Plant Disease  2021  105:3956-3966  https://doi.org/10.

1094/PDIS-03-21-0594-RE

Resistance to Phytophthora infestans Clonal Lineage US-23 in Potato Cultivars

and Its Relationship with Early Blight Resistance and Tuber Yield
Weiya Xue,1 Kathleen G. Haynes,2 and Xinshun Qu1,†
1
Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, PA 16802
2
Genetic Improvement of Fruits and Vegetables Laboratory, U.S. Department of Agriculture Agricultural Research Service, Beltsville,
MD 20705

Abstract
Resistance to late blight caused by Phytophthora infestans clonal line- showing resistance and 32 cultivars showing moderate resistance
age US-23 in 217 old and modern potato cultivars was evaluated in were identified. The 217 cultivars were also evaluated for foliar matu-
field trials in 2016 and 2017 in Pennsylvania. Significant differences rity, tuber yield, and resistance to early blight caused by Alternaria
in resistance were found among these cultivars (P < 0.0001). Signifi- solani. A few cultivars with late blight resistance independent of late
cant interaction between cultivars and environments was found (P < maturity were found. Late blight resistance and early blight resistance
0.0001). The values of relative area under the disease progress curve were positively correlated, and 17 cultivars possessed resistance to
ranged from 0 to 0.5841 in 2016 and from 0 to 0.5469 in 2017. both diseases. Yield trade-off associated with late blight resistance
Broad-sense heritability of late blight resistance was estimated to be was not observed among the cultivars in the absence of disease
0.91, with a 95% confidence interval of 0.88 to 0.93. Cluster analysis pressure.
classified the cultivars into five groups: resistant, moderately resistant,
intermediate, moderately susceptible, and susceptible. Thirty cultivars Keywords: disease management, oomycetes, vegetables

Late blight caused by oomycete pathogen Phytophthora infestans conditions are conducive to disease development. Frequent applica-
is the most economically important disease in potato production. The tion of fungicides has resulted in the emergence of fungicide insensi-
disease is favored by high humidity (>90%) and cool temperature tivity in P. infestans (Saville et al. 2015). Mazakova et al. (2011)
(12 to 18 C) (Hirst and Stedman 1960; Sujkowski 1987). The patho- found that 10.2% of 547 isolates of P. infestans were insensitive to
gen can infect leaves, stems, and tubers, and the disease can destroy metalaxyl in the Czech Republic from 2003 to 2008. Fluazinam was
the entire field production in just a few days under favorable envi- found to reduce efficacy against P. infestans in the Netherlands
ronmental conditions (Fry et al. 1983). In recent years, increases in (Schepers et al. 2018).
incidence and severity of late blight on potato have been reported, Cultivars possessing a high level of resistance or even partial
and new genotypes or clonal lineages of P. infestans have emerged resistance to late blight would provide a desirable alternative disease
in the eastern United States (Hansen et al. 2016; Fry et al. 2013). control option. After the Great Famine in Ireland in 1845 to 1849,
Before the early 1990s, P. infestans US-1 was found to be the major when potato production failed because of late blight, breeding pota-
lineage in the eastern United States (Goodwin et al. 1994). During toes for resistance to late blight became one of the main priorities of
the 1990s, US-8 and US-11 were the major lineages in the eastern potato breeders. Identification of genetic resistance resources is a
United States. From 2002 to 2009, US-8 was the dominant lineage basic prerequisite for successful resistance breeding. Various levels
in the eastern United States, although five other lineages (US-20, of resistance to late blight have been reported in tetraploid breeding
US-21, US-22, US-23, and US-24) were found (Hu et al. 2012). clones and cultivars and wild diploid relatives of potato. Platt and
Four lineages (US-8, US-22, US-23, and US-24) were found from McRae (1990) assessed 116 breeding lines and cultivars between
2009 to 2020, with US-23 as the major lineage in the eastern United 1980 and 1988; they found that most of the breeding lines and culti-
States (Fry et al. 2013; Hansen et al. 2016; USAblight [https:// vars were susceptible to P. infestans, and only 10 breeding lines and
usablight.org]). cultivars showed more resistance than the control Sebago. Douches
Currently, application of fungicides is commonly used to effec- et al. (1997) evaluated 147 potato cultivars and breeding lines and
tively control late blight in field. Different types of protective and found that two-thirds of the cultivars and breeding lines tested were
curative fungicides against late blight are available on the market. Lin- very susceptible to late blight. Enciso-Rodriguez et al. (2018) evalu-
eage US-23 is an A1 mating type and is generally sensitive to mefe- ated 273 tetraploid potatoes breeding clones and reference cultivars
noxam (Hu et al. 2012). This means that late blight caused by lineage against late blight over 9 years and found that host resistance to late
US-23 can be controlled with mefenoxam containing fungicides. blight varied among different environments and different genotypes
Although fungicides worked well on late blight, they raised produc- of P. infestans. Late blight resistance has been found in several wild
tion costs and environmental concerns. Fungicides should be sprayed diploid Solanum species. Douches et al. (2001a) identified 56 geno-
every 5 to 10 days to provide protection when environmental types of late blight-resistant germplasm among 618 wild Solanum
species accessions and hybrid cultivated potato × wild species. Wild
potato germplasm has been used broadly in breeding practice
†
Corresponding author: X. S. Qu; [email protected] (Darsow 1995; Swiezynski et al. 1991). Karki et al. (2021b) screened
384 accessions of wild relatives of potato against US-23 with a
*The e-Xtra logo stands for “electronic extra” and indicates that two detached leaf assay, and 39 accessions were found to be resistant.
supplementary figures and four supplementary tables are published online. With the emergence of new genotypes of P. infestans with US-23 as
the major clonal lineage in recent years in the eastern United States,
The author(s) declare no conflict of interest. there is a need to evaluate and identify resistance resources against
this pathogen lineage.
Accepted for publication 5 July 2021. Modern potato breeding is usually focused on many traits simulta-
neously, of which late blight resistance is only one of many. Other
© 2021 The American Phytopathological Society traits such as early maturity and resistance to other diseases are

