The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast

PLoS Genet. 2013;9(1):e1003194. doi: 10.1371/journal.pgen.1003194. Epub 2013 Jan 10.

Abstract

During meiosis, homologous chromosomes pair at close proximity to form the synaptonemal complex (SC). This association is mediated by transverse filament proteins that hold the axes of homologous chromosomes together along their entire length. Transverse filament proteins are highly aggregative and can form an aberrant aggregate called the polycomplex that is unassociated with chromosomes. Here, we show that the Ecm11-Gmc2 complex is a novel SC component, functioning to facilitate assembly of the yeast transverse filament protein, Zip1. Ecm11 and Gmc2 initially localize to the synapsis initiation sites, then throughout the synapsed regions of paired homologous chromosomes. The absence of either Ecm11 or Gmc2 substantially compromises the chromosomal assembly of Zip1 as well as polycomplex formation, indicating that the complex is required for extensive Zip1 polymerization. We also show that Ecm11 is SUMOylated in a Gmc2-dependent manner. Remarkably, in the unSUMOylatable ecm11 mutant, assembly of chromosomal Zip1 remained compromised while polycomplex formation became frequent. We propose that the Ecm11-Gmc2 complex facilitates the assembly of Zip1 and that SUMOylation of Ecm11 is critical for ensuring chromosomal assembly of Zip1, thus suppressing polycomplex formation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Centromere / genetics
  • Centromere / metabolism
  • Chromosome Pairing / genetics
  • Chromosomes, Fungal / metabolism
  • Fungal Proteins* / genetics
  • Fungal Proteins* / metabolism
  • Gene Expression Regulation, Fungal
  • Meiosis / genetics*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Protein Processing, Post-Translational
  • SUMO-1 Protein / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Synaptonemal Complex* / genetics
  • Synaptonemal Complex* / metabolism

Substances

  • Cell Cycle Proteins
  • Ecm11 protein, S cerevisiae
  • Fungal Proteins
  • Nuclear Proteins
  • SUMO-1 Protein
  • Saccharomyces cerevisiae Proteins
  • Zip1 protein, S cerevisiae