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

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.

Data availability

Source data and code are provided for each figure

Article and author information

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.

Metrics

  • 744
    views
  • 169
    downloads
  • 1
    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. 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

Further reading

    1. Developmental Biology
    Yanlin Hou, Zhengwen Nie ... Hans R Scholer
    Research Article

    During the first lineage segregation, mammalian embryos generate the inner cell mass (ICM) and trophectoderm (TE). ICM gives rise to the epiblast (EPI) that forms all cell types of the body, an ability referred to as pluripotency. The molecular mechanisms that induce pluripotency in embryos remain incompletely elucidated. Using knockout (KO) mouse models in conjunction with low-input ATAC-seq and RNA-seq, we found that Oct4 and Sox2 gradually come into play in the early ICM, coinciding with the initiation of Sox2 expression. Oct4 and Sox2 activate the pluripotency-related genes through the putative OCT-SOX enhancers in the early ICM. Furthermore, we observed a substantial reorganization of chromatin landscape and transcriptome from the morula to the early ICM stages, which was partially driven by Oct4 and Sox2, highlighting their pivotal role in promoting the developmental trajectory toward the ICM. Our study provides new insights into the establishment of the pluripotency network in mouse preimplantation embryos.

    1. Developmental Biology
    Yufei Wu, Sean X Sun
    Insight

    Proteins that allow water to move in and out of cells help shape the development of new blood vessels.