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

  1. Alan M V West
  2. Scott C Rosenberg
  3. Sarah N Ur
  4. Madison K Lehmer
  5. Qiaozhen Ye
  6. Götz Hagemann
  7. Iracema Caballero
  8. Isabel Uson
  9. Amy J MacQueen
  10. Franz Herzog
  11. Kevin D Corbett  Is a corresponding author
  1. University of California, San Diego, United States
  2. Ludwig-Maximilians-Universität München, Germany
  3. Institute of Molecular Biology of Barcelona, Spain
  4. Wesleyan University, United States

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.

Data availability

Primary diffraction data for M. musculus SYCP3 tetramer structures have been deposited with the SBGrid Data Bank (https://data.sbgrid.org) under dataset numbers 583 (P21 crystal form) and 584 (P1 form).Reduced diffraction data and refined structural models have been deposited with the Protein Data Bank (www.pdb.org) under accession numbers 6DD8 (P21 crystal form) and 6DD9 (P1 form)

The following data sets were generated

Article and author information

Author details

  1. Alan M V West

    Biomedical Sciences Graduate Program, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Scott C Rosenberg

    Department of Chemistry, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sarah N Ur

    Biomedical Sciences Graduate Program, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Madison K Lehmer

    Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qiaozhen Ye

    Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Götz Hagemann

    Gene Center Munich, Ludwig-Maximilians-Universität München, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Iracema Caballero

    Crystallographic Methods, Institute of Molecular Biology of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Isabel Uson

    Crystallographic Methods, Institute of Molecular Biology of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Amy J MacQueen

    Department of Molecular Biology and Biochemistry, Wesleyan University, Middletown, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Franz Herzog

    Gene Center Munich, Ludwig-Maximilians-Universität München, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8270-1449
  11. Kevin D Corbett

    Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, United States
    For correspondence
    kcorbett@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5854-2388

Funding

National Institutes of Health (R01 GM104141)

  • Alan M V West
  • Scott C Rosenberg
  • Madison K Lehmer
  • Qiaozhen Ye
  • Kevin D Corbett

Human Frontier Science Program (RGP0008/2015)

  • Franz Herzog
  • Kevin D Corbett

National Science Foundation (Graduate Research Fellowship)

  • Sarah N Ur

Ludwig Institute for Cancer Research

  • Kevin D Corbett

National Institutes of Health (R15 GM116109)

  • Amy J MacQueen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Bernard de Massy, Institute of Human Genetics, CNRS UPR 1142, France

Version history

  1. Received: July 24, 2018
  2. Accepted: January 18, 2019
  3. Accepted Manuscript published: January 18, 2019 (version 1)
  4. Version of Record published: January 28, 2019 (version 2)

Copyright

© 2019, West et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alan M V West
  2. Scott C Rosenberg
  3. Sarah N Ur
  4. Madison K Lehmer
  5. Qiaozhen Ye
  6. Götz Hagemann
  7. Iracema Caballero
  8. Isabel Uson
  9. Amy J MacQueen
  10. Franz Herzog
  11. Kevin D Corbett
(2019)
A conserved filamentous assembly underlies the structure of the meiotic chromosome axis
eLife 8:e40372.
https://doi.org/10.7554/eLife.40372

Share this article

https://doi.org/10.7554/eLife.40372

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