Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories

Abstract Digital cell lineages reconstructed from 3D+time imaging data of the developing zebrafish embryo are used to uncover mechanical cues and their role in morphogenesis. A continuous approximation of cell displacements obtained from cell lineages is used to assess tissue deformation during gastrulation. At this stage, embryonic tissues display multi-scale compressible fluid-like properties. The deformation rate at the mesoscopic level of the cell’s immediate surroundings appears noisy, in both space and time. The patterns identified by clustering the cells, according to the cumulative deformation rate along their trajectory throughout gastrulation, lead to a robust, ordered and coherent biomechanical map. The timing and amplitude of the biomechanical deformations provide a measurement of the phenotypic variability in small cohorts of specimens. We show that the biomechanical map matches the embryonic fate map of the zebrafish presumptive forebrain, in both wild type and Nodal pathway mutants (zoeptz57/tz57), where it reveals the biomechanical defects that lead to cyclopia.. The comparison of biomechanical patterns and the expression pattern of a transgenic reporter for the transcription factor goosecoid (gsc), supports the hypothesis that embryonic cells acquire, at an early developmental stage, a biomechanical signature that contributes to defining their fate.