Alternating polarity integrates chemical and mechanical cues to drive tissue morphogenesis

The spatial patterning of molecules, such as actin, laminin, or polarity factors, within a sheet of cells directs morphogenesis in many epithelial tissues. How such molecular localization patterns are established and how they lead to specific tissue folding and three dimensional cell rearrangements in time and space is, however, still an open question in most cases. Here we focus on tissue morphogenesis during eggshell formation in a Scaptodrosophila species where specific cell rearrangements lead to the formation of up to eight long tubes called dorsal appendages. Previously, Par3/Bazooka and aPKC were previously shown to localize to a set of cell edges destined to elongate and form the base of each eggshell dorsal appendage. The present study establishes that the mechanism underlying this localization pattern is a spatially alternating, in-plane polarization of the cells. A candidate screen identified several potential molecular players, whose epistatic relationships were then examined using a custom culture assay. These experiments demonstrated that positive feedback between actin polymerization and PI4P production leads to polarization of these cells individually, while mechanical force coordinates polarization among these cells. This work adds to the growing evidence for a role of mechanics in cell polarity, and also provides an example where morphological differences between species can be understood at the level of fundamental cell biological processes.