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

Abstract

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.

Systems Biology of Plant-Microbiome Interactions

“…Inoculation of barley with Pseudomonas spp., for example, increased crop resistance to the fungal pathogen Gaeumanomyces graminis, the causal agent of take-all disease (Fr€ ohlich et al, 2012). In Medicago truncatula, the AM fungus Rhizosphagus irregularis enhanced resistance to Xanthomonas campestris, and rhizobia increased resistance to Erysiphe pisi (Liu et al, 2007;Smigielski et al, 2019). In several cases, microbial mixtures have a more pronounced and consistent effect than inoculation with single strains.…”

Induced systemic resistance -like responses elicited by rhizobia

“…Many works provide data supporting the notion that inoculation of legumes with rhizobia results in the induction of an increased defense response effective against diverse pathogens (necrotrophs, biotrophs) and herbivores (Arfaoui et al 2005(Arfaoui et al , 2006(Arfaoui et al , 2007Chakraborty and Chakraborty 1989;Diaz-Valle et al 2019;Dutta et al 2008;Figueredo et al 2014Figueredo et al , 2017Kalantari et al 2018;Mabrouk et al 2007;Osdaghi et al 2011;Rabie 1998;Smigielski et al 2019) (Table 1). This effect was also observed in non legumes after rhizobial inoculation (Mishra et al 2006;Reitz et al 2000).…”

“…However, the role of JA as long distance signal of ISR and the importance of SA and JA -mediated signaling in rhizobium -legume symbiosis have not been demonstrated (Beardon et al 2014;Gutjahr and Paszkowski 2009). Interestingly, priming for SA accumulation and SA -mediated defense active against the powdery mildew fungi (biotroph) was observed in Medicago plants after rhizobial inoculation (Smigielski et al 2019). Moreover, even when suppression of SA -dependent defense responses seems to be widespread in rhizobial symbiosis, transcriptomic data indicates that peanut increase SA response during symbiosis development.…”

War and Peas: Molecular Bases of Resistance to Powdery Mildew in Pea (Pisum sativum L.) and Other Legumes

“…A later study performed on peas ( Pisum sativum ) and barrel medics ( Medicago truncatula Gaertn.) suggests that root symbiosis with rhizobia systemically primes plants for the salicylic-acid accumulation and defense-gene expression triggered by powdery mildew [ 90 ].…”