Esca-disease consequences on grapevine transcriptome and methylome

Plants are sessile organisms that must continuously adapt to their environment. Epigenetic mechanisms, including DNA methylation, play a central role in regulating plant stress responses, yet they remain poorly understood in perennial species. Woody plants such as grapevine are vulnerable to trunk diseases caused by pathogens that colonize the wood, disrupt their 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 their longevity. Esca-disease is a major cause of vineyard dieback, with rising incidence worldwide over the past decade. However, the molecular mechanisms underlying 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 common to those observed in symptomatic tissues, suggesting a systemic impact of 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 perennials.