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, one of the world’s most valuable crops, drought inhibits esca disease expression, but the underlying molecular interactions between 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 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. The levels of putative fungal 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.

The grapevine defense mechanisms induced by drought coupled with a low transpiration rate and a low abundance and virulence of F. mediterranea may account for esca leaf symptom inhibition upon water deficit.