The “eyeless” animal C. elegans possesses the sense of light and engages in phototaxis behavior mediated by photoreceptor cells. However, the molecular and cellular mechanisms underlying phototransduction in C. elegans remain largely unclear. By recording the photoreceptor neuron ASJ in wild-type and various mutant worms, here we show that phototransduction in ASJ is a G protein-mediated process and requires membrane-associated guanylate cyclases but not typical cGMP-cleaving phosphodiesterases (PDEs). In addition, we find that C. elegans phototransduction requires LITE-1, a candidate photoreceptor protein known to be a member of the invertebrate taste receptor family. Genetic, pharmacological and electrophysiological data suggest a model whereby LITE-1 transduces light signals in ASJ through G-protein signaling, which leads to up-regulation of the second messenger cGMP followed by opening of cGMP-sensitive CNG channels and thereby stimulation of photoreceptor cells. Our results identify a phototransduction cascade in C. elegans and implicate the function of a “taste receptor" in phototransduction.

Thermotaxis is a model to elucidate how nervous systems sense and memorize environmental conditions to regulate behavioral strategies in Caenorhabditis elegans. The genetic and neural imaging analyses revealed molecular and cellular bases of this experience-dependent behavior. Surprisingly, thermosensory neurons themselves memorize the sensed temperatures. Recently developed techniques for optical manipulation of neuronal activity have facilitated the revelation that there is a sophisticated information flow between sensory neurons and interneurons. Further studies on thermotaxis will allow us to understand the fundamental logics of neural processing from sensory perceptions to behavioral outputs.

Although a large proportion of molecules expressed in the nervous system are conserved from invertebrate to vertebrate, functional properties of such molecules are less characterized. Here, we show that highly conserved hydrolase AHO-3 acts as a novel regulator of starvation-induced thermotactic plasticity in Caenorhabditis elegans. As wild-type animals, aho-3 mutants migrated to the cultivation temperature on a linear thermal gradient after cultivation at a particular temperature with food. Whereas wild-type animals cultivated under food-deprived condition showed dispersed distribution on the gradient, aho-3 mutants exhibited tendency to migrate toward higher temperature. Such an abnormal behavior was completely rescued by the expression of human homologue of AHO-3, indicating that the molecular function of AHO-3 is highly conserved between nematode and human. The behavioral regulation by AHO-3 requires the N-terminal cysteine cluster, which ensures the proper subcellular localization of AHO-3 to sensory endings. Double-mutant analysis suggested that AHO-3 acts in the same pathway with ODR-3, a heterotrimeric G protein alpha subunit. Our results unveiled a novel neural protein in C. elegans, confirming its conserved role in behavioral regulation.