Self-organized tissue mechanics underlie embryonic regulation

Abstract

Early amniote development is a highly regulative and self-organized process, capable to adapt to interference through cell-cell interactions, which are widely believed to be mediated by molecules. Analyzing intact and mechanically perturbed avian embryos, we show that the mechanical forces that drive embryogenesis self-organize in an analog of Turing's molecular reaction-diffusion model, with contractility locally self-activating and the ensuing tension acting as a long-range inhibitor. This mechanical feedback governs the persistent pattern of tissue flows that shape the embryo and steers the concomitant emergence of embryonic territories by modulating gene expression, ensuring the formation of a single embryo under normal conditions, yet allowing the emergence of multiple, well-proportioned embryos upon perturbations. Thus, mechanical forces are a central signal in embryonic self-organization, feeding back onto gene expression to canalize both patterning and morphogenesis.

Geometric control of myosin II orientation during axis elongation

“…The geometric control of myosin orientation described here has close parallels to primitive streak formation in the early quail embryo ( Caldarelli et al, 2021 ) as well as to other model processes of convergent extension, the Drosophila wing disc ( Aigouy et al, 2010 ) and the Xenopus larval epithelium ( Chien et al, 2015 ). In the the latter two systems, planar cell polarity proteins orient according to mechanical inputs propagated over tissue-length scales.…”

Mechanochemical Principles of Spatial and Temporal Patterns in Cells and Tissues

“…This enables polarization of the front of migrating cells and prevents secondary fronts from appearing (Houk et al 2012) (Figure 4F). A similar mechanism operates at the tissue scale; the formation of the avian primitive streak occurs because mechanical tension inhibits constriction over a long range, ensuring the development of a single constriction site (Figure 4G) (Caldarelli et al 2021). Other examples include the establishment of polarity in the Caenorhabditis elegans embryo (Gross et al 2019;Mayer et al 2010), Hydra regeneration (Mercker et al 2015), and myosin patterns in stress fibers and sarcomeres (Dasbiswas et al 2018).…”

Quantitative Experimental Embryology: A Modern Classical Approach

“…Classical embryological experiments involving the bisection of the chick epiblast have long provided insight into the highly regulative nature of primitive streak formation in the early chick embryo [ 57 , 58 ]. A recent investigation in quails has combined laser-mediated bisection of the embryo with high resolution imaging to demonstrate that mechanical signals scale robustly following tissue removal [ 10 ] (Caldarelli et al, 2021; biorxiv). The formation of the primitive streak in the chick embryo is well documented to involve large scale tissue flows (reviewed in [ 59 ]).…”

“…Quantification of these movements in both chick and quail indicates that tissue contractility in the posterior of the embryo drives the formation of the primitive streak. This contraction must be balanced by tension from the embryonic margin in order to restrict the localisation of the streak [ 10 , 60 ]. Following bisection, the amount of embryonic margin has decreased, which increases the tension across the tissue and decreases the size of the contractile domain.…”

“…Following bisection, the amount of embryonic margin has decreased, which increases the tension across the tissue and decreases the size of the contractile domain. This facilitates scaling of the primitive streak and associated gene expression in the half-embryo [ 10 ]. These studies demonstrate the importance of combining cell removal techniques with modern quantification in order to understand the parameters of tissue patterning and signaling feedback.…”