Quantification of myosin distribution predicts global morphogenetic flow in the fly embryo

TL;DR

This study quantitatively links myosin distribution patterns to tissue flow during Drosophila embryogenesis, revealing a global model that predicts morphogenetic movements with high accuracy and uncovers new roles for basal myosin.

Contribution

The paper introduces a coarse-grained myosin tensor and a global physical model that accurately predicts tissue flow during embryogenesis, highlighting the importance of spatial myosin modulation and long-range mechanical interactions.

Findings

Embryo shape changes follow three flow configurations with characteristic myosin patterns.

A simple visco-elastic model with three parameters predicts up to 90% of tissue flow.

Basal myosin plays a novel role in generating dorsally directed flow.

Abstract

During embryogenesis tissue layers continuously rearrange and fold into specific shapes. Developmental biology identified patterns of gene expression and cytoskeletal regulation underlying local tissue dynamics, but how actions of multiple domains of distinct cell types coordinate to remodel tissues at the organ scale remains unclear. We use in toto light-sheet microscopy, automated image analysis, and physical modeling to quantitatively investigate the link between kinetics of global tissue transformations and force generation patterns during Drosophila gastrulation. We find embryo-scale shape changes are represented by a temporal sequence of three simple flow field configurations. Each phase is accompanied by a characteristic spatial myosin distribution, quantified in terms of a coarse-grained 'myosin tensor' that captures both concentration and anisotropy. Our model assumes tissue flow is driven by stress proportional to the myosin tensor, and is effectively visco-elastic with two parameters that control 'irrotational' and 'divergence-less' components of the flow. With just three global parameters, this model achieves up to 90% agreement between predicted and measured flow. The analysis uncovers importance of a) spatial modulation of myosin distribution and b) long-range spreading of its effect due to mechanical interaction of cells. In particular, we find germband extension phase is associated with the onset of effective areal incompressibility of the epithelium, which makes the relation of flow and myosin forcing strongly non-local. Our analysis also revealed a new function for basal myosin in generating a dorsally directed flow and, combined with mutant analysis, identified an unconventional control mechanism through twist dependent reduction of basal myosin levels on the ventral side. We conclude that understanding morphogenetic flow requires a fundamentally global perspective.