Comparative genomics of downy mildews reveals potential adaptations to biotrophy

Abstract

BackgroundSpinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the expanding spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable and 15 new races have been recognized in the past 30 years.ResultsWe 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 kb & 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5214-8) contains supplementary material, which is available to authorized users.

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

“…The genomes of Pfs race 13 and 14 have recently been published [82, 83], with a similar genome size (32.1 Mb, and 30.8 Mb respectively) and gene content (∼ 8000 gene models) compared to the assembly of Pfs1 . Contrary to our assembly method, the input data for those genome assemblies were filtered by alignment to an oomycete and bacterial database to discard reads that do not belong to the oomycete genus.…”

“…Recent sequencing of Peronospora species shows that they have remarkably small and compact genomes (32.3 – 63.1 Mb) compared to Phytophthora (82-240 Mb) species [29, 33, 82, 84]. The k- mer analysis predicts the Pfs1 genome to be 36.18 Mb containing 8.78 Mb of repeats (24%).…”

“…The k- mer analysis predicts the Pfs1 genome to be 36.18 Mb containing 8.78 Mb of repeats (24%). The predicted genome size of Pfs R13 and R14 based on k- mer prediction is 44.1 - 41.2 mb (repeats; 24 – 22%) [82]. The increased genome size of Phytophthora is attributed to an ancestral whole genome duplication in the lineage leading to Phytophthora and to an increase in the proportion of repetitive non-coding DNA [29, 85].…”

Genetic diversity of the spinach downy mildew pathogen based on hierarchical sampling

“…Some genome resources of P. effusa are now available and a large number of SNPs have been identified [18,42]. It may be possible to get additional insight of the population structure and evolution of P. effusa by using genome-wide SNPs.…”

“…The emergence and/or introduction of new races and genotypes would alter the genetic diversity of the P. effusa population. Tremendous variation has been observed in many other plantpathogenic oomycetes [16][17][18][19]. A number of mechanisms may contribute to the genetic variability of these oomycetes, including 1) during asexual reproduction, mitotic recombination and transposable elements could result in genetic variation [19,20]; 2) The meiotic recombination due to sexual reproduction could result in significant variation in the progeny and better adaptation to the environment [19,[21][22][23].…”