Noncell- and Cell-Autonomous G-Protein-Signaling Converges With Ca super(2+)/Mitogen-Activated Protein Kinase Signaling to Regulate str-2 Receptor Gene Expression in Caenorhabditis elegans

In the sensory system of C. elegans, the candidate odorant receptor gene str-2 is strongly expressed in one of the two AWC neurons and weakly in both ASI neurons. Asymmetric AWC expression results from suppression of str-2 expression by a Ca super(2+)/MAPK signaling pathway in one of the AWG neurons early in development. Here we show that the same Ca super(2+)/MAPK pathway promotes str-2 expression in the AWC and ASI neurons together with multiple cell-autonomous and noncell-autonomous G-protein-signaling pathways. In first-stage larvae and adult animals, signals mediated by the G alpha subunits ODR-3, GPA-2, GPA-5, and GPA-6 and a Ca super(2+)/MAPK pathway involving the Ca super(2+) channel subunit UNC-36, the CaMKII UNC-43, and the MAPKK kinase NSY-1 induce strong str-2 expression. Cell-specific rescue experiments suggest that ODR-3 and the Ca super(2+)/MAPK genes function in the AWC neurons, but that GPA-5 and GPA-6 function in the AWA and ADL neurons, respectively. In Dauer larvae, the same network of genes promotes strong str-2 expression in the ASI neurons, but ODR-3 functions in AWB and ASH and GPA-6 in AWB. Our results reveal a complex signaling network, encompassing signals from multiple cells, that controls the level of receptor gene expression at different developmental stages.