scholarly journals Genetic Change Within Populations of Phytophthora infestans in the United States and Canada During 1994 to 1996: Role of Migration and Recombination

1998 ◽  
Vol 88 (9) ◽  
pp. 939-949 ◽  
Author(s):  
Stephen B. Goodwin ◽  
Christine D. Smart ◽  
Robert W. Sandrock ◽  
Kenneth L. Deahl ◽  
Zamir K. Punja ◽  
...  
Keyword(s):  
United States ◽  
Sexual Reproduction ◽  
Phytophthora Infestans ◽  
High Sensitivity ◽  
The United States ◽  
Rapid Identification ◽  
Mating Types ◽  
Long Distance ◽  
New Genotype ◽  
The Us

Dramatic changes occurred within populations of Phytophthora infestans in the United States and Canada from 1994 through 1996. Occurrence of the US-8 genotype, detected rarely during 1992 and 1993, increased rapidly and predominated in most regions during 1994 through 1996. US-7, which infected both potato and tomato and made up almost 50% of the sample during 1993, was detected only rarely among 330 isolates from the United States analyzed during 1994. It was not detected at all in more limited samples from 1996. Thus, ability to infect both potato and tomato apparently did not increase the fitness of this genotype relative to US-8, as predicted previously. US-1, the previously dominant genotype throughout the United States and Canada, made up 8% or less of the samples analyzed during 1994 through 1996. A few additional genotypes were detected, which could indicate the beginnings of sexual reproduction of P. infestans within the United States and Canada. However, clonal reproduction still predominated in all locations sampled; opportunities for sexual reproduction probably were limited, because the A1 and A2 mating types usually were separated geographically. The high sensitivity of the US-1 genotype to the fungicide metalaxyl also could have reduced opportunities for contact between the mating types in fields where this compound was applied. The previous correlation between metalaxyl sensitivity and genotype was confirmed and extended to a new genotype, US-17: all US-1 isolates tested were sensitive; all isolates of the US-7, US-8, and US-17 genotypes tested to date have been resistant. Isolates of P. capsici and P. erythroseptica, two other species often found on tomato and potato, could be easily distinguished from each other and from P. infestans using a simple allozyme assay for the enzyme glucose-6-phosphate isomerase. This technique could be useful for rapid identification of species, in addition to genotype of P. infestans. It generally was not possible to predict which genotypes would be present in a location from 1 year to the next. Long-distance movement of US-8 in seed tubers was documented, and this was probably the primary means for the rapid spread of this genotype from 1993 through 1996.

scholarly journals Genetic Composition of Phytophthora infestans in Canada Reveals Migration and Increased Diversity

Plant Disease ◽  
2012 ◽  
Vol 96 (12) ◽  
pp. 1729-1735 ◽  
Author(s):  
Melanie L. Kalischuk ◽  
Khalil I. Al-Mughrabi ◽  
Rick D. Peters ◽  
Ron J. Howard ◽  
H. W. (Bud) Platt ◽  
...  
Keyword(s):  
Sexual Reproduction ◽  
Phytophthora Infestans ◽  
Prince Edward Island ◽  
Weather Conditions ◽  
The United States ◽  
Potato Seed ◽  
Polymorphism Analysis ◽  
Mating Types ◽  
Long Distance ◽  
Canadian Provinces

A dramatic increase in the incidence of late blight and changes within populations of Phytophthora infestans have been observed in various regions of Canada. In this study, the occurrence of several new genotypes of the pathogen was documented with associated phenotypes that dominated pathogen populations. Genotype US-23, previously detected only among isolates from the United States, dominated in the western Canadian provinces of British Columbia, Alberta (AB), Saskatchewan, and Manitoba (MB). Although isolates of US-23 infect both potato and tomato, these isolates were the only genotype recovered from commercial garden centers in Canada. Isolates of genotype US-8, previously dominant throughout Canada, represented the only genotype detected from the eastern Canadian provinces of New Brunswick and Prince Edward Island. Isolates of other genotypes detected in Canada included US-11 in AB, US-24 in MB, and US-22 in Ontario (ON). An additional genotype was detected in ON which appears to be a derivative of US-22 that may have arisen through sexual reproduction. However, evidence of clonal reproduction dominated among the isolates collected, and opportunities for sexual reproduction were probably limited because of a surprising geographic separation of the A1 and A2 mating types in Canada. Sensitivity of the US-22, US-23, and US-24 isolates to the fungicide metalaxyl, movement of potato seed and transplants, and weather conditions may have contributed to reduced opportunities for contact between the mating types in fields in Canada. All P. infestans isolates were readily distinguished from other related oomycetes with RG57 restriction fragment length polymorphism analysis. Long-distance movement in seed tubers and garden center transplants may have contributed to the rapid spread of the P. infestans genotypes across Canada. Tracking pathogen movement and population composition should improve the ability to predict the genotypes expected each year in different regions of Canada.

