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

Abstract
Data availability
Article and author information
Metrics

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

(2020) Single-cell transcriptomics of the Drosophila wing disc reveals instructive epithelium-tomyoblast interactions
NCBI Gene Expression Omnibus, GSE19373.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE155543

Article and author information

Author details

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.
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.

"This ORCID iD identifies the author of this article:" 0000-0001-9772-4985
Riku Yasutomi

Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2640-0462
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.

"This ORCID iD identifies the author of this article:" 0000-0001-9004-1225
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.

"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

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.