m6A demethylase OsALKBH5 is required for double-strand break formation and repair by affecting mRNA stability in rice meiosis

IF 8.3 1区生物学 Q1 PLANT SCIENCES

New Phytologist Pub Date : 2024-07-24 DOI:10.1111/nph.19976

Feiyang Xue, Jie Zhang, Di Wu, Shiyu Sun, Ming Fu, Jie Wang, Iain Searle, Hongbo Gao, Wanqi Liang

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引用次数: 0

Abstract

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.

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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。

N6- 甲基腺苷（m6A）RNA 修饰是真核生物中最常见的信使 RNA（mRNA）修饰，在基因表达调控中起着至关重要的作用。m6A 是一种可逆的 RNA 修饰，它由甲基转移酶（写入器）沉积，并由去甲基化酶（去除器）去除。m6A 侵蚀者在植物中的功能非常多样化，它们在谷类作物中的作用，尤其是在对作物产量至关重要的生殖发育中的作用，在很大程度上还不为人所知。在这里，我们证明水稻 OsALKBH5 是雄性减数分裂正常进行所需的 m6A 去甲基化酶。OsALKBH5 是一种核-胞质蛋白，在水稻花药减数分裂过程中高度富集，与 P 体和外显子连接复合体结合，表明它参与调节 mRNA 的加工和丰度。OsALKBH5 基因突变会导致双链断裂（DSB）形成减少、DSB 修复严重缺陷和减数分裂进程延迟，从而导致完全雄性不育。转录组分析和 m6A 分析表明，OsALKBH5 介导的 m6A 去甲基化直接或间接地稳定了多个减数分裂基因的 mRNA 水平，其中包括几个调控 DSB 形成和修复的基因。我们的研究揭示了 m6A 代谢在水稻减数分裂过程的转录后调控中不可或缺的作用。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

New Phytologist 生物-植物科学

自引率

5.30%

发文量

728

期刊介绍： New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.