Stored Elastic Energy Mediates Embryonic Body Folding

During embryonic development, amniote vertebrate embryos transform from a flat, multi-layered sheet into the definitive three-dimensional cylindrical body form, through ventral folding of the lateral sides of the sheet and their fusing in the ventral midline. Use of a novel chick embryo slice system reveals that the flat stage is characterized by balanced, opposing elastic bending forces in the lateral embryo, with a dorsal bending force in the dorsal somatopleuric layer and a ventral bending force in the ventral splanchnopleuric layer. An intact extracellular matrix is required for generating and maintaining these bending forces, as enzymatic digestion of somatopleuric or splanchnopleuric extracellular matrix completely dissipates the stored bending energy, while removal of the endodermal or ectodermal epithelial layers has no effect. As developmental proceeds, the stored elastic bending energy in the somatopleure decreases while that of the splanchnopleure is maintained, changing the balance of bending forces in the lateral embryo and promoting ventral folding. Dissipation of somatopleure elastic bending energy correlates with somatopleuric epithelial-mesenchymal transition, which fragments the extracellular matrix. Thus regulation of stored elastic bending energy in the extracellular matrix can drive large-scale embryonic tissue movements. Related mechanisms may operate in other instances of morphogenesis.