4.6 Article

SYP-5 regulates meiotic thermotolerance in Caenorhabditis elegans

Journal

JOURNAL OF MOLECULAR CELL BIOLOGY
Volume 13, Issue 9, Pages 662-675

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/jmcb/mjab035

Keywords

meiosis; thermotolerance; synaptonemal complex; crossover regulation; Caenorhabditis elegans; SYP-5

Categories

Funding

  1. National Natural Science Foundation of China [31871360, 32022018, 31701176, 31900557]
  2. Natural Science Foundation of Shandong Province [ZR2019PC050]

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The SYP-5 protein is identified as a critical regulator of meiotic thermotolerance, affecting crossover designation and bivalent formation. Homolog segregation errors become more severe at elevated temperature, with defects during the pachytene stage responsible for reduced viability in syp-5 mutants. These findings reveal a novel molecular mechanism for regulating meiotic thermotolerance.
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 degrees C but produced significantly fewer viable progeny at 25 degrees 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.

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