Stored elastic bending tension as a mediator of embryonic body folding

During development, amniote vertebrate embryos transform from a flat sheet into a three-dimensional cylindrical form through ventral folding of the lateral sides of the sheet (the lateral plate [LP]) and their fusion in the ventral midline. Using a chick embryo slice system, we find that the flat stage is actually a poised balance of opposing dorsal and ventral elastic bending tensions. An intact extracellular matrix (ECM) is required for generating tension, as localized digestion of ECM dissipates tension, while removal of endoderm or ectoderm layers has no significant effect. As development proceeds, dorsal bending tension dissipates coincident with epithelial-mesenchymal transition in the dorsal LP while ventral tension is maintained, changing the balance of forces to promote ventral folding. Interference with the elastic ECM component fibrillin reduces ventral bending tension and perturbs body folding in vivo. A model is presented for the accumulation and harnessing of LP bending tension to drive body folding.