3956 Plant Disease / Vol. 105 No. 12

considered in potato breeding programs. Late blight has been reported RS2012P1, RS2012P2, and RS2014P) of P. infestans clonal lineage
to be strongly associated with late maturity (Plich et al. 2016; US-23 were used as inoculum in both years. These four isolates
Toxopeus 1958; Visker et al. 2004). In general, late maturing varieties were isolated from naturally infected leaves of potatoes found in
are more resistant to late blight than the earlier maturing varieties. Pennsylvania in previous years and were maintained on Rye A
However, late maturity is not a desirable quality in potato cultivars. media (60 g rye, 20 g sucrose, 15 g agar per liter). The isolates were
Identification of cultivars with late blight resistance independent of genotyped by Cornell University through the USABlight project
late maturity would be an attractive solution to the problem. Early (https://usablight.org/), a national project on tomato and potato late
blight caused by fungal pathogen A. solani is increasing in frequency blight. Before the experiments, the isolates were grown on V8/Lima
in the United States and Europe because of climate changes bean agar to induce sporulation. On August 15, 2016. and August
(Runno-Paurson et al. 2015; Tymon et al. 2016). Growing cultivars 14, 2017, spreader rows were spray-inoculated with a mixture of the
that are resistant or partially resistant to both late blight and early four isolates of P. infestans clonal lineage US-23 at a concentration
blight would be a desirable option for potato growers, although no of 2.1 × 105 sporangia/ml and 8.8 × 104 sporangia/ml, respectively,
early blight immune germplasm has been found in previous research to promote a uniform spread of the pathogen to all treatment plots.
(Abuley et al. 2018; Boiteux et al. 1995; Xue et al. 2019). In breeding Overhead sprinklers were used for approximately 1 h daily when the
practice, multiple disease-resistant potato clones have been achieved weather was dry and hot to increase humidity in the plant canopy
(Jellis 1992; Platt et al. 2009). Jansky and Rouse (2003) found multi- after inoculation. A potato field infected with late blight 32 days after
ple disease resistance in interspecific hybrids of potatoes. Some newly inoculation in 2017 is shown in Supplementary Figure S1. Late
released cultivars such as Defender and Palisade Russet or advanced blight disease severity ratings were determined by visually assessing
breeding clones showed resistant to both early blight and late blight each plot and estimating the percentage of diseased foliage on a 0 to
(Novy et al. 2006; Novy et al. 2012; Meier et al. 2015). However, 100% scale. Disease assessments were made on August 25 and
correlations among different disease resistances have not been clearly September 1, 7, 12, and 16 in 2016 and on August 25 and Septem-
clarified in commercial potato cultivars. ber 1, 5, 8, 11, and 15 in 2017. Disease data were calculated as area
The deployment of late blight-resistant potato cultivars is the best under the disease progress curve (AUDPC) (Shaner and Finney
way to control the disease. However, a trade-off may occur between 1977) for each plot. AUDPC were transformed into relative AUDPC
resistance and yield, and susceptible cultivars tend to out-yield resis- (RAUDPC) by dividing by 100 times the duration of days of disease
tant cultivars in the absence of disease. It has been predicted that assessment (Fry 1978). It should be noted that the experiments were
R gene resistance to pathogens comes at the expense of plant fitness designed with two replications because of the large number of culti-
(Brown 2002). The development of cultivars with elite agronomic vars evaluated and the limited field size. There were no significant dif-
traits and production quality are major objectives in potato breeding. ferences in RAUDPC between replications in 2016 (P = 0.46) and in
Tuber yields have been increasing from an average of 5.6 t ha−1 to 2017 (P = 0.37). The 217 cultivars were evaluated for early blight
>50.8 t ha−1in the United States from 1920 to 2019 (Douches et al. resistance in separated trials in 2016 and 2017 as reported in our pre-
1996; https://www.nass.usda.gov). Thus, the correlation between vious study (Xue et al. 2019). Briefly, early blight was assessed by
potato yield and disease resistance needs to be addressed. This infor- visually assessing each plot and estimating the percentage of diseased
mation can help potato breeders in dissecting the fitness costs associ- foliage on a 0 to 100% scale after inoculation. The assessments were
ated with disease resistance in potatoes. made every 3 to 5 days. The disease data were expressed as relative
Although late blight has been studied widely, an assessment of the area under the disease progress curve (RAUDPC).
disease resistance among a large number of released cultivars under Foliar maturity and tuber yield assessment experiments. The
the same growing conditions is lacking, especially against new geno- 217 potato cultivars were planted on May 14, 2016, and May 16,
types of the pathogen. There are hundreds of old and modern potato 2017, at the Pennsylvania State University Russell E. Larson Agri-
cultivars in the United States, but the status of late blight susceptibility cultural Research Center in Pennsylvania Furnace, PA. The experi-
to lineage US-23 in most of these cultivars is unknown. In this study, mental design was a randomized complete block with two
we evaluated a collection of 217 old and modern tetraploid potato cul- replications. The plots were 1.82 m long, with eight seed pieces
tivars released in the United States and other countries for late blight planted 20.32 cm apart in each plot and 1.52-m breaks between plots
resistance, maturity, and yield. The objectives of this study were to (i) within a row. Commercial crop management practices were applied
determine the levels of foliar resistance to current predominant P. throughout the growing season. Late blight was not observed in the
infestans clonal lineage US-23 in these cultivars; (ii) determine the fields in both years. Tubers were harvested on September 28, 2016,
correlation between late blight and early blight resistance and identify and October 6, 2017, and yield data were collected.
cultivars with resistance to both diseases; and (iii) determine the fit- Foliar maturity of the potato cultivars was evaluated in 2017 and
ness cost in terms of yield of late blight resistance in potatoes. 2018 at the Pennsylvania State University Russell E. Larson Agri-
cultural Research Center in Pennsylvania Furnace, PA. Maturity was
rated at 6 levels: 1 = very early maturity; 2 = early maturity; 3 =
Materials and Methods medium early maturity; 4 = medium late maturity; 5 = late maturity;
Plant materials. The USDA ARS-Beltsville Potato Breeding Pro- and 6 = very late maturity. Maturity was assessed according to
gram maintains a collection of 217 tetraploid cultivars used in this leaves senescence at 100 days after planting. Cultivars Dark Red
study (Table 1) in Presque Isle, Maine. Tubers harvested in Presque Norland, Lehigh, and Torridon were used as check cultivars for very
Isle were shipped to Pennsylvania for field disease, yield, and matu- early maturity, medium late maturity, and very late maturity, respec-
rity evaluations. tively. The maturity of other cultivars was rated by comparing with
Field disease evaluation experiments. Field late blight evalua- the check cultivars. The maturity values represent the mean from
tion trials were conducted in 2016 and 2017 at the Pennsylvania 2 years (no significant year effect on maturity, P = 0.14).
State University Russell E. Larson Agricultural Research Center in Statistical analyses. The square root transformed RAUDPC data
Pennsylvania Furnace, PA. Weather data were collected from a in 2 years were combined for the analysis of variance with the soft-
weather station near the trial fields. A randomized complete block ware STAR version 2.0.1 (IRRI 2014). The correlations between late
design with two replications was used in this study. Cultivars were blight RAUDPC in 2 years (between late blight RAUDPC and early
planted on June 14, 2016, and June 14, 2017. Plots were 1.21 m blight RAUDPC, between late blight RAUDPC and maturity, and
long with five seed pieces planted 20.32-cm apart in each plot and between late blight RAUDPC and yield) were done with R statistical
1.21-m breaks between plots within a row. Each treatment row had software by the Spearman method (R Core Team 2018). Broad-
an adjacent row of a late blight-susceptible cultivar Atlantic as a sense heritability was calculated by the SOMMER R package with
spreader row. Standard crop management practices were followed Linear Mixed Model (Covarrubias-Pazaran 2016). A 95% confidence
throughout the growing season, with the exception that no fungicides interval of this estimate was also obtained (Knapp et al. 1985).
were sprayed for late blight. Natural late blight infection was not Maturity-adjusted RAUDPC values were computed from the lin-
observed in the fields in both years. Four isolates (PA2012P, ear regression of mean maturity on mean RAUDPC by year with the

