinothricin
228 R. Whitford et al.
Expressed sequence tag (EST) and micro-
array technologies are used to identify
promoters that meet specifc expression
requirements for a particular trait gene.
Trait gene-dependent expression require-
ments are particularly important to mini-
mize negative efects associated with trait
gene mis-expression.
Novel transactivation technologies such
as promoter tagging (Johnson et al., 2007)
can be used for promoter identifcation.
Chemically regulated promoter systems can
also be used to generate transgenics with
tightly regulated gene expression (Moore et
al., 2006).
Cisgenics
Cisgenes derived from the crop plant itself
or from a crossable species (Rommens et al.,
2004; Schouten et al., 2006; Conner et al.,
2007) can counter public concerns about
incorporating prokaryote DNA sequences
into crop species. Cisgenic plants are similar
to those bred by traditional introgression
and translocation breeding; they are faster
to generate than with traditional breeding
and can eliminate problems associated with
linkage drag. In time, cisgenics may be
accepted as an alternative to using prokary-
ote, vector-based systems.
Gene discovery
Gene discovery is the identifcation of gene
sequences, and variants, that contribute to a
trait or phenotype. It requires an under-
standing of the complex metabolic and
signal transduction pathways involved in a
traits expression. It involves the dissection,
and then manipulation, of fundamental
plant processes to improve crop plants. It
can be either targeted, starting with defn-
ing a trait of interest and then identifying
the controlling gene sequences, or non-
targeted, which is quite random.
Targeted gene discovery
MAP-BASED CLONNG Dense molecular genetic
maps for most crop species (Varshney et al.,
2004) have come from advances in molecu-
lar genetics and automation of the tech-
niques used to identify DNA sequence
variation. Te most common assays are for
SSRs or microsatellites and SNPs. Tey are
abundant and amenable to high-throughput
genotyping.
Example 22: Diversity Array Technology (DArT)
gained prominence because it could profle
genome-wide genetic variation without previous
sequence knowledge (Kilian et al., 2005).
Genetic maps are used for assigning traits of
interest to genomic loci and for map-based
cloning (MBC) where an interesting mutant
phenotype is identifed and then genetic fne
mapping occurs using a large number of
recombinant inbred lines (RILs), doubled
haploid, or F
2
progeny plants. Te genetic
map and markertrait associations are then
used for chromosome walking and landing,
with the help of large-insert DNA libraries
or physical maps to isolate the gene
(Azhaguvel et al., 2006).
Example 23: MBC is suited to the identifcation
of QTLs and has been used to identify genes
such as HKT, Sub1A, CBF, ALMT1 and Bot1,
which confer tolerance to salt, submergence,
freezing, aluminium and boron toxicity, respec-
tively (reviewed by Collins et al., 2008).
ASSOCATON MAPPNG LNKAGE DSEQULBRUM
Association mapping is based on linkage
disequilibrium (LD): the non-random associ
ation between markers, genes or QTLs in a
population. It takes advantage of events
that created genetic linkage in the relatively
distant past.
Example 24: Large structured breeding popula-
tions have been a valuable resource for associ-
ation mapping and have resulted in the
identifcation of markers for higher yield and
yield stability in barley (Kraakman et al., 2004),
as well as milling quality and kernal morphology
in wheat (Breseghello and Sorrells, 2006).
Biotechnology in Agriculture 229
For out-breeding species where LD extends
over very short distances, association
mapping is used to identify markers tightly
linked to agronomic traits. Tis can reduce
the time required for MBC of gene sequences
underlying the trait. Tis approach is not
suitable where genetic control of the trait is
complex or where there are confounding
factors that may afect trait expression.
Maturity and plant height can strongly
afect drought responses and association
mapping for drought tolerance using a
diverse germplasm collection is likely to only
reveal maturity and height loci.
COMPARATVE GENOMCS Comparison of
genetic maps indicates very good conserva-
tion in the order (colinearity) of molecular
markers and of QTLs for important agro-
nomic traits along the chromosomes within
diferent families of plants. Comparative
genomics has provided insight into plant
genome evolution: some of the major evolu-
tionary mechanisms during the past 5070
million years have been unravelled (Salse
and Feuillet, 2007).
Example 25: Recently, genetic and physical
maps have been integrated for plant families
with important domesticated crops, such as the
Poaceae (Devos, 2005), Fabaceae (Zhu et al.,
2005), Roseaceae (Dirlewanger et al., 2004),
Solanaceae (Mueller et al., 2005), Asteraceae
(Chapman et al., 2007) and Brassicaceae
(Schranz et al., 2007).
Evolutionary relationships have been estab-
lished between rice, Brachypodium and
members of the Triticeae. Isolation and
sequencing of large genomic DNA fragments
from diferent species has highlighted cross-
species gene-order conservation at the sub-
megabase level, that is micro-colinearity (for
example, Chen et al., 1997). In leguminous
species, gene order synteny has been estab-
lished between the model species Medicago
truncatula and Lotus japonicus and other
members of the Papilionoideae, including
soybean, broad bean, chickpea and clovers
(Varshney et al., 2009). Despite no local
micro-colinearity, good colinearity between
grass and legume genomes means that the
number of molecular markers in a targeted
region using restriction fragment length
polymorphism (RFLP) and EST probes may
be increased without additional molecular
markers being needed from the species of
interest (Feuillet and Keller, 2002).
Example 26: Colinearity has been used to iden-
tify gene sequences responsible for disease
resistance (e.g. Lrk, Rph7), development (e.g.
Vrn1, Ppd-H1) and quality (e.g. Ha, Glutenin)
(Salse and Feuillet, 2007). In legumes, compar-
ative mapping has helped to identify nodulation
and nitrogen fxation genes (Zhu et al., 2005).
ALLELE MNNG Allele mining is often used to
identify superior haplotypes of gene
sequence variants from wild or mutant
populations.
TILLING (Targeted Induced Local Lesions
IN Genomes) is a common way to discover
SNPs in induced mutant populations. It is a
high-throughput reverse genetic strategy
that is low in cost.
Example 27: TILLING populations have been
created for major crop species including maize,
rice, soybean, barley and wheat (Barkley and
Wang, 2008). Screening for natural variation
using this methodology is termed ecoTILLING.
The power of TILLING for hexaploid bread
wheat improvement was demonstrated by the
identifcation of 196 new alleles in the A and B
genome waxy genes (granule bound starch
synthase genes I, GBSS1) from a population of
1152 ethylmethane sulfonate (EMS) induced
mutant plants (Slade et al., 2005). Extending
this to tetraploid pasta wheat identifed 50 new
GBSS1 alleles from a population of only 768
individuals (Slade et al., 2005).
Non-targeted gene discovery
EST SEQUENCNG Gene sequences and varia-
tions can be directly obtained by randomly
sequencing complementary DNA (cDNA)
clone libraries yielding ESTs, a powerful tool
in the analysis of transcriptomes.
230 R. Whitford et al.
Example 28: Analysis of 580,000 wheat and
370,000 barley ESTs estimates the number of
unique genes to be about 122,000 (~40,000 per
homologous genome) and 50,000 for bread
wheat and barley, respectively (Stein, 2007). This
is comparable to the number of genes (~40,000)
predicted from the complete rice genome
sequence (IRGSP, 2009) and appears to be simi-
lar across many plant species.
Next Generation Sequencing Technologies
(i.e. Solexa and 454/FLX) make it possible to
mine transcriptomes of crop species for
which there is little genomics information.
Tis is rapidly contributing to the wealth of
EST resources (Varshney et al., 2009) which
are a source of sequence-level genetic vari-
ation and extensively used for functional
molecular marker development. EST-derived
SSR and SNP markers are now routinely
used in trait mapping and MAS. ESTs have
also been used to develop cDNA microarrays
used for transcript profling (Close et al.,
2004).
WHOLE GENOME OR GENE SPACE SEQUENCNG
Rice has the smallest cereal genome and was
the frst to be fully sequenced (Vij et al.,
2006). Te sequence has been used to local-
ize genes in other cereals by comparative
mapping (Bennetzen and Ma, 2003).
Te Arabidopsis genome sequence and
both the M. truncatula and the L. japonicus
genome sequences provided similar
resources for the Brassicaceae and
Papilionoideae, respectively (Schranz et al.,
2007; Young and Udvardi, 2009).
Growing evidence about sequence and
gene content variation between, and even
within, species means that species-specifc
genomic resources are needed (Wobus and
Sreenivasulu, 2006). ESTs partially fll this
gap.
Ordered physical maps are also being
generated from large insert-libraries (bacterial
artifcial chromosomes or BACs) for many of
these crops. Genetically anchored physical
maps are an important resource for MBC
strategies, as they will signifcantly reduce
the time required for candidate gene isola-
tion. Te National Center for Biotechnology
Information (NCBI) database lists genome
sequencing and analysis projects underway
for 128 species (NCBI, 2009) (Table 12.3).
Sequencing for grapevine and soybean has
also now been completed.
Current GM traits
GM crops are currently grown on 125 million
ha in 25 diferent countries (ISAAA, 2009)
and are largely based around herbicide and
pest resistance lines (Fig. 12.3).
Current pest-resistant GM crops ofer
signifcant value to producers because a large
reduction in the use of pesticides has occurred
and this has lowered production costs and
lessened environmental impact (Knox et al.,
2006). Reduced environmental impact
results from reduced energy consumption
required for pesticide manufacturing, trans-
port and on-farm application, and fewer
chemicals enter the environment. Te wide
use of herbicide tolerant crops in many parts
of the world has led to a major expansion of
minimum tillage production systems and
similarly, results in reduced on-farm fuel
consumption.
Many traits related to accommodating
climate change are still undergoing feld
evaluation but will appear in commercial
crops over the next few years. Among the
most advanced are several crops with
improved nitrogen-use efciency such as
those developed by Arcadia Biosciences
(Arcadia, 2009) and drought tolerance where
there have been extensive glasshouse and
feld trials (Bahieldin et al., 2005; Wang et
al., 2005; Hu et al., 2006; Nelson et al., 2007;
Rivero et al., 2007).
Table 12.3. Examples of sequencing projects.
Species Reference
Maize (MGSC, 2009)
Potato (PGSC, 2009)
Papaya (ASGPB, 2009)
Wheat (IWGSC, 2009)
Barley (IBSC, 2009)
Tomato (SGN, 2009)
Sorghum (DOE-JGI, 2009)
Biotechnology in Agriculture 231
On a precautionary note, glasshouse
performance and even some feld trial results
may not necessarily provide a reliable
assessment of the value of these genetic
modifcations to commercial performance in
the feld over multiple seasons and
environments (Passioura, 2006).
Capacity building
Signifcant international capacity building
has occurred in agricultural biotechnology
since it was identifed that biotechnology
could improve yield in food crops. Tis
capacity has comprised not only infrastruc-
ture and research capability but has included
a steady building of intangible assets such
as intellectual property (IP) portfolios and
germplasm. Capacity has been built to
develop genetically modifed organisms
(GMOs) and also to refne techniques used
in conventional plant breeding.
In the private sector, the promise of large
returns from agricultural biotechnology has
led to several large multinational seed
companies investing in signifcant infra-
structure and research capacity (Table 12.4).
Example 29: Monsanto has demonstrated that
there is a direct relationship between biotech-
nology research and development (R&D) spend-
ing and increases in gross proft (Monsanto,
2009b). By increasing R&D spending by 9% per
year since 2001, Monsanto has increased its
seed business gross proft by 24% a year
(Monsanto, 2009b). Other multinational
companies have made large investments in
people, infrastructure and germplasm needed
to deliver biotechnology. Germplasm acquired
during DuPonts amalgamation with Pioneer is
valued at US$975 million (SEC, 2008) among
its other intangible assets. In its last annual
report, as a result of its ongoing investment in
agricultural biotechnology, DuPont expected
that in 2009 its agriculture and nutrition division
would introduce 26 new soybean varieties and
96 new maize hybrids (SEC, 2008).
In the public sector, signifcant agricultural
biotechnology capacity has been developed in
many countries within universities, govern-
ment agricultural departments, special
research centres and so on. Various centres
and programmes have also been established
to assist the development of technologies for
the developing world.
Trait
C
o
m
m
e
r
c
i
a
l
i
z
e
d
G
M
v
a
r
i
e
t
i
e
s
(
%
)
0
5
10
15
20
25
30
35
40
Herbicide
tolerance
(HT)
Pest
resistance
(PR)
Stacked
HT & PR
Product
quality
Other
Fig. 12.3. United States Department of Agriculture (USDA)-approved commercialized GM varieties as of
May 2007, by trait (based on data from Oborne, 2009).
232 R. Whitford et al.
Example 30: The Consultative Group on
International Agricultural Research (CGIAR)
system alone provides over US$500 million to
8096 staff across 15 research centres and four
major research programmes the Challenge
Programs (CGIAR, 2007). Of this, US$19
million was invested in hard infrastructure, the
balance on intellectual capacity.
It is difcult to estimate the actual
amount invested by the public sector in
agricultural biotechnology but most
developed countries support large research
eforts. In the 2008 round of funding under
the National Science Foundations Plant
Genome Program, US$60 million was
awarded (NSF, 2008). Similar programmes
exist in most developed countries and total
investment from the public sector in plant
biotechnology research will be in the
hundreds of millions of dollars.
Technology Access
Te patent system grants monopoly rights
to patent owners so that they can exclude
others from practising patented technologies
for a period of time. Te quid pro quo is that
society is aforded free access to those
inventions upon the expiry of the patent.
Large international companies have
scrambled to gain market monopoly returns
by assembling large patent portfolios. Tese
portfolios not only include genetic tech-
nologies per se, but also so-called enabling
technologies such as trans formation methods,
selectable markers, promoters and so on. In
this area, 71% of the IP related to these
technologies is held by the private sector.
Monsanto and DuPont together hold 27% of
the agricultural biotechnology patents (Graf
et al., 2003). Tese large and complex IP
portfolios, and the use of overlapping groups
of patents, or patent thickets, have been
developed as a barrier to entry for
competitors. Te monopoly positions have
not only been built by developing IP within
these companies, but also by the strategic
acquisition of smaller companies with small,
but valuable, IP portfolios.
While this strategy appears to have
delivered above-average fnancial returns for
those companies, it may have had a negative
efect on the ability of publicly funded
scientists to conduct research using the
latest state of the art (Fig. 12.4). Some large
companies have been hesitant to provide
licences to their commercial know-how on
the basis that such licences may erode their
above average returns.
It has now become necessary for research
organizations to conduct extensive freedom
to operate searches and then if possible to
obtain the necessary licences so that they do
not infringe the patent rights of others.
Table 12.5 shows the IP rights attached to
various elements of the famous Golden
Rice product.
Table 12.4. Estimated 2006 R&D expenditures of relevance to
biotechnology by leading companies in each application (based on data from
Oborne, 2009).
Company (country)
Biotech R&D expenditure
(US$ millions)
Syngenta (Switzerland) 510
Monsanto (USA) 470
Bayer CropScience (Germany)
a
310
DuPont Pioneer (USA) 190
BASF (Germany) 170
LimaGrain (France) 85
KWS SAAT (Germany) 65
Dow Agrosciences (USA) 55
Total 1855
a
Bayer fgures are for 2007.
Biotechnology in Agriculture 233
Some countries have therefore legislated
research exemptions so that scientists may
access and use patented technologies for
research. In 2005, the Australian Advisory
Council on Intellectual Property recom
mended that the Australia Patent Act be
modifed to allow restricted experimental
use (ACIP, 2005). Tis recommendation
followed very limited experimental use
exemptions in the USA and more generous
exemptions in Europe. Such exemptions
vary widely in scope and there is little
harmonization across jurisdictions.
Delivery Pathways and Processes
MAS
MAS has enhanced conventional breeding
methods by providing greater fexibility and
new selection strategies than were previously
possible. Te delivery pathway for
bio technology has been facilitated by
training of a new generation of plant
breeders who have a thorough knowledge of
molecular biology, genetics and heritability.
Some of the key factors infuencing marker
application are listed in Table 12.6.
GM
From 1995 a new industry rapidly developed
to generate GM plants, but there have only
been a small number of successful exploit
ations. Large frms have commercialized
Obtain licence
or
Work around solutions
Infringe deliberately
(or unknowingly)
Avoid using technologies
Fig. 12.4. Intellectual property (IP) options for
scientists.
Table 12.5. Material Transfer Agreements (MTAs), licences, documents and agreements required for
Golden Rice (modifed from Kryder et al., 2000).
Component Source
Germplasm Rice lines used for transformation Taipei 309 from IRRI
Vector pGEM4 Promega
pBluescriptKS Stratagene
pCIB900 Ciba-Geigy (now Syngenta)
pKSP-1 Tom Okita, Washington State University
pUCET4 N. Misawa, Kirin Brewery Co.
pYPIET4 Clontech (now marketed through Life
Sciences)
Promoters CaMV 35S promoter Monsanto
GT-1 promoter Tom Okita, Washington State University
Terminators CaMV 35S terminator Monsanto
Selectable marker AphIV gene, hygromycin
phosphotransferase
Ciba-Geigy (now Syngenta)
Expression enhancement Pea Rubisco transit peptide N. Misawa, Kirin Brewery Co.
pPZP100 Pal Malinga, Rutgers University
Transformation process Electroporation apparatus Bio-Rad
Microprojectile bombardment
apparatus
Bio-Rad
Biolistic transformation DuPont
Trait gene Crt1 gene, phytoene desaturase N. Misawa, Kirin Brewery Co.
234 R. Whitford et al.
GM technologies mainly focusing on single
gene events conferring either herbicide or
pesticide resistance, selected because they
are of high commercial value, quick to
market and synergistic with chemical
businesses often owned by the same
companies. Many outcomes of more difcult
projects, such as conferring drought
tolerance, more efcient use of fertilizer,
resistance to salinity and so on, have yet to
be commercialized. Much of the gene
discovery work in these areas is occurring in
the public sector where public funding is
able to overcome the market failure issues
that arise from the extended time needed to
solve these difcult problems.
Te delivery pathway for GM technologies
is somewhat more complex than delivering
technologies via conventional breeding.
