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

• DOI: 10.48550/arxiv.1701.07100
• Publication Date: 2017-01-01
• Authors: Streichan, Sebast...; Lefebvre, Matthew F; Noll, Nicholas; Wieschaus, Eric F; Shraiman, Boris I
• Keywords: 0303 health sciences; 03 medical and health sciences; FOS: Biological sciences; Cell Behavior (q-bio.CB); Quantitative Biology - Cell Behavior; Quantitative Biology - Tissues and Organs; Tissues and Organs (q-bio.TO); Quantitative Biology - Quantitative Methods; Quantitative Methods (q-bio.QM)

15 total pages, with 9 total figures (7 pages main text with 4 figures and 8 pages SI text with 5 SI figures)<br/>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.<br/>