Generation of Cell Diversity during Early Embryogenesis in the Nematode Caenorhabditis elegans

Abstract

Caenorhabditis elegans zygotes undergo a series of four differentiative divisions to generate 5 somatic founder cells and a germ-line progenitor cell by the 16- to 24-cell stage of embryogenesis. The pattern of divisions, cell positions, and development of the embryonic cells are invariant from embryo to embryo. Through a combination of embryo manipulation, treatment of embryos with pharmacologic agents, and genetic analysis of maternal-effect embryonic-lethal mutants, researchers in several laboratories have investigated when and how cell differences are generated and cell fates are specified during embryogenesis: 1. Most blastomeres develop in a cell-autonomous manner. They do not need to undergo cell division and they do not require their normal neighbors to express differentiation products characteristic of their lineage. In embryos in which specific cells have been ablated, the fates of neighboring cells do not change to compensate for the missing cells. These observations suggest that most embryonic cells are determined by lineally transmitted internally segregated information. 2. There is at least one clear-cut example of inductive interactions during early development. The anterior daughter of AB gives rise to hypodermis, neurons, pharyngeal muscles, and body wall muscles. Interactions between ABa cells and P1-derived blastomeres are required between the 4- and 28-cell stage for ABa to generate pharyngeal and body wall muscles. ABa appears to be directed to generate hypodermis by internally segregated cues and directed to generate muscle by external cues. 3. Certain of the early internal segregation events require the participation of microfilaments. Disruption of the microfilament array leads to the missegregation of germ granules and of the potential of cells to undergo unequal germ-line-like divisions. Microfilaments may be involved in many other segregation events as well. 4. Several maternal-effect lethal mutants also perturb zygotic segregation events. These par mutants, which divide symmetrically and fail to segregate germ granules, may identify genes whose products interact with microfilaments or otherwise participate in cytoplasmic localization during the early divisions.