Coumarin biosynthesis genes are required after foliar pathogen infection for the creation of a microbial soil-borne legacy that primes plants for SA-dependent defenses

Plants shape the composition of the rhizosphere microbiome by the dynamic exudation of microbe-attracting and -repelling compounds to stimulate specific microbiome functions. Previously, we demonstrated that foliar infection of Arabidopsis thaliana by the biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) leads to a disease-induced modification of the rhizosphere microbiome. Soil conditioned with Hpa-infected plants provided enhanced protection against Hpa in a subsequent population of plants, a phenomenon dubbed the soil-borne legacy (SBL). We investigated Hpa-induced changes in root exudation and microbiome composition. We show that coumarin-deficient myb72 and f6h1 mutants were defective in creating a Hpa-induced SBL. Root exudation profiles changed significantly in Col-0 upon foliar Hpa infection, and this was accompanied by a compositional shift in the root microbiome that was significantly different from microbial shifts occurring on roots of Hpa-infected coumarin-deficient mutants. In addition, Hpa-induced SBL primes Col-0 plants growing in SBL-conditioned soil for salicylic acid (SA)-dependent defenses whereas the SA-signaling mutants sid2 and npr1 were unresponsive to the Hpa-induced SBL. In conclusion, plant-produced coumarins are important for the creation of a SBL. Moreover, the Hpa-induced shift in the root microbiome results in an induced systemic resistance that requires SA-signaling in the plant.