1. Developmental Biology
  2. Evolutionary Biology
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Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita

  1. Francesca Caroti
  2. Everardo González Avalos
  3. Viola Noeske
  4. Paula González Avalos
  5. Dimitri Kromm
  6. Maike Wosch
  7. Lucas Schütz
  8. Lars Hufnagel
  9. Steffen Lemke  Is a corresponding author
  1. Ruprecht Karls University, Germany
  2. Ruprecht Karls Universität, Germany
  3. European Molecular Biology Laboratory, Germany
Research Article
  • Cited 3
  • Views 837
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Cite this article as: eLife 2018;7:e34616 doi: 10.7554/eLife.34616

Abstract

Extraembryonic tissues contribute to animal development, which often entails spreading over embryo or yolk. Apart from changes in cell shape, the requirements for this tissue spreading are not well understood. Here we analyze spreading of the extraembryonic serosa in the scuttle fly Megaselia abdita. The serosa forms from a columnar blastoderm anlage, becomes a squamous epithelium, and eventually spreads over the embryo proper. We describe the dynamics of this process in long-term, whole-embryo time-lapse recordings, demonstrating that free serosa spreading is preceded by a prolonged pause in tissue expansion. Closer examination of this pause reveals mechanical coupling to the underlying yolk sac, which is later released. We find mechanical coupling prolonged and serosa spreading impaired after knockdown of M. abdita Matrix metalloprotease 1. We conclude that tissue-tissue interactions provide a critical functional element to constrain spreading epithelia.

Article and author information

Author details

  1. Francesca Caroti

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Everardo González Avalos

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Viola Noeske

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Paula González Avalos

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Dimitri Kromm

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Maike Wosch

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  7. Lucas Schütz

    Centre for Organismal Studies Heidelberg, Ruprecht Karls Universität, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. Lars Hufnagel

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  9. Steffen Lemke

    Centre for Organismal Studies Heidelberg, Ruprecht Karls University, Heidelberg, Germany
    For correspondence
    steffen.lemke@cos.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5807-2865

Funding

Deutsche Forschungsgemeinschaft (LE 2787/1-1)

  • Francesca Caroti
  • Paula González Avalos
  • Maike Wosch
  • Steffen Lemke

HSFP (RGY0082/2015)

  • Everardo González Avalos
  • Viola Noeske
  • Paula González Avalos

EMBL International PhD Programme

  • Dimitri Kromm

Center of Modeling and Simulation in the Biosciences , University of Heidelberg

  • Lars Hufnagel

HBIGS predoctoral fellowship

  • Lucas Schütz

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: December 22, 2017
  2. Accepted: October 24, 2018
  3. Accepted Manuscript published: October 30, 2018 (version 1)
  4. Version of Record published: November 12, 2018 (version 2)

Copyright

© 2018, Caroti 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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Further reading

    1. Developmental Biology
    2. Evolutionary Biology

    Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

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    Evolution of morphogenesis is generally associated with changes in genetic regulation. Here, we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.

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