Editors' ChoiceDevelopment

Guided by the Dying

Science Signaling  14 Jan 2014:
Vol. 7, Issue 308, pp. ec8
DOI: 10.1126/scisignal.2005064

During metamorphosis, the larval tissues of holometabolous insects such as the fruit fly Drosophila melanogaster are degraded and replaced by adult tissues formed by the proliferation and differentiation of stem cells. Chen and Krasnow demonstrate that growth of the adult Drosophila tracheal system in pupae from tracheal imaginal progenitor cells relies on the same growth factor signaling that guides tracheal development in the embryo. Tracheal imaginal progenitor cells, which arise during embryogenesis, migrated from their niche and along existing larval tracheal branches to form the posterior portion of the pupal abdominal tracheal system. This stereotyped migration required expression of branchless (bnl) in the larval tracheal cells and breathless (btl) in the migrating progenitor cells. Bnl is a fibroblast growth factor (FGF) that binds to the FGF receptor Btl. bnl expression in larval tracheae was temporally and spatially dynamic, with bnl expression appearing along the route as the progenitor cells migrated. Knocking down bnl in larval tracheal cells or expressing a dominant-negative form of Btl in tracheal progenitor cells prevented migration and reduced or eliminated formation of new tracheae. Ectopic expression of bnl in larval tracheae caused migrating tracheal progenitor cells to reorient toward the source of expression, and inducing ectopic expression of bnl in tracheal progenitor cells themselves halted their migration. This system recapitulates the one that directs development of the larval tracheal system during embryogenesis. Whereas tracheal outgrowth in the embryo is driven by Bnl produced in cells surrounding the trachea, tracheal outgrowth in the pupa is driven by Bnl produced by the decaying tracheal system that was itself initially induced by Bnl in the embryo. This developmental program redeployment allows a tissue that is destined for destruction to direct the formation of its replacement.

F. Chen, M. A. Krasnow, Progenitor outgrowth from the niche in Drosophila trachea is guided by FGF from decaying branches. Science 343, 186–189 (2014). [Abstract] [Full Text]