Parallel adaptation and admixture drive the evolution of virulence in the grapevine downy mildew pathogen

Plant pathogens can rapidly adapt to host defenses, threatening the durability of resistance in crop varieties. It is thus crucial to identify the genetic determinants of virulence and understand how it arises and spreads in pathogen populations. In Plasmopara viticola, the biotrophic oomycete causing grapevine downy mildew, virulent strains have recently emerged following the deployment of cultivars carrying partial resistance factors. To investigate the genetic bases of adaptation to grapevine resistances, we carried out a QTL mapping study using two P. viticola biparental populations segregating for the ability to overcome two major loci, Rpv10 and Rpv12. We identified the AvrRpv12 locus, in which strains virulent towards Rpv12 exhibited large homozygous deletions encompassing several RXLR effector genes. Population structure analyses further revealed that distinct alleles were selected independently in different winegrowing regions in Europe, highlighting multiple parallel adaptation events in response to resistance deployment. By contrast, the breakdown of Rpv10 was determined by a dominant locus, suggesting an active suppressor mechanism. The virulent haplotype showed extensive structural rearrangements and a divergent effector repertoire. The locus corresponds to an admixed genomic segment likely originating from a recent secondary introduction of P. viticola into Europe. Beyond merely identifying candidate effectors, these results illustrate the range of evolutionary pathways through which pathogen populations adapt to plant resistances.