Male meiotic spindle features that efficiently segregate paired and lagging chromosomes
- Technische Universität Dresden, Germany
- Zuse Institute Berlin, Germany
- Indiana University, United States
- San Francisco State University, United States
- 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
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Supplemental data for the publicationOpARA, doi:10.25532/OPARA-56.
Article and author information
Author details
Thomas Müller-Reichert
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
- Yukiko M Yamashita, University of Michigan, United States
Publication history
- Received: August 9, 2019
- Accepted: March 8, 2020
- Accepted Manuscript published: March 9, 2020 (version 1)
- Accepted Manuscript updated: March 10, 2020 (version 2)
- Version of Record published: March 27, 2020 (version 3)
- 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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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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