A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology

  1. Jérôme Lacoste  Is a corresponding author
  2. Hédi Soula
  3. Angélique Burg
  4. Agnès Audibert
  5. Pénélope Darnat
  6. Michel Gho  Is a corresponding author
  7. Sophie Louvet-Vallée  Is a corresponding author
  1. CNRS Sorbonne-Université, France
  2. Sorbonne Université, INSERM, France

Abstract

Spatiotemporal mechanisms generating neural diversity are fundamental for understanding neural processes. Here, we investigated how neural diversity arises from neurons coming from identical progenitors. In the dorsal thorax of Drosophila, rows of mechanosensory organs originate from the division of sensory organ progenitor (SOPs). We show that in each row of the notum, an anteromedial located central SOP divides first, then neighbouring SOPs divide, and so on. This centrifugal wave of mitoses depends on cell-cell inhibitory interactions mediated by SOP cytoplasmic protrusions and Scabrous, a secreted protein interacting with the Delta/Notch complex. Furthermore, when this mitotic wave was reduced, axonal growth was more synchronous, axonal terminals had a complex branching pattern and fly behaviour was impaired. We show that the temporal order of progenitor divisions influences the birth order of sensory neurons, axon branching and impact on grooming behaviour. These data support the idea that developmental timing controls axon wiring neural diversity.

Data availability

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

Article and author information

Author details

  1. Jérôme Lacoste

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    For correspondence
    jerome.lacoste@sorbonne-universite.fr
    Competing interests
    The authors declare that no competing interests exist.
  2. Hédi Soula

    NutriOmics Research Unit, Sorbonne Université, INSERM, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Angélique Burg

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Agnès Audibert

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Pénélope Darnat

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Michel Gho

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    For correspondence
    michel.gho@sorbonne-universite.fr
    Competing interests
    The authors declare that no competing interests exist.
  7. Sophie Louvet-Vallée

    UMR 7622 laboratory of Developmental Biology, CNRS Sorbonne-Université, Paris, France
    For correspondence
    sophie.louvet_vallee@sorbonne-universite.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7577-2329

Funding

Funding was provided by recurrent subsides from the Centre National de la Recherche Scientifique and the Sorbonne University. No external funding was receives for this work.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Publication history

  1. Preprint posted: March 10, 2021 (view preprint)
  2. Received: November 22, 2021
  3. Accepted: March 6, 2022
  4. Accepted Manuscript published: March 7, 2022 (version 1)
  5. Version of Record published: March 18, 2022 (version 2)

Copyright

© 2022, Lacoste 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. Jérôme Lacoste
  2. Hédi Soula
  3. Angélique Burg
  4. Agnès Audibert
  5. Pénélope Darnat
  6. Michel Gho
  7. Sophie Louvet-Vallée
(2022)
A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
eLife 11:e75746.
https://doi.org/10.7554/eLife.75746
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