Comparative genomics provide insight into the evolution of European <i>Aphanomyces euteiches</i> strains

Aphanomyces euteiches is an oomycete pathogen causing root rot in pea and other legumes, leading to devastating yield losses in pea production. Previously, three genetic groups of A. euteiches were identified in Europe based on simple sequence repeat markers. In this study, we determined the genome sequences of 68 European A. euteiches strains and performed a comparative genomic analysis with the aim to investigate the population genetic structure of A. euteiches, to delineate species boundaries and to identify gene families evolving under selection for gene gains or losses. Population genetic analysis based on genome-wide single nucleotide polymorphisms identified three genetic groups in Europe, where strains from Italy formed a distinct and genetically isolated group. Genealogical concordance phylogenetic species recognition analysis indicated that strains from Italy may represent a cryptic species. Aphanomyces strains differed in virulence on susceptible and partially resistant pea host genotypes, but virulence did not correlate with genetic groups. Analysis of virulence-related gene family evolution revealed a significant expansion of gene families acting in the detoxification of plant-derived secondary metabolites in plant pathogenic Aphanomyces species. Moreover, the carbohydrate esterase family 1 (CE1) was significantly expanded in A. euteiches, but not in the cryptic species represented by Italian strains. Modular structure analyses revealed exclusive presence of feruloyl esterase domains in CE1 homologs of plant pathogenic Aphanomyces species, indicating a role in plant cell wall degradation.