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

• Published in: Ecology and evolution 2017-08, Vol.7 (16), p.6231-6246
• Main Authors: Thomas, Anna, Carbone, Ignazio, Choe, Kisurb, Quesada‐Ocampo, Lina M., Ojiambo, Peter S.
• Format: Article
• Language: English
• Subjects: Airborne microorganisms; Citrullus lanatus; coalescent analysis; Comparative analysis; Cucumis melo; Cucurbita maxima; Cucurbita moschata; Cucurbita pepo; cucurbits; Deoxyribonucleic acid; disease resurgence; DNA; Downy mildew; Evolution; Gene sequencing; Genetic diversity; Genomes; Genomic analysis; lineage; Original Research; Paralomis cubensis; phylogenetic analysis; Pseudoperonospora cubensis; Specialization; Virulence
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.3194

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. Cucurbit downy mildew caused by Pseudoperonospra cubensis has resurged around the world in the last two decades. Comparative analysis of nine genomes confirmed the presence of two distinct evolutionary lineages. Lineage II that lacked genetic diversity had pathoytpes that have never been reported in the United States hinting to possible cause of the resurgence.