Hybrid rice is of superior yield and pathogen resistance widely planted for agricultural production in east, south, and southeast Asia, contributing greatly to global food security. Two-line hybrid rice system is the leading hybrid rice technology, which utilizes photo-/thermo-sensitive genic male sterile (P/TGMS) mutants for breading. Our previous work has demonstrated that the thermo-sensitive genic male sterile 5 (tms5), accounting for over 95% of the TGMS lines in current two-line hybrid rice, encodes a ribonuclease ZS1. However, the mechanism underlying tms5-mediated TGMS remains elusive.
Here, we found rice ribosome-associated quality control (RQC) components modulate tms5-mediated TGMS. We resolved the crystal structure of TMS5 and found that TMS5 functions in tRNA repair to remove 2′,3′-cyclic phosphate from cP-ΔCCA-tRNAs, which is essential for male fertility. Loss of TMS5 leads to over-accumulation of cP-ΔCCA-tRNAs and insufficiency of mature tRNAs, which was exacerbated by high temperature. Remarkably, the male fertility of the tms5 mutant under high temperature can be completely restored due to preventing the generation of cP-ΔCCA-tRNAs through knocking-out of OsVms1 which encodes the enzyme for cP-ΔCCA-tRNA generation. Together, our findings revealed that tRNA repair and recycling safeguards male fertility at high temperature, providing mechanistic insight into the further improvement of TGMS in hybrid crop development.