Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans

PLoS Genet. 2010 Nov 24;6(11):e1001219. doi: 10.1371/journal.pgen.1001219.

Abstract

The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2-dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / cytology*
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Proteins / metabolism*
  • Cell Nucleus / metabolism
  • Chromatin / metabolism
  • Chromosomes / metabolism*
  • Cytoskeleton / metabolism
  • DNA Breaks, Double-Stranded
  • Genotype
  • Meiotic Prophase I*
  • Mitosis
  • Models, Biological
  • Nuclear Proteins / metabolism*
  • Protein Structure, Quaternary
  • Protein Transport
  • Receptors, Cytoplasmic and Nuclear / chemistry
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Synaptonemal Complex / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • Chromatin
  • KDP-1 protein, C elegans
  • Nuclear Proteins
  • Receptors, Cytoplasmic and Nuclear
  • sun-1 protein, C elegans