Physiochemical interaction between osmotic stress and a bacterial exometabolite promotes plant disease

Various microbes isolated from healthy plants are detrimental under laboratory conditions, indicating the existence of molecular mechanisms preventing disease in nature. Here, we demonstrated that application of sodium chloride (NaCl) in natural and gnotobiotic soil systems is needed to induce plant disease caused by an otherwise non-pathogenic root-derived Pseudomonas brassicacearum isolate (R401). Disease caused by combinatorial treatment of NaCl and R401 triggered extensive, root-specific transcriptional reprogramming that did not involve down-regulation of host innate immune genes, nor dampening of ROS-mediated immunity. Instead, we identified and structurally characterized the R401 lipopeptide brassicapeptin A as necessary and sufficient to promote disease on salt-treated plants. Brassicapeptin A production transitions R401 from being beneficial to being detrimental on salt-treated plants by disturbing host ion homeostasis, thereby bolstering bacterial infection and susceptibility to osmolytes. We conclude that the interaction between a global change stressor and a bacterial exometabolite drives disease emergence in the plant microbiome. Root and shoot samples of Arabidopsis thaliana inoculated with heat-killed/alive Pseudomonas Root401 bacteria at NaCl concentration of 0mM/100mM