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.
The rhizosphere microbiome of plants is essential for plant growth and health. Recent studies have shown that upon infection of leaves with a foliar pathogen, the composition of the root microbiome is altered and enriched with bacteria that in turn can systemically protect the plant against the foliar pathogen. This protective effect is extended to successive populations of plants that are grown on soil that was first conditioned by pathogen-infected plants, a phenomenon that was coined "the soil-borne legacy." Here we provide a detailed protocol for soil-borne legacy experiments with the model plant Arabidopsis thaliana after infection with the obligate biotrophic pathogen Hyaloperonospora arabidopsidis. This protocol can easily be extended to infection with other pathogens or even infestation with herbivorous insects and can function as a blueprint for soil-borne legacy experiments with crop species.
Root-associated microbiota can protect plants against severe disease outbreaks. In the model-plant Arabidopsis thaliana, leaf infection with the obligate downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) results in a shift in the root exudation profile, therewith promoting the growth of a selective root microbiome that induces a systemic resistance against Hpa in the above-ground plant parts. Here we show that, additionally, a conserved subcommunity of the recruited soil microbiota becomes part of a pathogen-associated microbiome in the phyllosphere that is vertically transmitted with the spores of the pathogen to consecutively infected host plants. This subcommunity of Hpa-associated microbiota (HAM) limits pathogen infection and is therefore coined a resistobiome. The HAM resistobiome consists of a small number of bacterial species and was first found in our routinely maintained laboratory cultures of independent Hpa strains. When co-inoculated with Hpa spores, the HAM rapidly dominates the phyllosphere of infected plants, negatively impacting Hpa spore formation. Remarkably, isogenic bacterial isolates of the abundantly-present HAM species were also found in strictly separated Hpa cultures across Europe, and even in early published genomes of this obligate biotroph. Our results highlight that pathogen-infected plants can recruit protective microbiota via their roots to the shoots where they become part of a pathogen-associated resistobiome that helps the plant to fight pathogen infection. Understanding the mechanisms by which pathogen-associated resistobiomes are formed will enable the development of microbiome-assisted crop varieties that rely less on chemical crop protection.
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