The E3 ligase OsHel2 impedes readthrough of stalled mRNAs to regulate male fertility in thermosensitive genic male sterile rice
Wei Liu, Ji Li, Jun Sun, Chunyan Liu, Bin Yan, Can Zhou, Shengdong Li, Xianwei Song, Wei Yan, Yuanzhu Yang, Xiaofeng Cao
Abstract
Heterosis is extensively used in the 2-line hybrid breeding system. Photosensitive/thermosensitive genic male sterile (P/TGMS) lines are key components of 2-line hybrid rice, and TGMS lines containing tms5 have significantly advanced 2-line hybrid rice breeding. We cloned the TMS5 gene and found that TMS5 is a tRNA cyclic phosphatase that can remove 2',3'-cyclic phosphate (cP) from cP-ΔCCA-tRNAs for efficient repair to ensure maintenance of mature tRNA levels. tms5 mutation causes increased levels of cP-ΔCCA-tRNAs and reduced levels of mature tRNAs, leading to male sterility at restrictive temperatures. However, the regulatory network of tms5-mediated TGMS remains to be clarified. Here, we demonstrate that the E3 ligase OsHel2 cooperates with TMS5 to regulate TGMS at restrictive temperatures. Consistently, both the accumulation of cP-ΔCCA-tRNAs and the reduction in mature tRNAs in the tms5 mutant are largely recovered in the tms5 oshel2-1 mutant. A lesion in OsHel2 results in partial readthrough of the stalled sequences, thereby enabling evasion of ribosome-associated protein quality control (RQC) surveillance. Our findings reveal a mechanism by which OsHel2 impedes readthrough of stalled mRNA sequences to regulate male fertility in TGMS rice, providing a paradigm for investigating how disorders in components of the RQC pathway impair cellular functions and lead to diseases or defects in other organisms.