Plant Disease / December 2021 3957

Table 1. Mean relative area under the disease progress curve (RAUDPC) of late blight, foliage maturity, tuber yield, and late blight resistance cluster of
217 potato cultivars evaluated in 2016 and 2017 in Pennsylvania
RAUDPC Yield (kg ha−1)
a b
Cultivar 2016 2017 Maturity 2016 2017 Clusterc
Aracy 0.0261 0.0673 5.3 21,083.4 41,732.7 1
Arran Consul 0.0326 0.0895 5.8 18,975.1 32,059.2 1
Barbara 0.0233 0.0815 5.5 22,757.7 49,949.1 1
Buckskin 0.0133 0.0818 4.8 25,362.1 33,330.4 1
Bzura 0.0000 0.0000 6.0 19,378.1 50,600.2 1
CalRose 0.0273 0.0751 5.5 18,293.0 40,833.6 1
Cascade M 0.0359 0.0533 4.0 22,230.6 47,406.6 1
Chaposa 0.0047 0.0039 6.0 16,370.6 29,795.8 1
Cherokee 0.0027 0.0042 4.8 22,664.7 38,198.2 1
Chinook 0.0348 0.0830 5.5 25,331.1 47,592.7 1
Croft 0.0156 0.0085 5.8 31,098.0 50,197.1 1
Defender 0.0128 0.0029 5.5 25,703.1 44,988.3 1
Donna 0.0000 0.0632 3.5 23,129.7 30,167.9 1
Gorbea 0.0000 0.0108 5.3 29,516.8 42,941.9 1
Grand Falls 0.0032 0.0000 4.3 30,384.9 40,926.6 1
Greta 0.0057 0.0000 5.0 21,765.5 40,306.5 1
Iker 0.0119 0.0388 4.5 22,819.7 31,538.3 1
Jacqueline Lee 0.0000 0.1233 3.5 27,532.4 38,415.2 1
Kandidat 0.0015 0.0000 4.0 18,789.0 31,098.0 1
Libertas 0.0260 0.0425 5.3 15,781.5 29,423.7 1
LT-2 0.0038 0.0532 5.8 26,292.2 57,415.1 1
Michoacan 0.0000 0.0000 5.3 14,696.4 24,587.0 1
Muziranzara 0.0015 0.0000 5.5 18,758.0 42,631.9 1
Ontario 0.0302 0.0156 6.0 19,812.2 55,312.9 1
Pennchief 0.0009 0.0061 4.3 21,362.4 25,858.2 1
Serrana 0.0382 0.0823 5.0 23,222.7 31,811.1 1
Tacna 0.0000 0.0005 6.0 22,974.7 53,514.6 1
Torridon 0.0000 0.0000 6.0 25,176.1 41,949.8 1
Ursus 0.0000 0.0000 5.8 37,051.0 49,142.9 1
Zarevo 0.0000 0.0000 5.3 15,192.5 21,796.5 1
Alturas 0.0481 0.1489 6.0 20,091.2 50,941.2 2
Bannock Russet 0.0370 0.1348 5.8 15,006.4 48,677.9 2
Bertita 0.0211 0.1092 5.8 10,448.7 32,369.2 2
Blue Mac 0.0864 0.1507 5.5 26,168.2 61,451.9 2
Boone 0.0977 0.1187 5.5 25,269.1 43,252.0 2
Campbell 12 0.0306 0.1794 3.5 27,408.4 29,578.8 2
Cariboo 0.0913 0.1312 4.5 15,316.5 40,058.5 2
Desiree 0.0620 0.1351 5.0 21,579.5 45,360.3 2
Dorita 0.0358 0.1364 3.0 18,696.0 27,284.4 2
Elba 0.0349 0.1519 5.5 27,129.4 43,190.0 2
Ella 0.0825 0.1526 5.3 30,757.0 37,113.0 2
Eva 0.0202 0.1598 3.3 13,239.1 31,594.1 2
Ida Rose 0.0466 0.1949 5.0 22,478.6 51,158.3 2
LaSalle 0.1006 0.1467 4.8 30,788.0 46,972.6 2
Majestic 0.0615 0.1055 5.5 22,571.6 41,515.7 2
Merrimack 0.0143 0.1217 5.3 20,711.3 30,819.0 2
Mirton Pearl 0.0425 0.1514 3.8 27,842.5 43,841.1 2
Monota 0.0252 0.1044 4.8 25,672.1 43,003.9 2
Nampa 0.0884 0.1477 6.0 22,199.6 40,306.5 2
Pawnee 0.1136 0.1348 3.0 30,167.9 29,051.7 2
PennRose 0.1910 0.1354 5.0 29,888.8 40,585.5 2
Pontiac 0.0543 0.1614 3.3 29,330.7 32,183.2 2
Record 0.0495 0.0996 4.8 19,719.2 50,848.2 2
Redskin 0.1105 0.1518 5.0 31,625.1 57,514.3 2
Russet Katahdin 0.0401 0.0961 4.5 20,742.3 35,562.7 2
Russet Kennebec 0.0302 0.1264 5.3 25,269.1 35,965.8 2
Russet Rural 0.0320 0.1121 5.3 21,052.4 37,082.0 2
Saco 0.0893 0.1377 4.8 34,756.6 46,941.6 2
Sebago 0.0432 0.1121 5.3 29,020.7 45,856.4 2
Shepody 0.1113 0.1619 3.0 24,959.0 40,554.5 2
Stobrawa 0.0238 0.1020 4.5 27,222.4 48,770.9 2
Summit Russet 0.0376 0.1007 4.5 14,975.4 28,741.6 2
Acadia Russet 0.0977 0.1807 3.5 25,176.1 46,879.6 3
All Blue 0.0598 0.1595 4.5 27,439.4 40,833.6 3
Alpha 0.0899 0.2204 4.8 16,246.6 35,996.8 3
Anoka 0.1076 0.2507 5.0 21,269.4 37,609.1 3
Arenac 0.1042 0.1948 4.5 17,548.8 23,315.8 3
(Continued on next page)
a
Cultivars were alphabetically organized in each resistance category.
b
Maturity was recorded as 1 = very early maturity; 2 = early maturity; 3 = medium early maturity; 4 = medium late maturity; 5 = late maturity; and
6 = very late maturity. The values were the mean of 2 years’ maturity ratings.
c
Cluster indicates the late blight-resistant level: 1 = resistant; 2 = moderately resistant; 3, intermediate; 4 = moderately susceptible; and 5 = susceptible.