scholarly journals Phenotypic Characterization of Recent Clonal Lineages of Phytophthora infestans in the United States

Plant Disease ◽  
2013 ◽  
Vol 97 (7) ◽  
pp. 873-881 ◽  
Author(s):  
G. Danies ◽  
I. M. Small ◽  
K. Myers ◽  
R. Childers ◽  
W. E. Fry
Keyword(s):  
United States ◽  
Late Blight ◽  
Phytophthora Infestans ◽  
The United States ◽  
Phenotypic Characterization ◽  
Phenotypic Traits ◽  
Mating Types ◽  
Late Blight Disease ◽  
Blight Disease

Phytophthora infestans, the causal agent of late blight disease, has been reported in the United States and Canada since the mid-nineteenth century. Due to the lack of or very limited sexual reproduction, the populations of P. infestans in the United States are primarily reproducing asexually and, thus, show a simple genetic structure. The emergence of new clonal lineages of P. infestans (US-22, US-23, and US-24) responsible for the late blight epidemics in the northeastern region of the United States in the summers of 2009 and 2010 stimulated an investigation into phenotypic traits associated with these genotypes. Mating type, differences in sensitivity to mefenoxam, differences in pathogenicity on potato and tomato, and differences in rate of germination were studied for clonal lineages US-8, US-22, US-23, and US-24. Both A1 and A2 mating types were detected. Lineages US-22, US-23, and US-24 were generally sensitive to mefenoxam while US-8 was resistant. US-8 and US-24 were primarily pathogenic on potato while US-22 and US-23 were pathogenic on both potato and tomato. Indirect germination was favored at lower temperatures (5 and 10°C) whereas direct germination, though uncommon, was favored at higher temperatures (20 and 25°C). Sporangia of US-24 released zoospores more rapidly than did sporangia of US-22 and US-23. The association of characteristic phenotypic traits with genotype enables the prediction of phenotypic traits from rapid genotypic analyses for improved disease management.

scholarly journals Fungicide Sensitivity of U.S. Genotypes of Phytophthora infestans to Six Oomycete-Targeted Compounds

Plant Disease ◽  
2015 ◽  
Vol 99 (5) ◽  
pp. 659-666 ◽  
Author(s):  
Amanda Saville ◽  
Kim Graham ◽  
Niklaus J. Grünwald ◽  
Kevin Myers ◽  
William E. Fry ◽  
...  
Keyword(s):  
United States ◽  
Phytophthora Infestans ◽  
The United States ◽  
Effective Concentration ◽  
Response Curves ◽  
Baseline Sensitivity ◽  
Fungicide Sensitivity ◽  
The Past ◽  
The Us

Phytophthora infestans causes potato late blight, an important and costly disease of potato and tomato crops. Seven clonal lineages of P. infestans identified recently in the United States were tested for baseline sensitivity to six oomycete-targeted fungicides. A subset of the dominant lineages (n = 45) collected between 2004 and 2012 was tested in vitro on media amended with a range of concentrations of either azoxystrobin, cyazofamid, cymoxanil, fluopicolide, mandipropamid, or mefenoxam. Dose-response curves and values for the effective concentration at which 50% of growth was suppressed were calculated for each isolate. The US-8 and US-11 clonal lineages were insensitive to mefenoxam while the US-20, US-21, US-22, US-23, and US-24 clonal lineages were sensitive to mefenoxam. Insensitivity to azoxystrobin, cyazofamid, cymoxanil, fluopicolide, or mandipropamid was not detected within any lineage. Thus, current U.S. populations of P. infestans remained sensitive to mefenoxam during the displacement of the US-22 lineage by US-23 over the past 5 years.

