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

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.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE155543 | GEO | 2021/03/23

REPOSITORIES: GEO

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Project description:The highly conserved Epidermal Growth Factor-receptor (Egfr) pathway is required in all animals for normal development and homeostasis; consequently, aberrant Egfr signaling is implicated in a number of diseases. Genetic analysis of Drosophila melanogaster Egfr has contributed significantly to understanding this conserved pathway and has led to the discovery of new components and targets. Here we used microarray analysis of Drosophila third instar wing discs, in which Egfr signaling was perturbed, to identify new Egfr-responsive genes. Upregulated transcripts included five known targets suggesting the approach was valid. We investigated the function of 29 previously uncharacterized genes, which had pronounced responses. The Egfr pathway is important for wing-vein patterning and using reverse genetic analysis we identified five genes that showed venation defects. Three of these genes are expressed in vein primordia and all showed transcriptional changes in response to altered Egfr activity consistent with being targets of the pathway. Genetic interactions with Egfr further linked two of the genes, Sulfated (Sulf1), an endosulfatase gene, and CG4096, an ADAMTS (A Disintegrin And Metalloproteinase with ThromboSpondin motifs) gene, to the pathway. Sulf1 showed a strong genetic interaction with the neuregulin-like ligand vein (vn) and may influence binding of Vn to heparan-sulfated proteoglycans (HSPGs). Genetic evidence also shows that CG4096 functions by modulating activity of the Egfr ligands. The substrate(s) and how ligand activity is affected are unknown, but interestingly vertebrate EGF ligands are regulated by a related ADAMTS protein. We conclude Sulf1 and CG4096 are negative feedback regulators of Egfr signaling that function in the extracellular space to influence ligand activity. 3 replicates each of wing disc samples in which EGFR dominant negative (EGFR-DN) or EGFR activated (EGFR-TOP) transgenes were expressed with the 71B-Gal4 driver.

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

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