Robust spatiotemporal organization of mitotic events in mechanically perturbedC. elegansembryos

Abstract

ABSTRACTEarly embryogenesis of the nematodeCaenorhabditis elegansprogresses in an autonomous fashion within a protective chitin eggshell. Cell division timing and the subsequent, mechanically guided positioning of cells is virtually invariant between individuals, especially before gastrulation. Here, we have challenged this stereotypical developmental program in early stages by mechanically perturbing the embryo, without breaking its eggshell. Compressing embryos to about 2/3 of their unperturbed diameter only resulted in markedly slower cell divisions. In contrast, compressing embryos to half of their native diameter frequently resulted in a loss of cytokinesis, yielding a non-natural syncytium that still allowed for multiple divisions of nuclei. Although the orientation of mitotic axes was strongly altered in the syncytium, key features of division timing and spatial arrangement of nuclei remained surprisingly similar to unperturbed embryos in the first few division cycles. This suggests that few, very robust mechanisms provide a basic and resilient program for safeguarding the early embryogenesis ofC. elegans.STATEMENT OF SIGNIFICANCEEarly embryogenesis of the nematodeCaenorhabditis elegansprogresses in an autonomous fashion within a protective chitin eggshell. Cell division timing and cell positioning seemingly runs on autopilot, yielding a stereotypical development. Compressive forces, a potential hazard in the nematode’s native habitat, may jeopardize this. We show that compressing embryos to 2/3 of their native diameter results in markedly slower cell divisions but leaves the early embryonic program otherwise intact. Further compression of embryos impairs the formation of new cells while nuclei still divide in a common cytoplasm (’syncytium’) with basic features of division timing and spatial arrangement being surprisingly similar to unperturbed embryos. This suggests that few robust mechanisms provide a basic program for the early embryonic autopilot.