Plant Physiol. 2023 Dec 07. pii: kiad654. [Epub ahead of print]
Chuanlin Shi,
Wenli Zou,
Yiwang Zhu,
Jie Zhang,
Chong Teng,
Hua Wei,
Huiying He,
Wenchuang He,
Xiangpei Liu,
Bin Zhang,
Hong Zhang,
Yue Leng,
Mingliang Guo,
Xianmeng Wang,
Wu Chen,
Zhipeng Zhang,
Hongge Qian,
Yan Cui,
Hongshuang Jiang,
Ying Chen,
Qili Fei,
Blake C Meyers,
Wanqi Liang,
Qian Qian,
Lianguang Shang.
Temperature-sensitive male sterility is one of the core components for hybrid rice (Oryza sativa) breeding based on the two-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 multi-omics analysis of small RNA, degradome, and transcriptome, we found that 21-nt phasiRNAs account for the greatest proportion of the 21-nt small RNA (sRNA) species in rice anthers and are sensitive to low temperature and markedly down-regulated 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 up-regulation 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 two-line hybrid rice breeding in the future.
Keywords: 21-nt phasiRNAs; AGO1d; degradome; male sterility; rice