The Rpv3-3 haplotype and stilbenoid induction mediate downy mildew resistance in a grapevine interspecific population

The cultivated Eurasian grapevine (Vitis vinifera L.) is highly susceptible to downy mildew (DM) – caused by the biotrophic oomycete Plasmopara viticola (Berk. & M.A. Curtis) Berl. & De Toni – the major disease of temperate-humid climates among various pathogen threats. DM control relies mainly on the massive use of fungicides leading to environmental pollution, development of resistance and residual toxicity. The exploitation of DM-resistant wild genetic resources for the development of new resistant cultivars represents a promising alternative. Taking advantage of a segregating population derived from ‘Merzling’ (M, a mid-resistant hybrid) and ‘Teroldego’ (T, a susceptible landrace), recent studies have highlighted the importance of stilbenoids among phenolic compounds in conferring resistance to this oomycete. In order to elucidate the genetic bases of DM resistance and polyphenol biosynthesis upon P. viticola inoculation, 136 M×T F1 individuals were characterized by an integrative approach combining genetic, phenotypic and gene-expression data. An improved M×T linkage map was obtained by scoring 192 microsatellite markers. The progeny was further screened for degree of resistance and production of 42 phenolic compounds (including 18 different stilbenoids). Quantitative trait locus (QTL) mapping showed that DM resistance is associated with a specific haplotype at the Rpv3 locus – herein named Rpv3-3, derived from the French hybrid ‘Seyval’ – and identified 46 novel metabolic (m)QTLs linked to 30 polyphenol-related parameters. A list of the 76 most relevant candidate genes was generated by specifically exploring the genomic regions underlying the mQTLs associated with the stilbenoids induced by the infection. Finally, expression analysis of 13 genes in Rpv3-3+/- genotypes, displaying divergent DM resistance and stilbenoid accumulation, revealed significant candidates for the genetic control of stilbenoid biosynthesis and oligomerization. These findings emphasize that DM resistance can be mediated by the major Rpv3-3 locus and stilbenoid induction.