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SYP-5 regulates meiotic thermotolerance in Caenorhabditis elegans
Yuanyuan Liu1,† , Qiuchen Zhao1,† , Hui Nie1,† , Fengguo Zhang1,† , Tingting Fu1 , Zhenguo Zhang1 , Feifei Qi1 , Ruoxi Wang1 , Jun Zhou1 , Jinmin Gao1,*
1Institute of Biomedical Sciences, College of Life Sciences, Key Laboratory of Animal Resistance Biology of Shandong Province, Shandong Normal University, Jinan 250014, China
These authors contributed equally to this work.
*Correspondence to:Jinmin Gao , Email:jinmingao@sdnu.edu.cn
J Mol Cell Biol, Volume 13, Issue 9, September 2021, 662-675,  https://doi.org/10.1093/jmcb/mjab035
Keyword: meiosis, thermotolerance, synaptonemal complex, crossover regulation, Caenorhabditis elegans, SYP-5
Meiosis produces the haploid gametes required by all sexually reproducing organisms, occurring in specific temperature ranges in different organisms. However, how meiotic thermotolerance is regulated remains largely unknown. Using the model organism Caenorhabditis elegans, here, we identified the synaptonemal complex (SC) protein SYP-5 as a critical regulator of meiotic thermotolerance. syp-5-null mutants maintained a high percentage of viable progeny at 20°C but produced significantly fewer viable progeny at 25°C, a permissive temperature in wild-type worms. Cytological analysis of meiotic events in the mutants revealed that while SC assembly and disassembly, as well as DNA double-strand break repair kinetics, were not affected by the elevated temperature, crossover designation, and bivalent formation were significantly affected. More severe homolog segregation errors were also observed at elevated temperature. A temperature switching assay revealed that late meiotic prophase events were not temperature-sensitive and that meiotic defects during pachytene stage were responsible for the reduced viability of syp-5 mutants at the elevated temperature. Moreover, SC polycomplex formation and hexanediol sensitivity analysis suggested that SYP-5 was required for the normal properties of the SC, and charge-interacting elements in SC components were involved in regulating meiotic thermotolerance. Together, these findings provide a novel molecular mechanism for meiotic thermotolerance regulation.