Hydroxylated monoterpenes mimic bacterial attack to trigger jasmonate-dependent self-amplifying immunity in tomato

Abstract

Hydroxylated monoterpenes (HMTPs) are emitted during resistant tomato-Pseudomonas syringae interactions and confer antibacterial resistance, yet their integration into immune signalling remains poorly understood. Here we show that HMTPs act as endogenous mimics of pathogen attack that engage canonical defence pathways in tomato. Using -terpineol as a representative HMTP, we demonstrate that this volatile activates MPK kinase-, calcium- and reactive oxygen species (ROS)-dependent signalling, promotes jasmonate and salicylic acid accumulation, and induces pathogen-like stomatal immunity independently of abscisic acid. Functional analyses revealed that HMTPs biosynthesis depends on ROS and jasmonate signalling, and HMTPs further promote their own accumulation, establishing a self-reinforcing feed-forward mechanism. Moreover, in vitro oxidative conditions drive chemical remodelling and selective interconversion among HMTPs, contributing to volatile diversification and favouring the accumulation of highly bioactive hydroxylated forms. Consistently, deuterium-labelled linalool is incorporated into plant metabolism and converted into deuterated -terpineol in planta, providing direct evidence for volatile interconversion. Together, our findings establish HMTPs as dynamic amplifiers of tomato antibacterial immunity and key actors in pathogen-associated signalling.