3958 Plant Disease / Vol. 105 No. 12

Table 1. (Continued from previous page)
RAUDPC Yield (kg ha−1)
a b
Cultivar 2016 2017 Maturity 2016 2017 Clusterc
Asun 0.1003 0.2680 4.5 22,974.7 34,756.6 3
Avon 0.0841 0.3326 4.5 23,749.8 39,066.3 3
Beacon Chipper 0.0884 0.1735 4.0 18,975.1 35,345.7 3
Bounty 0.1406 0.2348 3.5 29,919.8 48,553.8 3
Butte 0.0867 0.1911 5.3 17,951.9 44,337.2 3
Calwhite 0.0619 0.2317 5.0 39,128.3 58,785.5 3
Campbell 14 0.0518 0.2192 4.3 17,796.9 27,935.5 3
Carola 0.0759 0.1906 5.0 34,601.6 51,065.2 3
Delta Gold 0.0651 0.1842 3.8 18,261.9 28,493.6 3
DeSota 0.1010 0.2792 3.8 32,524.2 37,826.1 3
Eide Russet 0.0768 0.2579 3.0 25,300.1 43,097.0 3
Erie 0.0799 0.1735 5.0 27,098.4 31,222.0 3
Essex 0.0780 0.2221 3.3 33,268.4 47,654.7 3
Fontenot 0.0565 0.2699 3.3 31,005.0 39,624.4 3
Hampton 0.0430 0.1967 4.3 25,021.0 46,073.4 3
High Plains 0.0932 0.2614 3.0 18,386.0 35,283.7 3
Islander 0.1057 0.3726 4.3 25,951.2 36,182.8 3
Kasota 0.0870 0.1751 3.3 17,517.8 29,826.8 3
Katahdin 0.0731 0.1985 4.3 23,036.7 34,508.6 3
Kennebec 0.0603 0.1829 4.8 30,943.0 50,011.1 3
Lamoka 0.0581 0.1729 3.0 20,339.3 34,260.5 3
LaRouge 0.1199 0.2149 3.8 33,330.4 51,964.4 3
Lehigh 0.0784 0.2913 4.0 12,371.0 34,074.5 3
Lemhi 0.0930 0.2251 5.3 23,098.7 46,476.5 3
Marcy 0.0631 0.2014 4.3 23,160.7 37,423.0 3
Nagore 0.1075 0.1757 3.8 28,648.6 35,283.7 3
New Norchip 0.0826 0.2110 4.8 21,982.5 42,972.9 3
NorDonna 0.0950 0.3306 3.0 20,742.3 35,934.8 3
Penn 71 0.0998 0.2663 3.8 27,997.5 35,035.7 3
Pike 0.0674 0.2918 4.3 21,610.5 32,896.3 3
Pioneer 0.1417 0.2637 2.8 25,207.1 44,492.2 3
Red Maria 0.0767 0.3376 4.5 22,168.6 41,577.7 3
Red Pontiac 0.0947 0.2233 4.0 29,392.7 51,406.3 3
Reliance 0.0657 0.2394 4.3 28,462.6 39,841.4 3
Rhine Red 0.0574 0.2215 4.8 24,587.0 42,476.9 3
Russet Burbank 0.1007 0.2233 4.5 26,385.3 40,554.5 3
Snowden 0.0803 0.3381 4.0 23,563.8 40,771.6 3
Somerset 0.0878 0.3283 4.5 22,044.6 30,446.9 3
Strawberry Paw 0.0786 0.2092 4.5 23,718.8 47,902.7 3
Suncrisp 0.1188 0.1860 5.8 21,827.5 40,244.5 3
Wyred 0.0844 0.2306 4.3 27,222.4 40,988.6 3
Alasclear 0.1574 0.2163 5.0 21,548.5 37,305.2 4
Allegany 0.1299 0.2092 4.5 15,719.5 33,392.4 4
Amey 0.1577 0.2733 5.3 23,315.8 29,733.8 4
BelChip 0.1197 0.2996 5.3 26,137.2 41,143.6 4
Belle Isle 0.1398 0.3396 4.5 22,044.6 40,399.5 4
Calgold 0.1597 0.3770 2.0 14,107.3 15,192.5 4
Caribe 0.1085 0.2830 3.8 24,866.0 40,089.5 4
Centennial Russet 0.1525 0.3561 3.0 16,277.6 23,129.7 4
Cherry Red 0.2481 0.4060 3.0 10,231.7 23,098.7 4
Chippewa 0.1525 0.2364 4.5 29,237.7 45,143.3 4
Denali 0.1213 0.2545 4.8 23,532.8 43,345.0 4
Early Gem 0.1144 0.2714 4.3 27,439.4 39,903.4 4
Emmet 0.1522 0.2851 5.0 20,773.4 39,283.3 4
Fundy 0.1794 0.2917 3.0 16,215.6 18,882.0 4
Green Mt 0.1730 0.3201 3.5 23,346.8 42,507.9 4
Hilite Russet 0.1701 0.4399 2.0 23,563.8 30,726.0 4
Kanona 0.1401 0.2775 3.8 20,184.3 28,617.6 4
Keswick 0.1248 0.2467 2.8 20,804.4 30,291.9 4
Keuka Gold 0.1038 0.2400 4.8 22,478.6 45,825.4 4
Langlade 0.1316 0.2190 4.8 35,593.7 49,298.0 4
Maine Chip 0.1523 0.3215 4.8 21,486.5 29,888.8 4
Navajo 0.2393 0.2614 3.3 8,619.4 14,231.3 4
NemaRus 0.1018 0.2074 3.0 20,215.3 21,579.5 4
Norchip 0.1622 0.2942 3.0 23,439.8 38,105.1 4
Norwis 0.0950 0.2174 2.5 16,308.6 28,524.6 4
Peter Wilcox 0.1434 0.2699 4.0 16,463.7 27,160.4 4
Plymouth 0.1322 0.1407 3.5 16,711.7 36,585.9 4
Prestile 0.1193 0.2657 5.0 23,718.8 39,903.4 4
Raritan 0.1011 0.2330 4.0 23,563.8 35,655.8 4
Red Burt 0.1568 0.2232 4.3 33,020.3 34,973.6 4
Red Kote 0.1430 0.2352 4.8 29,640.8 43,965.1 4
Rideau 0.1518 0.1919 4.5 23,098.7 28,121.5 4
(Continued on next page)

