1. Developmental Biology
  2. Physics of Living Systems
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From local resynchronization to global pattern recovery in the zebrafish segmentation clock

  1. Koichiro Uriu  Is a corresponding author
  2. Bo-Kai Liao
  3. Andrew C Oates
  4. Luis G Morelli
  1. Kanazawa University, Japan
  2. National Taiwan Ocean University, Taiwan
  3. École polytechnique fédérale de Lausanne, Switzerland
  4. Instituto de Investigación en Biomedicina de Buenos Aires, Argentina
Research Article
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Cite this article as: eLife 2021;10:e61358 doi: 10.7554/eLife.61358

Abstract

Integrity of rhythmic spatial gene expression patterns in the vertebrate segmentation clock requires local synchronization between neighboring cells by Delta-Notch signaling and its inhibition causes defective segment boundaries. Whether deformation of the oscillating tissue complements local synchronization during patterning and segment formation is not understood. We combine theory and experiment to investigate this question in the zebrafish segmentation clock. We remove a Notch inhibitor, allowing resynchronization, and analyze embryonic segment recovery. We observe unexpected intermingling of normal and defective segments, and capture this with a new model combining coupled oscillators and tissue mechanics. Intermingled segments are explained in the theory by advection of persistent phase vortices of oscillators. Experimentally observed changes in recovery patterns are predicted in the theory by temporal changes in tissue length and cell advection pattern. Thus, segmental pattern recovery occurs at two length and time scales: rapid local synchronization between neighboring cells, and the slower transport of the resulting patterns across the tissue through morphogenesis.

Article and author information

Author details

  1. Koichiro Uriu

    Natural Science and Technology, Kanazawa University, Kanazawa, Japan
    For correspondence
    uriu@staff.kanazawa-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1802-2470
  2. Bo-Kai Liao

    Department of Aquaculture, National Taiwan Ocean University, Keelung, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrew C Oates

    École polytechnique fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3015-3978
  4. Luis G Morelli

    Cellular Plasticity, Instituto de Investigación en Biomedicina de Buenos Aires, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5614-073X

Funding

Japan Society for the Promotion of Science (KAKENHI grant number 17H05762)

  • Koichiro Uriu

ANPCyT (PICT 2013 1301)

  • Luis G Morelli

ANPCyT (PICT 2017 3753)

  • Luis G Morelli

FOCEM-Mercosur (COF 03/11)

  • Luis G Morelli

Japan Society for the Promotion of Science (Short Term Grant S17064)

  • Koichiro Uriu
  • Luis G Morelli

Japan Society for the Promotion of Science (KAKENHI grant number 19H04955)

  • Koichiro Uriu

Japan Society for the Promotion of Science (KAKENHI grant number 19H04772)

  • Koichiro Uriu

Ministry of Science and Technology, Taiwan (MOST 108-2311-B-019-001-MY3)

  • Bo-Kai Liao

SNSF Project funding division III (31003A_176037)

  • Andrew C Oates

Wellcome Trust Senior Research Fellowship in Basic Biomedical Science (WT098025MA)

  • Andrew C Oates

European Research Council Starting Independent Research Grant (ERC-2007-StG: 207634)

  • Bo-Kai Liao
  • Andrew C Oates

Francis Crick Institute

  • Bo-Kai Liao
  • Andrew C Oates

ANPCyT (PICT 2012 1954)

  • Luis G Morelli

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

Ethics

Animal experimentation: Zebrafish experimentation was carried out in strict accordance with the ethics and regulations of the Saxonian Ministry of the Environment and Agriculture in Germany under licence Az. 74-9165.40-9-2001, and the Home Office in the United Kingdom under project licence PPL No. 70/7675.

Reviewing Editor

  1. Ingmar Riedel-Kruse

Publication history

  1. Received: July 23, 2020
  2. Accepted: January 27, 2021
  3. Accepted Manuscript published: February 15, 2021 (version 1)

Copyright

© 2021, Uriu 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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