Modulation of Gene Expression in the Embryonic Digestive Tract ofC. elegans

Abstract

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.

Molecular Characterization of a Novel, Cadmium-inducible Gene from the Nematode Caenorhabditis elegans

“…cdr-1 contains sequences that are 100% identical to the consensus sequences for a TATA box, a single metal response element, two antioxidant response elements, and a heat shock element (50 -52). In addition, cdr-1 contains two potential GATA-transcription factor-binding sites (53,54). A homologous cAMP-response element was also identified (55).…”

A Novel Heme-responsive Element Mediates Transcriptional Regulation in Caenorhabditis elegans

“…In C. elegans, ELT-2, ELT-4, and ELT-7 are all intestine-specific. However, elt-4 and elt-7 deletion mutants in C. elegans show a wild-type phenotype, indicating that ELT-2 is the major GATA factor in the intestine (27,33). ELT-2 controls expression of numerous intestinal genes.…”

Biochemical and molecular characterization of two cytidine deaminases in the nematode Caenorhabditis elegans

“…In contrast, with the cdd-2 reporter the intestinal cells were still strongly positive in the adult worm. Analysis of the upstream sequence of both genes revealed several potential control elements, which might direct gut-specific expression, including GATA elements, Skn-1 elements and, in Ce-cdd-2, an E-box domain [34][35][36][37]. Further analysis will be necessary to identify the functional elements that define tissue-specific expression in the intestine of C. elegans.…”