Da Guo, Jingrui Li, Peng Liu, Yuzhan Wang, Na Cao, Xiangling Fang, Tao Wang, Jiangli Dong
{"title":"The jasmonate pathway promotes nodule symbiosis and suppresses host plant defense in Medicago truncatula.","authors":"Da Guo, Jingrui Li, Peng Liu, Yuzhan Wang, Na Cao, Xiangling Fang, Tao Wang, Jiangli Dong","doi":"10.1016/j.molp.2024.06.004","DOIUrl":null,"url":null,"abstract":"<p><p>Root nodule symbiosis (RNS) between legumes 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 (JA) in the immune response has been extensively studied. Current research shows that JA can play either a positive or negative regulatory role in RNS depending on its concentration, but the molecular mechanisms remain to be elucidated. In this study, we found that inoculation with the rhizobia Sm1021 induces the JA pathway in Medicago truncatula, and blocking the JA pathway significantly reduces the number of infection threads. Mutations in the MtMYC2 gene, which encodes a JA signaling master transcription factor, significantly inhibited rhizobia infection, terminal differentiation, and symbiotic cell formation. Combining RNA sequencing and chromatin immunoprecipitation sequencing, we discovered that MtMYC2 regulates the expression of nodule-specific MtDNF2, MtNAD1, and MtSymCRK to suppress host defense, while it activates MtDNF1 expression to regulate the maturation of MtNCRs, which in turn promotes bacteroid formation. More importantly, MtMYC2 participates in symbiotic signal transduction by promoting the expression of MtIPD3. Notably, the MtMYC2-MtIPD3 transcriptional regulatory module is specifically present in legumes, and the Mtmyc2 mutants are susceptible to the infection by the pathogen Rhizoctonia solani. Collectively, these findings reveal the molecular mechanisms of how the JA pathway regulates RNS, broadening our understanding of the roles of JA in plant-microbe interactions.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":null,"pages":null},"PeriodicalIF":17.1000,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Plant","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.molp.2024.06.004","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/6/9 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Root nodule symbiosis (RNS) between legumes 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 (JA) in the immune response has been extensively studied. Current research shows that JA can play either a positive or negative regulatory role in RNS depending on its concentration, but the molecular mechanisms remain to be elucidated. In this study, we found that inoculation with the rhizobia Sm1021 induces the JA pathway in Medicago truncatula, and blocking the JA pathway significantly reduces the number of infection threads. Mutations in the MtMYC2 gene, which encodes a JA signaling master transcription factor, significantly inhibited rhizobia infection, terminal differentiation, and symbiotic cell formation. Combining RNA sequencing and chromatin immunoprecipitation sequencing, we discovered that MtMYC2 regulates the expression of nodule-specific MtDNF2, MtNAD1, and MtSymCRK to suppress host defense, while it activates MtDNF1 expression to regulate the maturation of MtNCRs, which in turn promotes bacteroid formation. More importantly, MtMYC2 participates in symbiotic signal transduction by promoting the expression of MtIPD3. Notably, the MtMYC2-MtIPD3 transcriptional regulatory module is specifically present in legumes, and the Mtmyc2 mutants are susceptible to the infection by the pathogen Rhizoctonia solani. Collectively, these findings reveal the molecular mechanisms of how the JA pathway regulates RNS, broadening our understanding of the roles of JA in plant-microbe interactions.
豆科植物与根瘤菌之间的根瘤共生(RNS)是农业系统中氮的主要来源。有效的共生需要精确调节植物的防御反应。防御激素茉莉酸在免疫反应中的作用已被广泛研究。目前的研究表明,茉莉酸可根据浓度的不同在 RNS 中发挥积极或消极的调控作用,但其分子机制仍有待阐明。在此,我们发现接种根瘤菌 Sm1021 会诱导美智子(Medicago truncatula)的 JA 通路反应,阻断 JA 通路会显著减少感染丝的数量。JA信号转导主转录因子MtMYC2基因的突变明显抑制了根瘤菌的感染、末端分化和共生细胞的形成。结合RNA-seq和ChIP-seq,我们发现MtMYC2可调控结核特异性MtDNF2、MtNAD1和MtSymCRK的表达,从而抑制宿主防御。MtMYC2激活MtDNF1的表达,从而调节MtNCR的成熟,进而促进类菌体的形成。更重要的是,MtMYC2 能促进 MtIPD3 的表达,从而参与共生信号转导。值得注意的是,MtMYC2-MtIPD3 转录调控模块专门存在于豆科植物中。此外,Mtmyc2突变体对根瘤菌表现出易感表型。总之,我们的研究结果揭示了 JA 通路在 RNS 中的分子机制,进一步拓宽了人们对 JA 在植物与微生物相互作用网络中的认识。
期刊介绍:
Molecular Plant is dedicated to serving the plant science community by publishing novel and exciting findings with high significance in plant biology. The journal focuses broadly on cellular biology, physiology, biochemistry, molecular biology, genetics, development, plant-microbe interaction, genomics, bioinformatics, and molecular evolution.
Molecular Plant publishes original research articles, reviews, Correspondence, and Spotlights on the most important developments in plant biology.