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

Abstract

Plants deposit photosynthetically-fixed carbon in the rhizosphere, the thin soil layer directly around the root, thereby creating a hospitable environment for microbes. To manage the inhabitants of this nutrient-rich environment, plant roots exude and dynamically adjust microbe-attracting and -repelling compounds to stimulate specific members of the microbiome. 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 foliar downy mildew infection in a subsequent population of plants, a phenomenon dubbed the soil-borne legacy (SBL). Here, we show that for the creation of the SBL, plant-produced coumarins play a prominent role as coumarin-deficient myb72 and f6’h1 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. Our data further show that the Hpa-induced SBL primes Col-0 plants growing in SBL-conditioned soil for salicylic acid (SA)-dependent defenses. The SA-signaling mutants sid2 and npr1 were unresponsive to the Hpa-induced SBL, suggesting that the protective effect of the Hpa-induced shift in the root microbiome results from an induced systemic resistance that requires SA-signaling in the plant.

Convergent and divergent responses of the rhizosphere chemistry and bacterial communities to a stress gradient in the Atacama Desert

“…succinic acid), including ursolic acid, were previously linked to soil quality and salt stress mitigation (19,62). Terpenes, flavonoids, coumarins and cinnamic acids were highlighted in both vegetation belts, in agreement with their functions at the plant-microbe interface (8,63). Additional markers, such as lipids, were mainly observed in the rhizosphere of J. frigida .…”

Congruent downy mildew-associated microbiomes reduce plant disease and function as transferable resistobiomes

“…The mechanism by which this HAM either directly or indirectly protects against Hpa should be further investigated. However, we previously found that mutant plants impaired in defense signaling that involves the plant hormone salicylic acid, are not protected by a Hpa -induced SBL, suggesting the SBL and associated HAMs work at least partly through activation of salicylic acid-dependent immunity 38 .…”

“…The creation of a SBL requires successful infection with the pathogen, as resistant plants that prevent Hpa -infection did not lead to a SBL. Moreover, we previously reported that foliar Hpa infection changes the root exudation profile, and that mutant plants impaired in the biosynthesis of root-secreted coumarins are not able to create a SBL even though they are just as susceptible as the wild type 38 . This indicates that it is the plant that actively assembles its resistobiome in response to attack.…”

“…Phyllosphere HAM resistobiome is recruited from the rhizosphere Previously, we demonstrated that conditioning of soil by Hpa-infected Arabidopsis makes the next planting growing on that soil more resistant to Hpa 13 . This phenomenon is called a soil-borne legacy (SBL) 18 and is associated with a shift in the rhizosphere microbiome that mediates an induced systemic resistance against Hpa in a next population of plants 13,38 . Interestingly, a number of the ASVs that became enriched in the rhizosphere upon foliar Hpa infection 13 are also found in the phyllosphere HAM resistobiome in the present study.…”

Exploring the connectivity between rhizosphere microbiomes and the plant genes: A way forward for sustainable increase in primary productivity

“…This process ensures a higher availability of iron in the soil and provides increased protection against pathogens. Notably, a recent study demonstrated the importance of the coumarin biosynthesis genes MYB72 and F6′H1 in the development of a microbial soil-borne legacy following foliar pathogen infection (Vismans et al, 2022). This soil-borne legacy, in turn, recruits a microbiome that induces disease resistance and primes salicylic acid-dependent defence mechanisms in plants.…”