SYP-5 regulates meiotic thermotolerance in Caenorhabditis elegans

Abstract

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 the 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.

Sexual dimorphic regulation of recombination by the synaptonemal complex

“…Primary antibodies (chicken anti-RAD-51, 1:1500 (K urhanewicz et al . 2020; T oraason et al . 2021); rabbit anti-SYP-1,1:1000 (gift from Silva Lab); rabbit anti-DSB-2, 1:5000; rabbit anti-OLLAS 1:1000 (Genscript, A01658)) were added and incubated overnight in a humid chamber with a parafilm cover.…”

“…The quantification of GFP::SYP-2 and mCherry::SYP-3 was performed using Imaris (Oxford Instruments) in combination with our whole gonad analysis, described in (T oraason et al . 2021).…”

“…Our whole gonad analysis was used to align the GFP::SYP-2 or mCherry::SYP-3 surfaced nuclei along the germline length (T oraason et al . 2021).…”

“…The SC is both required for the formation of crossovers and influences the frequency of crossovers occurring per homolog pair in multiple organisms (SYM et al 1993;YUAN et al 2000;PAGE AND HAWLEY 2001;MACQUEEN et al 2002;YUAN et al 2002;COLAIACOVO et al 2003;HILLERS AND VILLENEUVE 2003;ANDERSON et al 2005;COSTA et al 2005;DE VRIES et al 2005;HIGGINS et al 2005;BOLCUN-FILAS et al 2007;JEFFRESS et al 2007;SMOLIKOV et al 2007a;HAMER et al 2008;PAGE et al 2008;SMOLIKOV et al 2009;HAYASHI et al 2010;SCHRAMM et al 2011;YUAN et al 2012;LIBUDA et al 2013;COLLINS et al 2014;WOGLAR AND VILLENEUVE 2018;HURLOCK et al 2020;GORDON et al 2021;LIU et al 2021). Specific proteins within the SC can influence crossover distribution, DSB repair mechanisms, and specific steps in the crossover licensing process (JEFFRESS et al 2007;VOELKEL-MEIMAN et al 2015;VOELKEL-MEIMAN et al 2019;GORDON et al 2021;LASCAREZ-LAGUNAS et al 2022;VOELKEL-MEIMAN et al 2022).…”

“…To date, six SYP proteins have been identified (SYP-1 through SYP-6) (MACQUEEN et al 2002;COLAIACOVO et al 2003;SMOLIKOV et al 2007a;SMOLIKOV et al 2009;HURLOCK et al 2020;LIU et al 2021). The most well characterized central region SC proteins are SYP-1, SYP-2, and SYP-3 (Figure 1A).…”