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2021 - Xue - Resistance To Phytophthora Infestans Clonal Lineage US23
2021 - Xue - Resistance To Phytophthora Infestans Clonal Lineage US23
1094/PDIS-03-21-0594-RE
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
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
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.
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).
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.