Transcriptomic and functional analyses reveal a complex unexplored landscape of Botrytis cinerea colonization in rose

Botrytis cinerea (Bc) is a notorious necrotrophic fungal pathogen that colonizes different plant tissues. Gray mold caused by Bc is a great threat to roses (Rosa spp.), some of the most important ornamental plants worldwide, but colonization strategies of Bc in rose tissues remain unexplored. Here, we report a comprehensive investigation of the mechanisms underlying Bc colonization in rose (Rosa hybrida cv. Carola) leaf and petal by integrated transcriptomic and functional analyses. Multiple genes involved in the biogenesis of the ribosome, an organelle for protein synthesis, were commonly up-regulated during Bc colonization in leaf and petal. Application of inhibitors targeting fungal ribosome biogenesis, coupled with gene disruption assays, demonstrated the contribution of ribosome biogenesis to Bc colonization in leaf and petal. Notably, genes associated with nitrogen transport, carbohydrate metabolism, and protein glycosylation contributed to Bc colonization, and some of them were tissue-specific virulence factors. Through in silico secretome analysis and functional verification, we identified seven novel plant cell death-inducing effectors and one of them contributed to Bc colonization in leaf and petal. This study reveals a complex unexplored landscape of Bc colonization in rose and also advances the understanding of plant-pathogen interactions.