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

Nicholas J Everetts,Nir Yosef,Melanie I Worley,Iswar K Hariharan,Riku Yasutomi

doi:10.7554/elife.61276

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 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 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.

Highlights

The development of multicellular eukaryotes gives rise to organs that are composed of cells of many types, typically derived from different germ layers such as the ectoderm and the mesoderm
The wing-imaginal disc is composed of epithelial cells that form a sac-like structure and a population of adult muscle precursors (AMPs) that resides between the epithelial cells of the disc proper and the underlying basement membrane (Figure 1A)
We show that fibroblast growth factor (FGF) ligands emanating from the disc epithelium create an AMP niche that regulates AMP numbers and restricts them to the region of the notum

Summary

Introduction

The development of multicellular eukaryotes gives rise to organs that are composed of cells of many types, typically derived from different germ layers such as the ectoderm and the mesoderm. While vertebrate limbs are relatively complex structures, the Drosophila wing-imaginal disc, the larval primordium of the adult wing and thorax, is ideally suited to the study of cell–cell interactions in the context of organ development because of its relative simplicity and amenability to genetic analysis (Waddington, 1940; Cohen, 1993; Neto-Silva et al, 2009). The epithelial portion of the disc derives from a primordium of approximately 30 cells from the embryonic ectoderm that are specified during embryogenesis (Mandaravally Madhavan and Schneiderman, 1977; Worley et al, 2013; Requena et al, 2017). The AMPs, originally referred to as adepithelial cells (Poodry and Schneiderman, 1970), represent a subset of cells from the embryonic mesoderm that generate the adult flight muscles

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