Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop

Elife. 2017 Mar 27;6:e23437. doi: 10.7554/eLife.23437.

Abstract

The synaptonemal complex (SC) is an ultrastructurally conserved proteinaceous structure that holds homologous chromosomes together and is required for the stabilization of pairing interactions and the completion of crossover (CO) formation between homologs during meiosis I. Here, we identify a novel role for a central region component of the SC, SYP-4, in negatively regulating formation of recombination-initiating double-strand breaks (DSBs) via a feedback loop triggered by crossover designation in C. elegans. We found that SYP-4 is phosphorylated dependent on Polo-like kinases PLK-1/2. SYP-4 phosphorylation depends on DSB formation and crossover designation, is required for stabilizing the SC in pachytene by switching the central region of the SC from a more dynamic to a less dynamic state, and negatively regulates DSB formation. We propose a model in which Polo-like kinases recognize crossover designation and phosphorylate SYP-4 thereby stabilizing the SC and making chromosomes less permissive for further DSB formation.

Keywords: C. elegans; Polo-like kinase; SYP-4; cell biology; chromosomes; double-strand breaks; genes; meiosis; synaptonemal complex.

MeSH terms

  • Animals
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism*
  • DNA Breaks, Double-Stranded*
  • Feedback, Physiological*
  • Nuclear Proteins / metabolism*
  • Phosphorylation
  • Protein Processing, Post-Translational*
  • Protein Serine-Threonine Kinases / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • Nuclear Proteins
  • SYP-4 protein, C elegans
  • Protein Serine-Threonine Kinases
  • plk-1 protein, C elegans
  • polo-like kinase 2, C elegans