Volume 34, No 11, Nov 2024

ISSN: 1001-0602 
EISSN: 1748-7838 2018 
impact factor 17.848* 
(Clarivate Analytics, 2019)

Volume 34 Issue 11, November 2024: 763-775

ORIGINAL ARTICLES

Impaired 2′,3′-cyclic phosphate tRNA repair causes thermo-sensitive genic male sterility in rice

Bin Yan^1,† , Chunyan Liu^1,†,* , Jing Sun^1,2,3,† , Yang Mao^2,3,† , Can Zhou^1,4,† , Ji Li^1,4 , Wei Liu¹ , Shengdong Li^1,4 , Wei Yan⁵ , Chenjian Fu⁶ , Peng Qin⁶ , Xingxue Fu⁶ , Xinghui Zhao⁶ , Xianwei Song⁷ , Jiawei Nie^2,3,4 , Feng Gao^2,3 , Yuanzhu Yang^6,8,9,* , Yuhang Chen^2,3,4,* , Xiaofeng Cao^1,4,*

¹Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China
²Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Institute of Biotechnology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
³Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Institute of Biotechnology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China
⁴University of the Chinese Academy of Sciences, Beijing, China
⁵Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China
⁶Yuan Longping High-tech Agriculture Co., Ltd., Changsha, Hunan, China
⁷Key Laboratory of Seed Innovation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China
⁸State Key Laboratory of Hybrid Rice, Changsha, Hunan, China
⁹Key Laboratory of Rice Germplasm Enhancement in Southern China, Ministry of Agriculture and Rural Affairs, Changsha, Hunan, China
^†These authors contributed equally: Bin Yan, Chunyan Liu, Jing Sun, Yang Mao, Can Zhou
Correspondence: Chunyan Liu(cyliu@genetics.ac.cn)Yuanzhu Yang(yzhuyah@163.com)Yuhang Chen(yuhang.chen@genetics.ac.cn)Xiaofeng Cao(xfcao@geneitcs.ac.cn)

Hybrid rice, widely planted in Asia, is pathogen resistant and has superior yields, making it a major contributor to global food security. The two-line hybrid rice system, which utilizes mutants exhibiting photo-/thermo-sensitive genic male sterility (P/TGMS), is the leading hybrid rice breeding technology. Mutations in THERMO-SENSITIVE GENIC MALE STERILE 5 (TMS5) accounts for over 95% of current TGMS lines. We previously found that tms5 carries a mutation in ribonuclease ZS1. Despite its importance for breeding robust rice lines, the mechanism underlying tms5-mediated TGMS remains elusive. Here, we demonstrate that TMS5 is a tRNA 2′,3′-cyclic phosphatase. The tms5 mutation leads to accumulation of 2′,3′-cyclic phosphate (cP)-ΔCCA-tRNAs (tRNAs without 3′ CCA ended with cP), which is exacerbated by high temperatures, and reduction in the abundance of mature tRNAs, particularly alanine tRNAs (tRNA-Alas). Overexpression of tRNA-Alas in the tms5 mutant restores male fertility to 70%. Remarkably, male fertility of tms5 mutant is completely restored at high temperatures by knocking out OsVms1 which encodes the enzyme for cP-ΔCCA-tRNA generation. Our study reveals the mechanism underlying tms5-mediated TGMS in rice and provides mechanistic insight into the further improvement of TGMS in hybrid crop development.

https://doi.org/10.1038/s41422-024-01012-4

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