Coordination of ges-1 expression between the Caenorhabditis pharynx and intestine.

We have previously shown that the Caenorhabditis elegans gut-specific esterase gene (Ce-ges-1) has the unusual ability to be expressed in different modules of the embryonic digestive tract (anterior pharynx, posterior pharynx, and rectum) depending on sequence elements within the Ce-ges-1 promoter. In the present paper, we analyze the expression of the ges-1 homolog (Cb-ges-1) from the related nematode Caenorhabditis briggsae and show that Cb-ges-1 also has the ability to switch expression between gut and pharynx + rectum. The control of this expression switch centres on a tandem pair of WGATAR sites in the Cb-ges-1 5'-flanking region, just as it does in Ce-ges-1. We use sequence alignments and subsequent deletions to identify a region at the 3'-end of both Ce-ges-1 and Ce-ges-1 that acts as the ges-1 cryptic pharynx enhancer whose activity is revealed by removal of the 5' WGATAR sites. This region contains a conserved binding site for PHA-4 (the C. elegans ortholog of forkhead/HNF3 alpha, beta,gamma factors), which is expressed in all cells of the developing pharynx and a subset of cells of the developing rectum. We propose a model in which the normal expression of ges-1 is controlled by the gut-specific GATA factor ELT-2. We propose that, in the pharynx (and rectum), PHA-4 is normally bound to the ges-1 3'-enhancer sequence but that the activation function of PHA-4 is kept repressed by a (presently unknown) factor binding in the vicinity of the 5' WGATAR sites. We suggest that this control circuitry is maintained in Caenorhabditis because pharyngeal expression of ges-1 is advantageous only under certain developmental or environmental conditions. Copyright 2001 Academic Press.