Temporal control of structure and function during seamless tubulogenesis in the Drosophila respiratory system

The respiratory system of Drosophila melanogaster consists of a network of interconnected gas-filled epithelial tubes. Stellate-shaped terminal cells at the termini of each tracheal branch serve as the primary source of oxygen and grow continuously throughout larval stages in response to hypoxic signals. Each cytoplasmic branch of a terminal cell hollows out to form subcellular seamless tubes that lack epithelial junctions. It is known that over the course of larval development, tracheal terminal cells grow by extending new branches and lengthening existing branches. By the end of larval development, each branch of these highly ramified cells contains a subcellular lumen; the relationship between branch and tube extension over this period of immense growth has yet to be explored. Here we demonstrate that branch extension and intracellular lumen formation are spatially and temporally coupled throughout larval stages, however, nascent tubes formed during a larval instar are fluid-filled and do not inflate with air until the following molt. This has interesting implications for the delivery of oxygen to target tissues during the first 48 h of larval growth.