1. Cell Biology
  2. Developmental Biology
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Dpp from the anterior stripe of cells is crucial for the growth of the Drosophila wing disc

  1. Shinya Matsuda  Is a corresponding author
  2. Markus Affolter  Is a corresponding author
  1. Biozentrum der Universität Basel, Switzerland
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Cite this article as: eLife 2017;6:e22319 doi: 10.7554/eLife.22319

Abstract

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. 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. 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.

Article and author information

Author details

  1. Shinya Matsuda

    Biozentrum der Universität Basel, Basel, Switzerland
    For correspondence
    shinya.matsuda@unibas.ch
    Competing interests
    The authors declare that no competing interests exist.
  2. Markus Affolter

    Biozentrum der Universität Basel, Basel, Switzerland
    For correspondence
    markus.affolter@unibas.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5171-0016

Funding

Basel-Stadt

  • Markus Affolter

Basel-Land

  • Markus Affolter

JSPS postdoctoral fellowship for research abroad

  • Shinya Matsuda

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

Publication history

  1. Received: October 12, 2016
  2. Accepted: June 4, 2017
  3. Accepted Manuscript published: July 4, 2017 (version 1)
  4. Accepted Manuscript updated: July 5, 2017 (version 2)
  5. Version of Record published: August 17, 2017 (version 3)

Copyright

© 2017, Matsuda & Affolter

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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Further reading

    1. Cell Biology
    2. Developmental Biology
    Pablo Sanchez Bosch et al.
    Research Article Updated

    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.

    1. Cell Biology
    Ian F Price et al.
    Research Article Updated

    The germ line produces gametes that transmit genetic and epigenetic information to the next generation. Maintenance of germ cells and development of gametes require germ granules—well-conserved membraneless and RNA-rich organelles. The composition of germ granules is elusive owing to their dynamic nature and their exclusive expression in the germ line. Using Caenorhabditis elegans germ granule, called P granule, as a model system, we employed a proximity-based labeling method in combination with mass spectrometry to comprehensively define its protein components. This set of experiments identified over 200 proteins, many of which contain intrinsically disordered regions (IDRs). An RNA interference-based screen identified factors that are essential for P granule assembly, notably EGGD-1 and EGGD-2, two putative LOTUS-domain proteins. Loss of eggd-1 and eggd-2 results in separation of P granules from the nuclear envelope, germline atrophy, and reduced fertility. We show that IDRs of EGGD-1 are required to anchor EGGD-1 to the nuclear periphery while its LOTUS domains are required to promote the perinuclear localization of P granules. Taken together, our work expands the repertoire of P granule constituents and provides new insights into the role of LOTUS-domain proteins in germ granule organization.