Delineating the mechanisms and design principles of Caenorhabditis elegans embryogenesis using in toto high-resolution imaging data and computational modeling

The nematode (roundworm) Caenorhabditis elegans is one of the most popular animal models for the study of developmental biology, as its invariant development and transparent body enable in toto cellular-resolution fluorescence microscopy imaging of developmental processes at 1-min intervals. This has led to the development of various computational tools for the systematic and automated analysis of imaging data to delineate the molecular and cellular processes throughout the embryogenesis of C. elegans, such as those associated with cell lineage, cell migration, cell morphology, and gene activity. In this review, we first introduce C. elegans embryogenesis and the development of techniques for tracking cell lineage and reconstructing cell morphology during this process. We then contrast the developmental modes of C. elegans and the customized technologies used for studying them with the ones of other animal models, highlighting its advantage for studying embryogenesis with exceptional spatial and temporal resolution. This is followed by an examination of the physical models that have been devised—based on accurate determinations of developmental processes afforded by analyses of imaging data—to interpret the early embryonic development of C. elegans from subcellular to intercellular levels of multiple cells, which focus on two key processes: cell polarization and morphogenesis. We subsequently discuss how quantitative data-based theoretical modeling has improved our understanding of the mechanisms of C. elegans embryogenesis. We conclude by summarizing the challenges associated with the acquisition of C. elegans embryogenesis data, the construction of algorithms to analyze them, and the theoretical interpretation.