Esca Disease triggers local transcriptomic response and systemic DNA methylation changes in grapevine

Woody plants such as grapevine are vulnerable to trunk diseases caused by pathogens that colonize the wood, disrupt vascular function, and induce recurrent leaf symptoms associated with major metabolic disturbances and canopy decline. Over time, these diseases can irreversibly alter plant physiology and phenotype, ultimately reducing vine longevity. One of the most predominant of such diseases is esca, which is a major cause of vineyard dieback, with rising incidence worldwide over the past decade. However, the molecular mechanisms underlying esca symptom development remain unclear. In this study, we leveraged the heterogeneous expression of esca-symptoms within individual grapevines to investigate molecular responses in both symptomatic and asymptomatic leaf tissues. By combining metabolite profiling, RNA-seq and whole genome bisulfite sequencing, we show that metabolic alterations and extensive transcriptomic reprogramming are restricted to symptomatic leaves and are partially associated with local changes in DNA methylation. Asymptomatic leaves display distinct DNA methylation changes, some of which are shared with symptomatic tissues, suggesting a systemic response to the disease at the epigenetic level. Notably, subset of these methylation marks are observable prior to symptom emergence, highlighting the potential of epigenetic biomarkers for the early detection of trunk diseases in perennial plants.