{"title":"植物黄萎病毒力的DNA甲基化表观遗传调控。","authors":"Yun-Ya Chen, Chen Zhu, Jian-Hua Zhao, Ting Liu, Feng Gao, Ying-Chao Zhang, Cheng-Guo Duan","doi":"10.1007/s42994-023-00117-5","DOIUrl":null,"url":null,"abstract":"<div><p>As a conserved epigenetic mark, DNA cytosine methylation, at the 5’ position (5-mC), plays important roles in multiple biological processes, including plant immunity. However, the involvement of DNA methylation in the determinants of virulence of phytopathogenic fungi remains elusive. In this study, we profiled the DNA methylation patterns of the phytopathogenic fungus <i>Verticillium dahliae</i>, one of the major causal pathogens of <i>Verticillium</i> wilt disease that causes great losses in many crops, and explored its contribution in fungal pathogenicity. We reveal that DNA methylation modification is present in <i>V. dahliae</i> and is required for its full virulence in host plants. The major enzymes responsible for the establishment of DNA methylation in <i>V. dahliae</i> were identified. We provided evidence that DNA methyltransferase-mediated establishment of DNA methylation pattern positively regulates fungal virulence, mainly through repressing a conserved protein kinase VdRim15-mediated Ca<sup>2+</sup> signaling and ROS production, which is essential for the penetration activity of <i>V. dahliae</i>. In addition, we further demonstrated that histone H3 lysine 9 trimethylation (H3K9me3), another heterochromatin marker that is closely associated with 5-mC in eukaryotes, also participates in the regulation of <i>V. dahliae</i> pathogenicity, through a similar mechanism. More importantly, DNA methyltransferase genes <i>VdRid</i>, <i>VdDnmt5,</i> as well as H3K9me3 methyltransferase genes, were greatly induced during the early infection phase, implying that a dynamic regulation of 5-mC and H3K9me3 homeostasis is required for an efficient infection. Collectively, our findings uncover an epigenetic mechanism in the regulation of phytopathogenic fungal virulence.</p></div>","PeriodicalId":53135,"journal":{"name":"aBIOTECH","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2023-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638132/pdf/","citationCount":"0","resultStr":"{\"title\":\"DNA methylation-dependent epigenetic regulation of Verticillium dahliae virulence in plants\",\"authors\":\"Yun-Ya Chen, Chen Zhu, Jian-Hua Zhao, Ting Liu, Feng Gao, Ying-Chao Zhang, Cheng-Guo Duan\",\"doi\":\"10.1007/s42994-023-00117-5\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><p>As a conserved epigenetic mark, DNA cytosine methylation, at the 5’ position (5-mC), plays important roles in multiple biological processes, including plant immunity. However, the involvement of DNA methylation in the determinants of virulence of phytopathogenic fungi remains elusive. In this study, we profiled the DNA methylation patterns of the phytopathogenic fungus <i>Verticillium dahliae</i>, one of the major causal pathogens of <i>Verticillium</i> wilt disease that causes great losses in many crops, and explored its contribution in fungal pathogenicity. We reveal that DNA methylation modification is present in <i>V. dahliae</i> and is required for its full virulence in host plants. The major enzymes responsible for the establishment of DNA methylation in <i>V. dahliae</i> were identified. We provided evidence that DNA methyltransferase-mediated establishment of DNA methylation pattern positively regulates fungal virulence, mainly through repressing a conserved protein kinase VdRim15-mediated Ca<sup>2+</sup> signaling and ROS production, which is essential for the penetration activity of <i>V. dahliae</i>. In addition, we further demonstrated that histone H3 lysine 9 trimethylation (H3K9me3), another heterochromatin marker that is closely associated with 5-mC in eukaryotes, also participates in the regulation of <i>V. dahliae</i> pathogenicity, through a similar mechanism. More importantly, DNA methyltransferase genes <i>VdRid</i>, <i>VdDnmt5,</i> as well as H3K9me3 methyltransferase genes, were greatly induced during the early infection phase, implying that a dynamic regulation of 5-mC and H3K9me3 homeostasis is required for an efficient infection. Collectively, our findings uncover an epigenetic mechanism in the regulation of phytopathogenic fungal virulence.</p></div>\",\"PeriodicalId\":53135,\"journal\":{\"name\":\"aBIOTECH\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":4.6000,\"publicationDate\":\"2023-09-20\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638132/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"aBIOTECH\",\"FirstCategoryId\":\"1091\",\"ListUrlMain\":\"https://link.springer.com/article/10.1007/s42994-023-00117-5\",\"RegionNum\":4,\"RegionCategory\":\"农林科学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"aBIOTECH","FirstCategoryId":"1091","ListUrlMain":"https://link.springer.com/article/10.1007/s42994-023-00117-5","RegionNum":4,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
DNA methylation-dependent epigenetic regulation of Verticillium dahliae virulence in plants
As a conserved epigenetic mark, DNA cytosine methylation, at the 5’ position (5-mC), plays important roles in multiple biological processes, including plant immunity. However, the involvement of DNA methylation in the determinants of virulence of phytopathogenic fungi remains elusive. In this study, we profiled the DNA methylation patterns of the phytopathogenic fungus Verticillium dahliae, one of the major causal pathogens of Verticillium wilt disease that causes great losses in many crops, and explored its contribution in fungal pathogenicity. We reveal that DNA methylation modification is present in V. dahliae and is required for its full virulence in host plants. The major enzymes responsible for the establishment of DNA methylation in V. dahliae were identified. We provided evidence that DNA methyltransferase-mediated establishment of DNA methylation pattern positively regulates fungal virulence, mainly through repressing a conserved protein kinase VdRim15-mediated Ca2+ signaling and ROS production, which is essential for the penetration activity of V. dahliae. In addition, we further demonstrated that histone H3 lysine 9 trimethylation (H3K9me3), another heterochromatin marker that is closely associated with 5-mC in eukaryotes, also participates in the regulation of V. dahliae pathogenicity, through a similar mechanism. More importantly, DNA methyltransferase genes VdRid, VdDnmt5, as well as H3K9me3 methyltransferase genes, were greatly induced during the early infection phase, implying that a dynamic regulation of 5-mC and H3K9me3 homeostasis is required for an efficient infection. Collectively, our findings uncover an epigenetic mechanism in the regulation of phytopathogenic fungal virulence.