Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis

PLoS Genet. 2017 Mar 24;13(3):e1006670. doi: 10.1371/journal.pgen.1006670. eCollection 2017 Mar.

Abstract

During meiotic prophase, a structure called the synaptonemal complex (SC) assembles at the interface between aligned pairs of homologous chromosomes, and crossover recombination events occur between their DNA molecules. Here we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans, revealing dynamic properties of the SC that are modulated by recombination. We demonstrate that the SC incorporates new subunits and switches from a more highly dynamic/labile state to a more stable state as germ cells progress through the pachytene stage of meiotic prophase. We further show that the more dynamic state of the SC is prolonged in mutants where meiotic recombination is impaired. Moreover, in meiotic mutants where recombination intermediates are present in limiting numbers, SC central region subunits become preferentially stabilized on the subset of chromosome pairs that harbor a site where pro-crossover factors COSA-1 and MutSγ are concentrated. Polo-like kinase PLK-2 becomes preferentially localized to the SCs of chromosome pairs harboring recombination sites prior to the enrichment of SC central region proteins on such chromosomes, and PLK-2 is required for this enrichment to occur. Further, late pachytene nuclei in a plk-2 mutant exhibit the more highly dynamic SC state. Together our data demonstrate that crossover recombination events elicit chromosome-autonomous stabilizing effects on the SC and implicate PLK-2 in this process. We discuss how this recombination-triggered modulation of SC state might contribute to regulatory mechanisms that operate during meiosis to ensure the formation of crossovers while at the same time limiting their numbers.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Crossing Over, Genetic
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Fluorescence Recovery After Photobleaching
  • Kinetics
  • Meiosis / genetics*
  • Meiotic Prophase I / genetics
  • Microscopy, Confocal
  • Mutation
  • Protein-Serine-Threonine Kinases / genetics
  • Protein-Serine-Threonine Kinases / metabolism
  • Recombination, Genetic*
  • Synaptonemal Complex / genetics*
  • Synaptonemal Complex / metabolism

Substances

  • COSA-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • Protein-Serine-Threonine Kinases
  • polo-like kinase 2, C elegans