Resurgence of cucurbit downy mildew in the United States: Insights from comparative genomic analysis of Pseudoperonospora cubensis

Abstract

Pseudoperonospora cubensis, the causal agent of cucurbit downy mildew (CDM), is known to exhibit host specialization. The virulence of different isolates of the pathogen can be classified into pathotypes based on their compatibility with a differential set composed of specific cucurbit host types. However, the genetic basis of host specialization within P. cubensis is not yet known. Total genomic DNA extracted from nine isolates of P. cubensis collected from 2008 to 2013 from diverse cucurbit host types (Cucumis sativus, C. melo var. reticulatus, Cucurbita maxima, C. moschata, C. pepo, and Citrullus lanatus) in the United States were subjected to whole‐genome sequencing. Comparative analysis of these nine genomes confirmed the presence of two distinct evolutionary lineages (lineages I and II) of P. cubensis. Many fixed polymorphisms separated lineage I comprising isolates from Cucurbita pepo, C. moschata, and Citrullus lanatus from lineage II comprising isolates from Cucumis spp. and Cucurbita maxima. Phenotypic characterization showed that lineage II isolates were of the A1 mating type and belonged to pathotypes 1 and 3 that were not known to be present in the United States prior to the resurgence of CDM in 2004. The association of lineage II isolates with the new pathotypes and a lack of genetic diversity among these isolates suggest that lineage II of P. cubensis is associated with the resurgence of CDM on cucumber in the United States.

STAYGREEN, STAY HEALTHY: a loss‐of‐susceptibility mutation in the STAYGREEN gene provides durable, broad‐spectrum disease resistances for over 50 years of US cucumber production

“…S1). In the G9RIL population, Gy14 exhibited moderate resistance, although it showed slightly better performance in the NL trials than in the NC trials (Table S5), probably as a result of the differential virulence structure of the P. cubensis populations at the two locations (Thomas et al, 2017). With disease progress, the mean disease scores for Yel, Col and GI of the population increased (in NC trials) or decreased (in NL trials), suggesting greater overall severity of symptoms of plants in the whole population with increased exposure to the DM inoculum (note that the scoring scales used in NC and NL were opposite) (Table S5; Fig.…”

“…PI 197087-derived DM resistance was controlled by a single recessive gene (dm1) with a classical HR (Barnes & Epps, 1954;van Vliet & Meysing, 1974, 1977Fanourakis & Simon, 1987;Kennard et al, 1994;Horejsi et al, 2000). The dm1-conferred DM resistance has been widely deployed in commercial cucumber varieties, which have provided effective protection to cucumber production in the USA for over 50 years until 2004, when new DM strain(s) (post-2004 strains) emerged in the cucumber field rendering dm1 resistance less effective (Holmes et al, 2006;Thomas et al, 2017). Nevertheless, dm1 still exhibits moderate resistance to the prevailing post-2004 DM strains in the USA and sufficient resistance in many other countries.…”

“Jumping Jack”: Genomic Microsatellites Underscore the Distinctiveness of Closely Related Pseudoperonospora cubensis and Pseudoperonospora humuli and Provide New Insights Into Their Evolutionary Past

“…Third-generation sequencing and hybrid assembly tools should help decipher the problematic gene-sparse and repeat-rich genome regions (Haas et al, 2009;McGowan and Fitzpatrick, 2020), which are the common obstacle in the effective assembly of short reads. The genotyping-by-sequencing research seems a particularly attractive analytical approach for both species, taking advantage of the comparatively small genome sizes for such a massive tool (Thomas et al, 2017a;Gent et al, 2019).…”

“…They also developed five SSRs that were more polymorphic than the other tested, suggesting higher genetic uniformity of P. humuli in Europe than in North America and prompting their hypothesis of the pathogen being introduced to Europe (Kitner et al, 2021). Comparatively, several molecular approaches were used for population biology of P. cubensis (Quesada-Ocampo et al, 2012;Polat et al, 2014;Kitner et al, 2015;Naegele et al, 2016;Thomas et al, 2017a;Wallace and Quesada-Ocampo, 2017). Intersimple sequence repeat (ISSR) and sequence-related amplified polymorphism (SRAP) markers used for the analyses of P. cubensis from Israel, Turkey, and Czech Republic indicated high diversity both among and within the regions, with the samples from Israel forming a distinct clade (Polat et al, 2014).…”

Biological Characteristics and Assessment of Virulence Diversity in Pathosystems of Economically Important Biotrophic Oomycetes

“…This is contradictory to the definition of the term race given in Chapter I which demands host-independent characters of the pathogen for classification. However, to avoid confusion, the traditional concept will be kept here for the reviewed literature on P. cubensis, though knowing that virulence phenotypes of this pathogen infecting hosts of different genera are likely to consist of independent species as was indicated by recent whole-genome sequencing of different isolates of P. cubensis (Thomas et al, 2017a) The first differential set of seven species of the Cucurbitaceae was developed for the identification of P. cubensis pathotypes (Thomas et al, 1987). They used Cucumis sativus, C. melo var.…”