Planar cell polarity-directed cell crawling drives polarized epithelial morphogenesis

During epithelial morphogenesis, cell polarity aligns individual cell behaviors into collective motions that shape developing tissues. Here, we combine experiments with computational modeling to investigate how cell-scale forces oriented by planar cell polarity (PCP) direct the collective, counter-rotational cell flows that occur during hair placode morphogenesis. Unexpectedly, we find that junctional myosin and PCP protein localization are not co-correlated with junction shrinkage, indicating the role of PCP during placode polarization is not to direct apical neighbor exchanges. Instead, we find that PCP directs anterior-directed crawling of placode cells along the basal surface of the tissue through a mechanism that requires integrins and the cell-crawling regulator Rac1. Modeling the placode as a three-dimensional continuum viscoelastic fluid, we find that active forces from cell crawling at the basal surface are sufficient to generate the experimentally observed counter-rotational cell motion at the apical surface. Our results show an unexpected role for PCP in epithelial morphogenesis, centering the basal surface as the site of force generation.