Single-cell transcriptomics of the Drosophila wing disc reveals instructive epithelium-to-myoblast interactions

  1. Nicholas J Everetts
  2. Melanie I Worley
  3. Riku Yasutomi
  4. Nir Yosef  Is a corresponding author
  5. Iswar K Hariharan  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

In both vertebrates and invertebrates, generating a functional appendage requires interactions between ectoderm-derived epithelia and mesoderm-derived cells. To investigate such interactions, we used single-cell transcriptomics to generate a temporal cell atlas of the Drosophila wing disc from two developmental time points. Using these data, we visualized gene expression using a multi-layered model of the wing disc and catalogued ligand-receptor pairs that could mediate signaling between epithelial cells and adult muscle precursors (AMPs). We found that localized expression of the FGF ligands, Thisbe and Pyramus, in the disc epithelium regulates the number and location of the AMPs. In addition, Hedgehog ligand from the epithelium activates a specific transcriptional program within adjacent AMP cells, defined by AMP-specific targets Neurotactin and midline, that is critical for proper formation of direct flight muscles. More generally, our annotated temporal cell atlas provides an organ-wide view of potential cell-cell interactions between epithelial and myogenic cells.

Data availability

Sequencing data and aligned matrices have deposited in GEO (accession code GSE155543). Code will be accessible at https://github.com/HariharanLab/Everetts_Worley_Yasutomi. All other data generated are included in the manuscript and supporting files.

The following data sets were generated

Article and author information

Author details

  1. Nicholas J Everetts

    Department of Molecular and Cell Biology, Department of Electrical Engineering and Computer Science, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Melanie I Worley

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9772-4985
  3. Riku Yasutomi

    Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2640-0462
  4. Nir Yosef

    Department of Electrical Engineering and Computer Science and the Center for Computational Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    niryosef@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9004-1225
  5. Iswar K Hariharan

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    ikh@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6505-0744

Funding

National Institutes of Health (R35 GM122490)

  • Iswar K Hariharan

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

Copyright

© 2021, Everetts 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. Nicholas J Everetts
  2. Melanie I Worley
  3. Riku Yasutomi
  4. Nir Yosef
  5. Iswar K Hariharan
(2021)
Single-cell transcriptomics of the Drosophila wing disc reveals instructive epithelium-to-myoblast interactions
eLife 10:e61276.
https://doi.org/10.7554/eLife.61276

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https://doi.org/10.7554/eLife.61276

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