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

  • 790
    views
  • 170
    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
    Bin Zhu, Rui Wei ... Pei Liang
    Research Article

    Wing dimorphism is a common phenomenon that plays key roles in the environmental adaptation of aphid; however, the signal transduction in response to environmental cues and the regulation mechanism related to this event remain unknown. Adenosine (A) to inosine (I) RNA editing is a post-transcriptional modification that extends transcriptome variety without altering the genome, playing essential roles in numerous biological and physiological processes. Here, we present a chromosome-level genome assembly of the rose-grain aphid Metopolophium dirhodum by using PacBio long HiFi reads and Hi-C technology. The final genome assembly for M. dirhodum is 447.8 Mb, with 98.50% of the assembled sequences anchored to nine chromosomes. The contig and scaffold N50 values are 7.82 and 37.54 Mb, respectively. A total of 18,003 protein-coding genes were predicted, of which 92.05% were functionally annotated. In addition, 11,678 A-to-I RNA-editing sites were systematically identified based on this assembled M. dirhodum genome, and two synonymous A-to-I RNA-editing sites on CYP18A1 were closely associated with transgenerational wing dimorphism induced by crowding. One of these A-to-I RNA-editing sites may prevent the binding of miR-3036-5p to CYP18A1, thus elevating CYP18A1 expression, decreasing 20E titer, and finally regulating the wing dimorphism of offspring. Meanwhile, crowding can also inhibit miR-3036-5p expression and further increase CYP18A1 abundance, resulting in winged offspring. These findings support that A-to-I RNA editing is a dynamic mechanism in the regulation of transgenerational wing dimorphism in aphids and would advance our understanding of the roles of RNA editing in environmental adaptability and phenotypic plasticity.

    1. Developmental Biology
    Hanee Lee, Junsu Kang ... Junho Lee
    Research Article

    The evolutionarily conserved Hippo (Hpo) pathway has been shown to impact early development and tumorigenesis by governing cell proliferation and apoptosis. However, its post-developmental roles are relatively unexplored. Here, we demonstrate its roles in post-mitotic cells by showing that defective Hpo signaling accelerates age-associated structural and functional decline of neurons in Caenorhabditis elegans. Loss of wts-1/LATS, the core kinase of the Hpo pathway, resulted in premature deformation of touch neurons and impaired touch responses in a yap-1/YAP-dependent manner, the downstream transcriptional co-activator of LATS. Decreased movement as well as microtubule destabilization by treatment with colchicine or disruption of microtubule-stabilizing genes alleviated the neuronal deformation of wts-1 mutants. Colchicine exerted neuroprotective effects even during normal aging. In addition, the deficiency of a microtubule-severing enzyme spas-1 also led to precocious structural deformation. These results consistently suggest that hyper-stabilized microtubules in both wts-1-deficient neurons and normally aged neurons are detrimental to the maintenance of neuronal structural integrity. In summary, Hpo pathway governs the structural and functional maintenance of differentiated neurons by modulating microtubule stability, raising the possibility that the microtubule stability of fully developed neurons could be a promising target to delay neuronal aging. Our study provides potential therapeutic approaches to combat age- or disease-related neurodegeneration.