Nondefoliating and Defoliating Strains from Cotton Correlate with Races 1 and 2 of Verticillium dahliae

Verticillium wilt, caused by Verticillium dahliae, is an important disease of cotton worldwide. Isolates of V. dahliae can be characterized as race 1 or race 2 based on the responses of differential cultivars of tomato and lettuce, or as defoliating or nondefoliating based on symptom expression in cotton. To investigate the frequency and distribution of races and defoliation phenotypes of cotton-associated V. dahliae, 317 isolates from China, Israel, Turkey, and the United States were tested by polymerase chain reaction (PCR) using defoliating, nondefoliating, and race 1- and race 2-specific primers DF/DR, NDF/NDR, VdAve1F/VdAve1R, and VdR2F/VdR2R, respectively. Of the total, 97.2% of isolates genotyped as defoliating were also characterized as race 2, while 90.8% of isolates genotyped as nondefoliating were also genotyped as race 1. To verify these results, three cotton cultivars—‘FM 2484B2F’ (highly resistant), ‘98M-2983’ (highly susceptible), and ‘CA4002’ (partially resistant)—used as differentials were each inoculated with 10 isolates characterized by PCR: six defoliating/race 2 strains (GH1005, GH1021, HN, XJ2008, XJ592, and reference strain Ls17) and four nondefoliating/race 1 strains (GH1015, GH1016, GH1020, and reference strain Ls16). All defoliating/race 2 isolates except for Ls17 caused defoliation on 98M-2983 and CA4002. Isolate Ls17 caused defoliation on 98M-2983 only. The nondefoliating/race 1 isolates caused Verticillium wilt symptoms devoid of defoliation on 98M-2983. The greenhouse assays confirmed the molecular identification of race and defoliation phenotype. Although the existence of races has not been previously established among V. dahliae isolates from cotton, the long-established nondefoliating and defoliating population structure corresponded with V. dahliae races 1 and 2, respectively.

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Verticillium dahliae Race 2-Specific PCR Reveals a High Frequency of Race 2 Strains in Commercial Spinach Seed Lots and Delineates Race Structure

Phytopathology ◽

10.1094/phyto-09-13-0253-r ◽

2014 ◽

Vol 104 (7) ◽

pp. 779-785 ◽

Cited By ~ 22

Author(s):

Dylan P. G. Short ◽

Suraj Gurung ◽

Karunakaran Maruthachalam ◽

Zahi K. Atallah ◽

Krishna V. Subbarao

Keyword(s):

Verticillium Dahliae ◽

Disease Surveillance ◽

Population Biology ◽

Resistance Breeding ◽

Pcr Primers ◽

Specific Pcr ◽

Differential Cultivars ◽

Race 1 ◽

Polymerase Chain ◽

Race 2

Two pathogenic races of Verticillium dahliae have been described on lettuce and tomato. Host resistance to race 1 is governed by plant immune receptors that recognize the race 1-specific fungal effector Ave1. Only partial resistance to race 2 exists in lettuce. Although polymerase chain reaction (PCR) assays are available to identify race 1, no complementary test exists to positively identify race 2, except for lengthy pathogenicity assays on host differentials. Using the genome sequences of two isolates of V. dahliae, one each from races 1 and 2, we identified potential markers and PCR primers to distinguish the two races. Several primer pairs based on polymorphisms between the races were designed and tested on reference isolates of known race. One primer pair, VdR2F-VdR2R, consistently yielded a 256-bp amplicon in all race 2 isolates exclusively. We screened DNA from 677 V. dahliae isolates, including 340 from spinach seedlots, with the above primer pair and a previously published race 1-specific primer pair. DNA from isolates that did not amplify with race 1-specific PCRs amplified with the race 2-specific primers. To validate this, two differential lines of lettuce were inoculated with 53 arbitrarily selected isolates from spinach seed and their pathogenicity and virulence were assessed in a greenhouse. The reactions of the differential cultivars strongly supported the PCR data. V. dahliae race structure was investigated in crops in coastal California and elsewhere using primers specific to the two races. All artichoke isolates from California were race 1, whereas nearly all tomato isolates were race 2. Isolates from lettuce, pepper, and strawberry from California as well as isolates from spinach seed from two of four countries comprised both races, whereas only race 2 was observed in cotton, mint, olive, and potato. This highlights the importance of identifying resistance against race 2 in different hosts. The technique developed in this study will benefit studies in ecology, population biology, disease surveillance, and epidemiology at local and global scales, and resistance breeding against race 2 in lettuce and other crops.

