Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

Abstract

Cell apical constriction driven by actomyosin contraction forces is a conserved mechanism during tissue folding in embryo development. While much is now understood of the molecular mechanism responsible for apical constriction and of the tissue-scale integration of the ensuing in-plane deformations, it is still not clear if apical actomyosin contraction forces are necessary or sufficient per se to drive tissue folding. To tackle this question, we use the Drosophila embryo model system that forms a furrow on the ventral side, initiating mesoderm internalization. Past computational models support the idea that cell apical contraction forces may not be sufficient and that active or passive cell apico-basal forces may be necessary to drive cell wedging leading to tissue furrowing. By using 3D computational modelling and in toto embryo image analysis and manipulation, we now challenge this idea and show that embryo-scale force balance at the tissue surface, rather than cell-autonomous shape changes, is necessary and sufficient to drive a buckling of the epithelial surface forming a furrow which propagates and initiates embryo gastrulation.

A Markov chain Monte Carlo model of mechanical-feedback-driven progressive apical constrictions captures the fluctuating collective cell dynamics in the Drosophila embryo

“…Anteroposterior tension along the curved ventral region produces dorsoventral compression that pushes the field dorsally (inwards), as depicted in Figure 11A and investigated in [70,71]. This effect, analogous to the inward deformation of a soft tissue caused by a tight elastic band, is proportional to both the curvature and tension.…”

“…This effect, analogous to the inward deformation of a soft tissue caused by a tight elastic band, is proportional to both the curvature and tension. A recent thin-shell model [70] shows that the inward stress generated by apical constrictions can alone produce an invagination similar to ventral furrow. However, we expect that for a finite-thickness viscoelastic cell layer of an embryo, such an invagination would be hindered by elastic bending stresses arising in the cell layer that changes its curvature and buckles inward.…”

How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale

“…As mentioned in §2.2, the dynamics of the system can come either from an evolution of the prestress or from a passive relaxation of the material. With some notable exceptions [94], the evolution of the prestress is generally slower than the relaxation of the material. Indeed, biopolymer networks are in general very dynamic as they are being constantly remodelled by processes of (de)reticulation and (de)polymerization.…”

“…Recent data from the ventral furrow formation in Drosophila embryos showed the importance of the global ellipsoidal geometry of the embryo for an elongated ventral patch of myosin to achieve a fold along its long axis [131]. Indeed, heterogeneous prestress at the surface of a thin shell respecting this geometry leads to surface buckling initiating folding with the correct pattern of strain and dynamics [94].…”

Cellular mechanisms of reverse epithelial curvature in tissue morphogenesis

“…Some degree of basal relaxation is certainly required, as shown by the blocking of invagination by basal activation of myosin II during Drosophila gastrulation ( Krueger et al, 2018 ). Actomyosin-driven apical constriction is indeed sufficient to produce embryo-scale inward buckling in the Drosophila model indicating a relatively passive (relaxed) role for the basal parts of the cells ( Fierling et al, 2022 ). Another invagination mechanism, basal wedging, in which nuclei move basally to expand the bases of the narrow cells of the early neuroepithelium in a coordinated version of interkinetic nuclear migration, may or may not involve the actomyosin (microfilament) cytoskeleton ( Schoenwolf et al, 1988 ; Ybot-Gonzalez and Copp, 1999 ).…”