mRNA cleavage by 21-nucleotide phasiRNAs determines temperature-sensitive male sterility in rice

文献类型： 外文期刊

第一作者： Shi, Chuanlin

作者： Shi, Chuanlin;Zou, Wenli;Zhu, Yiwang;Wei, Hua;He, Huiying;He, Wenchuang;Liu, Xiangpei;Zhang, Bin;Zhang, Hong;Leng, Yue;Guo, Mingliang;Wang, Xianmeng;Chen, Wu;Zhang, Zhipeng;Qian, Hongge;Cui, Yan;Jiang, Hongshuang;Chen, Ying;Fei, Qili;Qian, Qian;Shang, Lianguang;Zhang, Jie;Liang, Wanqi;Meyers, Blake C.;Meyers, Blake C.;Qian, Qian;Qian, Qian;Shang, Lianguang

作者机构：

期刊名称：PLANT PHYSIOLOGY （ 影响因子：7.4； 五年影响因子：8.7 ）

ISSN： 0032-0889

年卷期： 2024 年 194 卷 4 期

页码：

收录情况： SCI

摘要： Temperature-sensitive male sterility is one of the core components for hybrid rice (Oryza sativa) breeding based on the 2-line system. We previously found that knockout of ARGONAUTE 1d (AGO1d) causes temperature-sensitive male sterility in rice by influencing phased small interfering RNA (phasiRNA) biogenesis and function. However, the specific phasiRNAs and their targets underlying the temperature-sensitive male sterility in the ago1d mutant remain unknown. Here, we demonstrate that the ago1d mutant displays normal female fertility but complete male sterility at low temperature. Through a multiomics analysis of small RNA (sRNA), degradome, and transcriptome, we found that 21-nt phasiRNAs account for the greatest proportion of the 21-nt sRNA species in rice anthers and are sensitive to low temperature and markedly downregulated in the ago1d mutant. Moreover, we found that 21-nt phasiRNAs are essential for the mRNA cleavage of a set of fertility- and cold tolerance-associated genes, such as Earlier Degraded Tapetum 1 (EDT1), Tapetum Degeneration Retardation (TDR), OsPCF5, and OsTCP21, directly or indirectly determined by AGO1d-mediated gene silencing. The loss of function of 21-nt phasiRNAs can result in upregulation of their targets and causes varying degrees of defects in male fertility and grain setting. Our results highlight the essential functions of 21-nt phasiRNAs in temperature-sensitive male sterility in rice and suggest their promising application in 2-line hybrid rice breeding in the future. Multiomics analysis of small RNAs, degradome, and transcriptome reveals 21-nucleotide phasiRNAs are essential for mRNA cleavage of genes for fertility and cold tolerance to determine temperature-sensitive male sterility in rice.

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