Whole plant metabolomic analysis reveals contrasted responses in tolerant and susceptible grapevine cultivars to infection with different isolates of Neofusicoccum parvum, a major trunk disease fungus

Vineyards worldwide are threatened by grapevine trunk diseases (GTDs) which are increasingly concerning in the context of climate change. Neofusicoccum parvum , a widespread highly aggressive Botryosphaeriaceae fungus, is associated with Botryosphaeria dieback (BD), one of the major GTDs. Despite the absence of fully resistant genotypes, tolerance to GTDs reflected by foliar symptom expression, vary among cultivars, but the underlying mechanisms remain poorly understood. To get further insight into contrasted cv responses to GTD, untargeted LC–MS-based metabolomic analyses were conducted on two grapevine cultivars (Chardonnay and Gewurztraminer) exhibiting contrasting responses to BD. Whole-plant dynamics were assessed by sampling wood, leaves and roots at different times following inoculation with two N. parvum isolates differing in aggressiveness. Pathogen colonization assays revealed contrasting wood invasion capacities between the two isolates, confirming their differing aggressiveness. Global metabolomic analyses showed that cultivar and fungal isolate were the main factors structuring metabolic variation, with additional effects of organ and time. In response to the most aggressive isolate, the two cultivars exhibited distinct responses in wood, particularly in stilbene and oxylipin profiles. Compared to Gewurztraminer, Chardonnay showed faster and higher induction of stilbenes and fatty acids synthesis in the wood, especially oxylipins, which could be involved in plant defense and signaling. Beyond the infection site, leaves and roots also exhibited early metabolic adjustments, more pronounced in Chardonnay, indicating a rapid systemic response. This study underlines that grapevine responses to Botryosphaeriaceae fungi show specificities depending on both plant cultivar and fungal isolate, supporting unique interaction mechanisms rather than common response to wood decay. Although pathogen growth was similar between the two cultivars, they are characterized by specific metabolite signature, especially in the wood. In addition, rapid metabolomic reprogramming at the whole plant level may reduce the impact of infection on host tissues in the tolerant cv Chardonnay. Altogether, these results contribute to a more integrated view of grapevine responses to Botryosphaeriaceae infection.