The Drosophila wing disc as a shape-programmed material

Throughout development tissues undergo multiple changes in 3D tissue architecture. Yet, unlike our knowledge of genetic patterning emerging before phenotypic realization of fate, we understand not, if tissue shape can be pre-determined similarly and how it manifests during morphogenesis. Such programmability of 3D shape has been demonstrated for certain inanimate materials, including liquid crystal solids. These materials undergo predefined in-plane deformations leading to specific, desired out-of-plane shape changes when stimulated.
We use the example of the 3D epithelial shape changes occurring in the Drosophila wing primordium at the larval-to-pupal transition to address in-plane contributions to 3D tissue shape change and effects of geometrical pre‑pattering during tissue morphogenesis. Via multi-angle light sheet imaging and cell segmentation, we quantify apical cell and tissue shape across different developmental timepoints. We use cell network topology to define spatio-temporal relationships between tissue regions and identify regional cell shape changes and cell rearrangements over development.
Using a modelling approach, we access the effective tissue shape changes resulting from the measured cellular behaviors, showing that the concept of shape programming can be used to model epithelial morphogenesis. Unlike previously described mechanisms for 3D tissue deformation, including localized apical/basal contractility or buckling instabilities, we propose a fundamentally different mechanism. Our work demonstrates that a tissue can deform itself in 3D through large-scale patterning of in-plane cellular behaviors, analogous to inanimate shape-programmable materials.