Dpp controls growth and patterning in Drosophila wing precursors through distinct modes of action

  1. Pablo Sanchez Bosch
  2. Ruta Ziukaite
  3. Cyrille Alexandre
  4. Konrad Basler
  5. Jean-Paul B Vincent  Is a corresponding author
  1. University of Zurich, Switzerland
  2. The Francis Crick Institute, United Kingdom
  3. Institute of Molecular Life Sciences, Switzerland

Abstract

Dpp, a member of the BMP family, is a morphogen that specifies positional information in Drosophila wing precursors. In this tissue, Dpp expressed along the anterior-posterior boundary forms a concentration gradient that controls the expression domains of target genes, which in turn specify the position of wing veins. Dpp also promotes growth in this tissue. The relationship between the spatio-temporal profile of Dpp signalling and growth has been the subject of debate, which has intensified recently with the suggestion that the stripe of Dpp is dispensable for growth. With two independent conditional alleles of dpp we find that the stripe of Dpp is essential for wing growth. We then show that this requirement, but not patterning, can be fulfilled by uniform, low level, Dpp expression. Thus, the stripe of Dpp ensures that signalling remains above a pro-growth threshold, while at the same time generating a gradient that patterns cell fates.

Article and author information

Author details

  1. Pablo Sanchez Bosch

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0574-4530
  2. Ruta Ziukaite

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Cyrille Alexandre

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Konrad Basler

    University of Zurich, Institute of Molecular Life Sciences, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Jean-Paul B Vincent

    The Francis Crick Institute, London, United Kingdom
    For correspondence
    jp.vincent@crick.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2305-5744

Funding

Medical Research Council (FC001204)

  • Jean-Paul B Vincent

European Research Council (WNTEXPORT 294523)

  • Jean-Paul B Vincent

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Unknown)

  • Konrad Basler

Wellcome (PhD Studentship 105382/Z/14/Z)

  • Ruta Ziukaite

Wellcome (FC001204)

  • Jean-Paul B Vincent

Cancer Research UK (FC001204)

  • Jean-Paul B Vincent

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

Reviewing Editor

  1. Utpal Banerjee, University of California, Los Angeles, United States

Version history

  1. Received: October 21, 2016
  2. Accepted: June 4, 2017
  3. Accepted Manuscript published: July 4, 2017 (version 1)
  4. Version of Record published: August 17, 2017 (version 2)

Copyright

© 2017, Sanchez Bosch 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

  • 3,500
    Page views
  • 648
    Downloads
  • 44
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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. Pablo Sanchez Bosch
  2. Ruta Ziukaite
  3. Cyrille Alexandre
  4. Konrad Basler
  5. Jean-Paul B Vincent
(2017)
Dpp controls growth and patterning in Drosophila wing precursors through distinct modes of action
eLife 6:e22546.
https://doi.org/10.7554/eLife.22546

Share this article

https://doi.org/10.7554/eLife.22546

Further reading

    1. Cell Biology
    2. Developmental Biology
    Shinya Matsuda, Markus Affolter
    Short Report Updated

    The Dpp morphogen gradient derived from the anterior stripe of cells is thought to control growth and patterning of the Drosophila wing disc. However, the spatial-temporal requirement of dpp for growth and patterning remained largely unknown. Recently, two studies re-addressed this question. By generating a conditional null allele, one study proposed that the dpp stripe is critical for patterning but not for growth (Akiyama and Gibson, 2015). In contrast, using a membrane-anchored nanobody to trap Dpp, the other study proposed that Dpp dispersal from the stripe is required for patterning and also for medial wing disc growth, at least in the posterior compartment (Harmansa et al., 2015). Thus, growth control by the Dpp morphogen gradient remains under debate. Here, by removing dpp from the stripe at different time points, we show that the dpp stripe source is indeed required for wing disc growth, also during third instar larval stages.

    1. Cell Biology
    2. Physics of Living Systems
    Jorge de-Carvalho, Sham Tlili ... Ivo A Telley
    Research Article

    Microtubule asters are essential in localizing the action of microtubules in processes including mitosis and organelle positioning. In large cells, such as the one-cell sea urchin embryo, aster dynamics are dominated by hydrodynamic pulling forces. However, in systems with more densely positioned nuclei such as the early Drosophila embryo, which packs around 6000 nuclei within the syncytium in a crystalline-like order, it is unclear what processes dominate aster dynamics. Here, we take advantage of a cell cycle regulation Drosophila mutant to generate embryos with multiple asters, independent from nuclei. We use an ex vivo assay to further simplify this biological system to explore the forces generated by and between asters. Through live imaging, drug and optical perturbations, and theoretical modeling, we demonstrate that these asters likely generate an effective pushing force over short distances.