Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction

Abstract

During Drosophila embryogenesis, the germband first extends to curl around the posterior end of the embryo and then retracts back; however, retraction is not simply the reversal of extension. At a tissue level, extension is coincident with ventral furrow formation, and at a cellular level, extension occurs via convergent cell neighbor exchanges in the germband, whereas retraction involves only changes in cell shape. To understand how cell shapes, tissue organization, and cellular forces drive germband retraction, we investigate this process using a whole-embryo, surface-wrapped cellular finite-element model. This model represents two key epithelial tissues—amnioserosa and germband—as adjacent sheets of two-dimensional cellular finite elements that are wrapped around an ellipsoidal three-dimensional approximation of an embryo. The model reproduces the detailed kinematics of in vivo retraction by fitting just one free model parameter, the tension along germband cell interfaces; all other cellular forces are constrained to follow ratios inferred from experimental observations. With no additional parameter adjustments, the model also reproduces quantitative assessments of mechanical stress using laser dissection and failures of retraction when amnioserosa cells are removed via mutations or microsurgery. Surprisingly, retraction in the model is robust to changes in cellular force values but is critically dependent on starting from a configuration with highly elongated amnioserosa cells. Their extreme cellular elongation is established during the prior process of germband extension and is then used to drive retraction. The amnioserosa is the one tissue whose cellular morphogenesis is reversed from germband extension to retraction, and this reversal coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, cellular force strengths are less important than the carefully established cell shapes that direct them. Video Abstract [Display omitted]