Alternating polarity integrates chemical and mechanical cues to drive tissue morphogenesis

Abstract

AbstractThe 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.Significance StatementTissue morphogenesis is driven by spatially patterned molecules; in many cases, this patterning is defined subcellularly, at the level of individual cellular edges. This study uncovers a pathway which integrates chemical signaling through actin and PI4P with mechanical force to generate alternating in-plane polarity in epithelial cells. This pathway is required for the formation of multiple epithelial tubes from a single primordium, and may be involved in other systems where repeating structures are formed from an initially uniform epithelium.