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Genetic Diversity of Verticillium dahliae Isolates From Mint Detected with Genotyping by Sequencing

Phytopathology ◽

10.1094/phyto-12-18-0475-r ◽

2019 ◽

Vol 109 (11) ◽

pp. 1966-1974 ◽

Cited By ~ 3

Author(s):

Jeremiah K. S. Dung ◽

Brian J. Knaus ◽

Henry L. S. Fellows ◽

Niklaus J. Grünwald ◽

Kelly J. Vining

Keyword(s):

Genetic Diversity ◽

Pacific Northwest ◽

Verticillium Wilt ◽

Verticillium Dahliae ◽

Genotyping By Sequencing ◽

The United States ◽

The Pacific ◽

Pathogenic Race ◽

Compatibility Group ◽

Race 2

Verticillium wilt is the most important disease threatening the commercial production of mint grown for essential oil. An important long-term goal for mint breeders is the production of cultivars with resistance to Verticillium wilt. Before that can be accomplished, a better understanding of the genetic variation within and among populations of Verticillium dahliae is needed. We characterized the extent of phenotypic and genetic diversity present in contemporary and archival populations of V. dahliae from mint fields in Oregon and other production regions of the United States using genotyping by sequencing, PCR assays for mating type and pathogenic race, vegetative compatibility group (VCG) tests, and aggressiveness assays. We report that the population in the Pacific Northwest can be described as one common genetic group and four relatively rare genetic groups. Eighty-three percent of the isolates belonged to VCG2B, and all isolates possessed the MAT1-2 idiomorph and were characterized as pathogenic race 2. These results indicate low levels of genetic diversity and a negligible risk of sexual recombination in populations of this host-adapted pathogen population. Knowledge of the genetic structure of V. dahliae in the Pacific Northwest will inform breeders about the diversity of pathogenicity factors that may need to be considered in their breeding programs.

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A Real-Time PCR Assay for Detection and Quantification of Verticillium dahliae in Spinach Seed

Phytopathology ◽

10.1094/phyto-10-11-0280 ◽

2012 ◽

Vol 102 (4) ◽

pp. 443-451 ◽

Cited By ~ 36

Author(s):

Dechassa Duressa ◽

Gilda Rauscher ◽

Steven T. Koike ◽

Beiquan Mou ◽

Ryan J. Hayes ◽

...

Keyword(s):

Real Time ◽

Verticillium Wilt ◽

Verticillium Dahliae ◽

Real Time Pcr ◽

The United States ◽

Infected Seed ◽

Polymerase Chain ◽

Reliable Quantification ◽

Pathogen Dna ◽

Detection And Quantification

Verticillium dahliae is a soilborne fungus that causes Verticillium wilt on multiple crops in central coastal California. Although spinach crops grown in this region for fresh and processing commercial production do not display Verticillium wilt symptoms, spinach seeds produced in the United States or Europe are commonly infected with V. dahliae. Planting of the infected seed increases the soil inoculum density and may introduce exotic strains that contribute to Verticillium wilt epidemics on lettuce and other crops grown in rotation with spinach. A sensitive, rapid, and reliable method for quantification of V. dahliae in spinach seed may help identify highly infected lots, curtail their planting, and minimize the spread of exotic strains via spinach seed. In this study, a quantitative real-time polymerase chain reaction (qPCR) assay was optimized and employed for detection and quantification of V. dahliae in spinach germplasm and 15 commercial spinach seed lots. The assay used a previously reported V. dahliae-specific primer pair (VertBt-F and VertBt-R) and an analytical mill for grinding tough spinach seed for DNA extraction. The assay enabled reliable quantification of V. dahliae in spinach seed, with a sensitivity limit of ≈1 infected seed per 100 (1.3% infection in a seed lot). The quantification was highly reproducible between replicate samples of a seed lot and in different real-time PCR instruments. When tested on commercial seed lots, a pathogen DNA content corresponding to a quantification cycle value of ≥31 corresponded with a percent seed infection of ≤1.3%. The assay is useful in qualitatively assessing seed lots for V. dahliae infection levels, and the results of the assay can be helpful to guide decisions on whether to apply seed treatments.

