Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans

Cell. 2005 Dec 16;123(6):1037-50. doi: 10.1016/j.cell.2005.09.034.

Abstract

We have investigated the role of pairing centers (PCs), cis-acting sites required for accurate segregation of homologous chromosomes during meiosis in C. elegans. We find that these sites play two distinct roles that contribute to proper segregation. Chromosomes lacking PCs usually fail to synapse and also lack a synapsis-independent stabilization activity. The presence of a PC on just one copy of a chromosome pair promotes synapsis but does not support synapsis-independent pairing stabilization, indicating that these functions are separable. Once initiated, synapsis is highly processive, even between nonhomologous chromosomes of disparate lengths, elucidating how translocations suppress meiotic recombination in C. elegans. These findings suggest a multistep pathway for chromosome synapsis in which PCs impart selectivity and efficiency through a "kinetic proofreading" mechanism. We speculate that concentration of these activities at one region per chromosome may have coevolved with the loss of a point centromere to safeguard karyotype stability.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Chromosome Deletion
  • Chromosome Painting
  • Chromosome Pairing / genetics
  • Chromosome Pairing / physiology*
  • Chromosomes / genetics
  • Chromosomes / physiology*
  • Crossing Over, Genetic / genetics
  • Disorders of Sex Development / genetics
  • Female
  • Heterozygote
  • Male
  • Meiosis / genetics
  • Meiosis / physiology*
  • Meiotic Prophase I / genetics
  • Meiotic Prophase I / physiology
  • Microscopy, Fluorescence
  • Models, Genetic
  • Recombination, Genetic / genetics
  • Synaptonemal Complex / genetics
  • Synaptonemal Complex / metabolism
  • X Chromosome / genetics

Substances

  • Caenorhabditis elegans Proteins