Abstract

Myogenesis is an evolutionarily conserved process. Little known, however, is how the morphology of each muscle is determined, such that movements relying upon contraction of many muscles are both precise and coordinated. Each Drosophila larval muscle is a single multinucleated fiber whose morphology reflects expression of distinctive identity Transcription Factors (iTFs). By deleting transcription cis-regulatory modules of one iTF, Collier, we generated viable muscle identity mutants, allowing live imaging and locomotion assays. We show that both selection of muscle attachment sites and muscle/muscle matching is intrinsic to muscle identity and requires transcriptional reprogramming of syncytial nuclei. Live-imaging shows that the staggered muscle pattern involves attraction to tendon cells and heterotypic muscle-muscle adhesion. Unbalance leads to formation of branched muscles, and this correlates with locomotor behavior deficit. Thus, engineering Drosophila muscle identity mutants allows to investigate, in vivo, physiological and mechanical properties of abnormal muscles.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Alexandre Carayon

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Laetitia Bataillé

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Gaëlle Lebreton

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Laurence Dubois

    UMR 5547, Univeristé de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Aurore Pelletier

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Yannick Carrier

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Antoine Wystrach

    CBI CRCA, French National Centre for Scientific Research, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Alain Vincent

    Centre de Biologie du Développement, Université de Toulouse, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2769-7501
  9. Jean-Louis Frendo

    CBI UMR 5547, Université de Toulouse, French National Centre for Scientific Research, Toulouse, France
    For correspondence
    jean-louis.frendo@univ-tlse3.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0118-5556

Funding

Centre National de la Recherche Scientifique

  • Alexandre Carayon
  • Laetitia Bataillé
  • Gaëlle Lebreton
  • Laurence Dubois
  • Aurore Pelletier
  • Yannick Carrier
  • Antoine Wystrach
  • Alain Vincent
  • Jean-Louis Frendo

Centre de Biologie Integrative de Toulouse (AOCBI2018)

  • Jean-Louis Frendo

AFM-Téléthon (Research grant 21887)

  • Alain Vincent

Agence Nationale de la Recherche (13-BSVE2-0010-01)

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

Version history

  1. Received: April 3, 2020
  2. Accepted: July 23, 2020
  3. Accepted Manuscript published: July 24, 2020 (version 1)
  4. Version of Record published: August 17, 2020 (version 2)

Copyright

© 2020, Carayon 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. Alexandre Carayon
  2. Laetitia Bataillé
  3. Gaëlle Lebreton
  4. Laurence Dubois
  5. Aurore Pelletier
  6. Yannick Carrier
  7. Antoine Wystrach
  8. Alain Vincent
  9. Jean-Louis Frendo
(2020)
Intrinsic control of muscle attachment sites matching
eLife 9:e57547.
https://doi.org/10.7554/eLife.57547

Share this article

https://doi.org/10.7554/eLife.57547

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