Abstract
The flight muscles, dorsal air sacs, wing blades, and thoracic cuticle of the Drosophila adult function in concert, and their progenitor cells develop together in the wing imaginal disc. The wing disc orchestrates dorsal air sac development by producing decapentaplegic and fibroblast growth factor that travel via specific cytonemes in order to signal to the air sac primordium (ASP). Here, we report that cytonemes also link flight muscle progenitors (myoblasts) to disc cells and to the ASP, enabling myoblasts to relay signaling between the disc and the ASP. Frizzled (Fz)-containing myoblast cytonemes take up Wingless (Wg) from the disc, and Delta (Dl)-containing myoblast cytonemes contribute to Notch activation in the ASP. Wg signaling negatively regulates Dl expression in the myoblasts. These results reveal an essential role for cytonemes in Wg and Notch signaling and for a signal relay system in the myoblasts.DOI: http://dx.doi.org/10.7554/eLife.06114.001
Highlights
Flight muscles of the Drosophila adult drive the coordinated movements of the wings and thoracic cuticle to power flight, and many thin tubes that emanate from the thoracic dorsal air sacs penetrate the muscles to oxygenate them
These figures show that the distal air sac primordium (ASP) extended beyond the myoblast domain; cytonemes that emanate from the distal tip and that take up FGF from wing disc (Sato and Kornberg, 2002; Roy et al, 2011, 2014) were visible
Expression of diaRNAi reduced contacts between myoblasts and the ASP. These results suggest that the Dl-containing myoblast cytonemes present Delta to the ASP and make contacts that activate Notch signaling in the ASP
Summary
Flight muscles of the Drosophila adult drive the coordinated movements of the wings and thoracic cuticle to power flight, and many thin tubes (tracheoles) that emanate from the thoracic dorsal air sacs penetrate the muscles to oxygenate them. The progenitor cells that produce these tissues develop together in the wing imaginal disc. We describe two other signaling systems that coordinate the progenitors of the flight muscles with the wing disc and trachea. Myoblasts that are the progenitors of the flight muscles are at the basal surface of the columnar epithelium, underneath the basement membrane, and in the vicinity of the tracheal branches. They proliferate during L3 to extend over most of the dorsal part of the disc where the cells that will produce the notum cuticle grow (Sudarsan et al, 2001; Gunage et al, 2014)
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