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

Abstract

Grapevine downy mildew, caused by the oomycetePlasmopara viticola, is a globally destructive disease that particularly affect the Eurasian wine grapeV. vinifera. While genetically resistant varieties are becoming more accessible, populations ofP. viticolaare 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 136P. viticolastrains 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 theP. viticolaINRA-Pv221 genome allowed to detect structural variations in this locus, including a major 30 Kbp deletion. At the avrRpv3.1 locus, virulentP. viticolastrains 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 ofP. viticolainvolved in the interaction with resistance gene provides valuable insights into the genetic mechanisms that enableP. viticolato adapt to grapevine resistance, laying a foundation for developing strategies to manage this damaging crop pathogen.