scholarly journals On Thai Transnational Subjectivity

MANUSYA ◽  
2009 ◽  
Vol 12 (4) ◽  
pp. 86-102
Author(s):  
Sudarat Musikawong
Keyword(s):  
United States ◽  
Cold War ◽  
The United States ◽  
Film Festivals ◽  
Long Distance ◽  
Satellite Television ◽  
Immigrant Identity ◽  
The Us ◽  
Thai People ◽  
The Cold War

This paper examines the formation of transnational subjectivity through Thai political engagements in the United States (US). Thai people in the US participate in Thai homeland politics, while negotiating for a Thai immigrant identity in the US. Thai diasporas exist through political and social experiences, in which Thai communities and persons engage in homeland politics. Political acts and protests by Thais in the United States are not new, but emerged in the aftermath of the Cold War. This paper asks how political exiles, popular protests, film festivals, and satellite television challenge what Benedict Anderson has termed “long-distance” nationalism and Arjun Appadurai’s mediascapes.

scholarly journals Genetic Structure of the Phytophthora infestans Population in Morocco

Plant Disease ◽  
2000 ◽  
Vol 84 (2) ◽  
pp. 173-176 ◽  
Author(s):  
M. Sedegui ◽  
R. B. Carroll ◽  
A. L. Morehart ◽  
T. A. Evans ◽  
S. H. Kim ◽  
...  
Keyword(s):  
Genetic Structure ◽  
Late Blight ◽  
Sexual Reproduction ◽  
Phytophthora Infestans ◽  
Mating Type ◽  
Potato Seed ◽  
Mating Types ◽  
Potato Field ◽  
New Genotype

ABSRACT In 1996 to 1998, a late-blight survey was conducted in potato- and tomato-growing regions of Morocco. A total of 149 isolates of Phytophthora infestans were collected and analyzed for the glucose-6-phosphate isomerase (Gpi) and peptidase (Pep) alleles, mating types, and metalaxyl sensitivities. Four genotypes were identified: MO-1 (mating type A1, Gpi 100/100, Pep 92/100), MO-2 (mating type A1, Gpi 86/100, Pep 92/100), MO-3 (mating type A2 Gpi 100/100, Pep 100/100), and MO-4 (mating type A1, Gpi 100/100, Pep 100/100). The potato isolates were MO-1 (1996 & 97), MO-3 (1998), and MO-4 (1998). The frequencies of A1 (MO-4) and A2 (MO-3) mating types in potato fields in 1998 were 26 and 74%, respectively. Potato isolates were pathogenic to both potatoes and tomatoes. The isolates collected from tomatoes in 1997 and 1998 were MO-2. Potato and tomato isolates were insensitive and sensitive to metalaxyl, respectively. The change of genotype population in 1998 was probably caused by migration of a new genotype from Europe associated with importation of potato seed. The detection of A1 and A2 mating types in the same potato field indicates the potential for sexual reproduction of P. infestans in Morocco.

scholarly journals First Report of Late Blight Caused by Phytophthora infestans Clonal Lineage US-23 on Potato in Idaho

Plant Disease ◽  
2015 ◽  
Vol 99 (3) ◽  
pp. 417-417 ◽  
Author(s):  
P. S. Wharton ◽  
P. Nolte ◽  
W. W. Kirk ◽  
S. Dangi ◽  
A. J. Gevens
Keyword(s):  
United States ◽  
Late Blight ◽  
Phytophthora Infestans ◽  
Agar Medium ◽  
The United States ◽  
Eastern United States ◽  
Clonal Lineage ◽  
Predominant Genotype ◽  
The Us ◽  
Pure Cultures

