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.

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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    2. Developmental Biology
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    Research Article Updated

    In emerging epithelial tissues, cells undergo dramatic rearrangements to promote tissue shape changes. Dividing cells remain interconnected via transient cytokinetic bridges. Bridges are cleaved during abscission and currently, the consequences of disrupting abscission in developing epithelia are not well understood. We show that the Rab GTPase Rab25 localizes near cytokinetic midbodies and likely coordinates abscission through endomembrane trafficking in the epithelium of the zebrafish gastrula during epiboly. In maternal-zygotic Rab25a and Rab25b mutant embryos, morphogenic activity tears open persistent apical cytokinetic bridges that failed to undergo timely abscission. Cytokinesis defects result in anisotropic cell morphologies that are associated with a reduction of contractile actomyosin networks. This slows cell rearrangements and alters the viscoelastic responses of the tissue, all of which likely contribute to delayed epiboly. We present a model in which Rab25 trafficking coordinates cytokinetic bridge abscission and cortical actin density, impacting local cell shape changes and tissue-scale forces.

    1. Developmental Biology
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    Actomyosin contractility is regulated by Rho-GTP in cell migration, cytokinesis and morphogenesis in embryo development. Whereas Rho activation by Rho-GTP exchange factor (GEF), RhoGEF2 is well known in actomyosin contractility during cytokinesis at the base of invaginating membranes in Drosophila cellularization, Rho inhibition by RhoGTPase activating proteins (GAP) remains to be studied. We have found that the RhoGAP, GRAF inhibits actomyosin contractility during cellularization. GRAF is enriched at the cleavage furrow tip during actomyosin assembly and initiation of ring constriction. Graf depletion shows increased Rho-GTP, increased Myosin II and ring hyper constriction dependent upon the loss of the RhoGTPase domain. GRAF and RhoGEF2 are present in a balance for appropriate activation of actomyosin ring constriction. RhoGEF2 depletion and abrogation of Myosin II activation in Rho Kinase mutants suppresses the Graf hyper constriction defect. Therefore, GRAF recruitment restricts Rho-GTP levels in a spatiotemporal manner for inhibiting actomyosin contractility during cellularization.