The invariant cleavage pattern displayed by ascidian embryos depends on spindle positioning along the cell's longest axis in the apical plane and relies on asynchronous cell divisions

  1. Rémi Dumollard  Is a corresponding author
  2. Nicolas Minc
  3. Gregory salez
  4. Sameh ben aicha
  5. Faisal bekkouche
  6. Celine hebras
  7. Lydia besnardeau
  8. Alex McDougall  Is a corresponding author
  1. Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, France
  2. Institut Jacques Monod, UMR7592 CNRS, France

Abstract

The ascidian embryo is an ideal system to investigate how cell position is determined during embryogenesis. Using 3D timelapse imaging and computational methods we analyzed the planar cell divisions in ascidian early embryos and found that spindles in every cell tend to align at metaphase in the long length of the apical surface except in cells undergoing unequal cleavage. Furthermore, the invariant and conserved cleavage pattern of ascidian embryos was found to consist in alternate planar cell divisions between ectoderm and endomesoderm. In order to test the importance of alternate cell divisions we manipulated zygotic transcription induced by β-catenin or downregulated wee1 activity, both of which abolish this cell cycle asynchrony. Crucially, abolishing cell cycle asynchrony consistently disrupted the spindle orienting mechanism underpinning the invariant cleavage pattern. Our results demonstrate how an evolutionary conserved cell cycle asynchrony maintains the invariant cleavage pattern driving morphogenesis of the ascidian blastula.

Article and author information

Author details

  1. Rémi Dumollard

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    For correspondence
    remi.dumollard@obs-vlfr.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8444-0630
  2. Nicolas Minc

    Institut Jacques Monod, UMR7592 CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Gregory salez

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Sameh ben aicha

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Faisal bekkouche

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Celine hebras

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Lydia besnardeau

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Alex McDougall

    Laboratoire de Biologie du Développement de Villefranche-sur-mer, Sorbonne Universités, Université Pierre-et-Marie-Curie, CNRS, villefranche sur mer, France
    For correspondence
    dougall@obs-vlfr.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-12-BSV2-0005-02)

  • Rémi Dumollard
  • Celine hebras
  • Lydia besnardeau
  • Alex McDougall

Fondation ARC pour la Recherche sur le Cancer (SFI20111203776)

  • Rémi Dumollard
  • Celine hebras
  • Lydia besnardeau
  • Alex McDougall

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

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Version history

  1. Received: June 30, 2016
  2. Accepted: January 24, 2017
  3. Accepted Manuscript published: January 25, 2017 (version 1)
  4. Version of Record published: February 21, 2017 (version 2)

Copyright

© 2017, Dumollard 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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  1. Rémi Dumollard
  2. Nicolas Minc
  3. Gregory salez
  4. Sameh ben aicha
  5. Faisal bekkouche
  6. Celine hebras
  7. Lydia besnardeau
  8. Alex McDougall
(2017)
The invariant cleavage pattern displayed by ascidian embryos depends on spindle positioning along the cell's longest axis in the apical plane and relies on asynchronous cell divisions
eLife 6:e19290.
https://doi.org/10.7554/eLife.19290

Share this article

https://doi.org/10.7554/eLife.19290

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