Late blight, caused by Phytophthora infestans (Mont.) de Bary, is a destructive disease of potato (Solanum tuberosum) and tomato (S. lycopersicum) in the United States. Prior to 2007, the US-8 clonal lineage was the predominant genotype in the United States (4). Since 2007, a significant genetic change in the population of P. infestans occurred in the eastern United States with the appearance of new isolates with unique genotypes and epidemiological characteristics (3). These new genotypes US-22, US-23, and US-24 are sensitive to metalaxyl and represent mating types A2, A1, and A1, respectively (1,2). Prior to 2012, only US-8 had been documented in Idaho (5). In 2013, late blight was discovered in late August on potato crops (cv. Russet Norkotah) in Bingham and Madison counties, ID. Infected foliage (four samples from Bingham County and five from Madison) was sent to Michigan State University and the University of Wisconsin for confirmation of P. infestans and characterization of the isolates. Five sections from the leading edge of lesions were excised with a sterilized scalpel and placed on potato tuber slices (‘Dark Red Norkotah’). Pathogen sporulation on the excised lesions was enhanced by incubation in plastic boxes lined with moistened paper towels for 5 days at 18°C in the dark. The sporulating lesions were transferred onto pea agar medium (160 g peas, 5 g sucrose, 15 g agar, 700 ml distilled water) amended with 50 mg/ml vancomycin. Ten pure cultures were obtained for each of 4 isolates per county by hyphal tipping. Cellulose acetate electrophoresis was conducted to determine Gpi allozyme genotype of the 4 isolates (4). The allozyme banding patterns were 100/100 at the Gpi locus, consistent with previously reported analyses of the US-23 genotype (1,2). Genomic DNA was extracted from 10 pure cultures using the DNeasy Plant Mini Kit (Qiagen, Germantown, MD), and SSR analyses were performed. Microsatellite markers Pi02, Pi4B, Pi63, PiG11, and D13 were used in SSR analyses. Pi02, Pi4B, and Pi63 had alleles of 162/164, 213/217, and 270/279 bp in size, respectively which is consistent with the reference US-23 genotype (1). However, heterozygosity was detected at locus D13 in the Idaho genotype with allele size of 134/210 bp and an additional allele of 140/155/176 bp at locus PiG11. This is different from the standard US-23 genotype (homozygous alleles 134/134 at locus D13 and two alleles 140/155 at locus PiG11). These allele changes indicate the isolates may be variants of US-23 isolates as all other phenotypic characteristics were similar to those of reference US-23 isolates. The Idaho genotypes were sensitive to metalaxyl both in vitro on rye A agar medium amended with metalaxyl at <0.1 ppm, and in vivo on Ridomil treated foliage tests at <0.1 ppm (1,2). Mating type assays confirmed the pathogen to be the A1 mating type. In the 2009 and 2010 late blight epidemics in the eastern United States, US-23 was the predominant genotype, but to our knowledge this genotype has never been reported previously in Idaho. Thus, this is the first known report of P. infestans genotype US-23 causing late blight on potato in Idaho, indicating a change in the population of P. infestans. In Idaho, the source of this genotype remains unknown, although infected tomatoes have been implicated in the widespread dissemination of this genotype of P. infestans in the eastern United States. References: (1) G. Danies et al. Plant Dis. 97:873, 2013. (2) C. Hu et al. Plant Dis. 96:1323, 2012. (3) K. Deahl. (Abstr.) Phytopathology 100:S161, 2010. (4) S. B. Goodwin et al. Plant Dis. 79:1181, 1995. (5) USAblight. Recent US Genotypes. Online: www.usablight.org/node/52 , retrieved 3 January 2014.

scholarly journals Implications of Sexual Reproduction for Phytophthora infestans in the United States: Generation of an Aggressive Lineage

Plant Disease ◽  
2000 ◽  
Vol 84 (7) ◽  
pp. 731-735 ◽  
Author(s):  
P. D. Gavino ◽  
C. D. Smart ◽  
R. W. Sandrock ◽  
J. S. Miller ◽  
P. B. Hamm ◽  
...  
Keyword(s):  
United States ◽  
Phytophthora Infestans ◽  
The United States ◽  
Mitochondrial Haplotype ◽  
Columbia Basin ◽  
Clonal Lineage ◽  
Large Area ◽  
The Us ◽  
Sexual Progeny

Phytophthora infestans isolates (n = 26) collected in the Columbia Basin of Oregon and Washington in 1993, which had been characterized previously for mating type, metalaxyl sensitivity, and alleles at the glucose-6-phosphate isomerase locus, were analyzed for nuclear restriction fragment length polymorphism (RFLP) bands detected by probe RG57 and mitochondrial haplotype. Analyses involving the larger set of markers indicated that this group of isolates satisfied expectations of a sexual progeny: they contained much greater genetic diversity than has been reported for most other epidemic populations of P. infestans in the United States and Canada (16 unique multilocus genotypes); both mating types were present in proximity; all possible combinations of alleles occurred at many pairs of polymorphic loci; and two distinct mitochondrial haplotypes were distributed among the isolates. An in vitro laboratory cross involving the putative parents (US-6 and US-7) as parental strains produced progeny with the same general characteristics as the field isolates. Among the field progeny were two genotypes, US-11 and US-16, that had been described previously but from subsequent and largely clonal collections. Isolates obtained from tomatoes (n = 40) and potatoes (n = 7) in 24 counties in California in 1998 were analyzed as described above, and all except one US-8 isolate from potatoes were of the US-11 clonal lineage, consistent with the hypothesis that the US-11 lineage is an especially fit clonal lineage that has survived over time and can dominate pathogen populations over a large area. We conclude that the 1993 Columbia Basin collection represents a sexual progeny that generated the US-11 lineage, and that this lineage is particularly fit when tomatoes are part of the agroecosystem.