Plant Disease / December 2021 3959

Table 1. (Continued from previous page)
RAUDPC Yield (kg ha−1)
a b
Cultivar 2016 2017 Maturity 2016 2017 Clusterc
Russet Norkotah 0.1161 0.3250 3.5 23,780.8 40,089.5 4
Russet Sebago 0.2131 0.3607 2.8 19,936.2 23,036.7 4
Russette 0.1350 0.2121 4.3 18,572.0 35,562.7 4
Saginaw Gold 0.2192 0.3327 3.8 21,920.5 34,415.6 4
Seneca 0.1466 0.1348 4.3 20,494.3 22,695.7 4
Shurchip 0.1678 0.2552 4.3 27,439.4 46,414.5 4
Super Red Norland 0.1788 0.2071 2.8 26,633.3 42,414.8 4
Viking 0.1310 0.2907 3.8 16,370.6 27,687.5 4
Vokal 0.1353 0.1930 2.3 13,084.1 26,695.3 4
Yukon Gold 0.1251 0.3215 3.0 18,975.1 37,020.0 4
Abnaki 0.2511 0.3698 3.5 23,067.7 46,228.5 5
Agassiz 0.4409 0.4119 4.0 20,618.3 25,672.1 5
Alamo 0.1640 0.3740 3.8 26,044.2 34,632.6 5
Atlantic 0.3769 0.3061 4.5 20,091.2 39,004.3 5
Bake King 0.2198 0.2632 4.8 21,083.4 34,198.5 5
Belmont 0.2580 0.3001 2.0 16,308.6 36,585.9 5
BelRus 0.4002 0.3239 3.3 14,231.3 24,618.0 5
Bison 0.4534 0.3465 1.8 15,998.6 23,222.7 5
Canoga 0.2182 0.2049 3.3 27,997.5 31,315.1 5
Chieftain 0.2968 0.2579 3.5 26,726.3 40,554.5 5
Climax 0.2713 0.3101 3.3 23,811.8 37,950.1 5
Coastal Chip 0.2559 0.2282 4.8 21,455.5 23,284.8 5
Coastal Russet 0.3570 0.3698 3.5 21,176.4 34,477.6 5
Cobbler 0.2641 0.3899 3.8 22,354.6 33,361.4 5
Dk. Red Norland 0.4645 0.4323 1.8 23,036.7 29,299.7 5
Early Blue 0.3386 0.2913 2.8 19,750.2 27,594.5 5
Envol 0.3114 0.4821 1.3 16,153.6 24,835.0 5
GemChip 0.2077 0.2431 5.3 21,548.5 32,648.3 5
Golden 0.3298 0.2955 5.0 24,010.3 42,786.9 5
Goldrus 0.4231 0.3775 2.8 16,215.6 18,199.9 5
Haig 0.2128 0.2437 3.3 18,044.9 29,330.7 5
Harley Blackwell 0.3360 0.3673 3.8 24,462.9 42,414.8 5
Hartford 0.3851 0.2829 2.8 18,044.9 33,919.5 5
Highlat 0.3945 0.4107 2.5 17,889.9 31,315.1 5
Houma 0.2980 0.3037 3.3 28,214.6 42,290.8 5
Huron 0.2858 0.3430 3.3 20,711.3 31,997.2 5
Ivory Crisp 0.2713 0.3524 4.3 28,152.5 41,546.7 5
Jemseg 0.2741 0.4417 1.8 21,579.5 29,051.7 5
Krantz 0.2122 0.2735 3.8 19,006.1 30,757.0 5
LaSoda 0.2383 0.3512 3.3 34,105.5 50,569.2 5
Menominee 0.3497 0.3555 2.5 18,727.0 32,418.8 5
Mesaba 0.5556 0.4268 2.5 21,486.5 27,532.4 5
Mohawk 0.2441 0.2360 4.5 18,696.0 30,136.9 5
Monona 0.2349 0.3781 4.3 18,448.0 29,361.7 5
Monticello 0.2491 0.3125 3.8 15,440.5 35,035.7 5
Norchief 0.2817 0.3625 3.8 28,431.6 47,313.6 5
Nordak 0.3540 0.3877 2.0 19,564.2 18,457.3 5
Norgold Russet 0.3318 0.2990 2.8 24,866.0 26,323.2 5
Norking 0.1974 0.3704 3.5 24,462.9 31,811.1 5
Norland 0.2782 0.4032 1.0 25,176.1 26,695.3 5
NorValley 0.1948 0.2412 3.8 23,222.7 37,578.1 5
Oceania 0.3273 0.3556 1.5 25,238.1 31,966.2 5
Ona 0.3500 0.4061 1.8 18,013.9 23,439.8 5
Onaway 0.2593 0.3769 3.0 26,819.3 40,988.6 5
Patrones 0.3026 0.4204 2.3 18,665.0 27,067.4 5
Penobscot 0.2832 0.3638 3.0 31,129.0 34,725.6 5
Purple Norland 0.3361 0.4477 1.3 22,044.6 28,369.6 5
Ranger Russet 0.2064 0.1838 5.0 23,253.8 40,151.5 5
Reba 0.2540 0.2625 4.5 21,021.4 48,088.8 5
Red LaSoda 0.1728 0.2912 2.5 34,973.6 34,446.6 5
Red Warba 0.3311 0.3768 1.8 17,207.8 35,172.1 5
Reddale 0.3891 0.4436 3.5 27,935.5 37,733.1 5
Rural New Yorker 0.2745 0.2401 5.0 20,277.3 34,167.5 5
Rushmore 0.2281 0.2586 4.5 19,347.1 33,826.5 5
Sable 0.2570 0.2656 3.8 21,579.5 31,408.1 5
Simco 0.3519 0.3490 3.0 20,339.3 23,904.9 5
Snowflake 0.2781 0.3144 2.3 20,618.3 29,950.8 5
Spartan Pearl 0.2125 0.3260 3.5 21,734.5 30,850.0 5
Superior 0.5841 0.4298 3.0 22,323.6 34,787.6 5
Teton 0.2167 0.3227 5.3 27,377.4 44,275.1 5
Trent 0.2240 0.2781 5.0 22,416.6 34,663.6 5
Waneta 0.2360 0.2293 2.8 19,409.1 38,663.2 5
Warba 0.3260 0.4494 3.8 24,121.9 32,803.3 5
(Continued on next page)

