Feiyang Xue, Jie Zhang, Di Wu, Shiyu Sun, Ming Fu, Jie Wang, Iain Searle, Hongbo Gao, Wanqi Liang
{"title":"在水稻减数分裂过程中,m6A 去甲基化酶 OsALKBH5 通过影响 mRNA 的稳定性来促进双链断裂的形成和修复。","authors":"Feiyang Xue, Jie Zhang, Di Wu, Shiyu Sun, Ming Fu, Jie Wang, Iain Searle, Hongbo Gao, Wanqi Liang","doi":"10.1111/nph.19976","DOIUrl":null,"url":null,"abstract":"<p><p>N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) RNA modification is the most prevalent messenger RNA (mRNA) modification in eukaryotes and plays critical roles in the regulation of gene expression. m<sup>6</sup>A is a reversible RNA modification that is deposited by methyltransferases (writers) and removed by demethylases (erasers). The function of m<sup>6</sup>A erasers in plants is highly diversified and their roles in cereal crops, especially in reproductive development essential for crop yield, are largely unknown. Here, we demonstrate that rice OsALKBH5 acts as an m<sup>6</sup>A demethylase required for the normal progression of male meiosis. OsALKBH5 is a nucleo-cytoplasmic protein, highly enriched in rice anthers during meiosis, that associates with P-bodies and exon junction complexes, suggesting that it is involved in regulating mRNA processing and abundance. Mutations of OsALKBH5 cause reduced double-strand break (DSB) formation, severe defects in DSB repair, and delayed meiotic progression, leading to complete male sterility. Transcriptome analysis and m<sup>6</sup>A profiling indicate that OsALKBH5-mediated m<sup>6</sup>A demethylation stabilizes the mRNA level of multiple meiotic genes directly or indirectly, including several genes that regulate DSB formation and repair. Our study reveals the indispensable role of m<sup>6</sup>A metabolism in post-transcriptional regulation of meiotic progression in rice.</p>","PeriodicalId":48887,"journal":{"name":"New Phytologist","volume":null,"pages":null},"PeriodicalIF":9.4000,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"m<sup>6</sup>A demethylase OsALKBH5 is required for double-strand break formation and repair by affecting mRNA stability in rice meiosis.\",\"authors\":\"Feiyang Xue, Jie Zhang, Di Wu, Shiyu Sun, Ming Fu, Jie Wang, Iain Searle, Hongbo Gao, Wanqi Liang\",\"doi\":\"10.1111/nph.19976\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) RNA modification is the most prevalent messenger RNA (mRNA) modification in eukaryotes and plays critical roles in the regulation of gene expression. m<sup>6</sup>A is a reversible RNA modification that is deposited by methyltransferases (writers) and removed by demethylases (erasers). The function of m<sup>6</sup>A erasers in plants is highly diversified and their roles in cereal crops, especially in reproductive development essential for crop yield, are largely unknown. Here, we demonstrate that rice OsALKBH5 acts as an m<sup>6</sup>A demethylase required for the normal progression of male meiosis. OsALKBH5 is a nucleo-cytoplasmic protein, highly enriched in rice anthers during meiosis, that associates with P-bodies and exon junction complexes, suggesting that it is involved in regulating mRNA processing and abundance. Mutations of OsALKBH5 cause reduced double-strand break (DSB) formation, severe defects in DSB repair, and delayed meiotic progression, leading to complete male sterility. Transcriptome analysis and m<sup>6</sup>A profiling indicate that OsALKBH5-mediated m<sup>6</sup>A demethylation stabilizes the mRNA level of multiple meiotic genes directly or indirectly, including several genes that regulate DSB formation and repair. Our study reveals the indispensable role of m<sup>6</sup>A metabolism in post-transcriptional regulation of meiotic progression in rice.</p>\",\"PeriodicalId\":48887,\"journal\":{\"name\":\"New Phytologist\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":9.4000,\"publicationDate\":\"2024-07-24\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"New Phytologist\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1111/nph.19976\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"Agricultural and Biological Sciences\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/nph.19976","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
m6A demethylase OsALKBH5 is required for double-strand break formation and repair by affecting mRNA stability in rice meiosis.
N6-methyladenosine (m6A) RNA modification is the most prevalent messenger RNA (mRNA) modification in eukaryotes and plays critical roles in the regulation of gene expression. m6A is a reversible RNA modification that is deposited by methyltransferases (writers) and removed by demethylases (erasers). The function of m6A erasers in plants is highly diversified and their roles in cereal crops, especially in reproductive development essential for crop yield, are largely unknown. Here, we demonstrate that rice OsALKBH5 acts as an m6A demethylase required for the normal progression of male meiosis. OsALKBH5 is a nucleo-cytoplasmic protein, highly enriched in rice anthers during meiosis, that associates with P-bodies and exon junction complexes, suggesting that it is involved in regulating mRNA processing and abundance. Mutations of OsALKBH5 cause reduced double-strand break (DSB) formation, severe defects in DSB repair, and delayed meiotic progression, leading to complete male sterility. Transcriptome analysis and m6A profiling indicate that OsALKBH5-mediated m6A demethylation stabilizes the mRNA level of multiple meiotic genes directly or indirectly, including several genes that regulate DSB formation and repair. Our study reveals the indispensable role of m6A metabolism in post-transcriptional regulation of meiotic progression in rice.
期刊介绍:
New Phytologist is a leading publication that showcases exceptional and groundbreaking research in plant science and its practical applications. With a focus on five distinct sections - Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology - the journal covers a wide array of topics ranging from cellular processes to the impact of global environmental changes. We encourage the use of interdisciplinary approaches, and our content is structured to reflect this. Our journal acknowledges the diverse techniques employed in plant science, including molecular and cell biology, functional genomics, modeling, and system-based approaches, across various subfields.