scholarly journals Sensitivity to Protectant Fungicides and Pathogenic Fitness of Clonal Lineages of Phytophthora infestans in the United States

1997 ◽  
Vol 87 (9) ◽  
pp. 973-978 ◽  
Author(s):  
Masayasu Kato ◽  
Eduardo S. Mizubuti ◽  
Stephen B. Goodwin ◽  
William E. Fry
Keyword(s):  
United States ◽  
Latent Period ◽  
Phytophthora Infestans ◽  
Potato Cultivar ◽  
The United States ◽  
Clonal Lineage ◽  
Fitness Components ◽  
Lesion Area ◽  
Simulation Experiments ◽  
The Us

Since 1991, dramatic changes have occurred in the genetic composition of populations of Phytophthora infestans in the United States. Clonal lineages recently introduced into the United States (US-7 and US-8) are more common now than the previously dominant lineage (US-1). To help determine why these changes occurred, four clonal lineages of P. in-festans common during the early 1990s in the United States and Canada were evaluated for sensitivity to the protectant fungicides mancozeb and chlorothalonil using amended agar assays for isolates collected from 1990 to 1994. No isolate or lineage was resistant to either mancozeb or chlorothalonil. There were significant differences among isolates for degree of sensitivity to one fungicide individually, but there were no significant (P = 0.05) differences among the US-1, US-6, US-7, and US-8 clonal lineages for degree of sensitivity to both fungicides. Therefore, resistance to protectant fungicides cannot explain the rapid increase in frequency of the US-7 and US-8 clonal lineages. Three components of pathogenic fitness (latent period, lesion area, and sporulation after 96 h) were tested for the three clonal lineages that were detected most commonly during 1994 (US-1, US-7, and US-8). All but one of the isolates in this analysis were collected during 1994 and evaluated within 10 months of collection by inoculating detached leaflets of the susceptible potato cultivar Norchip. There were significant differences between the US-1 and US-8 clonal lineages for lesion area and sporulation, and between US-1 and US-7 for latent period. The US-6 clonal lineage was excluded from the pathogenic fitness experiments, because no isolates of this lineage were collected during 1994. Compared with US-7 and US-8, US-1 had the longest latent period and the smallest lesions with the least sporulation. Incorporation of the differences between US-1 and US-8 in computer simulation experiments revealed that significantly more protectant fungicide (e.g., 25%) would be required to suppress epidemics caused by the US-8 clonal lineage compared with US-1. These differences in pathogenic fitness components probably contribute to the general predominance of the “new” clonal lineages (especially US-8) relative to the “old” US-1 lineage.

scholarly journals Genetic Structure and Subclonal Variation of Extant and Recent U.S. Lineages of Phytophthora infestans

2019 ◽  
Vol 109 (9) ◽  
pp. 1614-1627 ◽  
Author(s):  
Amanda Saville ◽  
Jean Beagle Ristaino
Keyword(s):  
United States ◽  
Genetic Structure ◽  
Phytophthora Infestans ◽  
Genetic Similarity ◽  
Genetic Relationships ◽  
The United States ◽  
Time Period ◽  
Rxlr Effector ◽  
The Us ◽  
Mexican Populations

