1. Cell Biology
Download icon

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
Research Article
  • Cited 4
  • Views 1,398
  • Annotations
Cite this article as: eLife 2020;9:e50988 doi: 10.7554/eLife.50988
Voice your concerns about research culture and research communication: Have your say in our 7th annual survey.
Take the Survey

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.

Metrics

  • 1,398
    Page views
  • 291
    Downloads
  • 4
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Categories and tags

Research organism

Further reading

    1. Cell Biology
    2. Chromosomes and Gene Expression

    Coordination between nucleotide excision repair and specialized polymerase DnaE2 action enables DNA damage survival in non-replicating bacteria

    Asha Mary Joseph et al.
    Research Article Updated

    Translesion synthesis (TLS) is a highly conserved mutagenic DNA lesion tolerance pathway, which employs specialized, low-fidelity DNA polymerases to synthesize across lesions. Current models suggest that activity of these polymerases is predominantly associated with ongoing replication, functioning either at or behind the replication fork. Here we provide evidence for DNA damage-dependent function of a specialized polymerase, DnaE2, in replication-independent conditions. We develop an assay to follow lesion repair in non-replicating Caulobacter and observe that components of the replication machinery localize on DNA in response to damage. These localizations persist in the absence of DnaE2 or if catalytic activity of this polymerase is mutated. Single-stranded DNA gaps for SSB binding and low-fidelity polymerase-mediated synthesis are generated by nucleotide excision repair (NER), as replisome components fail to localize in the absence of NER. This mechanism of gap-filling facilitates cell cycle restoration when cells are released into replication-permissive conditions. Thus, such cross-talk (between activity of NER and specialized polymerases in subsequent gap-filling) helps preserve genome integrity and enhances survival in a replication-independent manner.

    1. Cell Biology
    2. Structural Biology and Molecular Biophysics

    Membrane binding controls ordered self-assembly of animal septins

    Agata Szuba et al.
    Research Article Updated

    Septins are conserved cytoskeletal proteins that regulate cell cortex mechanics. The mechanisms of their interactions with the plasma membrane remain poorly understood. Here, we show by cell-free reconstitution that binding to flat lipid membranes requires electrostatic interactions of septins with anionic lipids and promotes the ordered self-assembly of fly septins into filamentous meshworks. Transmission electron microscopy reveals that both fly and mammalian septin hexamers form arrays of single and paired filaments. Atomic force microscopy and quartz crystal microbalance demonstrate that the fly filaments form mechanically rigid, 12- to 18-nm thick, double layers of septins. By contrast, C-terminally truncated septin mutants form 4-nm thin monolayers, indicating that stacking requires the C-terminal coiled coils on DSep2 and Pnut subunits. Our work shows that membrane binding is required for fly septins to form ordered arrays of single and paired filaments and provides new insights into the mechanisms by which septins may regulate cell surface mechanics.

    1. Cell Biology

    Adiponectin preserves metabolic fitness during aging

    Na Li et al.
    Research Article Updated

    Adiponectin is essential for the regulation of tissue substrate utilization and systemic insulin sensitivity. Clinical studies have suggested a positive association of circulating adiponectin with healthspan and lifespan. However, the direct effects of adiponectin on promoting healthspan and lifespan remain unexplored. Here, we are using an adiponectin null mouse and a transgenic adiponectin overexpression model. We directly assessed the effects of circulating adiponectin on the aging process and found that adiponectin null mice display exacerbated age-related glucose and lipid metabolism disorders. Moreover, adiponectin null mice have a significantly shortened lifespan on both chow and high-fat diet. In contrast, a transgenic mouse model with elevated circulating adiponectin levels has a dramatically improved systemic insulin sensitivity, reduced age-related tissue inflammation and fibrosis, and a prolonged healthspan and median lifespan. These results support a role of adiponectin as an essential regulator for healthspan and lifespan.