Condensin I protects meiotic cohesin from WAPL-1 mediated removal

PLoS Genet. 2018 May 16;14(5):e1007382. doi: 10.1371/journal.pgen.1007382. eCollection 2018 May.

Abstract

Condensin complexes are key determinants of higher-order chromatin structure and are required for mitotic and meiotic chromosome compaction and segregation. We identified a new role for condensin in the maintenance of sister chromatid cohesion during C. elegans meiosis. Using conventional and stimulated emission depletion (STED) microscopy we show that levels of chromosomally-bound cohesin were significantly reduced in dpy-28 mutants, which lack a subunit of condensin I. SYP-1, a component of the synaptonemal complex central region, was also diminished, but no decrease in the axial element protein HTP-3 was observed. Surprisingly, the two key meiotic cohesin complexes of C. elegans were both depleted from meiotic chromosomes following the loss of condensin I, and disrupting condensin I in cohesin mutants increased the frequency of detached sister chromatids. During mitosis and meiosis in many organisms, establishment of cohesion is antagonized by cohesin removal by Wapl, and we found that condensin I binds to C. elegans WAPL-1 and counteracts WAPL-1-dependent cohesin removal. Our data suggest that condensin I opposes WAPL-1 to promote stable binding of cohesin to meiotic chromosomes, thereby ensuring linkages between sister chromatids in early meiosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromatids / genetics
  • Chromatids / metabolism
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Chromosome Segregation / genetics
  • Cohesins
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • In Situ Hybridization, Fluorescence
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Meiosis / genetics*
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • RNA Interference
  • Synaptonemal Complex / genetics
  • Synaptonemal Complex / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Intercellular Signaling Peptides and Proteins
  • Multiprotein Complexes
  • Nuclear Proteins
  • condensin complexes
  • wapl-1 protein, C elegans
  • Adenosine Triphosphatases