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First Report of Race 2 of Colletotrichum trifolii Causing Anthracnose on Alfalfa (Medicago sativa) in Wisconsin

Plant Disease ◽

10.1094/pdis-08-13-0808-pdn ◽

2014 ◽

Vol 98 (6) ◽

pp. 843-843 ◽

Cited By ~ 2

Author(s):

D. A. Samac ◽

S. Allen ◽

D. Witte ◽

D. Miller ◽

J. Peterson

Keyword(s):

United States ◽

Medicago Sativa ◽

The United States ◽

Crown Rot ◽

Growth Chamber ◽

Its Sequence ◽

Colletotrichum Trifolii ◽

Differential Cultivars ◽

Race 1 ◽

Race 2

Anthracnose of alfalfa (Medicago sativa), caused by Colletotrichum trifolii, is widespread in the United States. In addition to loss of forage due to death of stems, the pathogen causes crown rot, reducing stand life and winter survival (2), making it one of the most serious diseases of alfalfa. Three physiological races have been described (2). Race 1 is reported to be the dominant race that is present wherever alfalfa is grown, while race 2 was reported in a limited area in the Mid-Atlantic states, and race 4 was found in Ohio (1). Conspicuous, straw-colored dead stems with a “shepherd's crook” wilt and large, sunken, diamond-shaped lesions with a dark border were observed in experimental plots and breeding nurseries of experimental lines in Clinton and West Salem, WI, in August 2011 and in West Salem, WI, in mid-August 2012. Acervuli with black setae and orange spore masses were observed in lesions placed in moist chambers for 2 days at room temperature with ambient room lighting. Conidia were germinated on 1% water agar and then single hyphae were transferred to potato dextrose agar (PDA) plates. DNA was extracted from pure cultures of strains DA-1 (Clinton, WI) and FGI-3 (West Salem, WI), the rDNA ITS1-5.8S-ITS2 region was amplified with primers ITS1 (5′-TCCGTAGGTGAACCTGCGG-3′) and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′), the products sequenced directly, and the sequences compared to the ITS region of known race 1 and race 2 strains of C. trifolii. The sequences from DA-1 and FGI-3 were identical to the ITS sequence of C. trifolii 2sp2 (race 1; KF444778) and C. trifolii SB-2 (race 2; KF444779), but distinct from the ITS sequence of C. destructivum (JQ005764) and C. dematium (JX567507), which can cause anthracnose on alfalfa (1). Conidia from DA-1 and FGI-3 were harvested from 7-day-old cultures grown on PDA plates, diluted to 2 × 106 conidia/ml, and sprayed to runoff on 10-day-old growth chamber grown plants of three differential cultivars: Saranac (susceptible to races 1 and 2), Arc (resistant to race 1, susceptible to race 2), and Saranac AR (resistant to races 1 and 2). Plants were maintained at 100% relative humidity for 48 h and then grown in a growth chamber at 24°C with a 16-h photoperiod. Symptoms were rated at 14 days after inoculation. In the three repetitions of the experiment using 75 plants of each cultivar in each experiment, less than 10% of the Saranac and Arc plants survived, while survival of Saranac AR was 31 to 44%. The approximate expected survival of differential cultivars inoculated with race 1 is 1% for Saranac, 65 to 70% for Arc, and 45% for Saranac AR (2). Aggressiveness of race 2 strains on Saranac AR is variable, ranging from 12 to 68% plant survival (3). The susceptibility of Arc when inoculated with DA-1 and FGI-3 is consistent with the reaction to race 2 strains, indicating that both strains are race 2. The isolation of race 2 strains in major alfalfa growing regions in Wisconsin indicates that this physiological race is currently more widespread than previously observed. Although most modern alfalfa cultivars have resistance to race 1, few cultivars with resistance to race 2 are available. The occurrence of C. trifolii race 2 in the Midwest United States should be considered in alfalfa breeding programs when developing multi-pest resistant alfalfa cultivars. References: (1) J. J. Ariss and L. H. Rhodes. Plant Dis. 91:1362, 2007. (2) N. R. O'Neill. Plant Dis. 80:450, 1996. (3) N. R. O'Neill et al. Phytopathology 79:750, 1989.

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Selection for Resistance to Verticillium Wilt Caused by Race 2 Isolates of Verticillium dahliae in Accessions of Lettuce (Lactuca sativa L.)

