A GUT-TO-PHARYNX TAIL SWITCH IN EMBRYONIC EXPRESSION OF THE CAENORHABDITIS-ELEGANS GES-1 GENE CENTERS ON 2 GATA SEQUENCES

The Caenorhabditis elegans ges-1 gene (gut esterase No. 1) is expressed only in the intestinal lineage, beginning when the developing gut has only four to eight cells. We analyze the sequence requirements for this tissue-specific gene regulation by injecting deleted/mutated constructs of the ges-l gene into a viable ges-l (null) strain of worms and assaying heritably transformed embryos by esterase histochemistry. Many deletion constructs accurately reconstitute the wildtype gut-specific ges-l expression. However, deletions in the neighborhood of 1100 bp upstream of the ges-l ATG abolish ges-l expression in the developing gut, while at the same time activating ges-l expression in cells of the pharynx/tail that appear to belong to the sister lineage of the gut. Deletions of a 36-bp DNA region containing two tandem WGATAR sequences are sufficient to cause this gut-to-pharynx/tail switch in expression pattern. Deletion of either one of the WGATAR sites or deletion of an adjoining downstream region directs ges-l expression only in a restricted set of cells of the anterior gut. The ges-1 GATA region acts like a gut-specific enhancer in that: (i) it restores ges-l gut expression when reinserted elsewhere into the GATA-deleted ges-1 gene; and (ii) multiple copies direct gut expression of an hsp16-lacZ reporter gene. The ges-l GATA-region also acts as the site of the pharynx/tail repression in that reinsertion elsewhere into the GATA-deleted ges-1 construct causes repression of ges-1 in the pharynx/tail. However, multiple copies of the GATA region are not able to repress the heat-induced expression of an hsp16-lacZ reporter gene, suggesting that the pharynx/tail repression mechanism is specific to the ges-l environment. Finally, mutation rather than deletion of the individual GATA sequences suggests that gut activation and pharynx/tail repression may be due to separate factors. We present a molecular model that summarizes these results. The ges-l control circuitry appears surprisingly complex for what might have been expected to be the simplest possible example of a nonessential gene expressed early in a clonal embryonic lineage. (C) 1995 Academic Press, Inc.