The jasmonate pathway promotes nodule symbiosis and suppresses host plant defense in Medicago truncatula

Root nodule symbiosis (RNS) between legume and rhizobia is a major source of nitrogen in agricultural systems. Effective symbiosis requires precise regulation of plant defense responses. The role of the defense hormone jasmonic acid in the immune response has been extensively studied. The current research shows that JA can play either a positive or negative regulatory role in RNS depending on its concentration, while the molecular mechanisms remain to be elucidated. Here, we found that inoculation with rhizobia Sm1021 induced the JA pathway response in Medicago truncatula, and blocking JA pathway significantly reduced the number of Infection threads. Mutations in the MtMYC2 gene, a JA signaling master transcription factor, significantly inhibited rhizobia Infection, terminal differentiation, and symbiotic cell formation. Combining RNA-seq and ChIP-seq, we discovered that MtMYC2 regulates the expression of nodule-specific MtDNF2, MtNAD1, and MtSymCRK to suppress host defense. MtMYC2 activates MtDNF1 expression to regulate the maturation of MtNCRs, which in turn promotes bacteroid formation. More importantly, MtMYC2 promotes the expression of MtIPD3 to participate in symbiotic signaling transduction. Notably, the MtMYC2-MtIPD3 transcriptional regulation module is specifically present in legumes. Additionally, The Mtmyc2 mutants exhibits a susceptible phenotype to Rhizoctonia solani. Collectively, our findings reveal the molecular mechanisms of the JA pathway in RNS and further broaden the understanding of JA in the plant-microbe interaction network.

Jasmonic acid; MYC2; Medicago truncatula; defense; symbiosis.