Systematic analysis of cell morphodynamics in C. elegans early embryogenesis

Abstract

The invariant cell lineage of Caenorhabditis elegans allows unambiguous assignment of the identity for each cell, which offers a unique opportunity to study developmental dynamics such as the timing of cell division, dynamics of gene expression, and cell fate decisions at single-cell resolution. However, little is known about the cell morphodynamics, including the extent to which they are variable between individuals, mainly due to the lack of sufficient amount and quality of quantified data. In this study, we systematically quantified the cell morphodynamics in 52 C. elegans embryos from the two-cell stage to mid-gastrulation at high spatiotemporal resolution, 0.5 m thickness of optical sections, and 30-second intervals of recordings. By comparing the morphodynamics between the embryos, we found high reproducibility of the dynamics. The median correlation coefficient of morphological features, such as volume and surface area, was 0.09, suggesting high reproducibility. Furthermore, the morphodynamics was significantly different from the other cell types in all cells before the onset of gastrulation, indicating high uniqueness of the dynamics. Furthermore, physical cell-cell contacts were quantified to analyze inter-cell relationships, and their reproducibility was calculated between the embryos. The number of contacts formed in every embryo was less than half of all detected contacts because variability in division timings and cell arrangements produced various combinations of brief contacts. In contrast, the area of contacts formed in every embryo occupied 96% of the total area, suggesting the high reproducibility of spatial occupancies and adjacency relationships of the cells. Our data further allowed detailed analyses of specific cellular features. By normalizing the sphericity dynamics, we found a significant increase in sphericity at the end of metaphase in every cell, indicating the universality of the mitotic cell rounding. Concomitant with the rounding, the volume also increased in most but not all cells, suggesting less universality of the mitotic swelling. Therefore, we demonstrate that our data provides a precise understanding of the cellular processes and could potentially be used to gain further insight into developmental mechanisms.