Identifying genes responsible for traits of
interest is in itself a long and costly process.
Many years of expensive research can elapse
before a traitgene relationship is discovered
and the gene is isolated. In the case of the
boron tolerance gene, Bot1, at least 4 years
of work was required before the gene was
discovered and patented (Sutton et al.,
2007).
After gene discovery, suitable plants must
be transformed with the gene of interest.
Te complex IP landscape in agricultural
biotechnology means that access must be
sought for the enabling technologies that
are used to create transgenic plants because,
as already mentioned, many of the enabling
technologies are patented. Generating GM
events means that vectors must be
constructed, often also using elements such
as promoters that are also patented (Fig.
12.5).
Transgenic plants are then subjected to
years of testing in glasshouses under
controlled and contained environments.
Monsantos product pipeline (see Table
12.7) describes just a 25% chance of
successfully delivering a technology once
that initial discovery work has been done.
Plants are then tested under feld
conditions at many sites, and usually over
several years, so that the full extent of the
plant improvements are understood and
validated. While initial work often occurs in
model plants that are easily transformable,
adapted germplasm must be selected that is
suitable for the target environment and
which must also be suitable for
transformation or, if not, then capable of
being backcrossed with material that has
been transformed.
Large multinational frms have resources
and expertise, access to complex patent
thickets, extensive access to germplasm and
Table 12.6. Factors related to effective delivery of marker technologies.
Factor Comments
Direct involvement of breeders in
defning targets and
germplasm
Molecular groups should act in a support capacity, challenging
breeders by questioning their methods and breeding strategies
Use cultivated germplasm pool
frst
For many crop species the level of understanding of variation and
the germplasm base is still poor and introgression of useful alleles
from landraces and wild relatives remains slow
Access suitable staff It remains diffcult to attract high-quality students and staff to
breeding-related programmes and to attract staff trained in
molecular techniques to breeding stations that are often in remote
locations
Outsource marker work High quality and cost-effective service labs are available but many
still believe that marker development and application is still a
research activity and is best carried out in-house
Use technology champions Success in marker application in the public sector is often driven by
a few individuals who had the energy to drive aggressive, and
often risky, new breeding strategies
Establish new generation of
breeders
Major advances in marker application are often driven by more
recently trained breeders
Biotechnology in Agriculture 235
well-developed pipelines for delivering
genetic technologies. It is for these reasons
that the only practical way of delivering new
GM technologies is for public sector organ-
izations to partner with such frms.
Regulation
GM organisms are subject to tight regulatory
approvals in countries where they are
developed and grown. Tese regulations
allow GM research only in suitably approved
containment facilities and by organizations
and staf who have the appropriate
qualifcations and experience.
For GM crops, feld evaluation is an
essential component of the development
and delivery process. Special approvals are
required for conducting such trials. In some
countries, the approval process is relatively
straightforward although the approval times
can range from several months to well over a
year and appear to be increasing. Tis means
that GM lines being evaluated are often not
the latest, or most suitable, for analysing
trait expression. In some jurisdictions,
notably in some European countries, the
costs of running a GM feld trial are
prohibitive and trials are frequently
destroyed by anti-GM lobby groups.
Full commercial release of a GM crop will
require full regulatory approval both in the
country of production and in all the
jurisdictions where the GM product may be
imported. Since 1995, the time to obtain
regulatory approval has increased markedly
in the USA and indeed no new crop obtained
approval in the USA in the 5 years from 2000
(Jafe, 2005).
Commercial seed companies have rarely
provided estimates of the costs to deregulate
a biotechnology crop. However, the costs are
many times higher than the regulatory costs
for a non-GM plant variety, which range
from US$5000 to US$11,000 (Oborne,
2009). Table 12.8 provides a summary of
some of the cost estimates.
Te international regulatory require-
ments are derived from the 1992 Rio
Declaration on Environment and Develop-
ment, Principle 15 where there are threats
of serious or irreversible damage, lack of
scientifc certainty shall not be used as a
reason for postponing cost-efective
measures to prevent environmental
degradation (UNEP, 1992). Tis requires
extensive evaluation and testing of any GM
crop.
Gene discovery
Access to IP
Construct vector
Transform
Validate in glasshouse
Validate in field
Advanced development
Pre-launch
Fig. 12.5. Technology development.
Table 12.7. Monsantos product pipeline (modifed from Monsanto, 2008).
Proof of concept
Early product
development
Advanced
development Pre-launch
Key activities Gene optimization
Crop transformation
Field evaluation
Large-scale
transformation
Trait development
Trait integration
Expanded feld
trials
Regulatory
submission
Seed bulk-up
Pre-regulatory data Regulatory data
generation
Pre-marketing
Average duration
Average
1224 months
25%
1224 months
50%
1224 months
75%
1236 months
90%
probability of
success
236 R. Whitford et al.
Te requirements for international
movement of a GM product are outlined in
the Cartagena Protocol on Biosafety (CBD,
2007) and Contribute to ensuring an
adequate level of protection in the feld of
the safe transfer, handling and use of living
modifed organisms . Tis agreement
prescribes a process for the transport of GM
products between countries known as the
Advanced Informed Agreement Procedure,
which requires the exporter to provide
detailed information to the importing
country. Te importing country must have a
competent national authority, which can
acknowledge receipt of information,
authorize shipment or give reasons for
rejection. Tis procedure only applies to the
frst movement of the GM product and is
not required if the GM plant is in transit, for
contained use or will go directly into food or
feed and will be rendered non-viable.
Governments are also able to notify the
Biosafety Clearing House of approval and
provide detailed information supporting
this (CBD, 2009). Tis provides a central
repository of regulatory and evaluation
information on GM crops and products.
As with regulations for GM research, feld
evaluation and commercial release, the regu-
lations covering the acceptance and use of
GM foods vary greatly between countries
with the most stringent in the European
Union. An extensive literature has been
developed around the safety assessment of
GM foods (FAO/WHO, 2000). Te complex-
ities associated with both the development
and the release of GM crops has meant that
most commercially grown GM crops have
been released by the private sector. However,
in some countries, notably China, strong
public sector and government support for
GM crops has led to the development and
release of several GM crops.
Conclusions
Biotechnology provides a range of new tools
and techniques that can provide increased
fexibility and efciency to plant breeders.
Some of the most promising targets are
described in Table 12.9.
Despite climate change, breeders will be
able to respond more rapidly to the require-
ments of cropping systems. Improvements
in conventional breeding are already being
realized by many programmes through the
application of molecular markers, the use of
doubled haploids and a greater understand-
ing of genetic diversity available for plant
improvement (see Reynolds et al., Chapter 5;
Braun et al., Chapter 7, this volume). Trough
climate change the environments being
targeted by breeders will also shift resulting
in changes in the disease and pest spectrum
being faced by farmers and in a direct reduc-
tion in the stability of yield through adverse
climate, such as increased frequency of
drought.
In addition to the direct impact of climate
change, the community is also expecting
agriculture to address production inefcien-
cies, such as high fuel, fertilizer, pesticide
and fungicide applications. In many cases,
these represent new targets for breeders but
they can be rapidly addressed through the
application of new molecular techniques.
Genetic engineering or modifcation
ofers a means to accelerate plant improve-
ment and to access diversity not available
within the crossable gene pool for many crop
species. Where farmers have access to GM
technology, extremely rapid adoption has
resulted in clear benefts to both the
pro ducer and the environment. However,
limited consumer acceptance of GM, partic-
ularly in Europe, has limited access to the
technology and led to high regulatory costs.
Table 12.8. Costs to deregulate a GM crop.
Cost estimate (US$) Source
4050 million Anecdotal from multinational companies
615 million for a herbicide-tolerant maize Kalaitzandonakes et al. (2006)
Up to 13.5 million Organisation for Economic Co-operation and
Development (OECD) report (Oborne, 2009)
B
i
o
t
e
c
h
n
o
l
o
g
y
i
n
A
g
r
i
c
u
l
t
u
r
e
2
3
7
Table 12.9. Towards 2030: the most promising biotech applications.
Climate change-related problem Application Recent developments Methods to ameliorate effects of climate change
Plants will be exposed to greater
extremes in conditions
Flowering time Gene sequences have been identifed that
determine fowering time for many crops.
Rapid fne tuning of crop phenology and life
cycle duration can maximize yield under
diverse climatic conditions
Match plant development to availability of
radiation, water and nutrient resources.
Minimize exposure to climatic extremes at
critical developmental stages (Craufurd and
Wheeler, 2009)
Water supply may become limited
or more variable
Drought tolerance and
yield under water-
limited conditions
Omic analyses have enabled better
understanding of regulatory networks
controlling plant responses to limited water
supply. Functional genomics has also enabled
the identifcation of genes regulating drought
responses
Tailor molecular drought response regulators to
engineer water-use effcient and drought-
tolerant crops. Modify drought tolerance
according to the time of onset of water
constraints
Higher temperatures are likely Heat tolerance Yields increase with temperature up to a critical
threshold and then decline sharply. Climate
change is predicted to increase the likelihood
of heat stress in many cropping regions
Identify physiological mechanisms and
associated molecular markers for application
in crop breeding programmes. Advances in
stress/trait dissection and rapid phenotyping
will enhance the understanding of the
physiological and genetic bases of heat
tolerance
Increasing soil salination from
coastal salt water inundation,
reduced rainfall and increased
irrigation
Salinity tolerance Identifcation of gene sequences and
quantitative trait loci controlling Na
+
exclusion and tissue tolerance
Select for salt tolerance using direct phenotyping
or molecular markers. Engineer cell-specifc
Na
+
exclusion using identifed gene sequences
as a more effcient strategy for salt-tolerant
crop development (Mller et al., 2009)
Fertilizer use and production emits
1.2% of the worlds greenhouse
gases (Wood and Cowie, 2004);
N fertilizer production consumes
ten times more energy than
other fertilizers (Lal, 2004)
Nutrient-use
effciency
Crops only recover around 50% of N supplied
(Eickhout et al., 2006). Identifcation of gene
sequences controlling N-use effciency has
led to more fertilizer-effcient rice (Shrawat et
al., 2008)
Transfer N-use effciency gene sequences to
other major crop species, including maize and
wheat, as a major target for commercial plant
breeding (Arcadia, 2009)
Disease infection and pest
infestations may increase
Disease/pest
resistance
The dependence of pest and disease dynamics
upon prevailing temperature and rainfall
profles makes future pest and disease
outbreaks notoriously diffcult to predict
(Gregory et al., 2009). Breeders may not be
able to keep pace with changes
Manipulate levels of existing anti-pathogen or
pest compounds (Delaunois et al., 2009;
Hexima, 2009) or, through using novel
biotechnology strategies (Nolke et al., 2004),
identify novel pathogens and monitoring
pathogen spread (Park, 2008)
238 R. Whitford et al.
Te high costs have virtually eliminated the
public sectors ability to deploy GM technol-
ogies and have restricted the types of traits
and the crops in use. However, there are
signs in several countries that community
attitudes to this technology are changing,
particularly with respect to the use of GM
crops to improve tolerance to environmental
stresses.
Te combination of new methods in plant
breeding, including MAS as well as the
opportunities provided by GM crops,
increase both the speed and the fexibility of
crop improvement. However, relatively few
breeding programmes have had the regula-
tory framework, skills, background informa-
tion and technology access needed to deploy
these methods. Tese limitations remain the
major impediment to the widespread use of
biotechnology and they will only be
addressed through strong international
collaboration and capacity building.
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CAB International 2010. Climate Change and Crop Production (ed. M.P. Reynolds) 245
13
Introduction
Te challenges that climate change presents
humanity require an unprecedented ability
to predict the responses of crops to environ-
ment and management. Geographic infor-
mation systems (GIS) and crop simulation
models are two powerful and highly comple-
mentary tools that are increasingly used for
such predictive analyses. Most notably, the
portions of the Fourth Assessment Report
(FAR) of the Intergovernmental Panel on
Climate Change (IPCC) (Easterling et al.,
2007) that dealt with agriculture made
extensive use of predictions from crop
models and in many cases, the regional
assessments that they summarized also
involved GIS (e.g. Tornton et al., 2006).
Te inherently spatial aspects of climate
and climate change make them readily amen-
able for incorporation into a GIS-based
analysis system. It is becoming ever more
apparent that climatic changes are occurring
non-uniformly across regions or agro-
ecosystems. GIS provides a useful tool to
capture this spatial heterogeneity and
provides powerful ways in which to visualize
and communicate the actual or potential
changes that are occurring. A GIS-based
framework has been the fundamental element
of several major assessments of the potential
impact of climate change on agriculture (e.g.
Tubiello et al., 2000; Fischer et al., 2002; Parry
et al., 2004).
Te fexibility of GIS-based analysis
systems to handle difering scenarios in
GIS and Crop Simulation
Modelling Applications in
Climate Change Research
David Hodson and Jeffrey White
Abstract
Te challenges that climate change presents to humanity require an unprecedented ability to predict
the responses of crops to environment and management. Geographic information systems (GIS) and
crop simulation models are two powerful and highly complementary tools that are increasingly used
for such predictive analyses. Te role of both technologies in predicting future situations centres
around extrapolation. For GIS, extrapolation from the past based on correlation in a very loose sense
plays an important role. For crop models, extrapolation based on how known processes respond to
factors of interest (i.e. simulation) is a key factor. GIS and crop models can be integrated, providing
predictions that combine the spatial perspective of GIS with the stronger representation of temporal
processes of simulation models. Tis chapter reviews the use of these two tools for predicting impacts
of climate change and examining options for adaptation. Increasingly, downscaled outputs from a
range of global general circulation models under difering future scenarios are used as key inputs for
both tools. Examples are given for major food crops and key agricultural zones, with a bias towards
tropical and subtropical regions. Consideration is also given to factors limiting efcient application of
the tools to climate change research. Both technologies will see increasing use in climate change
research and in applications of research in decision making. Credible studies of crop responses to
climate involve dealing with large sets of data and potentially millions of simulations, especially if
adaptation is considered. While the computational challenges are daunting, the greater challenge is
how to devise efcient protocols for selecting the most meaningful scenarios, interpreting the results
and summarizing outputs for decision makers.
246 D. Hodson and J. White
a rapid and efcient manner is another
important factor. Te suite of advanced
global general circulation models (GCMs)
that inform major assessments such as those
of the IPCC (e.g. Solomon et al., 2007), and
the accompanying emission scenarios devel-
oped for the IPCC assessments (IPCC, 2000)
form the basis of many climate change
assessments (e.g. Parry et al., 2004; Lobell et
al., 2008). Increasingly, the outputs of the
GCMs under difering emissions scenarios
are available in data formats suitable for
direct use in GIS-based systems (e.g. the
WorldClim data set (2009) see http://www.
worldclim.org/futdown.htm). Te avail-
ability of multiple GCM outputs, coupled to
GIS-based systems, has permitted increas-
ing opportunities for analysis of spatial
convergence or divergence of GCM outputs
at global or regional scales (Neelin et al.,
2006; Lobell et al., 2008).
Crop models integrate available informa-
tion on plant ecophysiology, soil chemistry,
agroclimatology and related felds, and simu-
late key processes thought to determine crop
performance in a given environment. For
climate change assessments, yield responses
for major crops are derived mainly from
applications of crop growth simulation
models coupled to global or regional climate
change models and run under a range of
emission scenarios. Coupling mainstream
crop simulation models such as ceres and
apsim to a suite of fve to ten widely accepted
advanced GCMs, for example the Hadley
Centres HadCM3 or CSIROs MK3, and
evaluation under the standard range of IPCC
emission scenarios has been a common
approach (e.g. Defra, 2004, 2005).
Meta-analysis of several such global simu-
lation studies as reported by the IPCC Tird
Assessment Report (TAR) (IPCC, 2001) and
supported by the IPCC FAR (2007) is, not
surprisingly, revealing diferences between
crops and regions, but several global trends
are apparent. With global warming, many
studies are now indicating an increasing
polarization between the high-latitude
developed countries and the low-latitude
developing regions (e.g. Parry et al., 2004).
Taking a major cereal crop like wheat as
example, slight increases in yields at mid- to
high latitudes are predicted if moderate
mean temperature increases (13C) occur.
However, further warming, even in temper-
ate regions, causes yields to decrease. In
subtropical and tropical regions, wheat is
often already near its limit of maximum
temperature tolerance, so small temperature
increases (12C) reduce yield. Outputs from
such simulation studies are providing useful
information to inform future decision-
making processes, although several uncer-
tainties still remain, for example the extent
and role of CO
2
fertilization efects (Long et
al., 2006; Tubiello et al., 2007).
Crop simulation models and GIS are vital
tools in predicting the impacts of climate
change in agricultural systems. Te two tools
are complementary and the role of both
technologies in predicting future situations
centres around extrapolation. For GIS,
extrapolation from the past based on correl-
ation in a very loose sense plays an import-
ant role. For crop models, extrapolation
based on how known processes respond to
factors of interest (i.e. simulation) is a key
factor, with the models often supported by
GIS.
Tis chapter reviews the use of these two
tools for predicting impacts of climate
change and examining options for adapta-
tion. GIS and crop models can be integrated,
providing predictions that combine the
spatial perspective of GIS with the stronger
representation of temporal processes of
simulation models.
Examples are given for major food crops
and key agricultural zones, with a bias
towards tropical and subtropical regions.
Consideration is also given to factors limit-
ing efcient application of the tools to
climate change research. Te focus is exclu-
sively on climate change and increased CO
2
,
but principles are similar for O
3
, N depos-
ition and other factors, which are often
included within global change.
Role and Applications of GIS
A GIS represents a computer-based system
for the management of geographically refer-
enced data that is, data that can be
GIS and Crop Simulation Modelling Applications 247
connected to a specifc location on the Earth
and mapped. Many defnitions of a GIS exist,
but one used by a major GIS software
company ESRI (Redlands, California) has
relevance in the context of this chapter:
GIS is a computer technology that uses a
geographic information system as an analytic
framework for managing and integrating
data; solving a problem; or understanding a
past, present, or future situation. GIS is,
therefore, about modelling and mapping the
world for better decision making.
