Investigating the intraspecific diversity of Vitis vinifera responses to esca with a physiopathology approach

Perennial plant dieback involves complex interactions between pathogens, plant morphology, ecophysiology, and environmental conditions. The factors driving intraspecific variation in dieback susceptibility remain unclear. Their identification could guide the selection of more resilient genotypes under global changes. We used a common garden containing 46 Vitis vinifera (grapevine) cultivars to test the hypothesis that differences in grapevine susceptibility to esca -- a complex vascular disease leading to dieback -- result from cultivar-specific interactions between leaf gas exchange, and the anatomical structure, metabolism and microbiome of stem wood. Cultivars with better water use and conservation strategies tended to be less susceptible to esca whereas xylem anatomy did not affect esca susceptibility. Symptomatic plants displayed decreases in leaf gas exchange, stem starch storage and theoretical hydraulic conductivity in response to esca, regardless of genotype, whereas microbial communities were unaffected. Symptomatic stems accumulated more secondary metabolites (mostly glycosylated flavonoids and terpenes) in highly susceptible than in weakly susceptible genotypes. Cultivar-specific physiological traits therefore shape esca susceptibility in grapevines and defence metabolites transported in the xylem may play a key role in the onset of leaf symptoms. Integrative studies unravelling plant-microorganism-environment interactions are crucial to improve our understanding of complex plant diseases.