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Sci Adv ; 10(32): eadp0860, 2024 Aug 09.
Article in English | MEDLINE | ID: mdl-39121221

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.


Subject(s)
Morphogenesis , Wings, Animal , Animals , Wings, Animal/growth & development , Drosophila Proteins/metabolism , Drosophila Proteins/genetics , Drosophila melanogaster/growth & development , Drosophila , Models, Biological , Imaginal Discs/metabolism , Imaginal Discs/growth & development
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