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.
Data availability
Source data and code are provided for each figure
Article and author information
Author details
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
-
- 723
- views
-
- 165
- 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)
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
-
- Developmental Biology
- Genetics and Genomics
Smads and their transcription factor partners mediate the transcriptional responses of target cells to secreted ligands of the transforming growth factor-β (TGF-β) family, including those of the conserved bone morphogenetic protein (BMP) family, yet only a small number of direct target genes have been well characterized. In C. elegans, the BMP2/4 ortholog DBL-1 regulates multiple biological functions, including body size, via a canonical receptor-Smad signaling cascade. Here, we identify functional binding sites for SMA-3/Smad and its transcriptional partner SMA-9/Schnurri based on ChIP-seq peaks (identified by modEncode) and expression differences of nearby genes identified from RNA-seq analysis of corresponding mutants. We found that SMA-3 and SMA-9 have both overlapping and unique target genes. At a genome-wide scale, SMA-3/Smad acts as a transcriptional activator, whereas SMA-9/Schnurri direct targets include both activated and repressed genes. Mutations in sma-9 partially suppress the small body size phenotype of sma-3, suggesting some level of antagonism between these factors and challenging the prevailing model for Schnurri function. Functional analysis of target genes revealed a novel role in body size for genes involved in one-carbon metabolism and in the endoplasmic reticulum (ER) secretory pathway, including the disulfide reductase dpy-11. Our findings indicate that Smads and SMA-9/Schnurri have previously unappreciated complex genetic and genomic regulatory interactions that in turn regulate the secretion of extracellular components like collagen into the cuticle to mediate body size regulation.
-
- Developmental Biology
The articles in this special issue highlight the diversity and complexity of research into reproductive health, including the need for a better understanding of the fundamental biology of reproduction and for new treatments for a range of reproductive disorders.
