Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1

Cell. 2009 Nov 25;139(5):920-33. doi: 10.1016/j.cell.2009.10.045. Epub 2009 Nov 12.

Abstract

Genome haploidization during meiosis depends on recognition and association of parental homologous chromosomes. The C. elegans SUN/KASH domain proteins Matefin/SUN-1 and ZYG-12 have a conserved role in this process. They bridge the nuclear envelope, connecting the cytoplasm and the nucleoplasm to transmit forces that allow chromosome movement and homolog pairing and prevent nonhomologous synapsis. Here, we show that Matefin/SUN-1 forms rapidly moving aggregates at putative chromosomal attachment sites in the meiotic transition zone (TZ). We analyzed requirements for aggregate formation and identified multiple phosphotarget residues in the nucleoplasmic domain of Matefin/SUN-1. These CHK-2 dependent phosphorylations occur in leptotene/zygotene, diminish during pachytene and are involved in pairing. Mimicking phosphorylation causes an extended TZ and univalents at diakinesis. Our data suggest that the properties of the nuclear envelope are altered during the time window when homologs are sorted and Matefin/SUN-1 aggregates form, thereby controling the movement, homologous pairing and interhomolog recombination of chromosomes.

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*
  • Checkpoint Kinase 2
  • Chromosome Pairing*
  • Chromosomes / metabolism
  • Meiosis*
  • Meiotic Prophase I
  • Microtubules / metabolism*
  • Mutation
  • Nuclear Envelope / metabolism
  • Phosphorylation
  • Protein Kinases / metabolism
  • Protein Structure, Tertiary
  • Receptors, Cytoplasmic and Nuclear / chemistry
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Serine / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Receptors, Cytoplasmic and Nuclear
  • sun-1 protein, C elegans
  • Serine
  • Protein Kinases
  • Checkpoint Kinase 2
  • CHK-2 protein, C elegans