Foliar infections by Botrytis cinerea modulate the tomato root volatilome and microbiome

The fungal pathogen Botrytis cinerea causes significant damage to aboveground plant parts, but its impact on root chemistry and microbiome composition is less understood. This study investigated how B. cinerea foliar infection influences the root volatilome and microbiome of two tomato genotypes: wild Solanum pimpinellifolium and domesticated Solanum lycopersicum var. Moneymaker. In the absence of infection, wild tomato roots emitted higher levels of monoterpenes such as α-pinene and terpinene compared to domesticated tomato roots. The fungal infection induced elevated levels of benzyl alcohol and benzofuran in the root headspace and/or rhizosphere of both genotypes, alongside genotype-specific changes. Multivariate analyses revealed that B. cinerea significantly altered bacterial and fungal community compositions in the rhizosphere and rhizoplane, with stronger bacterial community shifts in the rhizoplane. Taxa depletion and enrichment were observed, particularly among Proteobacteria and Ascomycota. Mantel tests showed significant correlations between rhizoplane bacterial community compositions and root-associated volatilome. Notably, enriched bacterial taxa such as Pelomonas and Comamonadaceae positively correlated with benzyl alcohol and benzofuran levels in the root volatilome. These findings demonstrate that B. cinerea foliar infection might induce profound changes in root-associated volatilome and microbiome composition, highlighting its systemic effects on plant root chemistry and microbiome composition.