Fungal Pathogen Activity and Stress-Dependent Responses of Grapevine Wood to Esca and Drought.

Biotic and abiotic stresses alter the physiology of perennial plants, with consequences for fungal endophytes and disease expression. In grapevine, drought inhibits esca disease expression, but the underlying molecular interactions between the plant and fungi are unknown. We combined wood metatranscriptomics, metabolomics, and metabarcoding to investigate these interactions in 30-year-old grapevines and eight wood-pathogenic fungi under conditions of drought or esca leaf symptom expression. Both esca and drought decreased grapevine transpiration, but with different underlying mechanisms that induced specific transcriptomic and metabolic signatures. Similar pathways were also activated, including the phenylpropanoid and stilbenoid synthesis pathways. These stress responses could potentially confer cross-tolerance and elicit different fungal molecular responses. Across all fungi, the total level of putative virulence factors increased significantly under both stresses. Under drought, only the relative abundance of Phaeomoniella chlamydospora and gene expression involved in anti-oxidative mechanisms, growth, and reproduction increased. Under esca expression conditions, only the relative abundance of Fomitiporia mediterranea and gene expression involved in wood degradation, competition, detoxification, and growth increased. Under drought, induced grapevine defenses and reduced transpiration, together with the low abundance and putatively weak virulence of F. mediterranea may account for the inhibition of esca leaf symptom.