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C. elegans phototransduction requires a G protein–dependent cGMP pathway and a taste receptor homolog

Abstract

The eyeless animal C. elegans is able to sense light and engages in phototaxis behavior that is 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, we found that phototransduction in ASJ is a G protein–mediated process and requires membrane-associated guanylate cyclases, but not typical phosphodiesterases. In addition, we found that C. elegans phototransduction requires LITE-1, a candidate photoreceptor protein known to be a member of the invertebrate taste receptor family. Our genetic, pharmacological and electrophysiological data suggest a model in which LITE-1 transduces light signals in ASJ via G protein signaling, which leads to upregulation of the second messenger cGMP, followed by opening of cGMP-sensitive CNG channels and stimulation of photoreceptor cells. Our results identify a phototransduction cascade in C. elegans and implicate the function of a 'taste receptor' in phototransduction.

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Figure 1: Phototransduction in ASJ is a G protein–mediated process.
Figure 2: Phototransduction in ASJ requires membrane-associated guanylate cyclases.
Figure 3: Guanylate cyclases act downstream of G proteins and upstream of CNG channels to mediate phototransduction.
Figure 4: Light, GTPγS and cGMP activate the same type of CNG channels in photoreceptor cells.
Figure 5: LITE-1 is required for phototransduction in photoreceptor cells.
Figure 6: LITE-1 functions upstream of G proteins.
Figure 7: Transgenic expression of LITE-1 can confer photo-sensitivity to the photo-insensitive neuron ASI.

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Acknowledgements

We thank P. Hu, A. Kumar and B. Ye for comments, M. Koelle for PTX plasmid and B. Decaluwe and S. Gu for technical assistance. Some strains were obtained from the Caenorhabditis Genetics Center, the Oklahoma Knockout Consortium and S. Mitani. A.W. was supported by a predoctoral training grant from the National Eye Institute (T32EY13934 to The University of Michigan). J.G. and Z.X. received support from the Chinese 111 project (CB06081). This work was supported by grants from the National Institute of General Medical Sciences and a Pew scholar award to X.Z.S.X.

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J.L. performed most of the electrophysiological recordings and analyzed the data. A.W. carried out most of the molecular biology, genetic and behavioral experiments and analyzed the data. J.G. and Z.X. performed some of the molecular biology, genetic and behavioral experiments. Y.D. and L.K. carried out some of the recordings. N.N., H.I. and I.M. isolated pde mutants. A.W. and D.M. isolated lite-1 mutants. A.W., Y.Y. and T.X. mapped lite-1 mutants. X.Z.S.X. supervised the project and wrote the paper with help from all of the other authors.

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Correspondence to X Z Shawn Xu.

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Liu, J., Ward, A., Gao, J. et al. C. elegans phototransduction requires a G protein–dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13, 715–722 (2010). https://doi.org/10.1038/nn.2540

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