From local resynchronization to global pattern recovery in the zebrafish segmentation clock
- Kanazawa University, Japan
- National Taiwan Ocean University, Taiwan
- École polytechnique fédérale de Lausanne, Switzerland
- Instituto de Investigación en Biomedicina de Buenos Aires, Argentina
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.
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All data generated or analyzed during this study are included in the manuscript and supporting files.
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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.
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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From local resynchronization to global pattern recovery in the zebrafish segmentation clock
eLife 10:e61358.
https://doi.org/10.7554/eLife.61358