3960 Plant Disease / Vol. 105 No. 12

Table 1. (Continued from previous page)
RAUDPC Yield (kg ha−1)
a b
Cultivar 2016 2017 Maturity 2016 2017 Clusterc
Wauseon 0.2251 0.2585 4.3 24,276.9 33,268.4 5
White Rose 0.2391 0.2205 4.3 33,702.4 55,530.0 5
Wischip 0.2790 0.3732 3.3 18,851.0 28,183.5 5
York 0.3949 0.3937 2.3 13,425.2 22,757.7 5

regression procedure in SAS, version 9.2, using the r (analysis of resid- Table 2. Analysis of variance of square root transformed late blight rela-
uals) and p (predicted values) options in the model statement. If the pre- tive area under the disease progress curve of 217 potato cultivars evaluated
dicted value of RAUDPC was significantly less than observed value in 2016 and 2017 in Pennsylvania
(studentized residuals more than two standard deviations, P = 0.05), Source DF Mean square Pr (>F)
then the cultivar was significantly more resistant to late blight than
expected based on its maturity. If the predicted value of RAUDPC was Year 1 1.2641 0.0137
Block within year 2 0.0177 0.0052
significantly higher than observed value, the cultivar was significantly
Cultivar 216 0.0927 <0.0001
more susceptible to late blight than expected based on its maturity. Year × cultivar 216 0.0084 <0.0001
The final disease severity score and the overall RAUDPC in each Pooled error 430 0.0033
of 2 years were used as variables for cluster analysis using a factoex- Total 865
tra R package. The optimal number of clusters was computed by the
fviz_nbclust function with k-means method, and the k-means and
fviz_cluster functions were applied to compute and visualize k-means interval of 0.88 and 0.93. Cultivar × environmental variation
clustering (Kassambara 2017). accounted for only 7.2% of the total variation.
Ranking late blight resistance in potato cultivars. Four varia-
bles (the final disease severity score, and overall RAUDPC in each
Results of the 2 years) were used to cluster the late blight-resistant ranks. All
Environments. The weather conditions during the growing seasons 217 cultivars were clustered into five groups (Fig. 3; Table 1): cluster
of 2016 and 2017 are recorded in Supplementary Table S1. The average 1 included 30 cultivars as resistant; cluster 2 included 32 cultivars as
temperature in 2016 was higher than in 2017 during the growing sea- moderately resistant; cluster 3 included 46 cultivars as intermediate;
son. During the late blight disease progression period (from the first rat- cluster 4 included 42 cultivars as moderately susceptible; and cluster
ing date to the last rating date), the average temperature was 20.7 C in 5 included 67 cultivars as susceptible. The pedigrees of all resistant
2016 and 15.7 C in 2017. The weather in 2016 was drier than in 2017, cultivars (cluster 1) are shown in Supplementary Table S2 as a refer-
as reflected by the total leaf wetness hours (3.2 h/day versus 4.3 h/day) ence for sources of resistance.
and relative humid (>90%) hours (10.0 h/day versus 13.9 h/day). How- Identification of late blight resistance independent of late
ever, the actual humidity in the field could have been similar between maturity. Late blight RAUDPC and maturity were correlated in
the 2 years because of overhead irrigation. The average RAUDPC in both years (r2016 = −0.60; r2017 = −0.64) (Supplementary Fig. S2).
2016 (0.1495) was significantly lower than in 2017 (0.2295) (P = To further dissect the maturity-related resistance and maturity-
0.0137) (Table 2). The mean RAUDPC of each cultivar ranged from 0 unrelated resistance, maturity-adjusted RAUDPC values were com-
to 0.5841 in 2016 and from 0 to 0.5469 in 2017 (Figure 1; Table 1). puted by linear regression analysis between maturity and RAUDPC
Distribution of late blight resistance among potato cultivars. (Supplementary Table S3). There was a genetic component of sus-
There were significant differences among the 217 cultivars for ceptibility independent of maturity for Agassiz, Atlantic, BelRus,
RAUDPC (P < 0.0001) (Table 2). Nine cultivars (Bzura, Donna, Gor- Golden, Mesaba, Reddale, and Superior in 2016 and Agassiz, Red-
bea, Michoacan, Tacna, Torridon, Ursus, Jacqueline Lee, and Zarevo) dale, Teton, and Warba in 2017. There was a genetic component of
showed high resistance to late blight (without visible disease symp- resistance independent of maturity for Cascade M, Cherokee, Donna,
toms) in 2016, and nine cultivars (Bzura, Grand Falls, Greta, Kandi- Grand Falls, Kandidat, and Pennchief only in 2017.
dat, Michoacan, Muziranzara, Torridon, Ursus, and Zarevo) showed Identification of cultivars with resistance to both late blight
high resistance to late blight in 2017 (Table 1). Five cultivars, Bzura, and early blight. In our previous study (Xue et al. 2019), early
Michoacan, Torridon, Ursus, and Zarevo, showed high resistance in blight resistance was evaluated in this collection of cultivars. The cor-
both years. When disease assessment was extended for 1 or 2 more relation between late blight RAUDPC and early blight RAUDPC was
weeks, weak late blight infection symptoms were observed on these moderately high in both years (r = 0.64 in 2016; r = 0.71 in 2017)
cultivars except Bzura and Ursus (data not shown), indicating these (Fig. 4A and B). There were 17 cultivars that possessed resistance to
cultivars were not immune but highly resistant to late blight. both diseases. These cultivars were Aracy, Arran Consul, Barbara,
Interaction between environment × cultivar. There were sig- Bzura, CalRose, Chaposa, Defender, Gorbea, Greta, Iker, Kandidat,
nificant interactions between environments and cultivars (P < Michoacan, Muziranzara, Ontario, Tacna, Torridon, and Ursus
0.0001) (Table 2). The RAUDPC of some cultivars, such as Red (Supplementary Table S4). Of those cultivars, only Kandidat was
Maria, Snowden, Avon, Somerset, Islander, Pike, NorDonna, Lehigh, with medium maturity; all others were with late or very late maturity.
Fontenot, Eide Russet, and Reliance, trended to the moderately resis- Correlation between late blight susceptibility and tuber yield.
tant side among all the cultivars in 2016 but to the moderately suscep- To address the fitness cost of late blight resistance, tuber yields were
tible side in 2017. The RAUDPC of some cultivars, such as Chieftain, evaluated for all the cultivars in the absence of late blight (Table 1),
White Rose, Plymouth, Super Red Norland, Canoga, Ranger Russet, and the correlations between late blight RAUDPC and tuber yield
Coastal Chip, Seneca, and Penn Rose, trended to the moderately sus- were calculated. RAUDPC and yield had a weak negative correlation
ceptible side in 2016 but to the moderately resistant side in 2017. All in both 2016 (r = −0.12; P = 0.07) (Fig. 4C) and 2017 (r = −0.34; P
these cultivars showed strong interaction with the environment. <0.001) (Fig. 4D), indicating that late blight resistance and yield had
Although there was interaction between environment and cultivar, the a weak positive correlation.
RAUDPC between 2 years was highly correlated (r = 0.83; P <
0.0001) (Fig. 2). This suggests, with the few exceptions noted above, Discussion
that late blight resistance is stable in different environments. In this study, we evaluated 217 old and modern potato cultivars
Heritability of late blight resistance in potato cultivars. Broad- for foliar late blight resistance against current predominant P. infes-
sense heritability for late blight resistance, as measured by combined tans clonal lineage US-23 under field conditions. Five cultivars
values of RAUDPC over 2 years, was 0.91, with a 95% confidence (Bzura, Michoacan, Torridon, Ursus, and Zarevo) possessed high

