Robust spatiotemporal organization of mitotic events in mechanically perturbed C. elegans embryos

Biophys J. 2024 Apr 4:S0006-3495(24)00243-1. doi: 10.1016/j.bpj.2024.03.041. Online ahead of print.

Abstract

Early embryogenesis of the nematode Caenorhabditis elegans progresses 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 two-thirds 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 those of 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 of C. elegans.