Physical determinants of asymmetric cell divisions in the early development of Caenorhabditis elegans

Rolf Fickentscher,Matthias Weiss

doi:10.1038/s41598-017-09690-4

Abstract

Asymmetric cell divisions are of fundamental importance for the development of multicellular organisms, e.g. for the generation of founder cells. Prime examples are asymmetric cell divisions in germline precursors during the early embryogenesis of the transparent roundworm Caenorhabditis elegans, one of the major developmental model organisms. However, due to a lack of quantitative data it has remained unclear how frequent unequal daughter cell sizes emerge in the worm’s early embryogenesis, and whether these originate from sterical or biochemical cues. Using quantitative light-sheet microscopy, we have found that about 40% of all cell divisions in C. elegans until gastrulation generate daughter cells with significantly different volumes. Removing the embryo’s rigid eggshell revealed asymmetric divisions in somatic cells to be primarily induced by steric effects. Division asymmetries in the germline remained unaltered and were correctly reproduced by a model based on a cell-size independent, eccentric displacement of the metaphase plate. Our data suggest that asymmetric cell divisions, imposed by physical determinants, are essential for establishing important cell-cell interactions that eventually fuel a successful embryogenesis.

Highlights

Asymmetric cell divisions are of crucial importance for developmental processes, e.g. in the context of tissue or body axis formation[1, 2]
For predominantly biochemically governed asymmetric cell divisions, i.e. for the P lineage, we were able to predict the degree of asymmetry via a simple model that relies on a cell-size independent, eccentric displacement of the mitotic spindle
Asymmetric cell divisions have been observed for cells of the P lineage (P0, ..., P3) and EMS2, 12, 16

Summary

Caenorhabditis elegans

Asymmetric cell divisions are of fundamental importance for the development of multicellular organisms, e.g. for the generation of founder cells. Using quantitative light-sheet microscopy, we have found that about 40% of all cell divisions in C. elegans until gastrulation generate daughter cells with significantly different volumes. A fair understanding of the associated formation of biochemical gradients, from Turing-like patterns[7, 9] to condensation phenomena[10], has been possible All of these and similar studies have been focusing on the single-cell stage and the first, asymmetric cell division since monitoring dynamic intracellular events in the comparatively large P0 cell is straightforward. As a consequence, extrapolated cell volumes are quite error-prone and may not report reliably on geometrical asymmetries in cell division events. For predominantly biochemically governed asymmetric cell divisions, i.e. for the P lineage, we were able to predict the degree of asymmetry via a simple model that relies on a cell-size independent, eccentric displacement of the mitotic spindle

Results and Discussion

Materials and Methods

Additional Information