Male meiotic spindle features that efficiently segregate paired and lagging chromosomes

  1. Gunar Fabig  Is a corresponding author
  2. Robert Kiewisz
  3. Norbert Lindow
  4. James A Powers
  5. Vanessa Cota
  6. Luis J Quintanilla
  7. Jan Brugués
  8. Steffen Prohaska
  9. Diana S Chu
  10. Thomas Müller-Reichert  Is a corresponding author
  1. Technische Universität Dresden, Germany
  2. Zuse Institute Berlin, Germany
  3. Indiana University, United States
  4. San Francisco State University, United States
  5. Max Planck Institute, Germany

Abstract

Chromosome segregation during male meiosis is tailored to rapidly generate multitudes of sperm. Little is known about mechanisms that efficiently partition chromosomes to produce sperm. Using live imaging and tomographic reconstructions of spermatocyte meiotic spindles in Caenorhabditis elegans, we find the lagging X chromosome, a distinctive feature of anaphase I in C. elegans males, is due to lack of chromosome pairing. The unpaired chromosome remains tethered to centrosomes by lengthening kinetochore microtubules, which are under tension, suggesting that a 'tug of war' reliably resolves lagging. We find spermatocytes exhibit simultaneous pole-to-chromosome shortening (anaphase A) and pole-to-pole elongation (anaphase B). Electron tomography unexpectedly revealed spermatocyte anaphase A does not stem solely from kinetochore microtubule shortening. Instead, movement of autosomes is largely driven by distance change between chromosomes, microtubules, and centrosomes upon tension release during anaphase. Overall, we define novel features that segregate both lagging and paired chromosomes for optimal sperm production.

Data availability

Data have been uploaded to the TU Dresden Open Access Repository and Archive system (OpARA) and are available as open access: http://dx.doi.org/10.25532/OPARA-56

The following data sets were generated

Article and author information

Author details

  1. Gunar Fabig

    Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
    For correspondence
    gunar.fabig@tu-dresden.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3017-0978
  2. Robert Kiewisz

    Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2733-4978
  3. Norbert Lindow

    Visualization and Data Analysis, Zuse Institute Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. James A Powers

    Light Microscopy Imaging Center, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Vanessa Cota

    Department of Biology, San Francisco State University, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Luis J Quintanilla

    Department of Biology, San Francisco State University, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jan Brugués

    Molecular Cell Biology and Genetics, Max Planck Institute, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Steffen Prohaska

    Visualization and Data Analysis, Zuse Institute Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Diana S Chu

    Department of Biology, San Francisco State University, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Thomas Müller-Reichert

    Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany
    For correspondence
    mueller-reichert@tu-dresden.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0203-1436

Funding

Deutsche Forschungsgemeinschaft (MU 1423/10-1)

  • Gunar Fabig
  • Thomas Müller-Reichert

Horizon 2020 Framework Programme (No. 675737)

  • Robert Kiewisz
  • Thomas Müller-Reichert

National Institutes of Health (R03 HD093990-01A1)

  • Vanessa Cota
  • Diana S Chu

National Science Foundation (RUI-1817611,DBI-1548297)

  • Vanessa Cota
  • Diana S Chu

National Institutes of Health (NIH1S10OD024988-01)

  • James A Powers

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

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Publication history

  1. Received: August 9, 2019
  2. Accepted: March 8, 2020
  3. Accepted Manuscript published: March 9, 2020 (version 1)
  4. Accepted Manuscript updated: March 10, 2020 (version 2)
  5. Version of Record published: March 27, 2020 (version 3)
  6. Version of Record updated: April 1, 2020 (version 4)

Copyright

© 2020, Fabig 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. Gunar Fabig
  2. Robert Kiewisz
  3. Norbert Lindow
  4. James A Powers
  5. Vanessa Cota
  6. Luis J Quintanilla
  7. Jan Brugués
  8. Steffen Prohaska
  9. Diana S Chu
  10. Thomas Müller-Reichert
(2020)
Male meiotic spindle features that efficiently segregate paired and lagging chromosomes
eLife 9:e50988.
https://doi.org/10.7554/eLife.50988
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