1. Developmental Biology
  2. Physics of Living Systems

Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing

  1. Romina Piscitello-Gómez
  2. Franz S Gruber
  3. Abhijeet Krishna
  4. Charlie Duclut
  5. Carl D Modes
  6. Marko Popović
  7. Frank Jülicher
  8. Natalie A Dye  Is a corresponding author
  9. Suzanne Eaton
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. University of Dundee, United Kingdom
  3. Laboratoire Physico-Chimie Curie, Institut Curie, France
  4. Center for Systems Biology Dresden, Germany
  5. Max Planck Institute for the Physics of Complex Systems, Germany
  6. Technische Universität Dresden, Germany
https://doi.org/10.7554/eLife.85581
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Cite this article
  1. Romina Piscitello-Gómez
  2. Franz S Gruber
  3. Abhijeet Krishna
  4. Charlie Duclut
  5. Carl D Modes
  6. Marko Popović
  7. Frank Jülicher
  8. Natalie A Dye
  9. Suzanne Eaton
(2023)
Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing
eLife 12:e85581.
https://doi.org/10.7554/eLife.85581
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Abstract

How morphogenetic movements are robustly coordinated in space and time is a fundamental open question in biology. We study this question using the wing of Drosophila melanogaster, an epithelial tissue that undergoes large-scale tissue flows during pupal stages. Previously, we showed that pupal wing morphogenesis involves both cellular behaviors that allow relaxation of mechanical tissue stress, as well as cellular behaviors that appear to be actively patterned (Etournay et al., 2015). Here, we show that these active cellular behaviors are not guided by the core planar cell polarity (PCP) pathway, a conserved signaling system that guides tissue development in many other contexts. We find no significant phenotype on the cellular dynamics underlying pupal morphogenesis in mutants of core PCP. Furthermore, using laser ablation experiments, coupled with a rheological model to describe the dynamics of the response to laser ablation, we conclude that while core PCP mutations affect the fast timescale response to laser ablation they do not significantly affect overall tissue mechanics. In conclusion, our work shows that cellular dynamics and tissue shape changes during Drosophila pupal wing morphogenesis do not require core PCP as an orientational guiding cue.

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Author details

  1. 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.

  2. Franz S Gruber

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2008-8460

  3. Abhijeet Krishna

    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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9291-500X

  4. Charlie Duclut

    Laboratoire Physico-Chimie Curie, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8595-6815

  5. Carl D Modes

    Center for Systems Biology Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Marko Popović

    Max Planck Institute for the Physics of Complex Systems, 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
    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

  8. Natalie A Dye

    DFG Excellence Cluster Physics of Life, Technische Universität Dresden, Dresden, Germany
    For correspondence
    natalie_anne.dye@tu-dresden.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

  9. Suzanne Eaton

    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.

Funding

Max Planck Society

  • Romina Piscitello-Gómez
  • Franz S Gruber
  • Abhijeet Krishna
  • Charlie Duclut
  • Carl D Modes
  • Marko Popović
  • Frank Jülicher
  • Natalie A Dye
  • Suzanne Eaton

Deutsche Forschungsgemeinschaft (EXC-2068-390729961)

  • Romina Piscitello-Gómez
  • Abhijeet Krishna
  • Carl D Modes
  • Frank Jülicher
  • Natalie A Dye
  • Suzanne Eaton

Deutsche Forschungsgemeinschaft (SPP1782)

  • Romina Piscitello-Gómez
  • Franz S Gruber
  • Natalie A Dye
  • Suzanne Eaton

Deutsche Krebshilfe (MSNZ-P2 Dresden)

  • Natalie A Dye

Austrian Academy of Sciences (DOC Fellowship)

  • Franz S Gruber

Agence Nationale de la Recherche (ANR-11-LABX-0071)

  • Charlie Duclut

Agence Nationale de la Recherche (ANR-18-IDEX-0001)

  • Charlie Duclut

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

  • Romina Piscitello-Gómez
  • Franz S Gruber
  • Natalie A Dye
  • Suzanne Eaton

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

Copyright

© 2023, Piscitello-Gómez 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. Romina Piscitello-Gómez
  2. Franz S Gruber
  3. Abhijeet Krishna
  4. Charlie Duclut
  5. Carl D Modes
  6. Marko Popović
  7. Frank Jülicher
  8. Natalie A Dye
  9. Suzanne Eaton
(2023)
Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing
eLife 12:e85581.
https://doi.org/10.7554/eLife.85581

Share this article

https://doi.org/10.7554/eLife.85581

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Further reading

    1. Cell Biology
    2. Physics of Living Systems

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

    Raphaël Etournay, Marko Popović ... Suzanne Eaton
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    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 constraints 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.

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    Oncogenic and teratogenic effects of Trp53Y217C, an inflammation-prone mouse model of the human hotspot mutant TP53Y220C

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