1. Developmental Biology
  2. Physics of Living Systems
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Self-organized patterning of cell morphology via mechanosensitive feedback

  1. Natalie A Dye  Is a corresponding author
  2. Marko Popovic
  3. K. Venkatesan Iyer
  4. Jana Fuhrmann
  5. Romina Piscitello-Gómez
  6. Suzanne Eaton
  7. Frank Jülicher  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. École Polytechnique Fédérale de Lausanne, Switzerland
  3. Max Planck Institute for the Physics of Complex Systems, Germany
Research Article
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Cite this article as: eLife 2021;10:e57964 doi: 10.7554/eLife.57964

Abstract

Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal disc during larval development. Using quantitative analysis of the cellular dynamics, we reveal a pattern of radially oriented cell rearrangements that is coupled to the buildup of tangential cell elongation. Developing a laser ablation method, we map tissue stresses and extract key parameters of tissue mechanics. We present a continuum theory showing that this pattern of cell morphology and tissue stress can arise via self-organization of a mechanical feedback that couples cell polarity to active cell rearrangements. The predictions of this model are supported by knockdown of MyoVI, a component of mechanosensitive feedback. Our work reveals a mechanism for the emergence of cellular patterns in morphogenesis.

Data availability

We have made all data analyzed during this study available. Data for Figs 1H-M, 2,4,5, and 7 are provided as source data files. The data on cell area and elongation in Figure 1A-F, 3F,G, and 6C are too large to be submitted here and are available on Dryad (doi:10.5061/dryad.jsxksn06b).

The following data sets were generated

Article and author information

Author details

  1. Natalie A Dye

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    dye@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4859-6670
  2. Marko Popovic

    Institute of Physics, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. K. Venkatesan Iyer

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Jana Fuhrmann

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Romina Piscitello-Gómez

    Molecular Cell Biology and Genetics, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Suzanne Eaton

    Developmental cell biology, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    For correspondence
    julicher@pks.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4731-9185

Funding

Max-Planck-Gesellschaft

  • Natalie A Dye
  • Marko Popovic
  • K. Venkatesan Iyer
  • Jana Fuhrmann
  • Romina Piscitello-Gómez
  • Suzanne Eaton
  • Frank Jülicher

Deutsche Forschungsgemeinschaft (EA4/10-1,EA4/10-2)

  • Natalie A Dye
  • K. Venkatesan Iyer
  • Suzanne Eaton

Swiss National Science Foundation (200021-165509)

  • Marko Popovic

Simons Foundation (454953)

  • Marko Popovic

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

Reviewing Editor

  1. Jaume Casademunt, University of Barcelona, Spain

Publication history

  1. Received: April 16, 2020
  2. Accepted: March 25, 2021
  3. Accepted Manuscript published: March 26, 2021 (version 1)

Copyright

© 2021, Dye 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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Further reading

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