Correct regionalisation of a tissue primordium is essential for coordinated morphogenesis

  1. Yara Sanchez-Corrales
  2. Guy B Blanchard
  3. Katja Röper  Is a corresponding author
  1. MRC Laboratory of Molecular Biology, United Kingdom
  2. University of Cambridge, United Kingdom

Abstract

During organ development, tubular organs often form from flat epithelial primordia. In the placodes of the forming tubes of the salivary glands in the Drosophila embryo, we previously identified spatially defined cell behaviours of cell wedging, tilting and cell intercalation that are key to the initial stages of tube formation. Here we address what the requirements are that ensure the continuous formation of a narrow symmetrical tube from an initially asymmetrical primordium whilst overall tissue geometry is constantly changing. We are using live-imaging and quantitative methods to compare wild-type placodes and mutants that either show disrupted cell behaviours or an initial symmetrical placode organisation, with both resulting in severe impairment of the invagination. We find that early transcriptional patterning of key morphogenetic transcription factors drives the selective activation of downstream morphogenetic modules, such as GPCR signalling that activates apical-medial actomyosin activity to drive cell wedging at the future asymmetrically-placed invagination point. Over time, transcription of key factors expands across the rest of the placode and cells switch their behaviour from predominantly intercalating to predominantly apically constricting as their position approaches the invagination pit. Misplacement or enlargement of the initial invagination pit leads to early problems in cell behaviours that eventually result in a defective organ shape. Our work illustrates that the dynamic patterning of the expression of transcription factors and downstream morphogenetic effectors ensures positionally fixed areas of cell behaviour with regards to the invagination point. This patterning in combination with the asymmetric geometrical set-up ensures functional organ formation.

Data availability

All data generated and analysed in the manuscript are included in the manuscript and supporting files.

Article and author information

Author details

  1. Yara Sanchez-Corrales

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Guy B Blanchard

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3689-0522
  3. Katja Röper

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    kroeper@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3361-766X

Funding

Medical Research Council (U105178780)

  • Yara Sanchez-Corrales
  • Katja Röper

Wellcome Trust (207553/Z/17/Z)

  • Guy B Blanchard

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

Reviewing Editor

  1. Danelle Devenport, Princeton University, United States

Publication history

  1. Preprint posted: August 29, 2020 (view preprint)
  2. Received: July 21, 2021
  3. Accepted: October 31, 2021
  4. Accepted Manuscript published: November 1, 2021 (version 1)
  5. Version of Record published: November 17, 2021 (version 2)

Copyright

© 2021, Sanchez-Corrales 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. Yara Sanchez-Corrales
  2. Guy B Blanchard
  3. Katja Röper
(2021)
Correct regionalisation of a tissue primordium is essential for coordinated morphogenesis
eLife 10:e72369.
https://doi.org/10.7554/eLife.72369
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