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 of
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. We have used both laser ablation experiments and genetic analysis to show that cells expressing the WGATAR-deleted
ges-1 transgene belong to all three non-gut 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 1-2 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. In addition to providing insight into the global regulation of digestive- tract-specific genes,
ges-1 transgenes also suggest subtleties in regulation within the digestive tract. For example, deletion from the
ges-1 promoter of either WGATAR site singly, or of an adjoining 45 bp region, results in anterior-gut-specific transgene expression. The molecular and genetic basis of this expression pattern is being investigated.