Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Deciphering the Genes for Taste Receptors for Fructose in Drosophila

  • Uchizono, Shun (Graduate School of Systems Life Sciences, Kyushu University) ;
  • Itoh, Taichi Q. (Graduate School of Systems Life Sciences, Kyushu University) ;
  • Kim, Haein (Department of Biological Sciences, Sungkyunkwan University) ;
  • Hamada, Naoki (Research Fellow of Japan Society for the Promotion of Science) ;
  • Kwon, Jae Young (Department of Biological Sciences, Sungkyunkwan University) ;
  • Tanimura, Teiichi (Graduate School of Systems Life Sciences, Kyushu University)
  • Received : 2017.02.02
  • Accepted : 2017.08.20
  • Published : 2017.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Taste sensitivity to sugars plays an essential role in the initiation of feeding behavior. In Drosophila melanogaster, recent studies have identified several gustatory receptor (Gr) genes required for sensing sweet compounds. However, it is as yet undetermined how these GRs function as taste receptors tuned to a wide range of sugars. Among sugars, fructose has been suggested to be detected by a distinct receptor from other sugars. While GR43A has been reported to sense fructose in the brain, it is not expressed in labellar gustatory receptor neurons that show taste response to fructose. In contrast, the Gr64a-Gr64f gene cluster was recently shown to be associated with fructose sensitivity. Here we sought to decipher the genes required for fructose response among Gr64a-Gr64f genes. Unexpectedly, the qPCR analyses for these genes show that labellar expression levels of Gr64d and Gr64e are higher in fructose low-sensitivity flies than in high-sensitivity flies. Moreover, gustatory nerve responses to fructose in labellar sensilla are higher in Gr64d and Gr64f mutant lines than in mutant flies of the other Gr64a-Gr64f genes. These data suggest the possibility that deletion of GR64D or GR64F may indirectly induce enhanced fructose sensitivity in the labellum. Finally, we conclude that response to fructose cannot be explained by a single one of the Gr64a-Gr64f genes.

Keywords

References

  1. Dahanukar, A., Foster, K., van der Goes van Naters, W.M., and Carlson, J.R. (2001). A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4, 1182-1186. https://doi.org/10.1038/nn765
  2. Dahanukar, A., Lei, Y.T., Kwon, J.Y., and Carlson, J.R. (2007). Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503-516. https://doi.org/10.1016/j.neuron.2007.10.024
  3. Damak, S., Rong, M., Yasumatsu, K., Kokrashvili, Z., Varadarajan, V., Zou, S., Jiang, P., Ninomiya, Y., and Margolskee, R.F. (2003). Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301, 850-853. https://doi.org/10.1126/science.1087155
  4. Fujii, S., Yavuz, A., Slone, J., Jagge, C., Song, X., and Amrein, H. (2015). Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing. Curr. Biol. 25, 621-627. https://doi.org/10.1016/j.cub.2014.12.058
  5. Hiroi, M., Meunier, N., Marion-Poll, F., and Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333-342. https://doi.org/10.1002/neu.20063
  6. Huang, W., Massouras, A., Inoue, Y., Peiffer, J., Ràmia, M., Tarone, A.M., Turlapati, L., Zichner, T., Zhu, D., Lyman, R.F., et al. (2014). Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 24, 1193-1208. https://doi.org/10.1101/gr.171546.113
  7. Jiao, Y., Moon, S.J., and Montell, C. (2007). A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc. Natl. Acad. Sci. USA 104, 14110-14115. https://doi.org/10.1073/pnas.0702421104
  8. Jiao, Y., Moon, S.J., Wang, X., Ren, Q., and Montell, C. (2008). Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18, 1797-1801. https://doi.org/10.1016/j.cub.2008.10.009
  9. Li, X., Staszewski, L., Xu, H., Durick, K., Zoller, M., and Adler, E. (2002). Human receptors for sweet and umami taste. Proc. Natl. Acad. Sci. USA 99, 4692-4696. https://doi.org/10.1073/pnas.072090199
  10. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the $2^{−{\Delta}{\Delta}CT}$ method. Methods 25, 402-408. https://doi.org/10.1006/meth.2001.1262
  11. Mackay, T.F.C., Richards, S., Stone, E.A., Barbadilla, A., Ayroles, J.F., Zhu, D., Casillas, S., Han, Y., Magwire, M.M., Cridland, J.M., et al. (2012). The Drosophila melanogaster Genetic Reference Panel. Nature 482, 173-178. https://doi.org/10.1038/nature10811
  12. Miyamoto, T., Slone, J., Song, X., and Amrein, H. (2012). A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151, 1113-1125. https://doi.org/10.1016/j.cell.2012.10.024
  13. Montell, C. (2009). A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19, 345-353. https://doi.org/10.1016/j.conb.2009.07.001
  14. Nelson, G., Hoon, M.A., Chandrashekar, J., Zhang, Y., Ryba, N.J.P., and Zuker, C.S. (2001). Mammalian sweet taste receptors. Cell 106, 381-390. https://doi.org/10.1016/S0092-8674(01)00451-2
  15. Slone, J., Daniels, J., and Amrein, H. (2007). Sugar receptors in Drosophila. Curr. Biol. 17, 1809-1816. https://doi.org/10.1016/j.cub.2007.09.027
  16. Stocker, R.F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a rewiew. Cell Tissue Res. 275, 3-26. https://doi.org/10.1007/BF00305372
  17. Tanimura, T., Isono, K., Takamura, T., and Shimada, I. (1982). Genetic dimorphism in the taste sensitivity to trehalose in Drosophila melanogaster. J. Comp. Physiol. 147, 433-437. https://doi.org/10.1007/BF00612007
  18. Uchizono, S., and Tanimura, T. (2017). Genetic variation in taste sensitivity to sugars in Drosophila melanogaster. Chem. Senses 42, 287-294. https://doi.org/10.1093/chemse/bjw165
  19. Ueno, K., Ohta, M., Morita, H., Mikuni, Y., Nakajima, S., Yamamoto, K., and Isono, K. (2001). Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr. Biol. 11, 1451-1455. https://doi.org/10.1016/S0960-9822(01)00450-X
  20. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D., and Carlson, J.R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
  21. Yavuz, A., Jagge, C., Slone, J., and Amrein, H. (2014). A genetic tool kit for cellular and behavioral analyses of insect sugar receptors. Fly 8, 189-196. https://doi.org/10.1080/19336934.2015.1050569
  22. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J.P., and Zuker, C.S. (2003). The receptors for mammalian sweet and umami taste. Cell 115, 255-266. https://doi.org/10.1016/S0092-8674(03)00844-4

Cited by

  1. Drosophila Gr64e mediates fatty acid sensing via the phospholipase C pathway vol.14, pp.2, 2017, https://doi.org/10.1371/journal.pgen.1007229
  2. On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet vol.72, pp.1, 2017, https://doi.org/10.1146/annurev-arplant-080620-010429