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

作者：Shi, Chuanlin; Zou, Wenli; Zhu, Yiwang; Zhang, Jie; Teng, Chong; 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; Meyers, Blake C.; Liang, Wanqi^*; Qian, Qian^*; Shang, Lianguang^*

来源：Plant Physiology, 2023.

DOI：10.1093/plphys/kiad654

• SMALL-INTERFERING RNAS
• REPRODUCTIVE DEVELOPMENT
• MALE-FERTILITY
• NONCODING RNA
• ANTHER
• ARGONAUTE
• ENCODES
• ROLES
• METABOLISM
• GENE

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.

• 单位
  上海交通大学