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Biomechanical control of meiotic chromosomal bouquet and germ cell morphogenesis by the zygotene cilium

Avishag Mytlis, Vineet Kumar, Qiu Tao, Rachael Deis, Neta Hart, Karine Levy, Markus Masek, Amal Shawahny, Adam Ahmad, Hagai Eitan, Farouq Nather, Shai Adar-Levor, Ramon Y. Birnbaum, Natalie Elia, Ruxandra Bachmann-Gagescu, Sudipto Roy, View ORCID ProfileYaniv M. Elkouby
doi: https://doi.org/10.1101/2021.02.08.430249
Avishag Mytlis
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Vineet Kumar
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Qiu Tao
3Institute of Molecular and Cell Biology, Proteos, 61 Biopolis Drive, Singapore 138673
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Rachael Deis
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Neta Hart
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Karine Levy
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Markus Masek
4Department of Molecular Life Sciences, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
5Institute of Medical Genetics, University of Zurich, Wagistrasse 12, 8952 Schlieren, Switzerland
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Amal Shawahny
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Adam Ahmad
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Hagai Eitan
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Farouq Nather
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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Shai Adar-Levor
6Departments of Life Sciences, Ben-Gurion University of the Negev, Beer Shave 84105, Israel
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Ramon Y. Birnbaum
6Departments of Life Sciences, Ben-Gurion University of the Negev, Beer Shave 84105, Israel
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Natalie Elia
6Departments of Life Sciences, Ben-Gurion University of the Negev, Beer Shave 84105, Israel
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Ruxandra Bachmann-Gagescu
4Department of Molecular Life Sciences, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
5Institute of Medical Genetics, University of Zurich, Wagistrasse 12, 8952 Schlieren, Switzerland
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Sudipto Roy
3Institute of Molecular and Cell Biology, Proteos, 61 Biopolis Drive, Singapore 138673
7Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543
8Department of Pediatrics, Yong Loo Lin School of Medicine, National University of Singapore, 1E Kent Ridge Road, Singapore 119288
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Yaniv M. Elkouby
1Department of Developmental Biology and Cancer Research, The Hebrew University of Jerusalem Faculty of Medicine, Ein-Kerem Campus, Jerusalem, Israel 9112102
2Institute for Medical Research – Israel-Canada (IMRIC), Ein-Kerem Campus, Jerusalem, Israel 9112102
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  • ORCID record for Yaniv M. Elkouby
  • For correspondence: yaniv.elkouby@mail.huji.ac.il
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Abstract

The hallmark of meiosis is chromosomal pairing and synapsis via synaptonemal complexes, but chromosomal pairing also depends on cytoplasmic counterparts that tether and rotate telomeres on the nuclear envelope. Telomeres slide on perinuclear microtubules, shuffling chromosomes and mechanically driving their homology searches. Pull of telomeres towards the centrosome drives formation of the “zygotene chromosomal bouquet”. These telomere dynamics are essential for pairing and fertility, and the bouquet, discovered in 1900, is universally conserved. Nevertheless, how cytoplasmic counterparts of bouquet formation are mechanically regulated has remained enigmatic. Here, we report the “zygotene cilium” - a previously unrecognized cilium, in oocytes. We show in zebrafish that this cilium specifically connects to the bouquet centrosome, constituting a cable system of the cytoplasmic bouquet machinery. Furthermore, zygotene cilia extend throughout the germline cyst, a conserved germ cell organization. Using multiple ciliary mutants and laser-induced excision, we demonstrate that the zygotene cilium is essential for chromosomal bouquet and synaptonemal complex formation, germ cell morphogenesis, ovarian development and fertility. Mechanistically, we provide evidence that the cilium functions at least partly via anchoring the bouquet centrosome in order to counterbalance telomere rotation and pulling. We also show that the zygotene cilium is conserved in both male and female meiosis in zebrafish, as well as in mammals. Our work uncovers the novel concept of a cilium as a critical player in meiosis and sheds new light on reproduction phenotypes in ciliopathies. We propose a cellular paradigm that cilia can control chromosomal dynamics.

Competing Interest Statement

The authors have declared no competing interest.

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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. All rights reserved. No reuse allowed without permission.
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Posted February 15, 2022.
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Biomechanical control of meiotic chromosomal bouquet and germ cell morphogenesis by the zygotene cilium
Avishag Mytlis, Vineet Kumar, Qiu Tao, Rachael Deis, Neta Hart, Karine Levy, Markus Masek, Amal Shawahny, Adam Ahmad, Hagai Eitan, Farouq Nather, Shai Adar-Levor, Ramon Y. Birnbaum, Natalie Elia, Ruxandra Bachmann-Gagescu, Sudipto Roy, Yaniv M. Elkouby
bioRxiv 2021.02.08.430249; doi: https://doi.org/10.1101/2021.02.08.430249
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Biomechanical control of meiotic chromosomal bouquet and germ cell morphogenesis by the zygotene cilium
Avishag Mytlis, Vineet Kumar, Qiu Tao, Rachael Deis, Neta Hart, Karine Levy, Markus Masek, Amal Shawahny, Adam Ahmad, Hagai Eitan, Farouq Nather, Shai Adar-Levor, Ramon Y. Birnbaum, Natalie Elia, Ruxandra Bachmann-Gagescu, Sudipto Roy, Yaniv M. Elkouby
bioRxiv 2021.02.08.430249; doi: https://doi.org/10.1101/2021.02.08.430249

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