Common tasks within a GIS include the input,
storage, manipulation, analysis and display
(often in the form of maps or graphs) of geo-
referenced data. Mapping is a key output of
any GIS, but it is certainly not the only func-
tionality. Common data inputs include data
in either vector or raster (gridded) formats.
Te latter are particularly useful for the repre-
sentation of continuous data (e.g. climatic
variables) and cell-by-cell modelling.
Globally, GIS is applied to disciplines
ranging from managing utility networks to
health, archaeology and ecology. Increasingly,
it is a common component of climate change
assessments. Te geographic aspect of GIS
makes it an interesting option for applica-
tion to agricultural problems and priority
setting because so many of the environ-
mental and socio-economic factors that
impact agriculture or agricultural research
vary greatly over regions (e.g. Benson, 1996).
Typical examples would include rainfall
patterns, soil variability, disease and pest
distribution, market locations, crop distri-
butions, land-use patterns and human
demographics (Table 13.1).
Historically, GIS has seen widespread use
for delineation of suitability zones and agro-
ecological zonation (e.g. Hartkamp et al.,
2001; Setimela et al., 2005). Te ability to
combine multi-thematic data based on
common geography has been an extremely
powerful tool. Common approaches to general
Table 13.1. Examples of typical application themes for GIS/spatial technologies.
Thematic area Comment Example reference
Rainfall/climate patterns Interpolated raster (gridded) surfaces
derived from meteorological station
data
Hijmans et al. (2005)
Soil variability Spatial variation of major soil types
and derived soil properties
Batjes (2009)
Disease and pest distribution Actual distributions and climatic
suitability zones
Sutherst et al. (1996), Sutherst
and Maywald (2005)
Market locations/accessibility Accessibility surfaces based on least
cost distance travel times
Uchida and Nelson (2009)
Crop distributions Spatial allocation of reported
agricultural census data into most
likely areas using land use and
suitability
Leff et al. (2004), You et al. (2009)
Land-use patterns Satellite-derived land-cover estimates
on varying spatial and temporal
scales
Bicheron et al. (2006)
Human demographics Gridded surfaces of human
population density
Budhendra et al. (2002), CIESIN,
Columbia University and CIAT
(2005)
Abiotic stresses Modelled spatial distributions of key
stresses, e.g. drought, heat
Thornton et al. (2006), Hodson
and White (2007)
Identifcation of wild species
collection sites/suitability
zones
Actual distributions and modelled
ecological niches for important wild
relatives of crop species
Jarvis et al. (2003)
Crop suitability zones and
agroecological zonation
Climate, soil and landform-based
agroecological zones for major
crops
Hartkamp et al. (2001), Setimela
et al. (2005)
248 D. Hodson and J. White
crop suitability mapping have included the
geographical overlay and intersection of key
factors such as optimal temperature and
moisture ranges, soil types and topographic
features. GIS is perfectly suited for undertak-
ing such analysis.
Similar approaches have been undertaken
to determine environmental niches in which
wild relatives of crops are most likely to
occur. Te example of the FloraMap and
Homologue tools developed at Centro
Internacional de Agricultura Tropical (CIAT)
(Jones and Gladkov, 2001; Jones et al., 2005)
typifes this approach. Climatic and environ-
mental conditions existing at known collec-
tion sites are used to derive a probabilistic
determination of extrapolated similarity
zones. Tis extrapolation, often based on
relatively sparse input data, has been used
to determine priority zones for future collec-
tion eforts of valuable genetic resources or
in situ conservation (Jarvis et al., 2003).
Both FloraMap and Homologue
output climate similarity probability maps
in GIS data formats.
Location-based climatic factors have also
formed the basis of zonations for targeting
germplasm of major food crops. Mega-
environment classifcations have been
defned by the International Maize and
Wheat Improvement Center (CIMMYT) for
both maize and wheat to delimit broadly
homogenous global production zones (Braun
et al., Chapter 7, this volume). Tey have
been used to assist with priority setting and
targeting of germplasm (Setimela et al.,
2005; Hodson and White, 2007). For wheat,
the extensive network of international
wheat trials was the foundation for mapping
mega-environments. GIS tools permitted
the extraction of climatic and edaphic data
from the trial sites and subsequent cluster
analysis determined quantitative limits for
separation of the major global environments
(Hodson and White, 2007). For maize a
similar approach was taken, with the climatic
and edaphic data extracted from trial site
locations being fundamental to the analysis.
In the case of maize, germplasm perform-
ance data from the trials was combined with
the environmental data and entered into a
genotype-by-environment (G E) analysis.
Te resulting mega-environment criteria
refected the major drivers of G E (Setimela
et al., 2005). For both maize and wheat, the
fnal mega-environments had clearly defned
quantitative climatic parameters as their
foundation, hence mapping of the spatial
distributions was a simple task.
Climate-based mapping of potential pest
and disease probability occurrence zones is
also relevant to the scope of this review. Tis
has been undertaken using very similar
approaches to those described for wild rela-
tives and crops. Te climex model devel-
oped by Sutherst and Maywald (1991)
combines climatic suitability (a growth
index) with stress indices to produce an
overall index of suitability for a given species
at a specifc location. Conditions under
which known distributions are found are
used to infer potential distributions in new
areas. Te model has been successfully
applied to a range of pest and disease species
(e.g. Sutherst et al., 1996; Sutherst and
Maywald, 2005). As in the case of
FloraMap, model outputs are displayed
in map form and exported in GIS data
formats.
Abiotic stresses, such as drought, have
also been assessed using GIS-based analyti-
cal approaches. Again climate is a key driver
and GIS captures the spatial variation that is
essential to interpretation in an agricultural
context. One example of an approach to
drought modelling was the failed season
approach described by Jones (see Tornton
et al., 2006) and applied to Africa. A water
balance model was used, coupled to derived
daily climate data for 30 years obtained from
the MarkSim weather generator (Jones
and Tornton, 2000). A season was deter-
mined to fail if an insufcient water balance
was maintained throughout the growing
season of a typical crop. Te fnal outputs
were mapped as a probability of failed
seasons at a 30 arc sec (approximately 1 km
2
grid) for the entire African continent.
Tese examples illustrate how GIS has
been the key technology applied to a range
of difering agroecological themes. Spatial
integration of multi-thematic data sets was
a common element, but so too was use of
climate data. Tis pivotal role of GIS in
GIS and Crop Simulation Modelling Applications 249
agroclimatic analysis is relevant whether the
analysis is based on current or historical
climate data or predicted future climate
data. Te increasing availability of outputs
from a range of GCMs under varying emis-
sion scenarios is permitting a range of
GIS-based assessments of the potential
characteristics of future crop production
zones, and associated abiotic and biotic
stresses. Several illustrative case studies will
be described in succeeding sections that
build upon the examples and themes already
outlined.
Role and Applications of Crop
Simulation Models
Crop simulation models use quantitative
descriptions of ecophysiological processes to
predict plant growth and development as
infuenced by environmental conditions and
crop management that are specifed for the
model as input data (Table 13.2). Many
models developed by a single researcher or
laboratory are used for a single purpose and
have a short life. Others evolve over time
and are similar to modern software pack-
ages. Among the longer lived models that
have seen widespread use in climate change
research are apsim (Keating et al., 2003), the
Cropping Systems Model (csm) series (Jones
et al., 2003; Hoogenboom et al., 2004),
CropSyst (Stockle et al., 2003) and epic
(Meinardus et al., 1998).
Te simplest models estimate daily
growth through conversion factors for inter-
cepted solar radiation to biomass, whereas
complex models may simulate growth at a
timescale of minutes and include routines to
simulate key biochemical pathways of photo-
synthesis. Hay and Porter (2006) provide a
general review of the physiological processes
described in models, and Tsuji et al. (1998)
describe multiple aspects of models, includ-
ing soil and weather processes and example
applications.
A typical model simulates assimilate
production by estimating gross photosyn-
thesis and then reducing the assimilate pool
through respiration and senescence. Te
resulting net pool is then allocated to
Table 13.2. Examples of data inputs required for a typical crop model that runs with daily time steps.
Variable Comments
Daily weather
Maximum and minimum air
temperatures
Affect almost all plant and atmospheric processes and are also used
to estimate soil temperatures
Solar radiation Key for establishing potentials for photosynthesis and
evapotranspiration. Data are often either unavailable or inaccurate
Precipitation Affects moisture levels in the soil profle and runoff
Dewpoint or vapour pressure
defcit
Affects potential evapotranspiration. Average relative humidity is often
reported but is a poor indicator of evaporative demand because of
confounding with temperature
Wind speed Affects potential evapotranspiration
Soil properties
Albedo Refectivity of soil to solar radiation. Affects soil temperature and
evaporation
Runoff characteristics Used to estimate what fraction of precipitation is lost to runoff
Infltration characteristics Used to estimate how moisture enters the profle, is distributed
through soil layers, or drains out of the profle
Initial water and nutrient levels Establishes soil conditions for germination and subsequent growth.
Preferably determined by soil horizons to the maximum depth of
root development
Crop management
Sowing rate Used to estimate initial stand of plants
Row spacing Used to estimate light interception by crop canopy
Fertilization Type, amount and date of application for any fertilizers
250 D. Hodson and J. White
diferent plant organs through partitioning
rules. Te rules assign priority to rapidly
growing tissues such as leaves, with onset of
reproductive growth representing a key
developmental switch. Priorities also shift in
order to satisfy the crop demand for water
and nutrients. If supplies are limiting, more
assimilate is allocated to root growth in order
to increase extraction from the soil. Tus,
under water or nutrient defcits, root growth
may be favoured over leaf, stem or reproduc-
tive growth. Furthermore, nutrients may be
mobilized from inactive tissues (e.g. older
leaves) to organs with high demand.
Te timing of key developmental stages
such as seedling emergence, end of main
stem leaf appearance, anthesis and physio-
logical maturity are simulated using proced-
ures that are analogous to the accumulation
of growing degree days (heat units). As
required for a given crop, however, the
procedures may consider vernalization and
photoperiod responses. Models for simulat-
ing root and tuber, forage and bioenergy
crops are similar to those for seed and grain
crops, but allocate assimilates to vegetative
storage organs (Singh et al., 1998).
Water and nutrient budgets are usually
modelled both for the plants and for the soil,
requiring descriptions of root growth
through the soil as well as the soil and atmos-
pheric processes that afect water and nutri-
ent dynamics.
Temperature responses
Te main efects of temperature are modelled
on assimilate production, phenology, soil
processes and evapotranspiration. Relatively
few models explicitly consider high tempera-
ture stresses causing abortion of reproductive
structures or irreversible damage to vegeta-
tive organs. For models that estimate daily
growth through a radiation use efciency
(RUE) approach, the potential RUE is adjusted
by a simple temperature function. In the
version of the ceres models implemented in
the csm series, these temperature functions
weight the daily maximum three times more
than the minimum, on the assumption that
daytime temperatures infuence growth more
than night-time temperatures. More complex
models such as those using the Farquhar
model may involve multiple temperature
responses that are evaluated at scales of
minutes, and the parameters are determined
by measuring component physiological
processes.
Te occurrence of stages such as fower-
ing and maturity is hastened by tempera-
ture, but interactions with vernalization (a
requirement for cold temperatures prior to
fowering) and day length can override the
basic efect of temperature on development.
Physical and chemical processes afecting
water and nutrient availability also respond
to temperature. Te net result is that the basic
temperature responses described by models
are more complex than one might expect.
Response to CO
2
In RUE-based models, the main efect of CO
2
is through a factor that scales RUE down-
wards or upwards, a key distinction being
whether the crop has a C
3
or C
4
photosyn-
thetic pathway. More complex models
combine descriptions of difusion of CO
2
into the leaves and of the biochemical
processes of photosynthesis.
Plants also respond to elevated CO
2
by
reducing stomatal conductance, so most
models also include an efect adjusting leaf
or canopy conductance or transpiration per
se (e.g. Tubiello and Ewert, 2002). In models
that simulate a complete energy balance,
reducing transpiration increases canopy
temperature. Tus, an indirect efect of
elevated CO
2
is to warm the plants, which
should further afect photosynthesis,
respiration and development.
Differences among species and cultivars
Qualitatively, the most important physio-
logical processes have proven to be similar
across crop species. Furthermore, soil and
atmosphere processes are largely species
independent. Tus, diferences among
species are simulated mainly through
changes in parameters rather than through
GIS and Crop Simulation Modelling Applications 251
fundamental diferences in physiology.
Exceptions include diferences between C
3
and C
4
photosynthetic mechanisms, the
nature of vernalization or photoperiod
responses and how these afect phenology,
and the ability of legumes to fx atmospheric
N. Morphological constraints are also
important, especially with regard to growth
of seeds, storage roots or other economically
important organs. Key parameters that
distinguish among species include response
curves for temperature and CO
2
, critical and
maximal levels of nutrients, factors for
sensitivity to water or nutrient defcits, and
parameters for potential growth of leaves,
stems, roots and seeds or fruits.
Parameters for diferences among culti-
vars can involve phenology, partitioning coef-
fcients and reference organ sizes (e.g.
maximal area of an individual leaf or mass of
a seed). Phenology requires consideration of
the relative duration of diferent phases, and
responses to vernalization (if present) and
photoperiod. Values of the parameters are
usually determined through iterative param-
eter adjustment and comparison with
observed data from feld trials (e.g. Piper et
al., 1996). Tis calibration process is problem-
atic because it requires that detailed sets of
accurate observations be available. Te error
inherent in data from feld studies makes it
difcult to discern whether diferences
between observed and simulated data are due
to incorrect parameter values or to errors in
the model per se. Various groups are explor-
ing how to use information from genetics or
genomics to parameterize cultivars more reli-
ably (e.g. White and Hoogenboom, 1996; Yin
et al., 2000; Messina et al., 2006).
Crop management
To simulate the growth of a crop, the model
must know how the crop is to be grown,
whether for a real world or hypothetical situ-
ation. Management information includes
the date and manner of planting, the culti-
var used, fertilization and irrigation prac-
tices, and for some crops, harvest practices
(Table 13.2). Tillage and residue manage-
ment may also be considered. Te informa-
tion either establishes the initial conditions
for the simulation or modifes aspects of the
environment, such as through addition of N
or water to the soil profle.
Basic application of crop models in
climate change research
Assuming an appropriate model is at hand
and a reference crop production scenario
exists, simulating the efects of climate
change mainly involves running the model
for the weather and CO
2
scenarios of inter-
est. For a single site or region, the scenarios
may be specifed as fxed (e.g. an increase in
daily mean temperature of 2C) or relative (a
20% decrease in daily precipitation). Tese
adjustments may be held constant over the
crop cycle or varied. Te choice depends on
the objectives and the source of the climate
change scenario. Because a season might be
unrepresentative of long-term trends, simu-
lations are usually run for 20 or more years.
Te requisite weather data may come from
historical records or from weather generator
software that reproduces the statistical
properties of historic conditions (e.g.
Mavromatis and Jones, 1998; Jones and
Tornton, 2003).
A single set of runs can be compared to
equivalent runs using unadjusted weather,
thus providing one estimate of the potential
impact of climate change on economic yield
or a diverse range of other traits. None the
less, such a comparison ignores the poten-
tial that producers will adapt their practices
to the changing environment. We examine
two hypothetical cases, one for soybean and
planting dates and one for maize and N
fertilizer response, to illustrate a few of the
issues that may be relevant. Both studies
assume an increase in CO
2
from 380 ppm
(the approximate level in 2005) to 580 ppm.
Soybean planting date
Crop response to planting date is readily
modelled to examine how warming might
afect the potential growing season. For
temperate climates, logical expectations are
that warming would allow earlier or later
252 D. Hodson and J. White
plantings, while elevated CO
2
should increase
growth and yield. However, warming accel-
erates development and causes earlier fow-
ering and maturity, which would reduce
growth, and at the higher temperatures in
summer months, growth might decline
further due to a decrease in photosynthesis
and increase in respiration.
For Gainesville, Florida (latitude 2938N;
elevation 10 m), the csm-cropgro-Soybean
model predicts that very early plantings result
in delayed fowering due to low temperatures,
and, as expected, warming reduces the delay
(Fig. 13.1a). By April, however, longer day
lengths begin to slow development for both
treatments. With an early May planting, the
warming regime is predicted to slow fower-
ing slightly due to supra-optimal tempera-
tures. Note that the model assumes no efect
of CO
2
on phenology.
Te yield responses suggest that the
benefcial efects of elevated CO
2
roughly
balance the detrimental efects of tempera-
ture up to early May, but subsequently,
65 (a)
(b)
55
45
35
0
1000
2000
3000
0
F
l
o
w
e
r
i
n
g
(
d
a
y
s
a
f
t
e
r
p
l
a
n
t
i
n
g
)
S
e
e
d
y
i
e
l
d
(
k
g
/
h
a
)
Planting (day of year)
Planting (day of year)
1 Feb 1 Apr 1 Jun 1 Aug 1 Oct
1 Feb 1 Apr 1 Jun 1 Aug 1 Oct
Historical temperature conditions
380 ppm/Historical temperatures
580 ppm/Historical temperatures
1.5/3.0C
380 ppm/1.5/3.0C
580 ppm/1.5/3.0C
Fig. 13.1. Simulated response of soybean to planting date (FebruarySeptember) at Gainesville, Florida.
(a) Flowering response under +1.5C daily maximum, +3.0C daily minimum air temperature versus
historical temperature conditions from 1988 to 2001. (b) Seed yield response under +380 ppm CO
2
or
+580 ppm CO
2
and +1.5C daily maximum, +3.0C daily minimum air temperature versus +380 ppm CO
2
or +580 ppm CO
2
with historical temperatures from 1988 to 2001. Simulations are from CSM-CROPGRO-
SOYBEAN for cultivar Bragg with irrigations applied as needed to avoid water defcit.
GIS and Crop Simulation Modelling Applications 253
elevated CO
2
provides a small but consistent
beneft equivalent to 510% of the yield
expected for historical conditions (Fig.
13.1b). For plantings around 1 April, addi-
tional yield beneft might be obtained by
substituting a later-fowering cultivar.
