Organic pollutant-induced long-distance ROS signaling drives plant systemic acquired acclimation via rhizomicrobiota

Plants can recruit beneficial rhizomicrobes to help themselves combat environmental stimuli. However, the upstream signaling through which plant senses local stress to initiate rhizomicrobial recruitment still remains unclear. This study elucidates the ubiquitous role of plant long-distance ROS signaling in driving the recruitment and colonization of beneficial rhizobacteria for the establishment of plant systemic acclimation upon local organic pollutant stress. Plant leaves sensed organic pollutants (e.g., herbicide, insecticide, fungicide, polycyclic aromatic hydrocarbon, and polychlorinated biphenyl) to generate reactive oxygen species (ROS), followed by the occurrence of a long-distance ROS wave from leaves to roots via Ca2+-RBOH-ROS signaling module. Elevated ROS in roots played dual functions. First, ROS stimulated the release of plant carbons, including primary and secondary metabolites, into rhizosphere by increasing the permeability of root cell membranes. The released carbon flux reshaped rhizosphere bacterial communities by enriching plant-beneficial bacterial genera (e.g., Lysobacter and Sphingomonas), which in turn promoted plant growth and pollutant degradation. Second, NO (nitric oxide) acted as downstream of ROS to loosen root cell wall, facilitating the colonization of rhizobacteria inside of plants. Our findings provide an answer to a pending question how plants deploy systemic signaling to ask for help from rhizomicrobes, which may extend our understanding for plant environmental adaptability.