Active shape programming drives Drosophila wing disc eversion

9 Aug 2024Science Advances

DOI : 10.1126/sciadv.adp0860

Authors

Jana F. Fuhrmann, Abhijeet Krishna, Joris Paijmans, Charlie Duclut, Greta Cwikla, Suzanne Eaton, Marko Popović, Frank Jülicher, Carl D. Modes, Natalie A. Dye

Abstract

How complex 3D tissue shape emerges during animal development remains an important open question in biology and biophysics. Here, we discover a mechanism for 3D epithelial shape change based on active, in-plane cellular events that is analogous to inanimate “shape programmable” materials, which undergo blueprinted 3D shape transformations from in-plane gradients of spontaneous strains. We study eversion of the Drosophila wing disc pouch, when the epithelium transforms from a dome into a curved fold, quantifying 3D tissue shape changes and mapping spatial patterns of cellular behaviors on the evolving geometry using cellular topology. Using a physical model inspired by shape programming, we find that active cell rearrangements are the major contributor to pouch eversion and validate this conclusion using a knockdown of MyoVI, which reduces rearrangements and disrupts morphogenesis. This work shows that shape programming is a mechanism for animal tissue morphogenesis and suggests that patterns in nature could present design strategies for shape-programmable materials.

Members

CHARLIE DUCLUT

Maître de conférences Sorbonne Université