Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing
- Max Planck Institute of Molecular Cell Biology and Genetics, Germany
- University of Dundee, United Kingdom
- Laboratoire Physico-Chimie Curie, Institut Curie, France
- Center for Systems Biology Dresden, Germany
- Max Planck Institute for the Physics of Complex Systems, Germany
- 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.
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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.
Reviewing Editor
- Marcos Nahmad, Center for Research and Advanced Studies (Cinvestav), Mexico
Version history
- Preprint posted: December 10, 2022 (view preprint)
- Received: December 15, 2022
- Accepted: December 18, 2023
- Accepted Manuscript published: December 20, 2023 (version 1)
- Version of Record published: February 2, 2024 (version 2)
- Version of Record updated: February 5, 2024 (version 3)
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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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
Further reading
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- Developmental Biology
- Physics of Living Systems
Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.
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