The oomycete Phytophthora infestans is an important plant pathogen on potato and tomato crops. We examined the genetic structure of extant 20th and 21st century U.S. lineages of P. infestans and compared them with populations from South America and Mexico to examine genetic relationships and potential sources of lineages. US-23, currently the most prevalent lineage detected in the United States, shared genetic similarity primarily with the BR-1 lineage identified in the 1990s from Bolivia and Brazil. Lineages US-8, US-14, and US-24, predominantly virulent on potato, formed a cluster distinct from other U.S. lineages. Many of the other U.S. lineages shared significant genetic similarity with Mexican populations. The US-1 lineage, dominant in the mid-20th century, clustered with US-1 lineages from Peru. A survey of the presence of RXLR effector PiAVR2 revealed that some lineages carried PiAVR2, its resistance-breaking variant PiAVR2-like, or both. Minimum spanning networks developed from simple sequence repeat genotype datasets from USABlight outbreaks clearly showed the expansion of US-23 over a 6-year time period and geographic substructuring of some lineages in the western United States. Many clonal lineages of P. infestans in the United States have come from introductions from Mexico, but the US-23 and US-1 lineages were most likely introduced from other sources.

scholarly journals First Report of Late Blight Caused by Phytophthora infestans Clonal Lineage US-23 on Tomato and Potato in Atlantic Canada

Plant Disease ◽  
2014 ◽  
Vol 98 (3) ◽  
pp. 426-426 ◽  
Author(s):  
C. P. Wijekoon ◽  
R. D. Peters ◽  
K. I. Al-Mughrabi ◽  
L. M. Kawchuk
Keyword(s):  
United States ◽  
Late Blight ◽  
New Brunswick ◽  
Phytophthora Infestans ◽  
Mating Type ◽  
Prince Edward Island ◽  
The United States ◽  
Clonal Lineage ◽  
Eastern Canada ◽  
The Us

Phytophthora infestans (Mont.) de Bary has produced significant losses in potato and tomato yield and quality during recent late blight epidemics in North America. During the 1990s, more aggressive and genetically diverse P. infestans genotypes migrated to Canada and the United States (2). For example, US-8 became predominant and was found to be more aggressive in potato than previous clonal lineages of P. infestans. Recent P. infestans genotypes in potato and tomato plants from the United States and Canada include US-22, US-23, and US-24 representing clonal lineages with unique epidemiological characteristics (2,3,4). Characteristic phenotypic traits have been described for P. infestans clonal lineages US-8, US-22, US-23, and US-24 based on the mating type, mefenoxam sensitivity, pathogenicity, and rate of germination suggesting an association between phenotypic variations and the genotype (1,4). Analysis of P. infestans isolates collected in Canada during 2010 revealed the presence of the US-23 clonal lineage in four different areas of western Canada but not in eastern Canada (4). Isolates of P. infestans collected from eastern Canada for several years prior to 2011 were all US-8 A2 mating type. Isolation and analysis of 98 P. infestans isolates in 2011 from New Brunswick and Prince Edward Island followed standard procedures (2,3,4). Results confirmed the presence of the US-23 clonal lineage in Atlantic Canada on potato and tomato leaves with late blight symptoms, increasing the genetic complexity of P. infestans in eastern Canada. Allozyme banding patterns at the glucose-6-phosphate isomerase (Gpi) locus showed a 100/100 profile in 10 P. infestans isolates, consistent with the US-23 clonal lineage (2,3,4). Furthermore, in vitro mefenoxam sensitivity was observed in all 10 P. infestans US-23 isolates from New Brunswick and Prince Edward Island. Mating type assays confirmed the isolates were of the A1 mating type. RFLP analysis of EcoR1-digested genomic DNA using the multilocus RG57 sequence as a probe produced the DNA pattern 1, 2, 5, 6, 10, 13, 14, 17, 20, 21, 24, 24a, 25, indicative of US-23 (2,4). Microsatellite analysis using polymorphic markers on New Brunswick and Prince Edward Island P. infestans isolates produced the Pi4B 213/217 bp, D13 134 bp, and PiG11 140/155 bp profile of P. infestans US-23 (1). These results show the presence of the P. infestans A1 and A2 mating types in New Brunswick and Prince Edward Island, which increases the probability of sexual recombination. To our knowledge, this is the first report of P. infestans clonal lineage US-23 causing late blight in New Brunswick and Prince Edward Island, increasing the genetic diversity from previous years in eastern Canada and underscoring the annual fluctuation occurring in the population composition. References: (1) G. Danies et al. Plant Dis. 97:873, 2013. (2) S. B. Goodwin et al. Phytopathology 84:553, 1994. (3) C. H. Hu et al. Plant Dis. 96:1323, 2012. (4) M. L. Kalischuk et al. Plant Dis. 96:1729, 2012.

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