The dynamic arms race during the early invasion of woodland strawberry by Botrytis cinerea revealed by dual dense high-resolution RNA-seq analyses

Abstract

Abstract Necrotrophic pathogens replicate massively upon colonizing plants, causing large-scale wilting and death of plant tissues. Understanding both mechanisms of pathogen invasion and host response processes prior to symptom appearance and their key regulatory networks is therefore important for defense against pathogen attack. Here, we investigated the mechanisms of interaction between woodland strawberry (Fragaria vesca) leaves and gray mold pathogen (Botrytis cinerea) at 14 infection time points during the first 12 hours of the infection period using a dense, high-resolution time series dual transcriptomic analysis, characterizing the arms race between strawberry F. vesca and B. cinerea before the appearance of localized lesions. Strawberry leaves rapidly initiated strong systemic defenses at the first sign of external stimulation and showed lower levels of transcriptomic change later in the infection process. Unlike the host plants, B. cinerea showed larger-scale transcriptomic changes that persisted throughout the infection process. Weighted gene co-expression network analysis identified highly correlated genes in 32 gene expression modules between B. cinerea and strawberry. Yeast two-hybrid and bimolecular fluorescence complementation assays revealed that the disease response protein FvRLP2 from woodland strawberry interacted with the cell death inducing proteins BcXYG1 and BcPG3 from B. cinerea. Overexpression of FvRLP2 in both strawberry and Arabidopsis inhibited B. cinerea infection, confirming these genes’ respective functions. These findings shed light on the arms race process by which B. cinerea invades host plants and strawberry to defend against pathogen infection.