Tip-Cell Migration Controls Stalk-Cell Intercalation during Drosophila Tracheal Tube Elongation

Abstract

Branching morphogenesis remodels epithelial tissues into tubular networks. This process is crucial to many organs, from the insect trachea to the vertebrate vasculature. Although Drosophila tracheal development has been well characterized morphologically and genetically, very little is known about the forces involved during morphogenesis. The repertoire of cell behaviors underlying tracheal primary branch remodeling is limited to cell migration, cell-shape changes, and stalk-cell intercalation (SCI), a process in which cells insert in between cells previously in contact with each other. Here, we identify the major forces that contribute to tracheal primary branch remodeling by using genetic and microsurgery experiments. As the tip cells migrate, they elongate the branches and create a tensile stress. This tensile stress triggers SCI, which, in turn, allows the branches to further elongate. The mechanism that we describe contrasts with "convergent extension by cell intercalation" acting during Drosophila germ band extension (GBE), where cell intercalation is the cause of epithelium elongation. Surprisingly, in tracheal branches, one or two leading cells produce enough mechanical power to intercalate many lagging cells. This may apply to other tubular networks.