The Caenorhabditis elegans digestive tract is composed of four distinc
t modules derived from separate cell lineages: anterior pharynx from t
he ABa lineage, posterior pharynx from the MS lineage, gut from tile 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 embryo
nic pharynx and tail by virtue of deleting a tandem pair of WGATAR sit
es 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 spat
ial distribution of ges-1 mRNA transcripts produced by either the WGAT
AR-deleted ges-1 transgene or the undeleted ges-l control transgene ap
pear 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 gene
s (skn-1, mex-1, pie-1, and pop-1) that alter early blastomere fate. M
oreover, the pharynx/tail expression of the WGATAR-deleted ges-1 trans
gene is abolished by mutations in the zygotic gene pha-4. Finally, we
use imprecise transposon excision to produce two independent C, elegan
s strains with 1- to 2-kb deletions that remove the tandem WGATAR site
s from the promoter of the endogenous chromosomal I gene: in both of t
hese strains, ges-1 is not expressed in the embryonic gut but is expre
ssed in cells of the embryonic pharynx; pharynx expression is weak but
incontrovertible, Overall, our results validate previous transgenic a
nalysis of ges-1 control and show further that ges-1 appears to be reg
ulated in a system-specific, rather than a lineage-specific, manner. T
he multiple facets of ges-l expression provide an opportunity to inves
tigate how a multicomponent organ system such as the digestive tract i
s established from diverse cell lineages. (C) 1996 Academic Press, Inc
.