Developmental milestones punctuate gene expression in the Caenorhabditis embryo

ABSTRACT: The complex process by which a metazoan develops from a single cell to a multi-cellular differentiated organism is typically organized by biologists into stages. For example, in the chordate embryo, the gastrula, the neurula and the tail-bud constitute characteristic processes. A debate runs through the history of embryology questioning whether such stages hint at the modularity of embryonic development1-3, or rather, that “stages exist in the mind of the biologist, and not in the larva”4 or embryo. It thus remains unclear which position accurately reflects the nature of development on a molecular, gene regulatory level. Here we demonstrate that development of five Caenorhabditis species proceeds through multiple distinct stages in which the transcriptome is resistant to differences in species-specific developmental timings. By comparing the complete protein-coding transcriptomes of individually staged embryos across ten morphological markers, we found that time-invariant stages occur throughout development, including a stage we identify as the nematode phylotypic stage. Between such stages, embryos follow transitory states characterized by an acceleration of transcriptional activity. Therefore, on a molecular level, development cannot be viewed as a single process continuously proceeding through time, but rather as a succession of discontinuous stages, or ‘milestones’. Comparing the nematode developmental transcriptome with that of the chordate we report on the macro evolution of a milestone by duplication and diversification. This modular view of development by milestones will allow for a more complete understanding of how the functional organization of the embryo has influenced the evolution of animal morphology and diversity.

ORGANISM(S): Caenorhabditis elegans Caenorhabditis remanei Caenorhabditis briggsae Caenorhabditis brenneri Caenorhabditis japonica

PROVIDER: GSE31422 | GEO | 2012/03/01

SECONDARY ACCESSION(S): PRJNA145833

REPOSITORIES: GEO