What basal membranes can tell us about viscous forces in Drosophila ventral furrow formation

Abstract

Ventral furrow (VF) formation in Drosophila melanogaster is an important model of epithelial folding. Previous models of VF formation require cell volume conservation to convert apically localized constriction forces into lateral cell elongation and tissue folding. Here, we investigated embryonic morphogenesis in anillin knockdown (scra RNAi) embryos, where basal cell membranes fail to form and therefore cells can lose cytoplasmic volume through their basal side. Surprisingly, the mesoderm elongation and subsequent folding that comprise VF formation occurred essentially normally. We hypothesized that the effects of viscous shear may be sufficient to drive membrane elongation, providing effective volume conservation, and thus driving tissue folding. Since this hypothesis may not be possible to test experimentally, we turned to a computational approach. A minimal model of VF formation accounting for fluid dynamics indicated that shear forces can indeed explain our experimental observation. However, this conclusion depended on specific values of the model parameters. To test whether viscous shear is a dominant force for morphogenesis in vivo, we developed a highly realistic computational model incorporating both accurate cell and tissue geometry and experimentally measured material parameters. Results from this model demonstrate that viscous shear generates sufficient force to drive cell elongation and tissue folding in vivo.