HortScience ◽

10.21273/hortsci.46.2.201 ◽

2011 ◽

Vol 46 (2) ◽

pp. 201-206 ◽

Cited By ~ 12

Author(s):

Ryan J. Hayes ◽

Karunakaran Maruthachalam ◽

Gary E. Vallad ◽

Steven J. Klosterman ◽

Krishna V. Subbarao

Keyword(s):

Genetic Variation ◽

Verticillium Wilt ◽

Verticillium Dahliae ◽

Partial Resistance ◽

Disease Incidence ◽

Greenhouse Experiments ◽

Complete Resistance ◽

Race 1 ◽

Selection For ◽

Race 2

Verticillium wilt of lettuce caused by Verticillium dahliae can cause severe economic damage to lettuce producers. The pathogen exists as two races (Races 1 and 2) in lettuce, and complete resistance to Race 1 is known. Resistance to Race 2 isolates has not been reported, and production of Race 1-resistant cultivars will likely increase the frequency of Race 2 strains. The objective of this research was to select lettuce accessions for resistance to Race 2 isolates of V. dahliae. Two independent populations totaling 314 randomly sampled PIs were evaluated for Verticillium wilt disease incidence (DI) caused by V. dahliae isolate VdLs17 in one unreplicated and two replicated greenhouse experiments. Selection for PIs with reduced DI was conducted between each experiment and plant stems were plated on semiselective media to identify colonized plants that remained non-symptomatic. No accession with complete resistance was identified, although accessions with partial resistance were selected. Genetic variation for the frequency of V. dahliae-colonized plants that remain symptomless was detected. Four PIs (169511, 171674, 204707, and 226641) were selected for further testing in three replicated greenhouse experiments and demonstrated significantly lower disease incidence than the susceptible control cultivars. The results indicate that lettuce has genetic variation for partial resistance to a Race 2 isolate of V. dahliae. The resistant PIs selected in this research are morphologically diverse, and no dependence between rate of bolting and resistance was found. PIs with partial resistance may be useful for breeding lettuce cultivars with resistance to Race 2 isolates of V. dahliae.

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Molecular Variation Among Isolates of Verticillium dahliae and Polymerase Chain Reaction-Based Differentiation of Races

Phytopathology ◽

10.1094/phyto-04-10-0122 ◽

2010 ◽

Vol 100 (11) ◽

pp. 1222-1230 ◽

Cited By ~ 31

Author(s):

K. Maruthachalam ◽

Z. K. Atallah ◽

G. E. Vallad ◽

S. J. Klosterman ◽

R. J. Hayes ◽

...

Keyword(s):

Polymerase Chain Reaction ◽

Genetic Variability ◽

Ssr Markers ◽

Verticillium Dahliae ◽

Cropping Systems ◽

Chain Reaction ◽

Pcr Assay ◽

Race 1 ◽

Polymerase Chain ◽

Race 2

Verticillium dahliae is a soilborne fungal pathogen that causes vascular wilt in a variety of economically important crops worldwide. There are two races of V. dahliae that infect tomato and lettuce. Although race-1-specific resistance has been identified in both tomato and lettuce, no resistant sources are available for race 2. Molecular analyses were employed to characterize the genetic variability and race structure of 101 isolates of V. dahliae from a variety of hosts, mainly from central and coastal California, and 10 isolates exotic to this area. Analyses of the 16 simple sequence repeat (SSR) markers illustrated that tomato subpopulations from central California were distinct relative to the marigold subpopulations. In contrast, cotton and olive isolates showed admixture with tomato isolates. Analyses of both the ribosomal DNA intergenic spacer regions and SSR markers revealed high genetic variability among isolates but were unable to delineate races of V. dahliae. However, a polymerase chain reaction (PCR) assay was applied to amplify a race-1-specific amplicon from the isolates in many hosts from different geographic areas, and was coupled with virulence assays for validation of the data. Results of the PCR assay showed 100% concordance with the virulence assay to differentiate race 1 from race 2 of 48 isolates from tomato. The results indicate that the PCR assay can be applied to differentiate the two races to support our related aim of breeding host resistance, and further reveal insights into the distribution of races in tomato and lettuce cropping systems in California.

