Organ-specific genetic and metabolic mechanisms underlying grapevine resistance to Botrytis cinerea

Gray mold disease, caused by the necrotrophic fungal pathogen Botrytis cinerea , poses a severe threat to global grapevine production. This study systematically investigated the genetic and metabolic mechanisms underlying grapevine resistance to B. cinerea using a hybrid population derived from the resistant material ‘Beihong’ ( Vitis vinifera L. × V. amurensis Rupr.) and susceptible cultivar ‘Red Globe’ ( V . vinifera L.). Detached-leaf inoculation assays of 176 F 1 progenies revealed a 1:1 segregation ratio of resistant-to-susceptible phenotypes in leaf tissues, with resistant (R) leaves showing enhanced antioxidant enzyme activities that alleviated oxidative stress and delayed fungal colonization. Fruit resistance followed a 1:7 resistant-to-susceptible ratio and showed no significant correlation with leaf resistance ( R = -0.1779), highlighting distinct organ-specific regulatory mechanisms. Untargeted metabolomic profiling of R and susceptible (S) fruits identified 550 differential accumulated metabolites. Susceptible fruits exhibited significant enrichment of the linoleic acid metabolism pathway, characterized by pathological accumulation of lipid peroxidation products that exacerbated membrane damage. Conversely, R fruits exhibited enhanced accumulation of flavonoid metabolites, which conferred resistance through direct antifungal activity. Both exogenous application of didymin, rutin, myricetin, and luteolin-7-glucuronide (≥ 250 mg · L -1 in vitro against B . cinerea and in vivo on fruits) and endogenous flavonoid extracts from R fruit (100 mg · L -1 in vitro ; 50 mg · L -1 for spore disruption) demonstrated significant antifungal activity against B . cinerea . This study reveals that grapevine resistance to B. cinerea is governed by the novel interplay between flavonoid-mediated defense and dysregulated linoleic acid metabolism. These findings identify critical metabolites for postharvest control of gray mold and offer a theoretical foundation for breeding Botrytis -resistant cultivars.