Maize response to warming,
elevated CO
2
and N
Maize crop growth was simulated for 25-year
periods at Palmira, Colombia, an equatorial
location (latitude 329N; elevation 965 m)
with a mean annual temperature of 25C. A
September planting date was used, corres-
ponding to the onset of the rainy season.
Te crop was assumed to be rainfed, fertil-
ized at 50, 100 or 200 kg N/ha, and other-
wise well managed.
Seed yield declines with increasing
temperature for the 200 kg/ha N at ambient
(380 ppm) CO
2
(Fig. 13.2a) and elevated CO
2
(Fig. 13.2b), but not at the other two N levels.
Warmer temperatures promote early fower-
ing (Fig. 13.2c), so a portion of the tempera-
ture efect on yield relates to the shorter
growth duration (Fig. 13.2d). One interpret-
ation of the response to N is that at lower N
levels, yield is limited by N and not assimilate
production. Alternatively, assumptions about
how to model interacting temperature and N
stresses in the csm-ceres-Maize model may
merit review.
Coupling GIS to crop models
GIS and simulation models complement each
other for data management, analysis and
presentation. Simulation models have
traditionally been used on a site-specifc
basis, but the coupling to GIS is appealing
because it permits the possibility for simul-
taneous investigation of spatial and temporal
8000
6000
4000
2000
50 100 200
8000
6000
4000
2000
0
70
66
62
58
54
0
0
Temperature increase (C)
Temperature increase (C)
1 2 3 4 5 6
0 1 2 3 4 5 6 54 58 62 66 70
50 100 200
0
Temperature increase (C)
1 2 3 4 5 6
8000
6000
4000
2000
0
S
e
e
d
y
i
e
l
d
(
k
g
/
h
a
)
F
l
o
w
e
r
i
n
g
(
d
a
y
s
a
f
t
e
r
p
l
a
n
t
i
n
g
)
(a)
S
e
e
d
y
i
e
l
d
(
k
g
/
h
a
)
S
e
e
d
y
i
e
l
d
(
k
g
/
h
a
)
(b)
(c) (d)
CO
2
= 380 ppm
CO
2
= 380 ppm
CO
2
= 580 ppm
N (kg/ha): N (kg/ha):
50 100 200
Flowering (days after planting)
N (kg/ha):
Fig. 13.2. Simulated response of maize to 50, 100 or 200 kg/ha N fertilization at Palmira, Colombia under
temperature increases over historical conditions of +0.5C to +5.5C from 1978 to 1997. (a) Seed yield
response under +380 ppm CO
2
. (b) Seed yield response under 580 ppm CO
2
. (c) Days to fowering
(response same for all N and CO
2
levels). (d) Seed yield response versus days to fowering under +380
ppm CO
2
. Simulations are from CSM-CERES-MAZE for cultivar Cargill 111S assuming rainfed conditions.
254 D. Hodson and J. White
phenomena. Visualization of model summary
outputs, for example yield response, via a
GIS also adds an extra dimension. As a result,
there has been a rapid growth in the number
of applications interfacing GIS and simula-
tion models since the late 1980s (Hartkamp
et al., 1999). Multiple examples now exist of
crop models, typifed by the Decision Support
System for Agrotechnology Transfer (dssat)
family, and linked to GIS at a range of spatial
scales from feld to region (see summary
table in Hartkamp et al., 1999). Simulations
run over large geographical regions extend
the model outputs to areas that have not
been validated, so serve more as a sensitivity
analysis for the model rather than a precise
calculation. However, such assessments do
permit the possibility for the evaluation of
multiple scenarios in relative terms within a
spatial framework. Te HarvestChoice
project (HarvestChoice, 2009a) is taking
such an approach, attempting to simulate
yield potential of major crops on a continent-
wide basis under a range of difering techno-
logical scenarios (see HarvestChoice, 2009b).
Availability of highly disaggregated data sets,
both spatial and temporal, is fundamental to
this approach, and although progress is being
made, several challenges still remain.
Case Studies of Applications of GIS
and Modelling to Climate Change
Te application of GIS-based systems to agro-
climatic analysis under current climate condi-
tions has already been outlined. Te
availability of a range of GCM outputs run
under a suite of emission scenarios is now
permitting similar approaches for potential
future climates. With any such approaches it
should always be borne in mind that outputs
from the GCMs are not precise and variation
occurs between diferent models and scenar-
ios. In addition, for agricultural assessments
downscaled GCM results are usually required
and this introduces another set of uncer-
tainty. Despite these caveats, the results of
such studies can provide useful indications of
the potential magnitude of change and the
spatial variation that may occur. Selected
examples are given below in order to illustrate
the range of approaches being undertaken.
Climate change and crop wild relatives
(genetic diversity)
Tools such as FloraMap and Homologue
have provided a useful means by which envir-
onmental niches and priority areas for wild
relative diversity can be identifed. Incorpor-
ation of future climate data into such tools is
providing indications on how the environ-
ments supporting wild relatives might
change. Using FloraMap with HadCM3
model data, Jones and Beebe (2001) looked
at predicted wild bean environments in
Central America in 2055. Teir conclusion
was striking: in fve out of the seven countries
studied, the results indicated the virtual
disappearance of suitable wild bean habitat
by 2055. Jarvis et al. (2001) used a similar
approach for wild Arachis species (the closest
relatives to cultivated groundnut) in South
America. Again the predicted scenarios for
2055 were striking: 12 out of 17 species were
predicted to go extinct and four of the remain-
ing fve likely to be dangerously threatened. A
comparative study of wild relatives of ground-
nut (Arachis), potato (Solanum) and cowpea
(Vigna) under future 2055 climate scenarios
reported similar results: high extinction rates,
decreased range sizes and increased fragmen-
tation of environments (Jarvis et al., 2008).
Such analyses have raised awareness of the
potential threat posed to wild relatives and
the subsequent loss of important genetic
diversity. Use of GIS has allowed graphic visu-
alization of the decline in suitable environ-
ments, highlighting where the major efects
might occur and providing a quantitative
assessment of fragmentation patterns.
Shifting abiotic and biotic stress
distribution
Te previously described mega-environment
concept used by CIMMYT captures
crop-stress related information. Heat stress
is an important yield-limiting factor for
wheat and this is captured in one of the
mega-environment defnitions (ME5).
GIS and Crop Simulation Modelling Applications 255
Redefn ition of the mega-environments
based on future climate data derived from
the ccm3 model (Govindasamy et al., 2003),
indicated substantial potential expansion of
these lower potential heat-stressed environ-
ments in South Asia by 2050 (Hodson and
White, 2007 see Fig. 13.3). Subsequent
incorporation of additional GCM data for
2020 (from HadCM3, CSIRO and CCCMA,
the Canadian Centre for Climate Modelling
and Analysis) also indicated a similar
considerable expansion of heat-stressed
wheat production environments.
Drought stress is another major concern
under climate change. Te failed season
model previously described provides a
framework for looking at future scenarios.
Using the HadCM3 A1 scenario for 2050,
Tornton et al. (2006) illustrated the poten-
tial shifts in frequencies of failed seasons
within sub-Saharan Africa. Results obtained
indicated a quite dramatic increase in the
probability of failed seasons across the agri-
cultural regions of Africa. Embedding the
model within a GIS environment permitted
clear visualization of the shifting spatial
distributions.
Changes in the distributions, species
composition and timing of occurrence of
agricultural pests and diseases are other
factors that will undoubtedly respond to
global change, but as a result of complex
dynamics between hosts and pests and large
variation in pest response to climatic condi-
tions and CO
2
levels, trends are difcult to
predict. In broad terms, warmer more humid
conditions usually favour insect pests and
diseases. Models such as climex provide
opportunities to determine suitability indi-
ces for particular species under future
climate scenarios (e.g. Sutherst et al., 2000).
Maize in Africa and Latin America
Jones and Tornton (2003) used csm-ceres-
Maize to examine impacts of climate change
on maize production in Africa and Latin
America to 2055. Using GIS, they excluded
non-maize regions and assigned soil data to
each pixel associated with weather data. Te
simulations considered four maize cultivars
varying in growth duration, and planting
dates were assigned based on mean onset of
the growing season. Only 50 kg N/ha was
applied so that results would correspond to
low-input, smallholder farming. Te results
suggested that climate change would reduce
yields by an average of 10%, but with import-
ant regional variation, especially in moun-
tainous areas.
Rice in Asia
A common concern in climate change stud-
ies is how sensitive projected impacts are to
projections for increased greenhouse gases
and to the GCM used. Masutomi et al. (2009)
compared projections based on difering
Special Report on Emissions Scenarios
(SRES) as used in 1418 GCMs, using rice
production in Asia as a test case. In the
2020s, all scenarios agreed that the yield-
reducing efects of climate would be large
enough to ofset possible benefts from
elevated CO
2
. Yield variability also increased
with rising CO
2
. Overall, the results
confrmed that while estimated impacts
varied depending on the SRES and GCM,
trends were consistent in showing that
production will be likely to decrease while
yield uncertainty increases.
Low-cost adaptation strategies for rainfed
and irrigated production in the
Midwestern USA
Easterling et al. (1992) examined adaptation
options with notable detail, considering
planting dates, N levels, and the possibility
of introducing a fallow. Teir paper also
stands out because potential adaptations
were selected based on input from experts.
Of 21 potential changes, however, only ten
could be simulated with the epic model.
Earlier planting, longer-season cultivars and
furrow dyking would reduce the impacts of
warming. Beyond adaptations for single crop
species, of course, one can compare how
diferent crops or crop sequences respond to
climate change (ONeal et al., 2005; Tomson
et al., 2006).
256 D. Hodson and J. White
Current
Current ME5
Current ME1
ME5 sites
ME1 sites
Future (2050)
Future (2050) ME1
Future (2050) ME1
Fig. 13.3. Comparison of relative distribution of irrigated spring wheat mega-environments (MEs) in
South Asia. ME1 is for favourable climatic conditions, and ME5 is for regions where heat stress is
expected. (a) MEs under current climatic conditions. (b) MEs for a 2050 scenario (2 CO
2
, CCM3 model;
Govindasamy et al., 2003). From Hodson and White (2007) reprinted with permission from Cambridge
University Press.
(a)
(b)
GIS and Crop Simulation Modelling Applications 257
Yield loss due to rice blast and warming
in Asia
Most simulation studies focus on crop
response to abiotic factors. Te study of Luo
et al. (1998) is one of the few cases where a
disease model, for rice blast, was coupled to a
crop model, ceres-Rice, to assess potential
impact of global warming. Tests were run for
30 years of generated weather data from 53
locations in fve countries. Yield impacts
varied with region. Blast is favoured by moist
conditions with moderate temperatures, so
impacts were greater in cooler rice producing
regions.
Knowledge, Data, Technology and
Intellectual Constraints
Te accuracy of crop models is constrained
by uncertainty over physiological processes
related to climate change. Tis includes
efects of CO
2
and temperature on photo-
synthesis (Crafts-Brandner and Salvucci,
2004) and net crop responses (Long et al.,
2006; Tubiello et al., 2007). Tere also is
evidence that CO
2
afects crop growth and
development through mechanisms besides
carbon fxation and transpiration. Elevated
CO
2
can either accelerate or slow develop-
ment, depending on the plant species (Reekie
et al., 1994; Ellis et al., 1995) and afect plant
morphology (Pritchard et al., 1999).
Ignoring whether data for CO
2
and
climate change scenarios are accurate (see
Jarvis, Chapter 2, this volume), basic avail-
ability and accuracy of data required for GIS
and modelling still pose major constraints.
Data limitations exist in several key areas.
Soils, crop distributions, land cover and
pest/disease distributions would all be good
examples. Crop distribution data sets are
inaccurate and incomplete even for major
crops at the global to regional scale. Te
combination of crop survey and census data
with remote sensing data, to produce grid
cell maps with crops allocated into the most
suitable areas, is a promising approach (Lef
et al., 2004; You and Wood, 2006; You et al.,
2009). However, poor quality inputs often
limit the utility of outputs in certain areas.
Tese and other data constraints imply that
future change scenarios may often be based
on imperfect current base scenarios. For
simulation models, the list of model inputs
in Table 13.2 indicates the dimensions of the
task. To accurately describe any production
situation, one needs information on manage-
ment. Ideally, the information should be
specifed as decision rules, such as for how a
producer decides when to plant rather than
an average planting date.
Standardized formats exist to describe
feld experiments (Hunt et al., 2001), and
integrated crop information systems ofer
the potential of linking management infor-
mation with crop genetics (e.g. McLaren et
al., 2005). Remote sensing may provide data
for crop distributions, yields and production
cycles (e.g. Lobell et al., 2003) as well as
facilitate high-resolution characterization of
soil and weather conditions (e.g. Minasny et
al., 2008; NASA, 2009).
Development of models and associated
software tools remains a largely individual-
istic process. Hundreds of models have been
programmed, but few have survived past
their initial publication. Modularization of
model components, discussed since at least
1985 (Reynolds and Acock, 1985), should
allow researchers to interchange compo-
nents and focus on science rather than
programming. However, there has been
minimal progress in establishing modelling
frameworks for modules where scientists
can readily test hypotheses about specifc
processes. More recently, computer scien-
tists have argued for use of the Unifed
Modelling Language (UML) as a way of
separating specifc scientifc hypotheses
from actual coding of software (Papajorgji,
2005).
Credible studies of crop responses to
climate involve dealing with large sets of
data and potentially millions of simulations,
especially if adaptation is considered. While
the computational challenges are daunting,
the greater challenge is how to devise ef-
cient protocols for selecting the most mean-
ingful scenarios, interpreting the results,
and summarizing outputs for non-
specialists . GIS-based mapping has special
value for communicating complex data, and
use in climate change might be enhanced
258 D. Hodson and J. White
through animation or dynamic user naviga-
tion interfaces.
Conclusions
GIS and crop simulation modelling will see
increasing use in climate change research
and in applications of research in decision
making. Maps are especially valuable for
allowing people to understand how climate
change impacts, as well as possible adapta-
tions vary, across the landscape.
Examples highlighted in this review illus-
trate how the combination of GIS and crop
models may assist with policy and breeding
decisions in relation to climate change.
Knowledge surrounding the potential shifts
of abiotic and biotic stresses can help guide
prioritization and targeting of key traits
within crop breeding programmes.
Increasingly, options exist to undertake
analysis under a range of future climate
scenarios that incorporate data from a range
of sophisticated GCMs. Such an approach
can lead to probabilistic outputs that can be
used to guide decisions regarding the likely
importance of specifc traits in diferent
geographic regions in the future. In combin-
ation with secondary data sets (e.g. crop
distributions and demographic data) this
can provide useful indicators regarding likely
focus areas for important traits (e.g. drought
and heat stress). Valuable information,
particularly from crop models, may also be
obtained on the potential value of specifc
adaptation mechanisms either in terms of
phenology or crop management.
Similarly, for decisions relating to the
conservation of plant genetic diversity and
plant genetic resources, outputs from a GIS/
modelling-based approach can provide
useful insights. Te case studies highlighted
here illustrate how priority regions, either
for in situ conservation of important wild
relatives or for prioritized collection eforts
for ex situ conservation, can be identifed. In
both the conservation of plant genetic
resources and the priority setting of breed-
ing traits the lead time to obtain the desired
results (e.g. a new variety or adequate
protection of a priority region) can be
considerable. Te application of GIS/model-
ling technology within a future climate
framework as outlined in this review is one
way that can guide decision making on an
appropriate time frame.
Limitations of the two technologies per
se relate to our incomplete knowledge of
physiological processes, the availability and
accuracy of data, and implementation of the
tools through software systems. Both tech-
nologies may provide useful insights for
future decision making, but it is unlikely
that they will capture in totality the full
complexity and unpredictability of a rapidly
changing climate.
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14
Introduction
Te urgent need to increase grain produc-
tion presents a serious challenge to agricul-
tural systems globally and locally; the
increase must come from raising grain yield
per unit area, given that the degree to which
the area of cultivated land can be expanded
is very limited. Te Green Revolution
enhanced overall agricultural productivity in
many areas of the world by generating
improved wheat varieties with high yield
potential under optimal high-input environ-
ments. However, low-input and less favour-
able environments have poor agroclimatic
potential and are highly afected by biotic
and abiotic stresses that show marked
climatic fuctuations from year to year. In
these less favourable environments, the
plant breeding approach should be diferent
from those used in more favourable high-
input environments. Furthermore, in the
near future many favourable environments
may become less favourable (in terms of soil
fertility and general climatic conditions) and
be plagued by biotic and abiotic stresses due
to extreme climate change. Climate change
is due to many factors such as rising global
mean temperatures, increased intensity and
frequency of storms, drought and fooding,
weather extremes, and altered hydrological
cycles and precipitation patterns. Annual
crop production will be greatly afected by
increases in mean temperature throughout
Statistical Models for Studying
and Understanding Genotype
Environment Interaction in an
Era of Climate Change and
Increased Genetic Information
Jos Crossa, Juan Burgueo and Mateo Vargas
Abstract
Annual crop production will be greatly afected by increases in mean temperature and climate change,
which will be likely to reduce agricultural production and decrease food availability. Plant breeding
will play an important role in developing more sustainable lines and varieties for less favourable
environments that will be subjected to extreme changes in biotic and abiotic stresses. Breeding
cultivars with enhanced tolerance to heat, moisture stress and salinity is essential for long-term
adaptation response to climate change. Multi-environment trials (METs) play a paramount role in
breeding cultivars for general and specifc adaptation and yield stability, studying genotype
environment (GE) interaction, and predicting the performance of new cultivars in future years and
new locations. METs produce a vast amount of useful data, including not only phenotypic
measurements of cultivars evaluated in diferent environments but also climatic and soil data as well
as molecular markers representing genetic data. Appropriate statistical models and analyses used to
study response patterns of genotypes and their molecular marker attributes across diferent
environments undergoing varying climatic changes will be of paramount importance for developing
sustainable and stable cultivars that are resistant/tolerant to diverse biotic and abiotic stresses. In
this chapter, we explain the theoretical basis of several statistical models and their application for
explaining the climatic and genetic causes of GE interaction.
264 J. Crossa et al.
this century, and climate change will be
likely to reduce agricultural production and
decrease food availability (Lobell et al.,
2005).
