A simplified synthetic rhizosphere bacterial community steers plant oxylipin pathways for preventing foliar phytopathogens

Rhizosphere-enriched microbes induced by foliar phytopathogen infection can be assembled into a functional community to enhance plant defense mechanisms. However, the functions of stably-colonizing rhizosphere microbiota are rarely investigated. In this study, Botrytis cinerea infection changed rhizosphere bacterial communities in tomato plants. The phytopathogen-infected plants recruited specific rhizosphere bacterial taxa, while several bacterial taxa stably colonized the rhizosphere, regardless of phytopathogen infection. Through the analysis of the rhizosphere bacterial community, we established a synthetic community harboring 8 phytopathogen-inducible and 30 stably-colonizing bacteria species. Furthermore, the 38-species community was simplified into a three-species community, consisting of one phytopathogen-inducible (Asticcacaulis sp.) and two stably-colonizing species (Arachidicoccus sp. And Phenylobacterium sp.). The simplified community provided a durable protection for the host plants by synergistic effects, with the phytopathogen-inducible species triggering plant defense responses and the stably-colonizing species promoting biofilm formation. The simplified community exhibited similar protective effects as the 38-species community. Moreover, the activation of oxylipin pathways in the phytopathogen-infected leaves was significantly intensified by the simplified community. However, the inhibited biosynthesis of antimicrobial divinyl ethers, including colneleic and colnelenic acid, fully abolished the community-induced plant disease resistance. In contrast, transgenic plants overexpressing SlLOX5 and SlDES1, with higher levels of divinyl ethers, displayed stronger resistance against B. cinerea compared to wild-type plants. Collectively, these findings provided insights into the utilization of the simplified community for preventing gray mold disease.