Global morphogenetic flow is accurately predicted by the spatial distribution of myosin motors.

Sebastian J Streichan,Nicholas Noll,Eric F Wieschaus,Matthew F Lefebvre,Boris I Shraiman

doi:10.7554/elife.27454

Sebastian J Streichan, Nicholas Noll + Show 3 more

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https://doi.org/10.7554/elife.27454

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Abstract

During embryogenesis tissue layers undergo morphogenetic flow rearranging and folding into specific shapes. While developmental biology has identified key genes and local cellular processes, global coordination of tissue remodeling at the organ scale remains unclear. Here, we combine in toto light-sheet microscopy of the Drosophila embryo with quantitative analysis and physical modeling to relate cellular flow with the patterns of force generation during the gastrulation process. We find that the complex spatio-temporal flow pattern can be predicted from the measured meso-scale myosin density and anisotropy using a simple, effective viscous model of the tissue, achieving close to 90% accuracy with one time dependent and two constant parameters. Our analysis uncovers the importance of a) spatial modulation of myosin distribution on the scale of the embryo and b) the non-locality of its effect due to mechanical interaction of cells, demonstrating the need for the global perspective in the study of morphogenetic flow.

Highlights

Animal development is characterized by highly dynamic rearrangements of mechanically coupled cells
Using optical flow velocimetry applied to cylinder projections of the Surface of Interest (SOI) passing through cells below the apical cell surface, we find that tissue remodeling during Drosophila gastrulation is characterized by three simple flow field configurations (Figure 1c–e)
The pre-ventral furrow (VF) flow associates with basal myosin that exhibits a pronounced Dorso Ventral (DV) asymmetry (Warn et al, 1980; Sokac and Wieschaus, 2008; Polyakov et al, 2014), with high levels of myosin on the dorsal and low levels on the ventral side (Figure 1f), while the apical pool appears uniform across the surface (Figure 1i, Figure 1—figure supplement 5d–g)

Summary

Introduction

Animal development is characterized by highly dynamic rearrangements of mechanically coupled cells. Live imaging has uncovered process-specific cell behaviors such as apical constriction of presumptive mesoderm cells during ventral furrow formation (Martin et al, 2009) and intercalation of neighboring cells in the lateral ectoderm during convergent extension (Zallen and Wieschaus, 2004; Bertet et al, 2004) These behaviors are associated with localized activity of the force generating non-muscle myosin II (Martin et al, 2009; Irvine and Wieschaus, 1994; Zallen and Wieschaus, 2004; Bertet et al, 2004).

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