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 while 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 2D cellular finite elements that are wrapped around an ellipsoidal 3D 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 failures of retraction when amnioserosa cells are removed to mimic U-shaped mutants or laser-microsurgery experiments. 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 in germband extension and retraction - serving as a store of morphological information that coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, and perhaps more generally, cellular force strengths are less important than the carefully established cell shapes that direct them.