Comparative genomics of downy mildews reveals potential adaptations to biotrophy

Authors: FLETCHER, KYLE - University Of California; Klosterman, Steven; DEREVNINA, LIDA - University Of California; Martin, Frank; BERTIER, LIEN - University Of California; KOIKE, STEVEN - University Of California - Cooperative Extension Service; CHIN-WO-REYES, SEBASTIAN - University Of California; Mou, Beiquan; MICHELMORE, RICHARD - University Of California

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/31/2018
Publication Date: 11/27/2018
Citation: Fletcher, K., Klosterman, S.J., Derevnina, L., Martin, F.N., Bertier, L.D., Koike, S.T., Chin-Wo-Reyes, S., Mou, B., Michelmore, R. 2018. Comparative genomics of downy mildews reveals potential adaptations to biotrophy. BMC Genomics. 19:851. https://doi.org/10.1186/s12864-018-5214-8.
DOI: https://doi.org/10.1186/s12864-018-5214-8

Interpretive Summary: Downy mildew on spinach is a disease caused by the oomycete pathogen Peronospora effusa. Peronospora effusa is a major production constraint for organic spinach in the US, and elsewhere where spinach is grown. Traditional fungicides cannot be applied for organic spinach production and it is difficult to breed plant resistance to P. effusa, because the pathogen is changing quickly to counteract the plant defenses. This study provides whole genome sequencing and analyses of the data for two different isolates of P. effusa collected in the Salinas Valley of California, and these were designated race 13 (R13) and race 14 (R14) based on their interactions on differential cultivars. This work revealed that candidate gene sets present in a related pathogen that causes extensive cell death in other plants during colonization of the plant are absent in P. effusa and other downy mildews, including some of those encoding transporters, pathogenesis, and enzymes with carbohydrate degrading activity. Of equal importance, this work provides valuable high quality reference genome sequences for future analyses of downy mildew genes important for niche adaptations in P. effusa and in its ability to cause disease.

Technical Abstract: Spinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the growing spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable with 15 new races being recognized in the past 30 years. We virulence phenotyped, sequenced, and assembled two isolates of P. effusa from the Salinas Valley, California, U.S.A. that were identified as race 13 and 14. These assemblies are high quality in comparison to assemblies of other downy mildews having low total scaffold count (784, 880), high contig N50s (48, 52 kb), high BUSCO completion and low BUSCO duplication scores and share many syntenic blocks with Phytophthora species. Comparative analysis of four downy mildew and three Phytophthora species revealed parallel absences of genes encoding conserved domains linked to transporters, pathogenesis, and carbohydrate activity in the biotrophic species. Downy mildews surveyed that have lost the ability to produce zoospores have a common loss of flagella/motor and calcium domain encoding genes. Our phylogenomic data support multiple origins of downy mildews from hemibiotrophic progenitors and suggest that common gene losses in these downy mildews may be of genes involved in the necrotrophic stages of Phytophthora spp. We present a high-quality draft genome of Peronospora effusa that will serve as a reference for Peronospora spp. We identified several Pfam domains as under-represented in the downy mildews consistent with the loss of zoosporegenesis and necrotrophy. Phylogenomics provides further support for a polyphyletic origin of downy mildews.