tRNA selectivity during ribosome-associated quality control regulates the critical sterility-inducing temperature in two-line hybrid rice

The two-line hybrid rice system, a cutting-edge hybrid rice breeding technology, has greatly boosted global food security. In thermo-sensitive genic male sterile (TGMS) lines, the critical sterility-inducing temperature (CSIT; the temperature at which TGMS lines change from male fertile to complete male sterile) acts as a key threshold. We recently uncovered that <i>thermo-sensitive genic male sterility 5</i> (<i>tms5</i>), a sterile locus presenting in over 95% of TGMS lines, leads to the overaccumulation of 2',3'-cyclic phosphate (cP)-ΔCCA-tRNAs and a deficiency of mature tRNAs, which underlies the molecular mechanism of <i>tms5</i>-mediated TGMS. However, there are a few reports on the regulatory mechanism controlling CSIT. Here, we identified a suppressor of <i>tms5</i>, an amino acid substitution (T552I) in the rice Rqc2 (ribosome-associated quality control 2), increases the CSIT in <i>tms5</i> lines through its C-terminal alanine and threonine modification (CATylation) activity. This substitution alters tRNA selectivity, leading to the recruitment of different tRNAs to the A-site of ribosome and CATylation rate by OsRqc2 during ribosome-associated quality control (RQC), a process that rescues stalled ribosomes and degrades abnormal nascent chains during translational elongation. Further, the mutation restores the levels of mature tRNA-Ser/Ile to increase the CSIT of <i>tms5</i> lines. Our findings reveal the origin of overaccumulated cP-ΔCCA-tRNAs in <i>tms5</i> lines, further deepening our understanding of the regulatory network in governing CSIT of TGMS lines containing <i>tms5.</i>

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2025-02-06
DOI
https://doi.org/10.1073/pnas.2417526122
Citations
4
Primary Topic
RNA modifications and cancer
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article
Field-Weighted Citation Impact
3.22

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article

tRNA selectivity during ribosome-associated quality control regulates the critical sterility-inducing temperature in two-line hybrid rice

Chenjian Fu, Xingxue Fu, Chunyan Liu, Wenfeng Qian et al.
4 citations
Proceedings of the National Academy of Sciences
RNA modifications and cancer
3.22
article

tRNA selectivity during ribosome-associated quality control regulates the critical sterility-inducing temperature in two-line hybrid rice

Chenjian Fu, Xingxue Fu, Chunyan Liu, Wenfeng Qian, Shengdong Li, Xianwei Song, Li Ji, Xiahe Huang, Yan‐Chao Wu, Yuanzhu Yang, Shuying Yang, Xiaofeng Cao, Wei Yan, Yingchun Wang, Jing Sun, Jia Wang, Peng Qin, Can Zhou, Bin Yan, Xinghui Zhao
article en
4 citations

Abstract

The two-line hybrid rice system, a cutting-edge hybrid rice breeding technology, has greatly boosted global food security. In thermo-sensitive genic male sterile (TGMS) lines, the critical sterility-inducing temperature (CSIT; the temperature at which TGMS lines change from male fertile to complete male sterile) acts as a key threshold. We recently uncovered that <i>thermo-sensitive genic male sterility 5</i> (<i>tms5</i>), a sterile locus presenting in over 95% of TGMS lines, leads to the overaccumulation of 2',3'-cyclic phosphate (cP)-ΔCCA-tRNAs and a deficiency of mature tRNAs, which underlies the molecular mechanism of <i>tms5</i>-mediated TGMS. However, there are a few reports on the regulatory mechanism controlling CSIT. Here, we identified a suppressor of <i>tms5</i>, an amino acid substitution (T552I) in the rice Rqc2 (ribosome-associated quality control 2), increases the CSIT in <i>tms5</i> lines through its C-terminal alanine and threonine modification (CATylation) activity. This substitution alters tRNA selectivity, leading to the recruitment of different tRNAs to the A-site of ribosome and CATylation rate by OsRqc2 during ribosome-associated quality control (RQC), a process that rescues stalled ribosomes and degrades abnormal nascent chains during translational elongation. Further, the mutation restores the levels of mature tRNA-Ser/Ile to increase the CSIT of <i>tms5</i> lines. Our findings reveal the origin of overaccumulated cP-ΔCCA-tRNAs in <i>tms5</i> lines, further deepening our understanding of the regulatory network in governing CSIT of TGMS lines containing <i>tms5.</i>

Proceedings of the National Academy of SciencesVol. 122(6)
Chinese Academy of Sciences (CN), Southern University of Science and Technology (CN), Czech Academy of Sciences, Institute of Biotechnology (CZ), Institute of Genetics and Developmental Biology (CN), Xi'an High Tech University (CN), Beijing Academy of Agricultural and Forestry Sciences (CN), Ministry of Agriculture and Rural Affairs (CN), University of Chinese Academy of Sciences (CN)
National Natural Science Foundation of China, Chinese Academy of Sciences, National Key Research and Development Program of China, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Institute of Genetics
Zero hunger
Openalex Percentile: Top 9%
RNA modifications and cancer
3.22
DOIOpen Access PDFOpenAlex
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