A model for boundary-driven tissue morphogenesis

Tissue deformations during morphogenesis can be active, driven by internal processes, or passive, resulting from stresses applied at their boundaries. Here, we introduce the Drosophila hindgut primordium as a model for studying boundary-driven tissue morphogenesis. We characterize its deformations and show that its complex shape changes can be a passive consequence of the deformations of the active regions of the embryo that surround it. First, we find an intermediate characteristic triangular shape in the 3D deformations of the hindgut. We construct a minimal model of the hindgut primordium as an elastic ring deformed by active midgut invagination and germ band extension on an ellipsoidal surface, which robustly captures the symmetry-breaking into this triangular shape. We then quantify the 3D kinematics of the tissue by a set of contours and discover that the hindgut deforms in two stages: an initial translation on the curved embryo surface followed by a rapid breaking of shape symmetry. We extend our model to show that the contour kinematics in both stages are consistent with our passive picture. Our results suggest that the role of in-plane deformations during hindgut morphogenesis is to translate the tissue to a region with anisotropic embryonic curvature and show that uniform boundary conditions are sufficient to generate the observed nonuniform shape change. Our work thus provides a possible explanation for the various characteristic shapes of blastopore-equivalents in different organisms and a framework for the mechanical emergence of global morphologies in complex developmental systems.

💡 Research Summary

This research paper presents a groundbreaking physical model to explain the complex morphological transformations observed during the development of the Drosophila hindgut primordium. A fundamental question in developmental biology is whether tissue deformations are driven by intrinsic, active cellular processes or are a passive response to mechanical stresses applied at the tissue boundaries. By focusing on the hindgut, the authors demonstrate that its intricate 3D shape changes can be understood as a passive consequence of the active deformations occurring in the surrounding embryonic regions, specifically the midgut invagination and germ band extension.

To investigate this, the researchers developed a minimal mechanical model where the hindgut is represented as an elastic ring situated on an ellipsoidal surface (representing the embryo). This model incorporates the active forces from the surrounding tissues and successfully captures the emergence of a characteristic intermediate triangular shape through a process of symmetry breaking. The study further quantifies the 3D kinematics of the tissue, identifying a distinct two-stage deformation process: an initial phase characterized by the translation of the tissue across the curved embryonic surface, followed by a rapid and dramatic breaking of shape symmetry.

The findings suggest that the primary role of in-plane deformations in the surrounding tissue is to transport the hindgut to regions of anisotropic embryonic curvature, where the geometry of the surface itself drives the non-uniform shape changes. This discovery is significant because it shows that uniform boundary conditions are sufficient to generate complex, non-uniform morphological outcomes. Ultimately, this work provides a robust physical framework for understanding how global morphologies and blastopore-equivalent structures emerge in various organisms, offering a potential explanation for the diverse characteristic shapes of blastopore-equivalents across different species through the lens of mechanical emergence.