Myoblast cytonemes mediate Wg signaling from the wing imaginal disc and Delta-Notch signaling to the air sac primordium

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

eLife digest

Fruit fly larvae undergo a remarkable physical transformation to become an adult fly. During this transformation, the tissues in the larvae change into the structures found in the adult. For example, the adult wings, flight muscles, and other structures needed for coordinated flight form from a pair of disc-like tissues called the wing imaginal discs.

For these structures to develop correctly, the cells in the wing imaginal discs need to receive coordinated instructions about what types of cells they need to become. Within the wing discs, finger-like projections called cytonemes link specific cells together to allow signal molecules to move between the cells; this controls the development of the wing disc itself as well as structures called dorsal air sacs, which supply oxygen to the flight muscles in the adult fly. However, it is not known if cytonemes allow the exchange of signal molecules between cells involved in the formation of other structures needed for flight.

Here, Huang and Kornberg investigated the role of cytonemes in the development of the flight muscles in fruit flies. The experiments reveal that cells called myoblasts—which will later become the flight muscle cells—form two sets of cytonemes with other cells. One set connects the myoblasts to cells in the developing air sac, which allows a signal protein called Delta to signal from the myoblasts into the air sac cells. The other set of cytonemes connects the myoblasts to wing disc cells. This enables another signal molecule called Wingless, which is produced in wing disc cells, to move into the myoblasts and block the production of Delta.

Huang and Kornberg's findings reveal a new role for cytonemes in coordinating the development of the flight muscles and the dorsal air sacs. A future challenge will be to understand how individual cytonemes are able to connect to specific cells.

DOI: http://dx.doi.org/10.7554/eLife.06114.002