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

Abstract

TheCaenorhabditis elegansdigestive 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. TheC. elegansgut esterase gene (ges-1) is normally expressed in the embryonic gut or E lineage. However, expression ofges-1can be switched into cells of the embryonic pharynx and tail by virtue of deleting a tandem pair of WGATAR sites in theges-1promoter. Here, we use both laser ablation experiments and genetic analysis to show that cells expressing the WGATAR-deletedges-1transgene belong to all three nongut lineages of the digestive tract: ABa, MS, and ABp. We also show that the molecular size and spatial distribution ofges-1mRNA transcripts produced by either the WGATAR-deletedges-1transgene or the undeletedges-1control transgene appear correctly regulated, suggesting that the spatial switch inges-1expression occurs at the level of transcription initiation. We further show that both the WGATAR-deleted and the undeletedges-1transgenes respond appropriately to mutations in a series of maternal effect genes (skn-1, mex-1, pie-1,andpop-1) that alter early blastomere fate. Moreover, the pharynx/tail expression of the WGATAR-deletedges-1transgene is abolished by mutations in the zygotic genepha-4.Finally, we use imprecise transposon excision to produce two independentC. elegansstrains with 1- to 2-kb deletions that remove the tandem WGATAR sites from the promoter of the endogenous chromosomalges-1gene: in both of these strains,ges-1is 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 ofges-1control and show further thatges-1appears to be regulated in a system-specific, rather than a lineage-specific, manner. The multiple facets ofges-1expression provide an opportunity to investigate how a multicomponent organ system such as the digestive tract is established from diverse cell lineages.