An effector deletion leads to the breakdown of partial grapevine resistance to downy mildew

Grapevine downy mildew, caused by the oomycete Plasmopara viticola, is a globally destructive disease that particularly affect the Eurasian wine grape V. vinifera. While genetically resistant varieties are becoming more accessible, populations of P. viticola are demonstrating rapid adaptability, successfully over-coming these resistances. Here we aimed to identify the avirulence genes involved in the interaction with the Rpv3.1-mediated resistance in grapevine. We sequenced the full genome of 136 P. viticola strains sampled in a natural population of Bordeaux (France) and characterized their development on both resistant and sensitive cultivars. The genome-wide association study allowed the identification of a genomic region associated with the breakdown of Rpv3.1 grapevine resistance (avrRpv3.1 locus). A diploid-aware reassembly of the P. viticola INRA-Pv221 genome allowed to detect structural variations in this locus, including a major 30 Kbp deletion. At the avrRpv3.1 locus, virulent P. viticola strains presented deletion on both haplotypes indicating that avirulence is recessive. The deletion involves two closely-related genes that encode proteins containing 800-900 amino acids with a signal peptide. The structure of the predicted proteins contains repeats of the LWY-fold structural modules, typical of oomycete effectors. Moreover, when these proteins were transiently expressed, they induced cell death in grapevines carrying Rpv3.1 resistance, confirming their avirulence nature. The first description of candidate effectors of P. viticola involved in the interaction with resistance gene provides valuable insights into the genetic mechanisms that enable P. viticola to adapt to grapevine resistance, laying a foundation for developing strategies to manage this damaging crop pathogen.