Nodulation Induces Systemic Resistance of Medicago truncatula and Pisum sativum Against Erysiphe pisi and Primes for Powdery Mildew-Triggered Salicylic Acid Accumulation.

Plants encounter beneficial and detrimental microorganisms both above- and belowground and the health status of the plant depends on the composition of this pan-microbiome. Beneficial microorganisms contribute to plant nutrition or systemically or locally protect plants against pathogens, thus facilitating adaptation to a variety of environments. Induced systemic resistance, caused by root-associated microbes, manifests as aboveground resistance against necrotrophic pathogens and is mediated by jasmonic acid/ethylene-dependent signaling. By contrast, systemic acquired resistance relies on salicylic acid (SA) signaling and confers resistance against secondary infection by (hemi)biotrophic pathogens. To investigate whether symbiotic rhizobia that are ubiquitously found in natural ecosystems are able to modulate resistance against biotrophs, we tested the impact of preestablished nodulation of Medicago truncatula and pea (Pisum sativum) plants against infection by the powdery mildew fungus Erysiphe pisi. We found that root symbiosis interfered with fungal penetration of M. truncatula and reduced asexual spore formation on pea leaves independently of symbiotic nitrogen fixation. Improved resistance of nodulated plants correlated with elevated levels of free SA and SA-dependent marker gene expression upon powdery mildew infection. Our results suggest that nodulation primes the plants systemically for E. pisi-triggered SA accumulation and defense gene expression, resulting in increased resistance.