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Host Range of Verticillium isaacii and Verticillium klebahnii from Artichoke, Spinach, and Lettuce

Plant Disease ◽

10.1094/pdis-12-14-1307-re ◽

2015 ◽

Vol 99 (7) ◽

pp. 933-938 ◽

Cited By ~ 14

Author(s):

Suraj Gurung ◽

Dylan P. G. Short ◽

Xiaoping Hu ◽

German V. Sandoya ◽

Ryan J. Hayes ◽

...

Keyword(s):

New Species ◽

Host Range ◽

Disease Severity ◽

Verticillium Wilt ◽

Agricultural Soils ◽

Phylogenetic Analyses ◽

Greenhouse Experiment ◽

Vascular Wilt ◽

Race 1 ◽

Race 2

Verticillium is a genus that includes major vascular wilt pathogens. Recently, multilocus phylogenetic analyses of the genus identified five new species, including Verticillium isaacii and V. klebahnii, both of which occur in agricultural soils in coastal California and have been isolated from asymptomatic and diseased spinach and lettuce plants. Little data are available regarding their pathogenicity and virulence on a broader range of crops important to the region. Four isolates each of V. isaacii and V. klebahnii along with two reference isolates of V. dahliae races 1 and 2 were inoculated on eight crops (artichoke, cauliflower, eggplant, lettuce, pepper, tomato, spinach, and strawberry) in a greenhouse experiment. After 8 weeks, plants were assessed for disease severity to determine the relative host ranges of Verticillium isolates. Additionally, 13 lettuce lines resistant to race 1 and partially resistant to race 2 of V. dahliae were screened against V. isaacii and V. klebahnii to evaluate their responses. Three of four V. isaacii and four of four V. klebahnii isolates tested were nonpathogenic on all crops tested except those indicated below. One V. isaacii isolate caused wilt on artichoke and ‘Salinas’ lettuce and most isolates of both species caused varying degrees of Verticillium wilt on strawberry. Lettuce lines resistant to V. dahliae race 1 and partially resistant to V. dahliae race 2 also exhibited resistance to all of the isolates of V. isaacii and V. klebahnii. Thus, at least some isolates in the populations of V. isaacii and V. klebahnii have the potential to become significant pathogens of coastal California crops. However, resistance developed against V. dahliae also offers resistance to the pathogenic isolates of both species, at least in lettuce.

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Transmission of Xylella fastidiosa, Causal Agent of Citrus Variegated Chlorosis, by the Glassy-Winged Sharpshooter, Homalodisca coagulata

Plant Disease ◽

10.1094/pd-90-0567 ◽

2006 ◽

Vol 90 (5) ◽

pp. 567-570 ◽

Cited By ~ 20

Author(s):

V. D. Damsteegt ◽

R. H. Brlansky ◽

P. A. Phillips ◽

Avijit Roy

Keyword(s):

Xylella Fastidiosa ◽

The United States ◽

Citrus Variegated Chlorosis ◽

Homalodisca Coagulata ◽

Causal Pathogen ◽

Polymerase Chain ◽

Species Specific ◽

Transmission Studies ◽

Test Plants ◽

Important Disease

Citrus variegated chlorosis (CVC) is an economically important disease of citrus in Brazil and Argentina. The causal pathogen is a strain of Xylella fastidiosa transmitted by several sharpshooter species. The glassy-winged sharpshooter (GWSS), Homalodisca coagulata, has become an important new pest of citrus and grapevines in California, where it transmits X. fastidiosa strains to several crops including grapes, oleander, and almonds. Transmission studies over a 3-year period at the USDA BSL3-P containment facility at Fort Detrick, MD, utilizing California field-collected GWSS, a Brazilian strain of CVC, and Madam Vinous sweet orange seedlings, have shown a consistent although low level of transmission of CVC. Test plants were observed for CVC symptoms, analyzed by polymerase chain reaction using species-specific primers for X. fastidiosa, membrane entrapment immunofluorescence, and scanning electron microscopy. X. fastidiosa was not detected in field-collected GWSS but was detected in GWSS following feeding on CVC-infected source plants. Transmission of the CVC strain of X. fastidiosa by GWSS increases the risk of establishment of CVC in the United States if it were introduced.

