ASSESSING NORMAL EMBRYOGENESIS IN CAENORHABDITIS-ELEGANS USING A 4D MICROSCOPE - VARIABILITY OF DEVELOPMENT AND REGIONAL SPECIFICATION

Caenorhabditis elegans is renowned for its invariant embryogenesis. Th is pattern of development is in apparent contrast to other organisms f rom Drosophila to higher vertebrates. With the aid of a 4D microscope system (multifocal, time-lapse video recording system) which permits t he extensive documentation and analysis of cell divisions, cell positi ons, and migrations in single embryos we have analyzed normal embryoge nesis of C. elegans. The instrumentation reveals a naturally occurring variability in cell division timing, cell positioning, and cell-cell contacts which could not have been detected by the direct observation used earlier (Sulston et al., 1983, Dev. Biol. 100, 64-119). Embryos a re very flexible and produce an essentially invariant premorphogenetic stage from variable earlier stages. An analysis of the distribution o f the descendants of the early founder blastomeres at the premorphogen etic stage shows that these establish discrete regions in the embryo, a process involving a considerable amount of cell movement, which agai n varies in different embryos. Only cell fate assignment remains invar iant. However, as shown earlier, this is not due to an autonomous inva riant specification of cell fates but due to the fact that cell-cell i nteractions occur very early when the topology of blastomeres in the e mbryo is still sufficiently precise to ensure reproducible patterns of inductions. A new concept that founder blastomeres produce embryonic regions in the embryo can explain the striking complexity of the linea ge per se and also the complicated asymmetric lineage patterns by whic h the bilateral symmetry of the embryo is established. Many cells, inc luding bilateral homologs, were apparently chosen for a specific fate solely by their position in the embryo, irrespectively of the lineage descent by which the cells are created. We postulate that the producti on of regions by cell-cell interactions is the pivotal principle guidi ng the embryogenesis of C. elegans and that the embryogenesis of the w orm follows the same basic principles as embryogenesis in other organi sms. (C) 1997 Academic Press.