A mechanochemical model recapitulates distinct vertebrate gastrulation modes

Abstract

Gastrulation is a critical event in vertebrate morphogenesis driven by cellular processes, and characterized by coordinated multi-cellular movements that form the robust morphological structures. How these structures emerge in a developing organism and vary across vertebrates remains unclear. Inspired by experiments on the chick, we derive a theoretical framework that couples actomyosin activity to tissue flow, and provides a basis for the dynamics of gastrulation morphologies. Our model predicts the onset and development of observed experimental patterns of wild-type and perturbations of chick gastrulation as a spontaneous instability of a uniform state. Varying the initial conditions and a parameter in our model, allows us to recapitulate the phase space of gastrulation morphologies seen across vertebrates, consistent with experimental observations in the accompanying paper. All together, this suggests that early embryonic self-organization follows from a minimal predictive theory of active mechano-sensitive flows.

Reconstruction of distinct vertebrate gastrulation modes via modulation of key cell behaviors in the chick embryo

“…These cell intercalations are driven by long myosin cables oriented along the long axis of the evolving mesendoderm territory (15). We have developed a mechanochemical model that, starting from an initial sickle-or ring-shaped mesendoderm precursor region containing a tension-dependent myosin recruitment mechanism, can explain the emergence of the tissue flows that drive the formation of the primitive streak and predict the dynamics of the domains of ingressing cells, which are in excellent agreement with those experimentally observed, both under normal and experimentally perturbed conditions (19). The model has highlighted and elucidated the importance of the mechanochemical feedback of the flow on myosin recruitment and organization of the epiblast tissue flow.…”

“…The measured negative isotropic strain rate at these stages of buckling indicates the disappearance of cells into the inside of the embryo rather than ingression. This situation reproduces some aspects of the tissue organization and flow during the closing blastopore in Xenopus , where tissue is invaginated as a continuous epithelial sheet ( 44 ) [see also figure 3H and movie 12 of ( 19 ) for the corresponding DM]. However, while Xenopus embryos invaginate their vegetal side during gastrulation, in LDN-treated chick embryos, the system resolves to engulf the central epiblast, corresponding to the animal side.…”

“…The resulting circular streak structure resembles the germ ring of teleost fish gastrulation, where cells undergo ingression and migrate toward the animal pole ( 33 – 36 ) [see also figure 3F and movie 9 of ( 19 ) for the corresponding DM]. Similarly, in FGF-treated embryos, cells that ingress in the circular streak migrate toward the center of the epiblast, the corresponding animal pole (movie S6).…”

“…While Eulerian quantities (decomposed strain rates) correlate with distinct cell behaviors, morphogenetic features arise from different processes integrated over space and time along cell trajectories. To account for this, we compute the dynamic morphoskeleton (DM) ( 18 ), which consists of Lagrangian attractors, their domain of attraction (DOA), and repellers that together organize tissue flows [figure 2 and movie 3 of the accompanying paper ( 19 )]. The DOA consists of the back projection of the attractor on the initial stage of development and reveals the extent of the sickle-shaped posterior-located mesendoderm precursors fated to ingress through the streak ( Fig.…”

Self-organized tissue mechanics underlie embryonic regulation

“…In that context, advection of polarity markers that feedback on contractility is the key to establish embryonic polarity. A model that couples a bistable system with advection has also been proposed for avian gastrulation (24), but in that case, the time scale of advection is essentially the time scale of primitive streak formation, thus mechanical feedback that depends on advection cannot support rapid regulation, as revealed by subdivision (Fig. 4) and obstacle-based perturbation experiments (Fig.…”