Plant breeding will play a paramount role
in developing more sustainable farming
systems in less favourable environments
subject to extreme biotic and abiotic stresses
(see Chapters 48, this volume). Developing
cultivars with enhanced tolerance to heat
and moisture stress and salinity is essential
to a long-term adaptation response to
climate change. In developing crops for the
21st century, breeders must keep in mind
that production environments will be more
variable and more stressful, yearly climate
variation will be greater, and feld sites and
test environments will essentially be rapidly
moving targets. Appropriate breeding strat-
egies will ensure the development: (i) in the
long term, of improved varieties, lines and
hybrids with adaptation to less favourable
environments and high yield stability; and
(ii) in the short term, of appropriate varieties ,
lines and hybrids to meet local farmers
needs. Breeding strategies are based mainly
on breeders in-depth knowledge of their
germplasm in general and of how genotypes
will respond under diferent environmental
conditions.
Regardless of the breeding strategy used,
in any breeding programme multi-
environment trials (METs) are essential for
assessing varietal adaptation and stability,
and for studying and understanding geno-
type environment (GE) interaction. For
example, signifcant progress has been made
in maize grain yield under drought stress by
selecting for component traits such as kernel
set, rapid silking and reduced barrenness in
METs. GE interaction refers to the diferen-
tial response of a set of plant materials (such
as lines, open-pollinated varieties or popula-
tions, etc., referred to as genotypes) when
evaluated in a set of environments charac-
terized by certain soil, climatic, pest, disease
and management conditions (referred to as
environments) in a given location and year.
In general, GE may be due to heterogeneity
of within-environment variance (HV) or
scale changes, or to crossover interaction
(COI) or changes in rank of genotypes in
diferent environments. In agricultural
production, the most important GE is that
due to COI.
Conventional breeding in conjunction
with marker assisted selection (MAS) may
bring about signifcant and predictable
incremental improvements in the drought
tolerance of new maize lines and hybrids
(Bnziger and Araus, 2007). Likewise, the
genetic dissection of maize performance in
drought-prone environments has greatly
benefted from the use of DNA markers
(Ribaut and Ragot, 2007). Te use of MAS in
plant breeding has increased consistently
since 1980, and molecular markers are now
considered a valuable breeding tool.
Advances in high-throughput genotyping
have reduced the cost of using molecular
markers, and their abundance and low cost
have led to selection based only on molecu-
lar markers (called marker-assisted recur-
rent selection, or MARS). Applying MARS
for one cycle based on phenotypic and
marker scores followed by two or three cycles
of selection based solely on marker score
information has increased genetic gains.
Genome-wide dense marker maps are now
available for many plant and animal species,
and genome-wide selection has become an
interesting option for increasing genetic
gains in diferent crops and animals
(Bernardo and Yu, 2007).
Important challenges are how: (i) marker
information should be incorporated into
statistical models that could be useful for
predicting genetic values in animal and plant
breeding programmes, or for predicting
diseases; (ii) the large number of candidate
genes known to have specifc trait efects
could be used in a practical breeding
programme; (iii) the large number of envir-
onmental variables and pests afecting
genotypes in METs could be used to better
predict genotypic and phenotypic perform-
ance so that the best genotypes are selected
as parents for the next generation; and (iv)
the powerful computer algorithms used in
crop modelling and simulation methods
could help breeders to better achieve their
goals.
Te massive accumulation of genetic and
environmental data confrms the urgent
Statistical Models for GE Interaction 265
need for suitable and efcient bioinforma-
tics, biometrical and statistical methods to
assess and incorporate GE studies into
conventional as well as MARS and genome-
wide selection breeding schemes for less
favourable environments. Te objective of
this chapter is to describe the theory and
practical applications of statistical models
and methods normally used for studying
and understanding GE and how they can be
applied in combination with molecular
markers in plant breeding.
Phenotypic Values, Genotypic Values and
Environments
Before describing statistical models for
studying the response of genotypes under
diferent environmental conditions, we
should explain that phenotypic (observed)
values are a function of genes that produce
genotypic (unobserved) values under certain
environmental conditions. Tis is clearly
explained by Bernardo (2002) for modelling
the phenotypic value of the kth individual
having a genotype A
l
A
m
(locus A has two
alleles , lth and mth), which is in turn afected
by a non-genetic component e .
lmk
Ten, the
phenotypic value will be P genetic =
lmk
non-genetic G e + = +
lm lmk
or P g = +
lmk lm
e +
lmk
(for the deviation from the popula-
tion mean, , of g G =
lm lm
) assuming
the genotypic value g
lm
and the non-genetic
e
lmk
values are uncorrelated. In general,
genotypic values include additive, and domi-
nance within locus and all types of epistatic
efects between loci. Te expected value of
P
lmk
for all individuals with genotype A
l
A
m
is
equal to the genotypic value g
lm
plus the
expectation of the non-genetic efects e .
lmk
Under the assumption that the expectation
of e
lmk
is equal to zero, then the expected
value of P g = +
lmk lm
and the expected value
of P
lmk
across all genotypes (and not only
genotype A
l
A
m
) is (implying that the
expected value of g
lm
is, in fact, zero). Tis
two-allele locus model can be extended to
any number of loci.
Although genotypic values cannot be
measured directly, they are estimated based
on phenotypic values and environmental
efects. Tis is the main reason why breeding
programmes need to have not only a clear
set of genotypes to be tested but also a clear
set of target environments where those
genotypes should be tested. Terefore, in
METs, just as genotypic values (estimated
based on phenotypic values) depend on the
environments in which the genotypes are
grown and the trait measured, so environ-
mental values depend on the genotypes
grown in those environments. In most
METs, the genotypic values g
lm
for diferent
genotypes are diferent in diferent environ-
ments; this constitutes GE.
The Basic Two-way Fixed-effect Linear
Model
Early approaches to GE analyses included
the conventional fxed-efect two-way model
with sum to zero constraints running over
indices. Te empirical response y
ijr
of the ith
genotype (i = 1, 2, , I) in the jth environ-
ment (j = 1, 2, , J) with r replications in
each of the I J cells is expressed as:
y ( ) e = + + + +
ijr i j ij ijr
(14.1)
where is the grand mean (over all geno-
types and environments),
i
is the additive
efect of the ith genotype,
j
is the additive
efect of the jth environment, ( )
ij
is the
non-additivity interaction (GE) of the ith
genotype in the jth environment (forming
matrix Z), and e
ijr
is the within-environment
error associated with the ith genotype in the
jth environment and the rth replicate.
Te phenotypic value averaged across
replicates in each environment is
y ,
ij
and
the least squares estimates of the genotypic
efect and the environmental efects are
.. ...
y y =
i i
(which satisfes the constraint
0 =
i
i
) and
...
y y =
j .j.
(which satisfes
the constraint =
0
j
j
) (Table 14.1), where
...
y is the least squares estimate of the overall
mean and y
i..
is the mean of the ith geno-
type averaged across environments and
replicates , and y
.j.
is the mean of the jth
environment across all genotypes and
replicates . Terefore, the least squares
266 J. Crossa et al.
estimate of the GE term in Eqn 14.1 is
= = +
...
( ) z y y y y
ij ij ij. i.. .j.
(which satis-
fes the constraints =
( )
ij
i j
= =
( ) ( ) 0
ij ij
j i
) (Table 14.2).
Note that the notation in Eqn 14.1 can be
used for models with fxed, mixed, or random
efects. For a complete random model, it is
assumed that
i
,
j
and ( )
ij
are normally
and independently distributed, with vari-
ances
2
,
2
and
2
, respectively.
Fixed-effect LinearBilinear Models
Williams (1952) was the frst to link the Eqn
14.1 model with principal components (PC)
analysis by considering the model
y = + + +
ij i i j ij
where is the larg-
est singular value of ZZ and ZZ (for Z =
y y
ij i.
), and
i
and
j
are the correspond-
ing eigenvectors. Gollob (1968) and Mandel
(1969, 1971) rediscovered and extended
Williams (1952) work by considering the
bilinear GE term as
=
=
1
( ) .
t
ij k ik jk
k
Tus,
the general formulation of the linear
bilinear model is:
= + + + +
=1
y
t
ij i j jk ij
k ik
k
(14.2)
where the constant
k
is the singular value
of the kth multiplicative component that is
ordered
1 2
...
t
; the
ik
elements
are elements of the kth left singular vector
of the true interaction and represent geno-
typic sensitivity to hypothetical environmental
factors represented by the kth right singular
vector with elements
jk
. Te
ik
and
jk
elements satisfy the ortho-normalization
constraints 0
= =
jk
ik ik jk
i j
for k k
and
2
=
ik
i
2
1. =
jk
j
When Eqn 14.2 is
saturated, the number of bilinear terms is t
= min(I 1, J 1), and for any smaller value,
the model is said to be truncated. Te GE
interaction parameters
k
,
ik
and
jk
are
estimated from the data.
Gabriel (1978) described the least squares
ft of Eqn 14.2 and explained how the resid-
ual matrix of the GE term, Z = y y
ij i.
..
y y , +
.j
is subjected to singular value
decomposition (SVD) after adjusting for the
additive (linear) terms. Te frst two compo-
nents can be displayed in a graph called a
biplot. Zobel et al. (1988) and Gauch et al.
(2008) named Eqn 14.2 the Additive Main
Efects and Multiplicative Interaction
(AMMI) model. Other types of linear
bilinear models, described by Cornelius et al.
(1996), are:
the Sites (environments) Regression (SREG)
model:
1
y
=
= + +
t
ij j k ik jk ij
k
(14.3)
the Genotypes Regression (GREG) model:
1
y
=
= + +
t
ij i k ik jk ij
k
(14.4)
the Completely Multiplicative Model
(COMM):
1
y
=
= +
t
ij k ik jk ij
k
(14.5)
and the Shifted Multiplicative Model
(SHMM):
1
y
=
= + +
t
ij k ik jk ij
k
(14.6)
Te SHMM was the frst linearbilinear
model that, along with other statistical tools,
was used for identifying subsets of geno-
types or environments in which genotypic
rank changes would be negligible (Cornelius
et al., 1992, 1993; Crossa and Cornelius,
1993; Crossa et al., 1993, 1995). Te SREG
(Crossa and Cornelius, 1997) model is very
useful in plant breeding because the bilinear
terms contain both the main efects of geno-
types (G) and GE. Te SREG model has been
preferred to SHMM for grouping environ-
ments without genotypic rank change
(Crossa and Cornelius, 1997). Te interac-
tion parameters
ik
and
jk
in the bilinear
terms model the behaviour of genotypes and
environments, and when (
1 2
,
i i
) and
1 2
( ,
j j
) are plotted together in the biplot
(Gabriel, 1978), useful interpretations of
the relationships between genotypes, envir-
onments, and GE are obtained. In the biplot,
the interaction between the ith genotype
and the jth environment is obtained by
projecting one vector on to the other. In the
AMMI model, the composition of the two-
S
t
a
t
i
s
t
i
c
a
l
M
o
d
e
l
s
f
o
r
G
E
I
n
t
e
r
a
c
t
i
o
n
2
6
7
Table 14.1. Least squares estimates of genotypic and environmental effects for a two-way table of genotypes and environments with i = 1, 2, , I genotypes,
j = 1, 2, , J environments and r replicates.
Environment 1 Environment 2 . . Environment J
Marginal mean
of genotypes Estimate of genotypic effect ( )
i
Genotype 1
11.
y
12.
y
. .
1 .
y
J 1..
y
1 1.. ...
y y =
Genotype 2
21.
y
22.
y
. .
2 .
y
J 2..
y
2 2.. ...
y y =
. . . . . . . .
. . . . . . . .
Genotype I
1.
y
I 2.
y
I
. .
.
y
IJ
y
I.. ...
y y =
I I..
Marginal mean of
environments
.1.
y
.2.
y
. .
. .
y
J
=
...
y
Estimate of
environmental
effect ( )
j
1 .1. ...
y y =
2 .2. ...
y y =
. .
. . ...
y y =
J J
268 J. Crossa et al.
way I J matrix to be subjected to singular
value decomposition is shown in Table 14.2,
where only the GE interaction (see Eqn 14.2)
is modelled by the bilinear terms. In the
SREG model, the bilinear term models the
main efects of genotypes (G) plus GE inter-
action (usually called a GGE biplot), and the
composition of the two-way I J matrix to
be subjected to singular value decompos-
ition (see Eqn 14.3) is shown in Table 14.3.
Recently there was an ongoing debate
examining the merits and demerits of AMMI
versus GGE biplots for genotype and envir-
onment identifcation (Yan et al., 2007;
Gauch et al., 2008). In a recent article, Yang
et al. (2009) pointed out the advantages and
disadvantages of these fxed efects linear
bilinear models and discussed relevant issues
concerning the use of biplot analysis as a
descriptive statistical tool. Te authors
pointed out that several issues afect the
validity of such analysis but are generally
ignored by the current biplot literature.
Some of these issues are:
What if genotypes or environments, or
both, are random efects?
Can biplot analysis contribute to detect-
ing crossover interaction?
How relevant is biplot analysis for under-
standing the nature and causes of inter-
action?
Mixed-effect LinearBilinear Models
What if genotypes or environments, or
both, are random effects?
A mixed-model analogue of biplot analysis
has been developed using the factor analytic
(FA) model for approximating the variance-
covariance GE structure (Piepho, 1998;
Smith et al., 2002). Research conducted by
Crossa et al. (2006) and Burgueo et al.
(2008) described how to model variance-
covariance GE and GGE using the FA model
and how to incorporate the additive (rela-
tionship A) matrix and the additive addi-
tive covariance matrix into the FA model
based on pedigree information. Burgueo et
al. (2008) also described the equivalence
between SREG2 and FA(2) for fnding
Table 14.2. Least squares estimate of the genotype environment (GE) term in Eqn 14.1 is
= = +
. .. . .
( ) z y y y y
ij ij ij i j
with i = 1, 2, , I genotypes, j = 1, 2, , J environments and r replicates.
Environment 1 Environment 2 . . Environment J
Genotype 1 +
11. 1.. .1. ...
y y y y +
12. 1.. .2. ...
y y y y
.
.
+
1 . 1.. . . ...
y y y y
J J
Genotype 2 +
21. 2.. .1. ...
y y y y +
22. 2.. .2. ...
y y y y
.
.
+
2 . 2.. . . ...
y y y y
J J
. .
.
.
. .
. .
.
.
. .
Genotype I +
1. .. .1. ...
y y y y
I I
+
2. .. .2. ...
y y y y
I I
+
. .. . . ...
y y y y
IJ I J
Table 14.3. Least squares estimates of the combined effects of genotype (G) plus the genotype
environment (GE) + = =
. . .
( ) z y y
i ij ij ij j
with i = 1, 2, , I genotypes, j = 1, 2, , J environments and
r replicates.
Environment 1 Environment 2 . . Environment J
Genotype 1
11. .1.
y y
12. .2.
y y
. .
1 . . .
y y
J J
Genotype 2
21. .1.
y y
22. .2.
y y
. .
2 . . .
y y
J J
.
. . . . .
. . . . . .
Genotype I
1. .1.
y y
I
2. .2.
y y
I . . .
y y
IJ J
Statistical Models for GE Interaction 269
subsets of genotypes and environments
without COI.
Factor analytic and sites regression
models for assessing crossover genotype
environment interaction
In the FA model, the random efect of the ith
genotype in the jth environment ( g
ij
) is
expressed as a linear function of latent
variables x
ik
with coefcients
jk
for k = 1,
2, t, plus a residual,
ij
, i.e.
=
= + +
1
g x ,
t
ij j jk ij
ik
k
so that the ijth
cell mean can be written as g y = +
ij ij ij
.
With only the frst two latent factors being
retained, g
ij
is approximated by
1 1 2 2
g x x + + +
ij j i j i j ij
. Terefore,
SREG2 (Eqn 14.3) can be perceived as
consisting of a set of multiple regression
equations (one for each environment), each
regression equation consisting of an envir-
onmental mean or environmental efect as
intercept plus two terms for regression on
two genotypic regressor variables,
1
i
and
2
i
(either observed or latent), with
1
j
and
2
j
as the regression coefcients. Tus
there is a clear connection between the
SREG2 and the FA(2) models, as described
by Burgueo et al. (2008). A similar connec-
tion between the AMMI2 and FA(2) models
was also established by Smith et al. (2002).
Under principal component rotation, the
directions and projections of the vectors of
FA(2) and SREG2 in the biplot are the same.
Terefore, the property of SREG by which
the frst principal component of SREG2
accounts for non-crossover interaction (non-
COI) and the second principal component of
SREG2 is due to COI variability should hold
for FA(2) as well. However, the absolute
values of genotypic and environmental
scores under the FA(2) and SREG2 models
may not necessarily be the same because
shrinkage is involved in Best Linear Unbiased
Predictions (BLUPs) (Henderson, 1984) of
random efects in the FA(2) model but not in
least squares estimates of fxed efects in the
SREG2 model. Other important diferences
between SREG and FA are: (i) the standard
errors of the estimable functions of fxed
efects under SREG difer from those of
predictable functions of a mixture of fxed
and random efects under FA; and (ii) FA
models are more fexible in handling unbal-
anced data (the SREG model does not handle
missing data).
Detecting Crossover Interaction
Under Fixed and Mixed Effects
LinearBilinear Models
Can biplot analysis help detect crossover
interaction?
Te most important GE in agriculture is COI
(Cornelius et al., 1993). In the absence of
COI, GE is simply due to diferences in scales,
and the best genotype in one environment
remains the best in all other environments.
Te usual AMMI2 biplot analysis does not
distinguish COIs from non-COIs. A SREG1
biplot based on a constrained singular value
decomposition (SVD) non-COI PC1 solution
(Crossa and Cornelius, 1997) has been used
to predict the absence of COIs based on
earlier work on a rank-one shifted multiplic-
ative model (SHMM1) by Cornelius et al.
