Ribosome-associated Quality Control Regulates Critical Sterility-inducing Temperature in Rice

thermo-sensitive genic male sterility 5 (tms5) is a widely used thermo-sensitive genic male sterile (TGMS) line for two-line hybrid rice production. The critical sterility-inducing temperature (CSIT) acts as a key threshold of TGMS lines. However, there are a few reports on the regulatory mechanism controlling CSIT.

 

In a study published in PNAS (https://doi.org/10.1073/pnas.2417526122), CAO Xiaofeng's team from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and YANG Yuanzhu's team from Yuan Longping High-tech Agriculture Co., Ltd., reported that Rqc2 (ribosome-associated quality control 2) regulates the CSIT in tms5 lines through its C-terminal alanine and threonine modification (CATylation) activity.

 

By screening an ethyl methanesulfonate–mutagenized population of rice line Zhu1S, a widely used classical tms5-based TGMS line with low CSIT (~23℃), researchers identified a suppressor sot4 and cloned its candidate gene OsRqc2. Functional analysis showed that the translation-stalling products in plants are subjected to CATylation by OsRqc2. The amino acid residues in the C-terminal tails produced by OsRqc2 are mainly Ala, along with Ser, Thr, Ile and others. Further, they discovered that T552I mutation of OsRqc2 in sot4 alters the composition of the C-terminal tails, resulting in a decreased CATylation rate. Thus, the level of mature tRNA-Ser/Ile are rescued by OsRqc2 T552I, increasing the CSIT of tms5 lines.

 

In summary, this study presents the following model: During the evolution of both unicellular and multicellular organisms, the “Thr”-type Rqc2, compared to the “Ile”-type, can bind to a broader range of tRNAs, thereby enabling a more efficient CATylation process that helps maintain protein homeostasis. As a result, this characteristic has been preserved through natural selection. In the suppressor tms5 osrqc2-1, the T552I mutation in OsRqc2 causes a shift from the “Thr”-type to the “Ile”-type, reducing its ability to bind tRNA-Ser/Ile. The unbound tRNA then “escapes” the RQC pathway, leading to the restoration of mature tRNA levels, which in turn raises the fertility transition temperature of the tms5 mutation.

 

Therefore, this study not only provides a compelling genetic example that underscores the biological significance of evolutionary tRNA selection for CATylation, particularly in an agriculturally important trait, but also offers a novel perspective on how engineering OsRqc2’s CATylation activity could help reduce CSIT of tms5-based TGMS lines.

 

 

Contact:

Dr. CAO Xiaofeng

Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

Email: xfcao@genetics.ac.cn