Force production and mechanical accommodation during convergent extension

Forces generated within the embryo during convergent extension (CE) must overcome mechanical resistance to push the head away from the rear. As mechanical resistance increases more than eightfold during CE and can vary twofold from individual to individual, we have proposed that developmental programs must include mechanical accommodation in order to maintain robust morphogenesis. To test this idea and investigate the processes that generate forces within early embryos, we developed a novel gel-based sensor to report force production as a tissue changes shape; we find that the mean stress produced by CE is 5.0 +/- 1.6 Pascal (Pa). Experiments with the gel-based force sensor resulted in three findings. (1) Force production and mechanical resistance can be coupled through myosin contractility. The coupling of these processes can be hidden unless affected tissues are challenged by physical constraints. (2) CE is mechanically adaptive; dorsal tissues can increase force production up to threefold to overcome a stiffer microenvironment. These findings demonstrate that mechanical accommodation can ensure robust morphogenetic movements against environmental and genetic variation that might otherwise perturb development and growth. (3) Force production is distributed between neural and mesodermal tissues in the dorsal isolate, and the notochord, a central structure involved in patterning vertebrate morphogenesis, is not required for force production during late gastrulation and early neurulation. Our findings suggest that genetic factors that coordinately alter force production and mechanical resistance are common during morphogenesis, and that their cryptic roles can be revealed when tissues are challenged by controlled biophysical constraints.