Plant Disease / December 2021 3961

resistance with no visible late blight symptoms during the disease highly susceptible to late blight under natural infected field condi-
scoring period in both years. Among those five cultivars, only Zar- tions at the Central Potato Research Institute in India (Gopal and
evo had intermediate to late maturity; the other four cultivars were Singh 2003), and it was used as a late blight-resistant control cultivar
late to very late in maturity. Zarevo was previously reported to be in another study (Pinto et al. 2002). Arran Consul was susceptible to
resistant to late blight (Douches et al. 1997). Bzura was previously late blight in west Bengal (Choudhuri 1967) but was also reported as
reported to have durable high resistance to late blight in a 10-year having low to high resistant levels by the European cultivated potato
field experiment, and its durable resistance was attributed to an database. Tacna (also named as Jizhangshu no. 8) was reported as
R2-like gene in its specific genetic background (Plich et al. 2015). low or moderately susceptible to late blight in China (Ma et al.
Karki et al. (2021a) used 79 F1 progeny derived from the cross 2007). The differences in resistance ratings between our and other
between Payette Russet and A0012–5 to map QTL resistant to researchers’ evaluations for these three cultivars (Aracy, Arran Con-
US-23. An R2 allele was found to contribute to resistance in Payette sul, and Tacna) might be due to the presence of different genotypes
Russet. We speculated that an R2 allele also provides resistance to of P.infestans or different environments. If so, this could indicate the
US-23 in Bzura. Torridon was considered to have broad-spectrum presence of race-specific genes involved in their resistance. The
resistance to late blight in different environments (Forbes et al. other six resistant cultivars (Buckskin, Cascade M, Gorbea, Grand
2005). Ursus was reported to have medium to high resistance to late Falls, Donna, and Pennchief) were first reported to be resistant to
blight in the European Cultivated Potato Database. The cultivar late blight in this study, and we did not find public reports about the
Michoacan was found to be highly resistant to late blight in India status of their late blight susceptibility. Brown-Donovan (2020) also
(Gopal and Singh 2003). In this study, the clonal lineage US-23 of evaluated some of these cultivars’ resistance to US-23 with a detached
P. infestans was used as inoculum, which is a different genotype leaf assay and field trials, and the results were mostly consistent with
from those in previous reports. The consistent resistance possessed the results of our study. Some of the late blight-resistant cultivars
by these five cultivars indicates that these cultivars possess broad- identified in this study are modern cultivars, but most are old culti-
spectrum resistance against different P. infestans genotypes in differ- vars. All the resistant cultivars evaluated in this study are maintained
ent environmental conditions.
In addition to the five cultivars possessing high resistance to late
blight, another 25 cultivars showed resistance to late blight in our
study. Sixteen of these cultivars (Barbara, CalRose, Chaposa, Chero-
kee, Chinook, Croft, Defender, Greta, Iker, Jacqueline Lee, Kandi-
dat, Libertas, LT-2, Muziranzara, Ontario, and Serrana) were
reported to be resistant to late blight in previous studies (Blodgett
and Stevenson 1946; Choudhuri 1967; Clark 1946; Colon et al.
1995; Douches et al. 2001b; European Cultivated Potato Database;
Gopal and Singh 2003; Mendoza 1989; Novy et al. 2006; Peterson
et al. 1954; Ruiz de Galarreta et al. 2006; Scott 1988), although the
genotypes of P. infestans used in those studies were different from
those used in our study. In our study, three cultivars, Aracy, Arran
Consul, and Tacna, were highly resistant to late blight, but that was Fig. 2. Scatterplots of mean late blight relative area under the disease progress curve
not so in some other studies. The cultivar Aracy was found to be (RAUDPC) between years among 217 potato cultivars evaluated in Pennsylvania.

Fig. 1. Frequency distribution of mean late blight relative area under the disease progress curve (RAUDPC) among 217 potato cultivars in 2016 and 2017 in Pennsylvania.

