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

O_LIPlasmopara viticola is a biotrophic oomycete responsible for grapevine downy mildew, one of the most destructive diseases in viticulture. Breeding for resistant varieties relies on the introgression of partial resistance factors from wild grapes, but virulent strains are rapidly emerging. C_LIO_LITo decipher the genetic bases of the adaptation to plant resistance in P. viticola, we carried out a QTL mapping study using two F1 populations segregating for the ability to overcome Rpv3.1, Rpv10 and Rpv12. Trajectories of virulence emergence were also compared by conducting a population structure analysis on a panel of diversity. C_LIO_LIWe confirmed the position of AvrRpv3.1 and identified the AvrRpv12 locus, in which strains overcoming Rpv12 presented large deletions encompassing several RXLR genes. Distinct virulent alleles were selected independently in different winegrowing regions. Unlike this standard case of recessive virulence, partial breakdown of Rpv10 was determined by a dominant locus, suggesting a suppressor activity. The virulent haplotype exhibits structural rearrangements and an extended effector repertoire. It corresponds to an admixed genomic segment likely originating from a secondary introduction of P. viticola into Europe. C_LIO_LIOn top of the identification of candidate effectors, these results illustrate the range of evolutionary pathways through which plant pathogen populations can adapt to plant resistances. C_LI