Modulation of gene expression in the embryonic digestive tract of C. elegans

The Caenorhabditis elegans digestive tract is composed of four distinct modules derived from separate cell lineages: anterior pharynx from the ABa lineage, posterior pharynx from the MS lineage, gut from the E lineage, and rectum from the ABp lineage. The C. elegans gut esterase gene (ges-1) is normally expressed in the embryonic gut or E lineage. However, expression ges-1 can be switched into cells of the embryonic pharynx and tail by virtue of deleting a tandem pair of WGATAR sites in the ges-1 promoter. Here, we use both laser ablation experiments and genetic analysis to show that cells expressing the WGATAR-deleted ges-1 transgene belong to all three nongut lineages of the digestive tract: ABa, MS, and ABp. We also show that the molecular size and spatial distribution of ges-1 mRNA transcripts produced by either the WGATAR-deleted ges-1 transgene or the undeleted ges-1 control transgene appear correctly regulated, suggesting that the spatial switch in ges-1 expression occurs at the level of transcription initiation. We further show that both the WGATAR-deleted and the undeleted ges-1 transgenes respond appropriately to mutations in a series of maternal effect genes (skn-1, mex-1, pie-1, and pop-1) that alter early blastomere fate. Moreover, the pharynx/tail expression of the WGATAR-deleted ges-1 transgene is abolished by mutations in the zygotic gene pha-4. Finally, we use imprecise transposon excision to produce two independent C. elegans strains with 1- to 2-kb deletions that remove the tandem WGATAR sites from the promoter of the endogenous chromosomal ges-1 gene: in both of these strains, ges-1 is not expressed in the embryonic gut but is expressed in cells of the embryonic pharynx; pharynx expression is weak but incontrovertible. Overall, our results validate previous transgenic analysis of ges-1 control and show further that ges-1 appears to be regulated in a system-specific, rather than a lineage-specific, manner. The multiple facets of ges-1 expression provide an opportunity to investigate how a multicomponent organ system such as the digestive tract is established from diverse cell lineages.