The processes that generate cellular morphology are not well understood. To investigate this problem, we use Drosophila melanogaster tracheal terminal cells, which undergo two distinct morphogenetic processes: subcellular branching morphogenesis and subcellular apical lumen formation. Here we show these processes are regulated by components of the PAR-polarity complex. This complex, composed of the proteins Par-6, Bazooka (Par-3), aPKC, and Cdc42, is best known for roles in asymmetric cell division and apical/basal polarity. We find Par-6, Bazooka, and aPKC, as well as known interactions between them, are required for subcellular branch initiation, but not for branch outgrowth. By analysis of single and double mutants, and isolation of two novel alleles of Par-6, one of which specifically truncates the Par-6 PDZ domain, we conclude that dynamic interactions between apical PAR-complex members control the branching pattern of terminal cells. These data suggest that canonical apical PAR-complex activity is required for subcellular branching morphogenesis. In addition, we find the PAR proteins are downstream of the FGF pathway that controls terminal cell branching. In contrast, we find that while Par-6 and aPKC are both required for subcellular lumen formation, neither Bazooka nor a direct interaction between Par-6 and aPKC is needed for this process. Thus a novel, noncanonical role for the polarity proteins Par-6 and aPKC is used in formation of this subcellular apical compartment. Our results demonstrate that proteins from the PAR complex can be deployed independently within a single cell to control two different morphogenetic processes.
FOR most cell types, morphology is key to cell function. A dramatic example of this association is seen in cells that undergo subcellular branching morphogenesis. In this process, cells send out extensions from their plasma membranes, which grow and undergo bifurcation events to form complex, branched networks. Examples of subcellular branching morphogenesis are seen in glial oligodendrocytes (Bauer et al. 2009) and in dendritic cells of the mammalian immune system (Makala and Nagasawa 2002), but by far the best studied examples of this process are in neurons (reviewed by Gibson and Ma 2011;Jan and Jan 2010). Indeed, neurons are frequently categorized entirely by differences in their branching morphologies (see Puelles 2009). However, despite the importance of subcellular branching morphogenesis, little is known about the molecular mechanisms that organize distinctive subcellular branching patterns.We are studying the process of subcellular branching morphogenesis in Drosophila tracheal terminal cells, a component of the insect respiratory system. Terminal cells reside at the ends of a network of cellular tubes that functions in delivering air to internal tissues (Guillemin et al. 1996). The cells are specified during embryogenesis, primarily through a process of competitive FGF signaling and lateral inhibition among tracheal precursors (Llimargas 1999;Ghabrial and Krasno...