Xiang Lu, Yao He, Jin-Qiao Guo, Yue Wang, Qian Yan, Qing Xiong, Hui Shi, Qingqing Hou, Junjie Yin, Yi-Bang An, Yi-Di Chen, Cheng-Shuang Yang, Ye Mao, Xiaobo Zhu, Yongyan Tang, Jiali Liu, Yu Bi, Li Song, Long Wang, Yihua Yang, Min He, Weitao Li, Xuewei Chen, Jing Wang
{"title":"表转录组的动态变化揭示了水稻在病原体感染期间由ac4C引导的翻译重编程过程","authors":"Xiang Lu, Yao He, Jin-Qiao Guo, Yue Wang, Qian Yan, Qing Xiong, Hui Shi, Qingqing Hou, Junjie Yin, Yi-Bang An, Yi-Di Chen, Cheng-Shuang Yang, Ye Mao, Xiaobo Zhu, Yongyan Tang, Jiali Liu, Yu Bi, Li Song, Long Wang, Yihua Yang, Min He, Weitao Li, Xuewei Chen, Jing Wang","doi":"10.1038/s41477-024-01800-1","DOIUrl":null,"url":null,"abstract":"Messenger RNA modifications play pivotal roles in RNA biology, but comprehensive landscape changes of epitranscriptomes remain largely unknown in plant immune response. Here we report translational reprogramming directed by ac4C mRNA modification upon pathogen challenge. We first investigate the dynamics of translatomes and epitranscriptomes and uncover that the change in ac4C at single-base resolution promotes translational reprogramming upon Magnaporthe oryzae infection. Then by characterizing the specific distributions of m1A, 2’O-Nm, ac4C, m5C, m6A and m7G, we find that ac4Cs, unlike other modifications, are enriched at the 3rd position of codons, which stabilizes the Watson–Crick base pairing. Importantly, we demonstrate that upon pathogen infection, the increased expression of the ac4C writer OsNAT10/OsACYR (N-ACETYLTRANSFERASE FOR CYTIDINE IN RNA) promotes translation to facilitate rapid activation of immune responses, including the enhancement of jasmonic acid biosynthesis. Our study provides an atlas of mRNA modifications and insights into ac4C function in plant immunity. By characterizing the dynamics of epitranscriptomes and translatomes upon Magnaporthe oryzae infection, the authors uncover that ac4C enriched in the 3rd nt of codons improves translation of mRNA to enhance rice resistance against M. oryzae.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8000,"publicationDate":"2024-09-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Dynamics of epitranscriptomes uncover translational reprogramming directed by ac4C in rice during pathogen infection\",\"authors\":\"Xiang Lu, Yao He, Jin-Qiao Guo, Yue Wang, Qian Yan, Qing Xiong, Hui Shi, Qingqing Hou, Junjie Yin, Yi-Bang An, Yi-Di Chen, Cheng-Shuang Yang, Ye Mao, Xiaobo Zhu, Yongyan Tang, Jiali Liu, Yu Bi, Li Song, Long Wang, Yihua Yang, Min He, Weitao Li, Xuewei Chen, Jing Wang\",\"doi\":\"10.1038/s41477-024-01800-1\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Messenger RNA modifications play pivotal roles in RNA biology, but comprehensive landscape changes of epitranscriptomes remain largely unknown in plant immune response. Here we report translational reprogramming directed by ac4C mRNA modification upon pathogen challenge. We first investigate the dynamics of translatomes and epitranscriptomes and uncover that the change in ac4C at single-base resolution promotes translational reprogramming upon Magnaporthe oryzae infection. Then by characterizing the specific distributions of m1A, 2’O-Nm, ac4C, m5C, m6A and m7G, we find that ac4Cs, unlike other modifications, are enriched at the 3rd position of codons, which stabilizes the Watson–Crick base pairing. Importantly, we demonstrate that upon pathogen infection, the increased expression of the ac4C writer OsNAT10/OsACYR (N-ACETYLTRANSFERASE FOR CYTIDINE IN RNA) promotes translation to facilitate rapid activation of immune responses, including the enhancement of jasmonic acid biosynthesis. Our study provides an atlas of mRNA modifications and insights into ac4C function in plant immunity. By characterizing the dynamics of epitranscriptomes and translatomes upon Magnaporthe oryzae infection, the authors uncover that ac4C enriched in the 3rd nt of codons improves translation of mRNA to enhance rice resistance against M. oryzae.\",\"PeriodicalId\":18904,\"journal\":{\"name\":\"Nature Plants\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":15.8000,\"publicationDate\":\"2024-09-24\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Nature Plants\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://www.nature.com/articles/s41477-024-01800-1\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"PLANT SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Nature Plants","FirstCategoryId":"99","ListUrlMain":"https://www.nature.com/articles/s41477-024-01800-1","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
Dynamics of epitranscriptomes uncover translational reprogramming directed by ac4C in rice during pathogen infection
Messenger RNA modifications play pivotal roles in RNA biology, but comprehensive landscape changes of epitranscriptomes remain largely unknown in plant immune response. Here we report translational reprogramming directed by ac4C mRNA modification upon pathogen challenge. We first investigate the dynamics of translatomes and epitranscriptomes and uncover that the change in ac4C at single-base resolution promotes translational reprogramming upon Magnaporthe oryzae infection. Then by characterizing the specific distributions of m1A, 2’O-Nm, ac4C, m5C, m6A and m7G, we find that ac4Cs, unlike other modifications, are enriched at the 3rd position of codons, which stabilizes the Watson–Crick base pairing. Importantly, we demonstrate that upon pathogen infection, the increased expression of the ac4C writer OsNAT10/OsACYR (N-ACETYLTRANSFERASE FOR CYTIDINE IN RNA) promotes translation to facilitate rapid activation of immune responses, including the enhancement of jasmonic acid biosynthesis. Our study provides an atlas of mRNA modifications and insights into ac4C function in plant immunity. By characterizing the dynamics of epitranscriptomes and translatomes upon Magnaporthe oryzae infection, the authors uncover that ac4C enriched in the 3rd nt of codons improves translation of mRNA to enhance rice resistance against M. oryzae.
期刊介绍:
Nature Plants is an online-only, monthly journal publishing the best research on plants — from their evolution, development, metabolism and environmental interactions to their societal significance.