3962 Plant Disease / Vol. 105 No. 12

in potato breeding programs and/or at the Potato Genebank and could highly correlated in both years. The variations between replications
be used as genetic resources of late blight resistance. were well controlled, although there were only two replications in
Weather conditions were different between the 2 years of this our current study. Our population was not the same as in previous
study. Late blight was more severe in 2017 than in 2016. Owing to studies. The broad sense heritability can be higher in our population
irrigation after inoculation, variations in moisture might be much less than other populations. It could be common that the stability of late
in the research field than indicated by the difference between weather blight resistance in different populations might vary (Kaila 2015).
records at the weather station in those 2 years. In 2016 the average The high estimates of broad-sense heritability suggests that late
temperature was 5.0 C higher than in 2017 during disease develop- blight resistance is stable from one generation to the next.
ment after inoculation. Thus, cooler temperatures could have resulted Late blight and early blight are two important diseases in potato
in more severe late blight in 2017 than in 2016. production. In our study, the susceptibility of the 217 cultivars to
Early-maturing potato cultivars complete their life cycle in 75 to these two diseases was positively correlated in both years. Seventeen
90 days, whereas 120 to 135 days are required for late-maturing cul- cultivars resistant to both diseases identified in this study could be
tivars. Strong correlations between late blight resistance and maturity used as genetic resources for breeding for disease resistance. Both
have been reported in previous research studies (Massa et al. 2015; diseases have strong correlations with maturity. In fact, the correla-
Toxopeus 1958; Visker et al. 2004), and our results confirmed that tion between late blight resistance and early blight resistance was
correlation. However, in this study, six cultivars (Cascade M, greater than the correlation between late blight resistance and matu-
Cherokee, Donna, Grand Falls, Kandidat, and Pennchief) were sig- rity. There may be other genome regions contributing to early blight
nificantly more resistant to late blight than expected based on their and late blight resistance other than just the maturity genome region
maturity in 2017. That suggested that there were genetic components alone. In previous late blight resistance mapping studies, R genes
independent of maturity contributing to late blight resistance among were distributed on chromosomes IV, V, VI, VIII, and IX
these cultivars. However, genetic components independent of matu- (Vleeshouwers et al. 2011). Meta-QTLs governing partial resistance
rity was not detected in these cultivars in 2016, and we speculated to late blight have been observed on each chromosome (Danan et al.
that the cultivar × environment interaction might play a role. 2011). In early blight resistance studies, no cultivars showed immu-
Although the cultivar × environment interaction (G × E) of late nity (Abuley et al. 2018; Xue et al. 2019). There was only one pub-
blight resistance was significant in this study, it accounted for only lished report on early blight QTL mapping in potato (Zhang 2005).
7.2% of the total experimental variation and did not appear to affect Five QTLs on chromosomes IV, V, IX, XI, and XII were identified
the ranking of the cultivars for resistance or susceptibility. The esti- for early blight resistance explaining 62.2% of the total phenotypic
mate of broad-sense heritability of late blight resistance was high variation. Three QTLs for early blight resistance on chromosomes
(0.91) in this study. Broad-sense heritability is an important parame- IX, XI, and XII accounted for 33.1% of the total phenotypic varia-
ter for breeders to estimate how much of the variation in a trait is tion and were not linked to foliage maturity. These early blight
due to genetic variation. Trognitz et al. (2001) estimated broad-sense QTLs regions occurred in the same chromosome regions as previ-
heritability for late blight from 0.43 to 0.60 in a diploid potato prog- ously mapped late blight QTLs (Danan et al. 2011). This is an inter-
eny, which is lower than ours. However, the G × E interaction was esting result because P. infestans and A. solani are completely
higher (12.4%) in their study than in ours (7.2%). Haynes and Christ different pathogens and infect potato via different pathways and
(1999) estimated broad-sense heritability as 0.79 in a diploid hybrid mechanisms, but resistances to these pathogens are correlated. The
potato population, and their G × E interaction (6%) was similar to mechanisms behind this phenomenon need to be further investigated.
ours. Costanzo et al. (2004) estimated broad-sense heritability for However, in other studies, Pinto et al. (2002) found no obvious cor-
late blight resistance as 0.67 in a diploid full-sib potato family. relation between early blight and late blight resistance in 192 potato
Enciso-Rodriguez et al. (2018) estimated genetic heritability for late breeding clones. Christ and Haynes (2001) also found a moderately
blight at about 0.46, combining 7 years’ data. Higher broad-sense low correlation between early blight resistance and late blight resis-
heritability in our study than in previous studies could come from tance. These different results may be due to disease inoculation
lower G × E interaction. In our study, there was no significant differ- methods. In our study, we artificially inoculated plants for both dis-
ent between replications, RAUDPC between two replications were eases. However, in the studies by Pinto et al. (2002) and Christ and

Fig. 3. Cluster analysis of late blight resistance among 217 potato cultivars evaluated in 2016 and 2017 in Pennsylvania. Different colors indicate different cluster
groups from susceptible (left) to resistant (right).

Plant Disease / December 2021 3963

Haynes (2001), plants were naturally infected. With natural infection, resistance to Magnaporthe oryzae compared with wildtype but
late blight or early blight disease could be unevenly distributed, and leaded to reduction in yield and grain quality in rice under normal
disease expression more variable, in comparison with artificial growth conditions (Qiao et al. 2010). In some other cases, resistance
inoculation. genes showed no yield or fitness cost, such as bsr-d1-mediated resis-
It is commonly assumed that plant disease resistance requires tance to blast in rice (Li et al. 2017) and resistance genes to barley
energy expenditure and is therefore accompanied by trade-offs with powdery mildew (Kolster et al. 1986) under no pathogen stress con-
other fitness components such as yield, quality, or an agronomic ditions. Plants with silenced bsr-d1gene did not show any defect of
property of a cultivar (Bergelson and Purrington 1996). Plants that growth or yield. In potato, Pinto et al. (2002) found a weak negative
carry resistance are expected to have lower yield than susceptible correlation (r = −0.24) between tuber yield and late blight suscepti-
plants in the absence of disease pressure in some plants. bility (AUDPC) under no late blight stress condition. Clones with
Vanderplank (1963) brought out the concept of costs of resistance in good levels of resistance to both early blight and late blight yielded
his study of the resistance of potato late blight. It was found that more tubers than did the controls under both presence and absence
decline in partial resistance to late blight in an isolated population of early blight. Halterman et al. (2008) transformed late blight-
without late blight-resistant selection could be because of fitness pen- resistant gene RB from Solanum bulbocastanum into cultivated
alty. In Arabidopsis, Tian et al. (2003) showed that the resistance potato without a significant effect on tuber size or yield in transgenic
gene RPM1 against pathogen Pseudomonas syringae reduced seed potato without late blight stress. In our study, late blight resistance
yield in field conditions without pathogen P. syringae. Bai et al. and yield had a weak positive correlation among the 217 cultivars,
(2000) recommended that pyramiding resistance genes be guided by indicating that no yield trade-off was associated with late blight
the degree of fitness penalty in rice. A mutant of SPL28 increased resistance in our population. The weak correlation could also suggest

Fig. 4. Scatterplots of mean late blight relative area under the disease progress curve (RAUDPC) against mean early blight RAUDPC and tuber yield among 217 potato
cultivars in 2 years in Pennsylvania. A, Late blight (LB) against early blight (EB) in 2016. B, Late blight against early blight in 2017. C, Late blight against tuber yield
in 2016. D, Late blight against tuber yield in 2017.

3964 Plant Disease / Vol. 105 No. 12

that fitness costs and their interactions with the environment need to Fry, W. E., McGrath, M. T., Seaman, A., Zitter, T. A., McLeod, A., Danies,
be further investigated. G., Small, I. M., Myers, K., Everts, K., Gevens, A. J., Gugino, B. K.,
Johnson, S. B., Judelson, H., Ristaino, J., Roberts, R., Secor, G., Seebold,
In conclusion, a few potato cultivars with resistance to late blight
K., Snover-Clift, K., Wyenandt, A., Grunwald, N. J., and Smart, C. D. 2013.
caused by newly emerged P. infestans clonal lineage US-23 and a The 2009 late blight pandemic in the eastern United States - causes and
few cultivars with resistance to both late blight and early blight were results. Plant Dis. 97:296-306.
identified in this study. Yield trade-off associated with late blight Goodwin, S. B., Cohen, B. A., Deahl, K. L., and Fry, W. E. 1994. Migration
resistance was not observed among the cultivars in the absence of from northern Mexico as the probable cause of recent genetic changes in
disease pressure. The results will be a useful reference for other populations of Phytophthora infestans in the United-States and Canada. Phy-
topathology 84:553-558.
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