Organization of Embryonic Morphogenesis via Mechanical Information

Embryonic organizers establish gradients of diffusible signaling molecules to pattern the surrounding cells. Here, we elucidate an additional mechanism of embryonic organizers that is a secondary consequence of morphogen signaling. Using pharmacological and localized transgenic perturbations, 4D imaging of the zebrafish embryo, systematic analysis of cell motion, and computational modeling, we find that the vertebrate tail organizer orchestrates morphogenesis over distances beyond the range of morphogen signaling. The organizer regulates the rate and coherence of cell motion in the elongating embryo using mechanical information that is transmitted via relay between neighboring cells. This mechanism is similar to a pressure front in granular media and other jammed systems, but in the embryo the mechanical information emerges from self-propelled cell movement and not force transfer between cells. The propagation likely relies upon local biochemical signaling that affects cell contractility, cell adhesion, and/or cell polarity but is independent of transcription and translation. [Display omitted] •Positive feedback between Bmp signaling and eve1 functions in the tail organizer•Perturbation of organizer signaling has long-range effects on cell motion•These long-range effects are beyond the range organizer signaling•These long-range effects are mediated by mechanical information Das, Jülich, and Schwendinger-Schreck et al. find that the zebrafish tail organizer orchestrates morphogenesis over distances beyond the range of its secreted cell-signaling proteins. The organizer regulates cell migration in the elongating embryo using mechanical information that propagates via relay between neighboring cells.