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

Author:

Everetts Nicholas J12ORCID,Worley Melanie I1ORCID,Yasutomi Riku1ORCID,Yosef Nir2ORCID,Hariharan Iswar K1ORCID

Affiliation:

1. Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

2. Department of Electrical Engineering & Computer Science, Center for Computational Biology, UC Berkeley, University of California, Berkeley, 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 theDrosophilawing disc from two developmental time points. Using these data, we visualized gene expression using a multilayered model of the wing disc and cataloged ligand–receptor pairs that could mediate signaling between epithelial cells and adult muscle precursors (AMPs). We found that localized expression of the fibroblast growth factor 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 targetsNeurotactinandmidline, 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.

Funder

National Institutes of Health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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