Stress-dependent responses of grapevine wood and fungal pathogen activity under esca and drought

Biotic and abiotic stresses impact perennial plants, altering plant physiology with consequences on fungal endophytes and disease expression. In grapevine, one of the world’s most valuable crops, drought inhibits esca disease expression, but the underlying plant and fungi molecular interactions are unknown.

We integrated wood metatranscriptomics, metabolomics, and metabarcoding to investigate such interactions in 30 year-old grapevine and eight key wood pathogenic fungi under drought or esca leaf symptom expression.

While both esca and drought led to reduced grapevine transpiration, they involved distinct transcriptomic and metabolic signatures, including similar pathways activation such as phenylpropanoid and stilbenoid synthesis. Putative fungal virulence factors increased significantly under both stresses. Under drought, only Phaeomoniella chlamydospora relative abundance and gene expression, including anti-oxidative mechanisms, growth, and reproduction increased. Under esca expression, only Fomitiporia mediterranea relative abundance and gene expression increased, including wood degradation, competition, detoxification, and growth genes.

Drought and esca had distinct impacts on the transcriptome and metabolome of grapevine wood and overlapping metabolic pathways, which may confer cross-tolerance, eliciting different fungal molecular responses. Grapevine defense mechanisms induced by drought coupled to low transpiration rate, and low abundance and virulence of F. mediterranea, may be responsible for esca leaf symptom inhibition under water deficit.