Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

  1. Raphaël Etournay
  2. Marko Popović
  3. Matthias Merkel
  4. Amitabha Nandi
  5. Corinna Blasse
  6. Benoît Aigouy
  7. Holger Brandl
  8. Gene Myers
  9. Guillaume Salbreux
  10. Frank Jülicher
  11. Suzanne Eaton  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Max Planck Institute for the Physics of Complex Systems, Germany
  3. Institut de Biologie du Développement de Marseille, France

Abstract

How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constrains exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

Article and author information

Author details

  1. Raphaël Etournay

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  2. Marko Popović

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  3. Matthias Merkel

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  4. Amitabha Nandi

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  5. Corinna Blasse

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  6. Benoît Aigouy

    Institut de Biologie du Développement de Marseille, Marseille, France
    Competing interests
    No competing interests declared.
  7. Holger Brandl

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  8. Gene Myers

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    No competing interests declared.
  9. Guillaume Salbreux

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  10. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    Frank Jülicher, Reviewing editor, eLife.
  11. Suzanne Eaton

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    eaton@mpi-cbg.de
    Competing interests
    No competing interests declared.

Reviewing Editor

  1. Helen McNeill, The Samuel Lunenfeld Research Institute, Canada

Version history

  1. Received: February 24, 2015
  2. Accepted: June 18, 2015
  3. Accepted Manuscript published: June 23, 2015 (version 1)
  4. Version of Record published: September 22, 2015 (version 2)

Copyright

© 2015, Etournay 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.

Metrics

  • 8,622
    views
  • 2,380
    downloads
  • 232
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Raphaël Etournay
  2. Marko Popović
  3. Matthias Merkel
  4. Amitabha Nandi
  5. Corinna Blasse
  6. Benoît Aigouy
  7. Holger Brandl
  8. Gene Myers
  9. Guillaume Salbreux
  10. Frank Jülicher
  11. Suzanne Eaton
(2015)
Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing
eLife 4:e07090.
https://doi.org/10.7554/eLife.07090

Share this article

https://doi.org/10.7554/eLife.07090