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 expresse d only in the intestinal lineage, beginning when the developing gut ha s only four to eight cells. We analyze the sequence requirements for t his tissue-specific gene regulation by injecting deleted/mutated const ructs of the ges-l gene into a viable ges-l (null) strain of worms and assaying heritably transformed embryos by esterase histochemistry. Ma ny deletion constructs accurately reconstitute the wildtype gut-specif ic 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 th e pharynx/tail that appear to belong to the sister lineage of the gut. Deletions of a 36-bp DNA region containing two tandem WGATAR sequence s are sufficient to cause this gut-to-pharynx/tail switch in expressio n pattern. Deletion of either one of the WGATAR sites or deletion of a n adjoining downstream region directs ges-l expression only in a restr icted set of cells of the anterior gut. The ges-1 GATA region acts lik e a gut-specific enhancer in that: (i) it restores ges-l gut expressio n 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 repre ssion in that reinsertion elsewhere into the GATA-deleted ges-1 constr uct causes repression of ges-1 in the pharynx/tail. However, multiple copies of the GATA region are not able to repress the heat-induced exp ression of an hsp16-lacZ reporter gene, suggesting that the pharynx/ta il repression mechanism is specific to the ges-l environment. Finally, mutation rather than deletion of the individual GATA sequences sugges ts that gut activation and pharynx/tail repression may be due to separ ate factors. We present a molecular model that summarizes these result s. The ges-l control circuitry appears surprisingly complex for what m ight have been expected to be the simplest possible example of a nones sential gene expressed early in a clonal embryonic lineage. (C) 1995 A cademic Press, Inc.