JA-dependent ROS modulation by acetoin-rich volatiles from amyloliquefaciens FZB42 triggers stomatal closure and enhances abiotic stress tolerance in Arabidopsis

Abstract

Microbial volatile organic compounds (VOCs) are key mediators of plant stress resilience. However, the redox-mediated mechanisms by which VOCs from beneficial bacteria remotely orchestrate aerial plant defenses remain elusive. Here, we demonstrate that VOCs from Bacillus amyloliquefaciens FZB42 reprogram Arabidopsis thaliana redox homeostasis, inducing a primed state that confers broad-spectrum tolerance to subsequent abiotic stresses. This pre-adaptive response is characterized by a dual-phase modulation of reactive oxygen species (ROS): enhancing H₂O₂ levels and inducing stomatal closure under normal conditions, while suppressing excessive ROS generation under drought. We identified acetoin as the key bioactive VOC, whose effect is abolished in bacterial mutants (ΔalsS, ΔalsD) and rescued by exogenous application. Genetic and transcriptomic evidence reveals that stomatal closure is mediated by a jasmonic acid (JA)–ROS signaling module and requires the ABA pathway component OST1. Moreover, these VOC-induced stomatal adjustments are associated with enhanced FZB42 rhizosphere colonization, which is linked to concurrent changes in root exudate profiles file. Our findings decode how rhizobacteria co-opt ROS signaling via volatiles to systemically prime plant defenses, offering a sustainable strategy for improving crop fitness through rhizosphere engineering.