Multivirulent Plasmopara viticola strains from Cilaos on Réunion Island break down Rpv1, Rpv3.1 and Rpv10 mediated resistance of grapevine

Grapevine downy mildew, caused by Plasmopara viticola, is one of the most destructive diseases in viticulture. Resistance-based management strategies rely on grapevine varieties carrying major resistance loci (Rpv). Although breakdown of several loci has been reported, Rpv1 had remained effective until now. Here, we provide the first evidence of Rpv1 breakdown by P. viticola in Cilaos on Réunion Island (France) and the first case of strains simultaneously overcoming three resistances of grapevine. We combined pathogenicity assays with whole-genome sequencing to characterize strains of P. viticola collected in Cilaos in 2023, alongside a panel reference strains. Hypersensitive response and sporulation were assessed for each strain on Chardonnay (susceptible variety) and four resistant varieties carrying Rpv1, Rpv3.1, Rpv10, or Rpv12. The strains collected in Cilaos were able to overcome not only Rpv1 but also Rpv3.1 and Rpv10. On Rpv1, we observed a complete loss of host recognition with high sporulation. On Rpv3.1, the phenotype was consistent with previous breakdowns, and the strains carried the vir1 allele previously described in France. By contrast, the breakdown of Rpv10 differed from that reported in European populations: whereas European strains displayed only partial breakdown of resistance, the strains of Cilaos showed complete loss of host recognition with high sporulation. Moreover, genomic analyses revealed a novel mutation, a large homozygous deletion in the corresponding avr locus. Population genomic analyses further suggests that the P. viticola strains from Cilaos share a genetic background with populations from western Europe, raising serious concerns about the potential emergence and spread of multivirulent lineages in that area. These findings highlight the need for large-scale virulence monitoring of P. viticola and improved strategies for the sustainable management of grapevine resistance in Europe.