Microtubule re-organization during female meiosis in C elegans

  1. Ina Lantzsch
  2. Che-Hang Yu
  3. Yu-Zen Chen
  4. Vitaly Zimyanin
  5. Hossein Yazdkhasti
  6. Norbert Lindow
  7. Erik Szentgyoergyi
  8. Ariel M Pani
  9. Steffen Prohaska
  10. Martin Srayko
  11. Sebastian Fürthauer  Is a corresponding author
  12. Stefanie Redemann  Is a corresponding author
  1. Technische Universitaet Dresden, Germany
  2. University of California, Santa Barbara, United States
  3. University of Virginia, United States
  4. Zuse Institute Berlin, Germany
  5. University of Alberta, Canada
  6. Flatiron Institute, United States

Abstract

The female meiotic spindles of most animals are acentrosomal and undergo striking morphological changes while transitioning from metaphase to anaphase. The ultra-structure of acentrosomal spindles, and how changes to this structure correlate with such dramatic spindle rearrangements remains largely unknown. To address this, we applied light microscopy, large-scale electron tomography and mathematical modeling of female meiotic C. elegans spindles undergoing the transition from metaphase to anaphase. Combining these approaches, we find that meiotic spindles are dynamic arrays of short microtubules that turn over on second time scales. The results show that the transition from metaphase to anaphase correlates with an increase in the number of microtubules and a decrease in their average length. Detailed analysis of the tomographic data revealed that the length of microtubules changes significantly during the metaphase-to-anaphase transition. This effect is most pronounced for those microtubules located within 150 nm of the chromosome surface. To understand the mechanisms that drive this transition, we developed a mathematical model for the microtubule length distribution that considers microtubule growth, catastrophe, and severing. Using Bayesian inference to compare model predictions and data, we find that microtubule turn-over is the major driver of the observed large-scale reorganizations. Our data suggest that in metaphase only a minor fraction of microtubules, those that are closest to the chromosomes, are severed. The large majority of microtubules, which are not in close contact with chromosomes, do not undergo severing. Instead, their length distribution is fully explained by growth and catastrophe alone. In anaphase, even microtubules close to the chromosomes show no signs of cutting. This suggests that the most prominent drivers of spindle rearrangements from metaphase to anaphase are changes in nucleation and catastrophe rate. In addition, we provide evidence that microtubule severing is dependent on the presence of katanin.

Data availability

Electron microscopy models of microtubules and chromosome surfaces will be made available on Dryad under doi.org/10.5061/dryad.x3ffbg7k5. Example data and analysis code is available at https://github.com/SebastianFuerthauer/SpindleRerrangement

The following data sets were generated
    1. Redemann S.
    (2021) C. elegans meiotic spindles
    Dryad Digital Repository, doi.org/10.5061/dryad.x3ffbg7k5.
The following previously published data sets were used
    1. Redemann
    (2018) Meiosis I spindles of Metaphase, early Anaphase and Anaphase
    https://www.cell.com/current-biology/fulltext/S0960-9822(18)30911-4?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS0960982218309114%3Fshowall%3Dtrue.

Article and author information

Author details

  1. Ina Lantzsch

    Faculty of Medicine Carl Gustav Carus, Technische Universitaet Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Che-Hang Yu

    Department of Electrical and Computer Engineering, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0353-9752
  3. Yu-Zen Chen

    University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Vitaly Zimyanin

    University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Hossein Yazdkhasti

    University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Norbert Lindow

    Zuse Institute Berlin, Zuse Institute Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Erik Szentgyoergyi

    Faculty of Medicine Carl Gustav Carus, Technische Universitaet Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Ariel M Pani

    University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Steffen Prohaska

    Visualization and Data Analysis, Zuse Institute Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Martin Srayko

    University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. Sebastian Fürthauer

    Center for Computational Biology, Flatiron Institute, New York, United States
    For correspondence
    sfuerthauer@flatironinstitute.org
    Competing interests
    The authors declare that no competing interests exist.
  12. Stefanie Redemann

    University of Virginia, Charlottesville, United States
    For correspondence
    sz5j@virginia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2334-7309

Funding

Deutsche Forschungsgemeinschaft (MU 1423/3-1)

  • Ina Lantzsch

Deutsche Forschungsgemeinschaft (MU 1423/3-2)

  • Ina Lantzsch

Deutsche Forschungsgemeinschaft (MU 1423/8-1)

  • Erik Szentgyoergyi

Technische Universität Darmstadt (Frauenhabilitation)

  • Stefanie Redemann

Natural Sciences and Engineering Research Council of Canada

  • Martin Srayko

National Science Foundation (DMR-0820484)

  • Che-Hang Yu

National Science Foundation (NeuroNex #1934288)

  • Che-Hang Yu

National Institutes of Health (1R01GM104976-01)

  • Che-Hang Yu

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

Reviewing Editor

  1. Thomas Surrey, Centre for Genomic Regulation (CRG), Spain

Publication history

  1. Received: May 14, 2020
  2. Accepted: May 24, 2021
  3. Accepted Manuscript published: June 11, 2021 (version 1)
  4. Version of Record published: June 24, 2021 (version 2)

Copyright

© 2021, Lantzsch 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. Ina Lantzsch
  2. Che-Hang Yu
  3. Yu-Zen Chen
  4. Vitaly Zimyanin
  5. Hossein Yazdkhasti
  6. Norbert Lindow
  7. Erik Szentgyoergyi
  8. Ariel M Pani
  9. Steffen Prohaska
  10. Martin Srayko
  11. Sebastian Fürthauer
  12. Stefanie Redemann
(2021)
Microtubule re-organization during female meiosis in C elegans
eLife 10:e58903.
https://doi.org/10.7554/eLife.58903

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