A Geometric Tension Dynamics Model of Epithelial Convergent Extension

TL;DR

This paper presents a geometric tension dynamics model explaining epithelial tissue convergent extension, highlighting how force balance remodeling and tension feedback drive cell rearrangements and tissue deformation during morphogenesis.

Contribution

It introduces a novel model linking tension feedback and force balance to tissue flow, emphasizing the role of cellular order and tension coherence in morphogenetic movements.

Findings

The model reproduces germ band elongation features in Drosophila.

Tissue deformation depends on initial cellular packing order.

Loss of tension order correlates with flow slowdown.

Abstract

Convergent extension of epithelial tissue is a key motif of animal morphogenesis. On a coarse scale, cell motion resembles laminar fluid flow; yet in contrast to a fluid, epithelial cells adhere to each other and maintain the tissue layer under actively generated internal tension. To resolve this apparent paradox, we formulate a model in which tissue flow in the tension-dominated regime occurs through adiabatic remodeling of force balance in the network of adherens junctions. We propose that the slow dynamics within the manifold of force-balanced configurations is driven by positive feedback on myosin-generated cytoskeletal tension. Shifting force balance within a tension network causes active cell rearrangements (T1 transitions) resulting in net tissue deformation oriented by initial tension anisotropy. Strikingly, we find that the total extent of tissue deformation depends on the initial cellular packing order. T1s degrade this order so that tissue flow is self-limiting. We explain these findings by showing that coordination of T1s depends on coherence in local tension configurations, quantified by a geometric order parameter in tension space. Our model reproduces the salient tissue- and cell-scale features of germ band elongation during Drosophila gastrulation, in particular the slowdown of tissue flow after approximately twofold longation concomitant with a loss of order in tension configurations. This suggests local cell geometry contains morphogenetic information and yields experimentally testable predictions. Defining biologically controlled active tension dynamics on the manifold of force-balanced states may provide a general approach to the description of morphogenetic flow.