Physical mechanisms shaping the Drosophila dorsoventral compartment boundary

Abstract

Background: Separating cells with distinct identities and fates by straight and sharp compartment boundaries is important for growth and pattern formation during animal development. The physical mechanisms shaping compartment boundaries, however, are not fully understood.

Results: We combine theory and quantitative experiments to investigate the roles of different mechanisms to shape compartment boundaries. Our theoretical work shows that cell elongation created by anisotropic stress, cell proliferation rate, orientation of cell division, and cell bond tension all have distinct effects on the morphology of compartment boundaries during tissue growth. Our experiments using the developing Drosophila wing reveal that the roughness of the dorsoventral compartment boundary is dynamic and that it decreases during development. By measuring tissue relaxation in response to laser ablation of cell bonds at different developmental times, we demonstrate that decreased boundary roughness correlates with increased cell bond tension along the compartment boundary. Finally, by using experimentally determined values for cell bond tension, cell elongation and bias in orientation of cell division in simulations of tissue growth, we can reproduce the main features of the time evolution of the dorsoventral compartment boundary shape.

Conclusions: Local increase of cell bond tension along the boundary as well as global anisotropies in the tissue contribute to shaping boundaries in cell networks. We propose a simple scenario that combines time-dependent cell bond tension at the boundary, oriented cell division, and cell elongation in the tissue that can account for the main features of the dynamics of the shape of the dorsoventral compartment boundary.