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Male meiotic spindle features that efficiently segregate paired and lagging chromosomes

View ORCID ProfileGunar Fabig, View ORCID ProfileRobert Kiewisz, Norbert Lindow, James A. Powers, Vanessa Cota, View ORCID ProfileLeslie Mateo, Jan Brugués, Steffen Prohaska, Diana S. Chu, View ORCID ProfileThomas Müller-Reichert
doi: https://doi.org/10.1101/737494
Gunar Fabig
1Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany
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Robert Kiewisz
1Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany
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Norbert Lindow
2Zuse Institute Berlin, 14195 Berlin, Germany
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James A. Powers
3Light Microscopy Imaging Center, Indiana University, Bloomington, IN 47405, USA
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Vanessa Cota
4Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
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Leslie Mateo
4Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
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Jan Brugués
5Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
6Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
7Centre for Systems Biology Dresden, 01307 Dresden, Germany
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Steffen Prohaska
2Zuse Institute Berlin, 14195 Berlin, Germany
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Diana S. Chu
4Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
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Thomas Müller-Reichert
1Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany
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  • For correspondence: mueller-reichert@tu-dresden.de
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Abstract

Chromosome segregation during male meiosis is tailored to rapidly generate multitudes of sperm. Little, however, is known about the mechanisms that efficiently segregate chromosomes to produce sperm. Using live imaging in Caenorhabditis elegans, we find that spermatocytes exhibit simultaneous pole-to-chromosome shortening (anaphase A) and pole-to-pole elongation (anaphase B). Electron tomography unexpectedly revealed that spermatocyte anaphase A does not stem from kinetochore microtubule shortening. Instead, movement is driven by changes in distance between chromosomes, microtubules, and centrosomes upon tension release at anaphase onset. We also find that 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 continuously lengthening kinetochore microtubules which are under tension, suggesting a ‘tug of war’ that can reliably resolve chromosome lagging. Overall, we define features that partition both paired and lagging chromosomes for optimal sperm production.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 19, 2019.
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Male meiotic spindle features that efficiently segregate paired and lagging chromosomes
Gunar Fabig, Robert Kiewisz, Norbert Lindow, James A. Powers, Vanessa Cota, Leslie Mateo, Jan Brugués, Steffen Prohaska, Diana S. Chu, Thomas Müller-Reichert
bioRxiv 737494; doi: https://doi.org/10.1101/737494
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Male meiotic spindle features that efficiently segregate paired and lagging chromosomes
Gunar Fabig, Robert Kiewisz, Norbert Lindow, James A. Powers, Vanessa Cota, Leslie Mateo, Jan Brugués, Steffen Prohaska, Diana S. Chu, Thomas Müller-Reichert
bioRxiv 737494; doi: https://doi.org/10.1101/737494

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