Strain maps characterize the symmetry of convergence and extension patterns during Zebrafish gastrulation

Abstract

During gastrulation of the zebrafish embryo, the cap of blastoderm cells organizes into the axial body plan of the embryo with left-right symmetry and head-tail, dorsal-ventral polarities. Our labs have been interested in the mechanics of early development and have investigated whether these large-scale cells movements can be described as tissue-level mechanical strain by a tectonics-based approach. The first step is to image the positions of all nuclei from mid-epiboy to early segmentation by digital sheet light microscopy (DSLM), organize the surface of the embryo into multi-cell spherical domains, construct velocity fields from the movements of these domains and extract 3D strain rate maps. Tensile/expansive and compressive strains in the axial and equatorial directions are detected during gastrulation as anterior and posterior expansion along the anterior-posterior axis and medial-lateral compression across the dorsal-ventral axis corresponding to convergence and extension. In later stages in development are represented by localized medial expansion at the onset of segmentation and anterior expansion at the onset of neurulation. Symmetric patterns of rotation are first detected in the animal hemispheres at mid-epiboly and then the vegetal hemispheres by the end of gastrulation. By analysing the temporal sequence of large scale movements, deformations across the embryo can be attributed to a combination of epiboly and dorsal convergence-extension.\n\nSignificanceStrain is an emergent property of tissues that originates from the mechanical coupling of cell-cell and cell-substrate interactions, individual cell shape changes, and cell level forces. By imaging the positions of nuclei from mid-epiboly to early segmentation of the zebrafish embryo we are able to calculate three types of strain maps by a plate tectonics based method. The regions of expansive and compressive axial and equatorial strain correspond to areas undergoing convergence and extension, a major step in the formation of the embryonic body plan as well as the formation of somite and head structures. The most striking signatures of strain are: 1. the bilateral symmetry of linear strain across the anterior-posterior, dorsal-ventral axis during gastrulation, 2. the complementary counter-rotational strains or curl in the animal hemisphere at mid epiboly, and 3. a divergence or saddle point in the region of the dorsal organizer, head-trunk boundary. These strains represent a general method to describe large-scale tissue-level mechanics not only of embryonic development but also tissue homeostasis and disease.