(1992). If the SHMM1 model is an adequate
approximation to two-way GE data and the
primary efects of environments (PC1 scores)
are either all non-positive or non-negative,
then the SHMM1 model has the two propor-
tionality properties. First, diferences
between genotypes in any single environ-
ment are proportional to genotypic difer-
ences in any other environment. Secondly,
diferences between environments in terms
of the performance of any single genotype
are proportional to those of the performance
of any other genotype. Te second propor-
tionality restriction is not required for assess-
ing genotypic non-COI status and is removed
in the SREG1 model. If the PC1 scores have
diferent signs, SHMM1 and SREG1 biplots
show the presence of COIs. Te SHMM2 and
SREG2 biplots of the frst two PCs would
represent the graph of non-COI variation
(PC1) versus COI variation (PC2).
Detection of COI using SREG (and
SHMM) has generally been done within the
270 J. Crossa et al.
fxed efect linearbilinear framework. Te
approach proposed by Crossa et al. (2004)
uses the fxed linearbilinear SREG and
SHMM models for constructing the cluster-
ing of environments and genotypes with
non-COI, and subsequently uses a linear
mixed model to test the statistical hypothe-
sis of perfect genetic correlations between
environments or genotypes within the
subset. Yang (2007) recognized that in
statistical analyses of METs, either geno-
types or environments, or both, should be
considered as random efects and, therefore,
COI detection must consider that the difer-
ence between genotypic efects in a random
environment is a predictable function that
involves Best Linear Unbiased Estimators
(BLUEs) as well as BLUPs.
Burgueo et al. (2008) proposed an inte-
grated methodology for: (i) clustering envir-
onments and genotypes with negligible COI
based on results obtained from ftting FA to
MET data; and (ii) detecting COI using
predictable functions based on the linear
mixed model with FA and BLUPs of geno-
types. Te authors were able to discriminate
COI from heterogeneity of variances (HV).
Te advantages of this methodology are
that: (i) it allows researchers to use a more
realistic statistical model with fxed as well
as random efects; (ii) the association among
environments is taken into account and
modelled; (iii) the association among geno-
types is easily introduced (although it is not
included in Burgueo et al., 2008); and (iv)
the approach can be used with unbalanced
and missing data.
Burgueo et al. (2008) used the linear
bilinear mixed model methodology based on
FA(2). Tey demonstrated the use of this
approach in two data sets. One data set
consists of grain yield from an International
Maize and Wheat Improvement Center
(CIMMYT) maize MET with nine genotypes
(A, B, C, D, E, F, G, H, I) arranged in a rand-
omized complete four block design evalu-
ated in 20 international environments. Te
biplot in Fig. 14.1 gives general descriptive
patterns of genotypes and environments,
and makes it possible to identify extreme
pairs of genotypes and sites with COI, for
example, genotypes D and H with environ-
ments 11 and 8. However, the biplot by itself
does not clearly delineate the subsets of
environments and genotypes with statistic-
ally signifcant COI. After clustering
Fig. 14.1. Biplot from the factor analytic (FA(2)) model of maize grain yield data including nine genotypes
(A, B, C, D, E, F, G, H, I) and 20 environments (120) (adapted from Burgueo et al., 2008).
Statistical Models for GE Interaction 271
environments and genotypes based on the
mixed linearbilinear model, the fnal
subsets of environments with negligible COI
are subsets (1-3-10), (2-6-7-19-14), (4-5-16-
9-17-20-15), (11-13-12-18), and the single-
member subset (8), whereas the fnal subsets
of genotypes with negligible COI are
(A-B-C-G) and (D-E-F-I), with H as a single-
member group.
Results indicate that when one environ-
mental subset or one genotypic subset was
considered, no signifcant COI was found.
When subsets of environments located in
opposite quadrants of the biplot in Fig. 14.1
are combined, there is a greater increase in
the number of signifcant COIs than when
subsets of environments from the same
quadrant of the biplot are combined (Table
14.4). From a breeders perspective, it may
be important to consider combining certain
environmental subsets into one larger
cluster that may better represent certain
hypothetical target populations of environ-
ments. When environment (8) is combined
with (1-3-10) (both subsets with negative
loadings), no signifcant COIs are added, but
when (8) is combined with (4-5-9-15-16-17-
20), the number of signifcant COIs increases
to 12 (Table 14.4). Environment 8 is difer-
ent from all other environmental subsets
except subset (1-3-10). Tese results are in
agreement with a plant breeders main inter-
est, which is developing genotypes with local
as well as wide adaptation. Tis can be better
achieved by stratifying environments (and/
or genotypes), which in turn increases selec-
tion gains at both regional and local levels.
Regions and subregions may be better delin-
eated based on COI and non-COI. Tis
approach should be useful for fnding poten-
tial new subsets of regions and subregions
that could be afected by new climate change,
drought and/or heat stress. Since climate
change is very dynamic and can be drastic
year after year, data from successive METs
in several years should be systemat ically
analysed to fnd response patterns of geno-
types to new environmental conditions.
Table 14.4. Total number of tetrads among subsets of environments and genotypes, total number of
signifcant tetrads, number (n) and percentage (%) of signifcant COI, and number (n) and percentage
(%) of signifcant non-COI due to heterogeneity of variance (HV) (adapted from Burgueo et al., 2008).
Subsets Total tetrads
a
Signifcant
tetrads
Signifcant
COI
Signifcant non-COI
due to HV
n % n % n %
---------------------------------------------------------- Among subsets of environments ---------------------------------
(1-3-10)(4-5-9-15-16-17-20) 756 135 17.86 19 14 116 86
(1-3-10)(11-12-13-18) 432 54 12.50 21 39 33 61
(1-3-10)(2-6-7-14-19) 540 25 4.63 11 44 14 56
(1-3-10)(8) 108 2 1.85 0 0.0 2 100
(4-5-9-15-16-17-20)(11-12-13-18) 1008 51 5.06 0 0.0 51 100
(4-5-9-15-16-17-20)(2-6-7-14-19) 1260 39 3.10 0 0.0 39 100
(4-5-9-15-16-17-20)(8) 252 61 24.21 12 20 49 80
(11-12-13-18)(2-6-7-14-19) 720 58 8.06 0 0.0 58 100
(11-12-13-18)(8) 144 39 27.08 4 10 35 90
(2-6-7-14-19)(8) 180 22 12.22 3 14 19 86
Total 6840 567 8.29 70 12.3 497 87.7
-----------------------------------------------------------Among subsets of genotypes--------------------------------------
(A-B-C-G)(D-E-F-I) 3040 315 10.4 26 8.3 289 91.7
(A-B-C-G)(H) 760 40 5.3 6 15.0 34 85.0
(D-E-F-I)(H) 760 212 27.9 38 17.9 174 82.1
Total 6840 567 8.29 70 12.3 497 87.7
a
Number of tetrads counted is within subsets of environments and genotypes when one environmental subset and one
genotypic subset are considered and between subsets of environments and genotypes when two subsets of
environments or genotypes are considered.
272 J. Crossa et al.
Incorporating External Covariables
for Explaining Genotype
Environment Interaction
Tis section is related to the issue outlined
by Yang et al. (2009), which is how relevant
is biplot analysis for understanding the
nature and causes of interaction? Factorial
regression (FR) or partial least squares (PLS)
analysis (e.g. Vargas et al., 1999; van Eeuwijk
et al., 2005) is useful for studying the efects
of both genetic and environmental covari-
ables and to develop functional relationships
and predictability with explanatory covari-
ables. Te structural equation model (SEM)
using endogenous and exogenous variables
is a useful alternative for overcoming some
of the limitations of the FR and PLS
approaches.
Linear models for mapping quantitative
trait loci (QTLs) and adding external
covariables for studying QTL
environment interaction (QEI) analysis in
genetics and plant breeding
In important maize growing areas of the
world, grain yield reduction is caused by
drought at fowering time as well as low
nitrogen content in the soil. Drought delays
silking, increases the anthesissilking inter-
val (ASI) and, therefore, decreases grain
yield. Tus, under drought stress, selection
for short ASI in maize should be correlated
with grain yield improvement, and ASI
becomes an important secondary trait with
relatively high heritability and more stabil-
ity than grain yield. Nevertheless, few stud-
ies have been conducted on mapping QTLs
responsible for the expression of morpho-
logical traits under abiotic stresses.
In plant breeding, much research is
directed at locating regions of the chromo-
somes that are involved in the physiological
processes underlying phenotypical traits.
Tese regions are called QTLs. When these
regions difer between genotypes in relation
to changes in the environment, QTL envir-
onment interaction (QEI) occurs. Te statis-
tical problem can be interpreted as a
multivariate multiple regression of pheno-
typic traits as observed over a set of environ-
ments on a set of genetic predictors. FR
provides a suitable framework for QEI analy-
sis. Crossa et al. (1999) give examples of how
FR can be used for assessing the chromo-
somal location of QTLs and QEI and the
importance of their efects.
Tere are approaches in which the GE is
modelled directly using regression on envir-
onmental (and/or genotypic) variables, rather
than regression on the environmental mean.
A useful linear model for incorporating exter-
nal environmental (or genotypic) variables is
the FR model (Denis, 1988; van Eeuwijk et al.,
1996). FR models are ordinary linear models
that approximate the GE efects of Eqn 14.1
by the products of one or more of the follow-
ing: (i) genotypic covariables (observed)
environmental potentialities (estimated); (ii)
genotypic sensitivities (estimated) environ-
mental covariables (observed); and (iii) scale
factor (estimated) genotypic covariables
(observed) environmental covariables
(observed). Te aim of FR is to replace, in the
GE subspace, genotypic and environmental
factors with a small number of genotypic and
environmental covariables. Vargas et al.
(2006) further developed the statistical
approaches described by Crossa et al. (1999)
and van Eeuwijk et al. (2000, 2002) for model-
ling QTLs and QEI. Te main objectives of
their research were to demonstrate the use
of: (i) FR for estimating efects and locations
of QTLs and QEI; and (ii) FR for modelling
and interpreting QEI in terms of products of
genetic predictors and environmental vari-
ables.
In FR, genotypic covariables, x
a
(a = 1
A) with values x
ia
, can be introduced for the
genotypic main efect, G
i
:
G x residual, = +
i ia a
where
a
is the regres-
sion coefcient for the regression of G
i
on x
a
.
For more than one genotypic covariable, this
becomes
=
= +
1
G x residual.
A
i ia a
a
When the
genotypic covariable x
a
is replaced by genetic
predictors x
q
(when attempting to map
QTLs), the FR framework can also be used to
do a genome scan for QTL efects. Analogous
to the genotypic main efect, in FR, the envir-
onmental main efect, E
j
, can also be regressed
on environmental covariables, z
b
with
Statistical Models for GE Interaction 273
values z
jb
. Te corresponding partitioning is
= + E z residual
j jb b
for one environmental
covariable, or
=
= +
1
E z residual
B
j jb b
b
for
multiple environmental covariables. Te
parameters
b
represent the regression
coefcients of the regression of the environ-
mental main efect on z
b
.
Within a QTL analysis by FR, a multiple
QEI model follows easily from models for
GE: (GE)
ij
=
=
+
1
x residual,
Q
iq jq
q
where
jq
represents a QEI efect, i.e. a diferential QTL
expression in relation to the main efect QTL
expression, for the qth QTL in environment j.
QEI for a QTL q can be further modelled by
regressing it on an environmental covariable,
z
b
: = +
' '
(GE) x z residual.
ij q b iq jb
For multiple
QTLs, this generalizes to:
= =
= +
1 1
(GE) x z residual.
Q B
ij qb iq jb
q b
One or more QTL main efects can be
tested by comparing the model
=
= + + +
1
y x E residual
Q
ij iq q j
q
with the
model = + y E
ij j
. When main efect QTL
expression and QEI are considered
together, this is equivalent to ftting
diferent QTLs to each environment. A
specifc test for QEI compares
= =
= + + + +
1 1
y x E x residual
Q Q
ij iq q j iq jq
q q
to
=
= + + +
1
y x E residual.
Q
ij iq q j
q
F-tests can
be constructed from ratios of regression
mean squares to the independent error
term.
Table 14.5 shows parts of the analysis of
variance table for one example comprising a
population of F
2
-derived F
3
families evalu-
ated across eight environments difering in
the level of drought stress and soil nitrogen
content, at position 140 cM of chromosome
1 (Vargas et al., 2006). Te frst part shows
the usual analysis of variance for a two-way
table of grain yield measured in 211 geno-
types with partitioning of the joint efect of
G+GE into G and GE efects. Te middle part
shows the variability due to QTL+QEI efects
in parts of the genome other than chromo-
some 1 (i.e. due to QTLs on chromosomes
210), the variability due to G+GE after
correction for QTLs on the other chromo-
somes, and the corresponding partitioning
into G and GE components. Approximately
28.8% of the original G+GE was associated
with QTLs on other chromosomes. Te last
part shows the partitioning of G+GE
adjusted for the QTLs on chromomosomes
210 into variation due to QTL+QEI at
pos ition 140 cM of chromosome 1 and
deviations from the QTL-model.
For grain yield, Fig. 14.2 depicts the
profle of R
2
QTL
, R
2
QEI
and R
2
QTL+QEI
and the
corresponding critical values for = 0.01
based on 1000 randomizations. Tere is
good reason to believe that there are envir-
onment-specifc QTLs between 105 cM and
180 cM of chromosome 1 (Fig. 14.2)
(QTL+QEI and QEI efects were both signif-
cant). In contrast, only main efect QTLs
were observed in other chromosomes. Te
QEI at the end of chromosome 4 and near
the end of chromosome 9 were ignored
because those QEI peaks did not coincide
with the corresponding QTL+QEI peaks. A
signifcant dominant main efect QTL was
also found on chromosome 4 (not shown).
Te environmental covariable that
explained the QEI best, at 77.6%, was mini-
mum temperature during fowering (Table
14.5). Te efect of this environmental
covariable was highly signifcant by an F-test
for the regression mean square over the
deviations from the regression (F =
76.675/3.686 = 20.8, p = 0.0038), and even
more so when the denominator in the F-test
was the intra-block error.
Linear mixed models for multitrait multi-
environment QTL analysis
A general formulation of a linear mixed
model for the multitrait multi-environment
(MTME) is presented by Malosetti et al.
(2008). Te initial model is = + + . y X Zu e
Te response vector y is modelled by a set of
fxed efects collected in vector and random
efects collected in vectors u and e; X and Z
are design matrices assigning fxed and
random efects to the observations. Random
genetic efects are assumed to be normally
distributed, u ~ N(0, G), with G the genetic
274 J. Crossa et al.
(co)variance matrix (vcov
G
). Finally, e is a
vector of non-genetic residuals associated
with each observation and normally distrib-
uted, e ~ N(0, R). Te phenotypic (co)vari-
ance is given by V(y) = ZGZ + R. From a
breeders point of view, the vcov
G
is of special
interest as it refects the magnitude and
pattern of relationships between genetic
efects. A QTL model arises by including the
efect of a putative QTL as follows:
= + + + .
QTL
y X X Zu * e Te extra term in
the model is composed of a design matrix
X
QTL
, which is derived from molecular
marker information and a vector of fxed
QTL efects (). In an MTME model, vector
has dimensions JK 1 and contains the
additive genetic QTL efects for all the traits
in each of the environments. Te random
Table 14.5. Partitioning of yield variation at position 140 cM of chromosome 1. For comparison, an error
estimated from the median intra-block error was 0.75 (adapted from Vargas et al., 2006).
Source of variation Degrees of freedom
a
Sum of squares Mean squares
Environment (E) 7 12777.169 1825.310
G + GE 1680 3212.868 1.914
QTL + QEI chrom.
b
210 925.806
G + GE chrom. 1 adj.
b
1680 2287.062
F
2
family (G) adj. 210 693.358 3.302
GE adj. 1470 1593.704 1.084
G + GE chrom. 1 adj. 1680 2287.062
QTL + QEI chrom. 1 140 cM 8 153.775 19.222
QTL main effect 1 54.986 54.986
QEI 7 98.789 14.113
Min. temp. fow.
b
1 76.675 76.675
Residual QEI 6 22.114 3.686
Deviations 1672 2133.287 1.276
a
For the correction of the grain yield data due to genetic effects on chromosomes 210, degrees of freedom might be
discounted.
b
chrom., chromosome; adj., adjusted; Min. temp. fow., minimum temperature during fowering.
8
7
6
5
4
3
2
1
0
0
Position (cM)
QTL+QEI
QTL+QEI
QTL
QTL
QEI
QEI
R
2
a
d
d
i
t
i
v
e
20 40 60 80 100 120 140 160 180 200 220 240 260
Fig. 14.2. Profle of R
2
for the additive effects of QTL (
____
), QEI (
..
), and QTL+QEI (
_
--
_
) on grain yield
for chromosome 1 (additive). The horizontal lines mark the appropriate threshold for the effects QTL+QEI,
QTL, and QEI (adapted from Vargas et al., 2006).
Statistical Models for GE Interaction 275
genetic efects, now collected in a vector u*,
result from the efects of QTLs outside the
tested region, that is, the genetic back-
ground. Genetic background efects are
assumed normally distributed: u ~ N(0, G*).
Note that G* represents the part of the
genetic (co)variance that is not explained
by the QTL. Te extension from a single-
QTL model to a multi-QTL model is
straight forward and given by
=
= + + +
.
Q
QTL q
q 1
y X Xq Zu * e
Bilinear models with external covariables
When environmental (or genotypic) covari-
ables show high collinearity, interpretation
of the least squares regression coefcients
from the FR is complicated because they are
estimated very imprecisely. Noise on the
response variable also complicates the
interpretation of FR parameters.
Furthermore, least squares estimation of
parameters in FR models is not unique when
the number of covariables is larger than the
number of observations; therefore, an alter-
native estimation method is needed. Partial
least squares (PLS) regression can be used.
