Transcriptome, hormonome, and metabolome of susceptible grape berries under powdery mildew infection

Vitis vinifera berries are extremely sensitive to infection by the biotrophic pathogen Erysiphe necator causing powdery mildew disease and deleterious effects on grape and wine quality. The combined analysis of the transcriptome and metabolome associated with this common fungal infection has not been previously carried out in any fruit. In order to identify the molecular, hormonal and metabolic mechanisms associated with infection, healthy and naturally infected ‘Carignan’ berries were collected at two developmental stages: late green (EL33) and early véraison (EL35). RNA sequencing combined with GC-EI/TOF-MS, GC-EI/QUAD-MS and LC-MS/MS analyses revealed that powdery mildew-susceptible grape berries were able to activate defensive mechanisms with the involvement of salicylic acid and jasmonates and to accumulate defence-associated metabolites (e.g., phenylpropanoids, fatty acids). The defensive strategies also indicated organ-specific responses namely the activation of fatty acid biosynthesis. However, defence responses were not enough to restrict fungal growth. The fungal metabolic program during infection involves secretion of effectors related to effector-triggered susceptibility, carbohydrate-active enzymes and activation of sugar, fatty acid and nitrogen uptake and could be under epigenetic regulation. This study also identified potential metabolic biomarkers such as gallic, eicosanoic and docosanoic acids, and resveratrol, that can be used to monitor early stages of infection.