A conserved filamentous assembly underlies the structure of the meiotic chromosome axis

Elife. 2019 Jan 18:8:e40372. doi: 10.7554/eLife.40372.

Abstract

The meiotic chromosome axis plays key roles in meiotic chromosome organization and recombination, yet the underlying protein components of this structure are highly diverged. Here, we show that 'axis core proteins' from budding yeast (Red1), mammals (SYCP2/SYCP3), and plants (ASY3/ASY4) are evolutionarily related and play equivalent roles in chromosome axis assembly. We first identify 'closure motifs' in each complex that recruit meiotic HORMADs, the master regulators of meiotic recombination. We next find that axis core proteins form homotetrameric (Red1) or heterotetrameric (SYCP2:SYCP3 and ASY3:ASY4) coiled-coil assemblies that further oligomerize into micron-length filaments. Thus, the meiotic chromosome axis core in fungi, mammals, and plants shares a common molecular architecture, and likely also plays conserved roles in meiotic chromosome axis assembly and recombination control.

Keywords: A. thaliana; HORMAD protein; S. cerevisiae; Zygosaccharomyces rouxii; chromosomes; coiled-coil; gene expression; meiotic chromosome axis; meiotic recombination; molecular biophysics; mouse; structural biology.

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
  • Arabidopsis / metabolism*
  • Cell Cycle Proteins / metabolism
  • Chromosomal Proteins, Non-Histone / metabolism
  • Chromosomes / ultrastructure*
  • DNA Breaks, Double-Stranded
  • Haploidy
  • Kinetics
  • Mass Spectrometry
  • Meiosis*
  • Mice
  • Mutation
  • Nuclear Proteins / metabolism
  • Protein Domains
  • Protein Interaction Mapping
  • Recombination, Genetic
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Scattering, Radiation
  • Synaptonemal Complex / metabolism
  • Synchrotrons
  • Two-Hybrid System Techniques
  • Zygosaccharomyces / metabolism

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Nuclear Proteins
  • RED1 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins