Esca disease triggers local transcriptomic response and DNA methylation changes in grapevine

Woody plants such as grapevine (Vitis vinifera L.) are vulnerable to trunk diseases caused by pathogens that disrupt vascular function and induce severe leaf symptoms associated with major metabolic disturbances and canopy decline. Over time, these diseases can irreversibly alter the plant's physiology and phenotype, ultimately reducing vine longevity. One of the most predominant trunk 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 in individual grapevines to investigate molecular responses in symptomatic and asymptomatic leaf tissues collected in the field. 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. In addition, asymptomatic leaves display distinct DNA methylation changes, a few of which are shared with symptomatic tissues, suggesting a global plant epigenetic response to the disease. Notably, a subset of these methylation marks are observed before symptom development, highlighting the potential of epigenetic markers for the early detection of trunk diseases in perennial plants.