Active shape programming drives Drosophila wing disc eversion

How complex 3D tissue shape emerges during animal development remains an important open question in biology and biophysics. In this work, we study eversion of the Drosophila wing disc pouch, a 3D morphogenesis step when the epithelium transforms from a radially symmetric dome into a curved fold shape via an unknown mechanism. To explain this morphogenesis, we take inspiration from inanimate ”shape-programmable” materials, which are capable of undergoing blueprinted 3D shape transformations arising from in-plane gradients of spontaneous strains. Here, we show that active, in-plane cellular behaviors can similarly create spontaneous strains that drive 3D tissue shape change and that the wing disc pouch is shaped in this way. We map cellular behaviors in the wing disc pouch by developing a method for quantifying spatial patterns of cell behaviors on arbitrary 3D tissue surfaces using cellular topology. We use a physical shape-programmability model to show that spontaneous strains arising from measured active cell behaviors create the tissue shape changes observed during eversion. We validate our findings using a knockdown of the mechanosensitive molecular motor MyoVI, which we find to reduce active cell rearrangements and disrupt wing pouch eversion. This work shows that shape programming is a mechanism for animal tissue morphogenesis and suggests that there exist intricate patterns in nature that could present novel designs for shape-programmable materials.

Methods
Drosophila wing discs of various stages starting from late larval through 6hr after puparium formation were dissected and imaged live in low melting agarose using multi-angle light sheet microscopy. Tissue shape was manually extracted in 2 orthogonal cross-sections (along and across dorsal-ventral boundary), and its shape and calculated curvature are included here. Apical cell cross-sections were segmented in individual views, and the 3d position was recorded from the full 3d image stack. The CellProperties file includes information about cell size, shape, and position, measured using an updated 3d version of the software TissueMiner.