Multivariate PLS regression models
(Aastveit and Martens, 1986; Helland, 1988)
are a special class of bilinear models. When
genotypic responses over environments (Y)
are modelled using environmental covari-
ables, the J H matrix Z of H (h = 1, 2, , H)
environmental covariables can be written in
bilinear form as:
Z = t
1
p
1
+ t
2
p
2
+ + t
M
p
M
+ E
M
= TP + E (14.7)
where the matrix T contains the t
1
t
J
J 1
vectors called latent environmental covari-
ables or Z-scores (indexed by environments)
and the matrix P has the p
1
p
H
H 1 vectors
called Z-loadings (indexed by environmental
variables), and E has the residuals. Similarly,
the response variable matrix Y in bilinear
form is:
Y = t
1
q
1
+ t
2
q
2
+ + t
M
q
M
+ F
M
= TQ + F (14.8)
where the matrix T is as in Eqn 14.7, the
matrix Q contains the q
1
q
I
I 1 vectors
called Y-loadings (indexed by genotypes),
and F has the residuals. Te relationship
between Y and Z is transmitted through
latent variable T. Te PLS algorithm
performs separate (but simultaneous) prin-
cipal component analysis of Z and of Y that
allows reducing the number of variables in
each system to a smaller number of hope-
fully more interpretable latent variables.
Treatment environment interaction
analysis in an agronomy trial using PLS
A parsimonious description of the treatment
environment interaction (T E) occurring
in 24 agronomic treatments (tillage, summer
crop, manure and nitrogen, N) evaluated
during 10 consecutive years (19881997) was
conducted by Vargas et al. (2001) using FR
and PLS. Results of the fnal multiple FR
(MFR) analysis were compared with those of
PLS regression to achieve extra insight into
the T E. Te MFR was applied on the six
most important components of the T E
terms: Year Tillage, Year Summer Crop,
Year Manure, Year N, Year Summer Crop
N, and Year Manure N. Results for the
MFR of the 27 environmental covariables
tillage interactions showed that evaporation
in December (EVD) tillage sum of squares
accounted for 68% of the whole year tillage
interaction. For year summer crop, evap-
oration in April (EVA) accounted for 36% of
the year summer crop. For year manure,
precipitation in December (PRD) and sun
hours in February (SHF) contributed 56% of
the year manure sum of squares. Year N
interaction determined the major part of year
treatment interaction sum of squares.
Te PLS biplot separated the nine highest
yielding treatments (T9, T19, T21, T17, T11,
T12, T10, T23 and T18) from the nine lowest
yielding treatments (T1, T2, T3, T4, T5, T6,
T7, T8 and T16) (Fig. 14.3). Te nine lowest
yielding treatments showed positive inter-
action with year 1995, which had high mTUF,
mTF and MTA (see Fig. 14.3 for explanation
of terms), but negative interaction with year
1988 (opposite quadrant). Te PLS biplot
contains roughly fve clusters of correlated
environmental covariables. Te order of
276 J. Crossa et al.
inclusion of these covariables in the MFR
with the stepwise procedure for each factor
efect corresponds to selecting covariables
for the diferent cluster groups depicted in
Fig. 14.3.
Structural equation model (SEM)
Te SEM approach is similar to multiple
regression that simultaneously analyses a
system of equations in which each equation
describes a causal relationship among vari-
ables considered in the system. Te SEM
approach may be used to model intermedi-
ate traits (i.e. yield components) and their
interrelationships with other variables, as
well as with grain yield. Also, the SEM allows
a researcher to test hypotheses on cause
efect relationships between variables in a
complex system. Te initial defnition of
SEM comprises a path diagram that refects
the theoretical model and outlines the vari-
ous levels of observed (or latent) independ-
ent or dependent variables, as well as the
directions of causal relationships among
variables. Te functional relationships
between variables are represented by arrows
or paths.
Te SEM was proposed by Dhungana
(2004) to study GE of grain yield and its
components, and to account for the import-
ance of intermediate traits associated with
yield components. Te author explained yield
GE with cross-products of genotypic and
environmental covariates as exogenous (inde-
pendent) variables and observed yield compo-
nent GE as endogenous (dependent/
independent) variables. Te author con cluded
that SEM on observed variables was an efec-
tive way of describing yield GE in wheat, given
that the interrelationships and role of yield
Fig. 14.3. Biplot of the frst and second PLS (partial least squares) factors representing the Z-scores
(latent environmental covariable vectors) of 10 years (19881997), and the Y-loadings (response variable
vectors) of the 24 practice treatments (T1T24) enriched with the Z-loadings (environmental variable
vectors) of 27 environmental variables. EV, total monthly evaporation; PR, total monthly precipitation; SH,
sun hours per day; mT, mean minimum temperature sheltered; MT, mean maximum temperature
sheltered; mTU, mean minimum temperature unsheltered; D, December; J, January; F, February; M,
March; A, April; N, nitrogen (adapted from Vargas et al., 2001).
Statistical Models for GE Interaction 277
component GE can be incorporated simulta-
neously in a single model. Diagrams repre-
senting the structural model known as path
diagrams are useful for visualizing complex
models and variable relationships.
Vargas et al. (2007) showed how the SEM
method may be used on observed yield GE,
yield components GE, and other intermedi-
ate traits, together with residuals from
observed cross-product between genotypic
and environmental covariates, for studying
the causes and efects of GE on grain yield,
biomass, yield components, and other inter-
related variables acting at diferent develop-
ment stages in wheat trials. Te proposed
model that formulates the hypotheses
between the endogenous variables associ-
ated with grain yield (YLD
GE
) and yield
components and the other variables (Y) at
diferent stages of crop development, and
the adjusted cross-products of genotypic and
environmental covariates (X) is given in Fig.
14.4. Te given structural equation model
explained 0.96 of total variability of yield GE
(Table 14.6). Te variables that contributed
most to explaining yield GE were GEs of yield
components GM2, TKW, GSP and SM2 (see
Table 14.6 for explanation of terms), with
total efects of 1.09, 0.64, 0.56 and 0.54,
respectively (Table 14.6 and Fig. 14.5). Te
GEs of GM2, TKW, GSP and SPM explained
0.90, 0.43, 0.44 and 0.42, respectively, of
total variability. Yield component SM2 had a
very small R
2
value (0.04), but a signifcant
indirect efect on grain yield GE (0.54). Te
model indicated that GEs of yield compo-
nents GM2 and TKW had the largest positive
direct association with yield GE (1.09 and
0.64, respectively) and no indirect efects
(0.0), while GSP and SM2 GEs had the great-
est indirect efects on yield GE (0.61 and
0.54, respectively) and a low negative direct
efect (GSP = 0.05) or no direct efect at all
(SM2 = 0.0) on yield GE (Table 14.6).
Fig. 14.4. Proposed model hypothesizing the relationship between yield GE (YLD) and yield components
GE, grains per square metre (GM2), thousand kernel weight (TKW), spikes per square metre (SM2),
grains per spike (GSP), biomass at anthesis (BMA), spike mass (SPM), relative duration of spike growth
(RSG), crop growth rate during spike growth (dBMb), biomass at the vegetative stage (BMV), and
adjusted cross-products (X
ij
) of the i th genotypic covariate and j th environmental covariate (i = 1, 2, ,
k; j = 1, 2, , l ) . Arrows represent the direction of the variables infuence. The s and bs next to the
arrow lines represent the standardized coeffcients to be estimated (e.g. b
ij1
is the coeffcient for effect of
the cross-product of the ith genotypic covariate with the j th environmental covariate on yield (frst
variable)) (adapted from Vargas et al., 2007).
BMV
dBMb
RSG
X
ij
X
ij
SPM
BMA
SM2
GSP
YLD
TKW
GM2
b
ij 2
b
ij 1
b
ij 5
b
ij 3
b
ij 4
b
ij 7
b
ij 9
12
25
56
68
78
79
810
910
34
47
278 J. Crossa et al.
Fig. 14.5. Path estimates of the structural equation model for endogenous variables associated with
grains per square metre GE (GM2), grains per spike GE (GSP), thousand kernel weight GE (TKW), spikes
per square metre GE (SM2), relative duration of spike growth GE (RSG), crop growth rate during spike
growth GE (dBMb), biomass at anthesis GE (BMA), spike mass (SPM), biomass at the vegetative stage
GE (BMV), and yield GE (YLD), and cross-products (variables environmental covariates). MXT, mean
daily maximum temperature; MNT, mean daily minimum temperature; RAD, solar radiation; suffxes 1, 2, 3
and 4 stand for the frst, second, third and fourth crop development stages. Arrows represent the direction
of the variables infuence, and the numbers on the arrow lines represent the estimated standardized
coeffcients. Critical values for a signifcance level of 0.05, 0.01, 0.001 and 0.0001 are 2.00, 2.67, 3.48 and
4.20, respectively, using a two-tailed t-test with 60 degrees of freedom (adapted from Vargas et al., 2007).
Table 14.6. Direct and indirect effects of yield components GE and adjusted cross-product covariates on
grain yield GE (R
2
= 0.96) (adapted from Vargas et al., 2006).
Variable Direct effect Indirect effect Total effect R
2
Grains per square metre (GM2) 1.09 0.00 1.09 0.90
Thousand kernel weight (TKW) 0.64 0.00 0.64 0.43
Grains per spike (GSP) 0.05 0.61 0.56 0.44
Spikes per square metre (SM2) 0.00 0.54 0.54 0.04
Spike mass (SPM) 0.00 0.05 0.05 0.42
Relative duration of spike growth (RSG) 0.00 0.09 0.09
Crop growth rate during spike growth (dBMb) 0.00 0.07 0.07
MXT4 GM2
a
0.00 0.39 0.39
a
MXT, mean daily maximum temperature; MNT, mean daily minimum temperature; RAD, solar radiation; suffxes 1, 2, 3
and 4 denote the frst, second, third and fourth crop development stage, respectively.
Statistical Models for GE Interaction 279
Searching for Associations Between
Molecular Markers and Phenotypic
Variability While Modelling Genotype
Environment Interaction
Te main feature of linear mixed model
methodology applied to plant phenotypic
data collected in METs is that it allows accu-
rate prediction of genotypic performance by
using covariance structures that consider
correlations between sites, years and plots
in the feld, as well as genetic associations
between relatives. Te genetic covariance
between relatives for any pair of related indi-
viduals (i and i), due to their additive genetic
efects, is equal to two times the coefcient
of parentage (COP = f
ii
), also known as coef-
fcient of coancestry, times the additive
genetic variance (i.e. 2f
ii
2
a
= A
2
a
where A
is the additive relationship matrix and
2
a
is
the additive genetic variance). Using the
linear mixed model methodology, the genetic
covariance matrix can be estimated and
BLUPs can be obtained. Te efectiveness of
exploiting relationships among strains
tested in METs and the usefulness of these
BLUPs for simultaneously modelling the
main efects of genotypes and GE has been
studied by Crossa et al. (2006). Te authors
obtained BLUPs of breeding values using
genetic variance-covariance structures
constructed as the Kroneker product (direct
product) of a structured matrix of genetic
variances and covariances across environ-
ments and a matrix of genetic relationships
between strains, A.
Usually association studies do not include
modelling GE simultaneously to the incorp-
oration of matrices Q (representing infor-
mation from population structure) and A
(denoting the additive relationship matrix).
Furthermore, COP information is rarely
incorporated in association mapping stud-
ies. We show how information on covariance
among relatives together with population
structure and GE can be used to search for
relationships between marker polymor-
phism and phenotypic variability.
Linear mixed model with covariance
between relatives and population
structure
Tis model is the same as that used by Crossa
et al. (2006) for ftting data from g geno-
types, s sites and r replicates (in each site),
assuming that the relationship of the geno-
types is measured by the g g COP = f
ii
matrix:
S R G
Y = X b + Z r +Z g +e (14.9)
where
S
X is the design matrix of 0s and 1s
relating Y to the fxed efects of sites (b), and
R
Z and
G
Z are the design matrices of 0s and
1s relating Y to the random efects of repli-
cates within sites (r) and genotypes within
sites (g), respectively. Te random efect e
contains random efects of residuals within
sites. Vectors r, g and e are assumed to be
normally distributed with zero mean vectors
and variance-covariance matrices R, G and
E, respectively. Te variance-covariance
matrix G combines the main efect of geno-
types and GE.
For each Diversity Array Technology
(DArT) marker, the BLUPs of the lines were
used to create the contrast for testing the
null hypothesis of no diference between the
BLUPs of the lines with the mth DArT marker
= 0 and the BLUPs of the lines with the mth
DArT marker = 1. Tis was done using the
variance-covariance matrix of the BLUPs of
the lines obtained from Eqn 14.9. An overall
test for the null hypothesis was developed
and used across all subpopulations obtained
from the population structure study.
Results
Results from application of this linear mixed
model to an analysis of DArT markers in
relation to disease traits in historical
CIMMYT wheat trials show that some mark-
ers were signifcantly associated with the
measured traits in chromosomal regions
where genes or QTLs have been previously
reported; also, signifcantly associated
2
8
0
J
.
C
r
o
s
s
a
e
t
a
l
.
Table 14.7. Location of signifcant DArT markers (prefxed wPt) associated with leaf rust found in three historical CIMMYT Elite Spring Wheat Yield Trials
(ESWYT) for each chromosome and the reported Lr genes and QTLs (adapted from Crossa et al., 2007).
a
Short arm (S) Long arm (L) Unknown arm
Chromosome DArT (wPt) Lr gene and QTL DArT (wPt) Lr gene and QTL DArT (wPt) Lr gene
1A 5374f, 2872, 4029, 6709 Lr10 8016, 0128
1B 1328, 3465, 4434, 0974,
6427, 8986, 1781,
5065, 2614, 5678,
5363, 6777, 5801,
6117, 6833, 8616, 2315
Lr26, QTL 0944, 2526, 4129 Lr46 2019, 5316,
1139
Lr33, Lr44, Lr55,
Lr51
1D Lr21, QTL 3743 Lr40, Lr42, Lr43
2A 3114 Lr17a, Lr17b, Lr35, Lr45 Lr38 6207 Lr11
2B 0100, 8326 Lr13, Lr16, Lr23, QTL 0049 Lr50 0094, 4559 Lr35
2D Lr2a, Lr2b, Lr2c, Lr15,
Lr22a, Lr22b, Lr39,
Lr41, QTL
Lr54
3A 1562, 9268, 1688 QTL
3B 0365, 7015, 7142, 5716,
9310, 9170, 6047,
5105, 6802, 5769,
0384, 8096
Lr27
3D 1336, 9401 Lr24 Lr32
4A 4620 Lr28 5434, 7924 Lr25
4B 1272, 3908 Lr12, Lr31, QTL Lr30
4D QTL
5A 0605 4249
5B Lr52 3569, 4996, 5896, 3030,
9598
Lr18 4703
5D 1400 Lr1
6A 7475, 0864, 8006, 7938,
9075
4229 Lr56
6B 3130, 4720, 3733 Lr36, Lr53 Lr3a, Lr3bg, Lr3ka,
Lr9
7A 6034, 8789 Lr47 Lr20 4553
7B 7887, 4300, 0600, 7108 Lr14a, Lr14b, QTL 9746
7D 1269, 3328 Lr29, Lr34 Lr19 0934, 5150,
0366
a
The location of Lr genes as per USDA-ARS-Cereal Disease Lab (http://www.ars.usda.gov/Main/docs.htm?docid=10342) and other publications. QTLs at these locations were reported
in other publications. The signifcant DArT markers and Lr genes with unknown location are given in the last two columns.
Statistical Models for GE Interaction 281
markers were found in regions where neither
genes nor QTLs have been reported for these
traits. Several of the known catalogued
genes, such as Lr47, were recently trans-
ferred from alien or related species and thus
not expected to be present in the material
included in this study.
Concerning disease traits, the variation of
pathogen races occurring at diferent loca-
tions is likely to reduce the identifcation of
race-specifc resistance. Most of the known
catalogued genes are race-specifc and efec-
tive only in some geographic areas. In this
study, disease pathogens may not have been
present at high frequencies in the years when
genotypes were evaluated in multiple loca-
tions. For example Lr3a (Table 14.7), which
occurs in several CIMMYT wheat lines, could
not be chosen in this study because virulence
to this gene is common worldwide. Virulence
to Lr1 is also common in most wheat grow-
ing areas, and the gene would have been dif-
cult to detect even if more markers had
mapped to the chromosome containing Lr1.
Loss of efectiveness due to the presence of
virulent races is probably the reason why we
could not detect the chromosomal regions
for some genes known to be present in
CIMMYT wheat materials. Only a few genes,
such as Lr34/Yr18, Lr46/Yr29 and Yr30/Sr2,
are non-race specifc in nature and should
have small-to-intermediate efects across
diferent environments. Analyses did, in fact,
identify chromosomal regions carrying the
above genes (Table 14.7).
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Index
285
abiotic stresses 3
engineering solutions 34, 107, 108
heat 73, 74
inundation 98100
low fertility (low-N) 132133
salinity 9596
anthropogenic, extent 93, 93
toxicity, mineral 72, 79, 93, 128, 188
water defcit 7274, 73, 220
waterlogging 9698
adaptation
agronomic strategies 77, 107108, 255
assessment tools 117118
autonomous 4344
to combined stress factors 72, 108109, 220
genetic traits 24, 7778, 219220
planned 44
aerobic rice 129130, 189190
aerosols 10, 16
agricultural pests and diseases 23, 2528, 42
chemical control 65, 200201
cultural control measures 6465, 182,
205212
dispersal 5657, 63
epidemiology
disease triangle 5152, 52
infection and colonization 5356
latency 56
modelling and forecasting 6566, 248,
255, 257
evolutionary forces 57, 5859, 60
gene expression 6162
geographical gene fow 61
interspecifc hybridization 62
mutation and genetic drift 57
reproduction and diversity 62
survival rate, pathogen/pest 53
see also diseases; pests; soilborne diseases;
weeds
agricultural systems
choice of crops 6465, 182
conservation agriculture 5, 170, 179188
integrated management 63, 66, 107108
low-input ideotypes 146147, 263
monoculture or rotation 64, 169170,
209210, 211212
sustainability 107, 170171
workforce 39
allele mining 229
amphiploids 102104, 220221
anthesissilking interval (ASI), maize 82, 272
aquaporins 78
backcrossing, marker-assisted 223
barley, climate response predictions 45, 45
biological control 27, 65, 201202
biological nitrifcation inhibition (BNI) 165
biophysical interactions 24, 25
biotechnology 219, 221223, 222, 237
see also genetic modifcation
Page numbers in bold refer to fgures and tables.