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Suppression of Fusarium Wilt Caused by Fusarium oxysporum f. sp. niveum Race 2 on Grafted Triploid Watermelon

Plant Disease ◽

10.1094/pdis-01-14-0005-re ◽

2014 ◽

Vol 98 (10) ◽

pp. 1326-1332 ◽

Cited By ~ 13

Author(s):

Anthony P. Keinath ◽

Richard L. Hassell

Keyword(s):

Fusarium Oxysporum ◽

Fusarium Wilt ◽

Disease Incidence ◽

The United States ◽

Infested Soil ◽

Marketable Yield ◽

Race 1 ◽

Susceptible Control ◽

Triploid Watermelon ◽

Race 2

Fusarium wilt of watermelon, caused by the soilborne fungal pathogen Fusarium oxysporum f. sp. niveum race 2, is a serious, widespread disease present in major watermelon-growing regions of the United States and other countries. ‘Fascination,’ a high yielding triploid resistant to race 1, is grown in southeastern states in fields that contain a mixture of races 1 and 2. There is some benefit to using cultivars with race 1 resistance in such fields, even though Fascination is susceptible to Fusarium wilt caused by race 2. Experiments in 2012 and 2013 were done in fields infested primarily with race 2 and a mixture of races 1 and 2, respectively. Fascination was grafted onto four rootstock cultivars: bottle gourd (Lagenaria siceraria) ‘Macis’ and ‘Emphasis’ and interspecific hybrid squash (Cucurbita maxima× C. moschata) ‘Strong Tosa’ and ‘Carnivor.’ Nongrafted and self-grafted Fascination were used as susceptible control treatments. In both experiments, mean incidence of plants with symptoms of Fusarium wilt was ≥52% in the susceptible control treatments and ≤6% on the grafted rootstocks. Disease incidence did not differ between rootstock species or cultivars. In both years, Fascination grafted onto Strong Tosa and Macis produced more marketable-sized fruit than the susceptible control treatments. Grafted Emphasis and Carnivor also produced more fruit than the control treatments in 2012. The cucurbit rootstocks suppressed Fusarium wilt caused by race 2 and increased marketable yield of triploid watermelon grown in infested soil.

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Characterization of Race-Specific Interactions Among Isolates of Verticillium dahliae Pathogenic on Lettuce

Phytopathology ◽

10.1094/phyto-96-1380 ◽

2006 ◽

Vol 96 (12) ◽

pp. 1380-1387 ◽

Cited By ~ 49

Author(s):

Gary E. Vallad ◽

Qing-Ming Qin ◽

Rebecca Grube ◽

Ryan J. Hayes ◽

Krishna V. Subbarao

Keyword(s):

Verticillium Dahliae ◽

Field Experiments ◽

Sequence Data ◽

Intergenic Spacer ◽

Distinct Subgroup ◽

Race 1 ◽

Race 2 ◽

The 1960S ◽

Significant Disease

Verticillium wilt, caused by Verticillium dahliae, poses a major threat to lettuce (Lactuca sativa) production in California. Incorporation of resistance into commercial lettuce cultivars offers the least expensive technique of sustaining production in infested areas. To test the breadth of the resistance identified in field experiments, a pair of susceptible (‘Salinas’ and ‘Sniper’) and resistant (‘La Brillante’ and ‘Little Gem’) lettuce cultivars were used as differentials and individually inoculated with 29 isolates of V. dahliae and two isolates of V. albo-atrum from several hosts, including lettuce, in replicated greenhouse experiments. The reactions of the four cultivars were determined based on the disease severity at maturity. None of the V. albo-atrum isolates or V. dahliae isolates from cruciferous hosts caused significant disease on lettuce. Both Salinas and Sniper were susceptible to many isolates of V. dahliae (21 of 23) from noncruciferous hosts, and the isolates varied in their overall virulence. However, of these, only three isolates caused significant disease on the resistant cvs. La Brillante and Little Gem. These three isolates also were distinct from the other V. dahliae isolates based on sequence data from the intergenic spacer (IGS) region of the nuclear ribosomal RNA gene, suggesting that they form a phylogenetically distinct subgroup that differs in virulence toward specific lettuce genotypes. Accordingly, isolates of V. dahliae virulent on all tested cultivars, including the resistant La Brillante and Little Gem, were designated as race 2, whereas those virulent only on the susceptible Salinas and Sniper were designated as race 1. Although a range of virulence among isolates has been described in other hosts, this is the first description of distinct virulence phenotypes in V. dahliae since a similar race structure was described in tomato in the 1960s.

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