286 Index
biotic stresses see agricultural pests and diseases;
weeds
Brassica sp. seed meal, soil amendment
206208, 207, 208
breeding see crop breeding
C
3
and C
4
crops
introduction of C
4
genes 78, 142, 145, 223
irrigation needs 74, 76
responses to CO
2
levels 42, 139140
canopy temperature (CT)
factors afecting 75, 250
as root development indicator 8182
carbon capture see photosynthetic efciency;
sequestration, carbon
carbon dioxide (CO
2
)
abundance and global warming potential
177178, 178
acclimation 30, 74
elevated levels 139
efect on disease susceptibility 62
fertilizing efect 25, 2830, 41, 4142, 139
interaction with heat and drought 74,
76, 140
response modelling 250
root/shoot partitioning 144
emissions projection 15, 15, 152
fxation 141143
Cartagena Protocol on Biosafety (CBD) 236
cereals
global production and trade 39, 46, 115116
response to warming 40, 120, 126, 126
temperate (wheat, barley) 72
tropical (rice, sorghum, maize) 71
CIMMYT see International Maize and Wheat
Improvement Center
cisgenics 228
climate change
20th century observations 10
historical impacts 1
predictions 12, 1011
annual variability 42, 126
extreme events 2021, 94
rainfall patterns 1920, 92, 94, 179
sea level rise 21, 2122, 92, 94
temperature 1819, 71
rate of change 141
see also modelling, climate
conservation agriculture (CA) 5, 170
adoption encouragement 192193
economic benefts 179180
efects on soil properties 184188, 185
impact on GHG emissions
carbon dioxide 188189
methane 189190
nitrous oxide 190192
principles 180
crop rotation 181
ground cover and residue retention
181184, 183, 184
zero tillage 169, 181, 192
range of applicability 180181
Consultative Group on International
Agricultural Research (CGIAR) 44
consumption patterns, food
related to wealth 39
urban and rural 39
cotton, climate response predictions 23
Coupled Model Intercomparison Project (CMIP)
12
cover crops 182
crop breeding
for abiotic stress tolerance 34, 117118
heat and drought 77, 78
salinity, waterlogging and inundation
100, 101, 108109
cultivar design 78, 221223
feld testing
in disease hot spots 127
managed stress screening 130, 132134
multi-environment trials (METs)
117118, 129, 264, 271
shuttle breeding 117118, 131
statistical analysis see statistical models
germplasm resources 4, 84, 100101, 102,
146
international collaboration 116117,
133134, 232233
pest and disease resistance 23, 6364, 201
selection performance indicators
canopy temperature 8182
glaucousness 81
grain yield 132
relative growth rate (RGR) 103
root porosity 97
success prediction 135
techniques 6, 7980, 106107, 220221
speed of delivery 219, 225, 234
see also genetic modifcation; marker assisted
selection
crop productivity
carbon dioxide enhancement efects 2830,
41, 4142, 139
Index 287
empirical analysis 23
mechanistic crop modelling 2324,
249251
niche-based model approaches 2425
predicted yield impacts 2225, 4445, 45
crops
choice of 6465, 182
genetic diversity 220221
induced 221
varieties
diferences, modelling parameters
250251, 265
geographical range 117, 271
older, useful traits in 143
wild relatives 79, 80, 101104, 165, 220
priority geographical niches 248, 254
cultivable land, global 24
cuticular wax thickness 81
Decision Support System for Agrotechnology
Transfer (dssat) 23, 254
diseases
ecosystem introductions 61, 62
pre-emptive breeding 127
efects of microclimate 2728
food safety impacts 28
fungal infection and humidity 53
pathogen species shifts 53, 56
responses to host stress 56, 78
spread 27, 5657, 63
virulence 62
virus vectors 28, 53
see also soilborne diseases
Distichlis spp. (saltgrass) 104
drought
failed season models 248, 255
frequency and intensity 20, 179
impact on poor farmers 44
stress adaptations 72, 73, 220
economy, food
autonomous market responses 43
climate change impacts 38
global 4547, 46
regional 47
consumption patterns 39, 115, 116
food prices 46
non-climatic trends 3940
total food production 39, 115116
trade 39, 46
use and limitations of economic models 46
edaphic factors see soils
El Nio-Southern Oscillation (ENSO) 10,
2021, 42
emissions reduction measures
agricultural options, potential 152, 156,
188192
agrochemical input reduction 145146, 230
IPCC guidelines terminology 158
nitrifcation inhibitors 84, 146, 164165
environments
characterization techniques 74, 131133, 135
increasing variability of 263264
marginal 78
target population of (TPE) 117, 129, 271
epidemics
climate change impacts 51, 57, 66
eruption conditions 5152, 52
forecasting 6566
Erosion Productivity Impact Calculator (epic)
23, 249, 255
erosion, soil 169, 180, 182
ethylene, heat stress signalling 78
evapotranspiration (ET) 40, 140
expressed sequence tag (EST) mapping 228,
229230
extreme weather events 2021, 94
factorial regression (FR) analysis 272275
farmers
adaptation to climate change 38, 4344
adoption of new practices 192193
choice of crop varieties 129
Eh control water management 161162
fertilizer efciency savings 166167
optimal land use assessment 108
fertilizers
application practices 163164
management technologies
leaf colour charts 162
sensor-based 163, 166167
nitrifcation inhibitor additives 164165,
190191
nitrogen inputs 144, 145146, 162
organic amendments 206208
P/K/N balance 165
slow/controlled release 164
fooding, coastal 22, 94
food security 22
geographical regions at risk 47, 128
global coordination 1, 116117
improvement strategies 78
288 Index
fossil fuels, use in agriculture 167, 168, 188
Fourth Assessment Report (IPCC, 2007) 9, 11, 18,
42, 245
free-air CO
2
enrichment (FACE) experiments
2930, 30, 41, 4142, 45
Fusarium head blight (FHB) 28, 53, 209
General Large Area Model (glam) 23, 24
genetic modifcation (GM) 4, 6
adoption needs and prospects 147148,
230231, 231
development pathways 233235, 235
regulation 235236, 236
technology access 232233, 233, 236,
238
candidate genes 8485, 104, 105106, 227,
228230
drought tolerance improvement 142
economic implications 231232, 232,
233234
herbicide resistance 145
root architecture and functions 146
rhizosphere disease suppression 212
Rubisco CO
2
fxation 78, 141142, 223
transformation techniques 226228
genomic (genome-wide) selection (GS/GWS) 86,
134, 264
genomics research 221222, 226
non-targeted mapping 229230, 230
targeted mapping 228229
genotype environment (GE) interactions 7, 85
defnition and causes 264
crossover interaction (COI) 269271,
271
error in estimates 129
phenotype and molecular marker
associations 279281, 280
trial data analysis 248
measurable values 265
see also statistical models
geographic information systems (GIS) 67, 131
coupling with crop simulation models
253254
defnition 246247
integration with climate modelling data 246,
254, 255
range of uses 247, 247249
global climate models (GCMs) 1112, 13, 16
spatial resolution 1617
government/international measures 43, 44
active stakeholder participation 193
agricultural research 116117
GM technology development 231232,
232, 234236
early warning systems, disease outbreaks 66
tools for decision making 258
green manures 208209
Green Revolution 1, 4, 44, 79
wheat breeding achievements 117118
greenhouse gases (GHGs) 13, 139, 151152
agriculture contribution 144145, 151, 152,
177180
efects of management practices 157,
160170, 188192
fossil fuel use 167, 168, 188
anthropogenic sources 177179, 178
national inventories (NIGs) 158
groundnut, climate response predictions 23
halophytes, domestication 104, 108
harvest index (HI) 73, 77, 144
heat stress
adaptation traits 73
avoidance, rice fowering 84
evaporative cooling 74
managed stress screening, rice 130131
physiological consequences 7677
short-term heat exposure 42, 77, 140
herbicide tolerance 145, 181
selectable markers 227, 227
Hordeum marinum, trait selection 102104, 103
humanitarian climate change impacts 39
food security 22, 47, 128
malnourishment 46, 46
hurricanes 20
hypoxia, waterlogged roots 9697, 103
in vitro induced variation 221
infrastructure 39, 44
insertional mutagenesis 221
intellectual property and patents 232233, 233
Intergovernmental Panel on Climate Change
(IPCC)
emissions scenario development 1314
Fourth Assessment Report (FAR, 2007) 9, 11,
18, 42, 245
guidelines for emissions statistics 158, 158
Tird Assessment Report (TAR, 2001) 9, 10
Working Group I (WGI) 10
International Maize and Wheat Improvement
Center (CIMMYT) 7980, 117118,
126127, 133
Index 289
International Rice Research Institute (IRRI) 79,
83, 130, 131
irrigation management guidelines 161162
International Wheat Improvement Network
(IWIN) 118
Internet, use in epidemic forecasting 66
introgression techniques 84, 102, 104, 220
inundation
conservation agriculture benefts 184, 187,
187
physical stresses 9899
tolerance and amelioration strategies
99100, 130
ion toxicity 95, 95, 97
tolerance mechanisms 9596
transgene candidates for tolerance 105
irrigation 42
brackish water, consequences 9394
cost of expansion 44
management techniques 161162
permanent raised beds 181, 186
water source reliability 128, 179
land use and land cover change (LULCC) 12
latency period, pests and diseases 56
livestock, global production and trade 39
fodder sources 104, 182
maize
anthesissilking interval (ASI) 82, 272
breeding programmes for drought stress 82,
132133
foret abortion in drought 7778
genomic selection (GS) 134
global production 152, 154
mega-environment identifcation 131132,
248
response predictions 23, 24, 4445, 45
with simulation models 253, 253, 255
management practices 251
cropping systems 156, 169170
fertilizer application 162167
organic residue retention 168, 181184,
183, 184
pest/disease control 6465, 182, 205209
tillage 165, 168169, 181, 192193
mapping, genetic 228230
marker assisted selection (MAS) 3, 6, 7980, 85
high throughput pheno/genotyping 225226
marker systems 223, 224225
recurrent (MARS) 86, 130, 264
screening support, conventional breeding
223224, 233, 234
mechanistic crop modelling 2324, 249251
mega-environments (MEs) 4, 118, 120, 126,
135136
maize, identifcation using GIS data
131132, 248
rice, hydrological 128, 129
wheat, CIMMYT classifcation 118126,
119, 121125, 248
related to potential heat stress 254255,
256
metabolite profling 224
methane (CH
4
)
abundance and global warming potential
152, 178, 178
emissions from irrigated rice 144, 156,
158160, 159, 189190
microbial communities 168, 169, 182
analytical tools 213
introduction of biocontrol agents 202
model species 147, 222
modelling, climate 2
confdence level improvements 11
global circulation (GCMs) 1112, 13, 16
GIS data compatibilty 246, 255
regional climate (RCMs) 1618
Special Report Emissions Scenarios (SRES)
10, 1215, 14, 255
uncertainty 10, 1516, 107, 254
modelling, crop productivity see simulation
modelling; statistical models
monsoons 42
multi-location testing
advantages and disadvantages 117, 135136
germplasm distribution networks 131,
133134
trial data interpretation 132133
using genomic selection 134
mutagenesis 221
National Center for Atmospheric Research
(NCAR) 19, 21
niche-based (agroecological zoning) approaches
2425
nitrous oxide (N
2
O)
abundance and global warming potential
152, 178, 178179
emissions from arable cropping 159, 160,
164
290 Index
nitrous oxide (N
2
O) continued
emissions from arable cropping continued
infuence of tillage/residue regime
190192
mid-season paddy-feld drainage 161
nitrifcation inhibition 84, 146,
164165
surplus inorganic nitrogen 162164,
165167
nutrients, mineral
cycling 162, 167, 190191
defciencies, micronutrient 72, 76
nitrogen use efciency (NUE) 143144, 144,
147
uptake efciency 77
see also fertilizers
osmotic adjustment 96
ozone (O
3
) 42
partial least squares (PLS) regression analysis
275, 276
partitioning, root/shoot 144, 223, 250
pesticide use and toxicity 28, 65
pests
biological control 27, 65, 201202
distribution and abundance 26
integrated pest management (IPM) 65, 66,
182
phytosanitary precautions 63
resistance, molecular markers 80
winter survival 26, 53
phenology and stress avoidance 77, 99, 251
phenotyping 86
high-throughput technologies 225226
marker-assisted recurrent selection (MARS)
86
and predictive plant modelling 222
photorespiration 76, 77, 140, 142
photosynthetic efciency
carbon metabolism factors 141142
at high temperatures 140, 143
related to nitrogen uptake 143144
simulation model parameters 249250
sink plasticity 143, 223
under water stress 142
phytoremediation 212
population growth 39
potato late blight 56, 62, 65
probability distribution function (pdf) 44
productivity see crop productivity
promoters (DNA transcription) 227228
quantitative trait loci (QTL)
colinearity, evolutionary 229
drought and heat adaptations 78, 83, 8586
environmental covariables 272276, 276
genome-wide selection (GWS) 86
identifcation of key genes 146, 225, 228
multitrait multi-environment analysis
273275
pyramiding multiple traits 224
radial oxygen loss (ROL) barriers 9798
radiation use efciency (RUE) 73, 250
rainfall patterns
bufering by conservation agriculture 184,
186, 186187, 187
failed season modelling 248, 255
predicted changes 1920, 4041, 92, 94
regional climate models (RCMs) 1618
rice
climate change response predictions 23, 40,
41, 255, 257
irrigated and rainfed crops 128129
fowering, drought stress responses 8384
global production 152, 153
comparison of fooded and aerobic 190
fooding management regimes 129, 152,
158, 161162
hydrological mega-environments 128, 129
inundation tolerance 99100, 102, 130
methane emission from rice felds 144, 156,
158161, 159, 189190
root growth, near-isogenic lines (NILs) 83
roots
biological nitrifcation inhibition (BNI) 165
exudates 209
interactions with rhizobacteria 205
nutrient uptake optimization, transgenic 146
porosity (aerenchyma) 97, 98, 99
radial oxygen loss (ROL) barriers 9798
role in heat/drought stress mitigation 77
rotation, crop 169170, 181, 209210
Rubisco enzyme activity 78, 141142, 223
salinity
increase, with sea level rise 22, 94
physiological tolerance 9596
Index 291
primary and secondary causes 93
toxic efects 95, 95, 97
saltbushes (Atriplex spp.), as fodder 104
sea level rise 21, 2122, 92, 94
seasonal forecasting 1718
senescence delay, sorghum 83
sequestration, carbon 152, 167170, 188189
shuttle breeding 117118, 131
simulation modelling 67, 74, 224
accuracy and data availability 257
data inputs required 249, 249251
named examples in use 246, 249
operation 251253, 252, 253
use of GIS data 253254
smallholder/subsistence farming 22, 47, 255
sodicity 93, 188
soilborne diseases 56, 56
control alternatives 200202, 201, 211
naturally suppressive soils 202203
efect of green manures 208209
examples showing disease decline
203204
functional microbial populations
204205
infuence of crop cultivar genotype
210211
responses to organic amendments
205208, 207, 208
prevalence and yield losses 200
responses to crop rotation 209210,
211212
soils
erosion 169, 180, 182
microbial community 168, 169, 182,
202204
moisture level, crop responses 4041,
189190
organic carbon (SOC) pool 167170
porosity 187188
temperature 188
water-holding capacity 72, 182, 184
sorghum
crop importance and uses 8283
stay-green drought breeding 8283
soybean
planting date modelling 251253, 252
response predictions 23
Special Report Emissions Scenarios (SRES) 10,
1215, 14, 255
starch synthase, soluble 78, 85
statistical models
factorial regression (FR) 272275
linear two-way fxed-efect 265266, 267
linearbilinear 269271
fxed-efect 266, 268, 268
mixed-efect 268269
partial least squares (PLS) 275, 276
structural equation (SEM) 272, 276277
sterility, caused by heat/drought stress 77, 78,
8384
suppressive soils see soilborne diseases
sustainable technologies 46, 170171, 192193
temperature changes
canopy temperature (CT) 75, 78, 8182
critical maximum, for pollination 140
crop growth
optima 74, 246
radiation use efciency (RUE) 73, 250
responses to increased warmth 40, 77,
140, 143
efect on disease resistance genes 61, 201
efects on seawater/ice 21, 92
pathogen/pest survival 53
predicted rate and extent 1819
Tird Assessment Report (IPCC, 2001) 9, 10
tillage 4, 5
alternative weed control measures 181
efects on GHG emissions 165, 168169,
188192
intensive, long-term efects 180
stubble-borne disease risk 65
transcript profling 222
transformation, genetic 226228
transgenic technologies see genetic modifcation
(GM)
transpiration efciency 77, 78
impact on nitrogen uptake 144
uncertainty
climate projections 10, 1516, 107, 254
temperature sensitivity, crop 40
urbanization, efect on consumption patterns
39
vegetative index, crop canopy 163
warming, global
potential (GWP) of gases 152
predictions 1819
292 Index
water supplies 42, 72
management in rice cultivation 161162
quality, and water table depth 93, 94
see also irrigation
water use efciency (WUE) 62, 72, 79, 81, 144
waterlogging
root-zone hypoxia 9697, 103
tolerance mechanisms 9798
weeds 181, 190
wheat
amphiploidy, with wild grasses 102104,
220221
breeding for wide geographical range
117118, 126128
climate change response predictions 23, 24,
45, 45, 120
drought adaptation breeding approaches
7980, 127128
Australian breeding programme 79
hot, dry environments 8081
fungal diseases 53, 56, 63, 64, 203
global production 152, 155
hot, irrigated environments 81
mega-environments 118126, 119,
121125, 179
model prediction of heat/drought stress
254255, 256
root characteristics 81
salt-tolerant cultivars 102
Yaqui Valley case study 163, 165167
wide crossing techniques 7980, 84
Yaqui Valley spring wheat case study 163,
165167
yield
impacts of climate change 2225, 4445, 45
temperature increase and cereals 120,
126, 126
improvement through breeding 79, 80
component traits 142143, 277278,
278
heritability (H), broad-sense 132
trial SEM analysis 276277, 277
optimization potential 145, 223
stability 126127, 143, 264