Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol

Nature Neuroscience volume 14, pages 1534–1541 (2011)Cite this article

Subjects

Abstract

Very little is known about how stimuli that are typically not rich in sugars, such as beer, trigger attractive gustatory responses in Drosophila. We identified a member of the gustatory receptor family, Gr64e, as a receptor that is required for feeding preference for beer and other sources that have fermenting yeast. We found that Gr64e is required for neuronal and behavioral responses to glycerol, an abundant component of growing yeast and fermentation products. Ectopic expression of Gr64e in an olfactory neuron conferred responsiveness to glycerol. We also found that Drosophila species that are predicted to carry pseudogenes of Gr64e had reduced glycerol sensitivity. Our results provide insight into the molecular mechanisms of feeding acceptance of yeast products and raise the possibility that Gr64e contributes to specific evolutionary variations in appetitive selectivity across Drosophila species.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Feeding preference to yeast fermentation products is reduced in Gr64e mutants.
Figure 2: Gr64e-GAL4 is broadly expressed in taste acceptance neurons.
Figure 3: Gr64e is necessary for glycerol recognition in sugar-sensing taste neurons.
Figure 4: Gr64e is necessary for behavioral responses to glycerol.
Figure 5: Heterologous expression of Gr64e in the ab1C olfactory neuron confers sensitivity to glycerol.
Figure 6: Gr64e pseudogenization correlates with absence of cellular response to glycerol.
Figure 7: Gr64e pseudogenization correlates with reduced behavioral response to glycerol.

Similar content being viewed by others

References

  1. Amrein, H. & Thorne, N. Gustatory perception and behavior in Drosophila melanogaster. Curr. Biol. 15, R673–R684 (2005).

    Article  CAS  Google Scholar 

  2. Gordesky-Gold, B., Rivers, N., Ahmed, O.M. & Breslin, P.A. Drosophila melanogaster prefers compounds perceived sweet by humans. Chem. Senses 33, 301–309 (2008).

    Article  CAS  Google Scholar 

  3. Keller, A. Drosophila melanogaster's history as a human commensal. Curr. Biol. 17, R77–R81 (2007).

    Article  CAS  Google Scholar 

  4. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065–1079 (2004).

    Article  CAS  Google Scholar 

  5. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981–991 (2004).

    Article  CAS  Google Scholar 

  6. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285–295 (2006).

    Article  CAS  Google Scholar 

  7. Dahanukar, A., Lei, Y.T., Kwon, J.Y. & Carlson, J.R. Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503–516 (2007).

    Article  CAS  Google Scholar 

  8. Fischler, W., Kong, P., Marella, S. & Scott, K. The detection of carbonation by the Drosophila gustatory system. Nature 448, 1054–1057 (2007).

    Article  CAS  Google Scholar 

  9. Robertson, H.M., Warr, C.G. & Carlson, J.R. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100, 14537–14542 (2003).

    Article  CAS  Google Scholar 

  10. Kent, L.B. & Robertson, H.M. Evolution of the sugar receptors in insects. BMC Evol. Biol. 9, 41 (2009).

    Article  Google Scholar 

  11. Dahanukar, A., Foster, K., van der Goes van Naters, W.M. & Carlson, J.R. A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4, 1182–1186 (2001).

    Article  CAS  Google Scholar 

  12. Jiao, Y., Moon, S.J. & Montell, C. 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 (2007).

    Article  CAS  Google Scholar 

  13. Slone, J., Daniels, J. & Amrein, H. Sugar receptors in Drosophila. Curr. Biol. 17, 1809–1816 (2007).

    Article  CAS  Google Scholar 

  14. Jiao, Y., Moon, S.J., Wang, X., Ren, Q. & Montell, C. Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18, 1797–1801 (2008).

    Article  CAS  Google Scholar 

  15. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D. & Carlson, J.R. The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258–272 (2011).

    Article  CAS  Google Scholar 

  16. Bamforth, C.W. Beer, carbohydrates and diet. J. Inst. Brew. 111, 259–264 (2005).

    Article  CAS  Google Scholar 

  17. Intelmann, D. et al. Three TAS2R bitter taste receptors mediate the psychophysical responses to bitter compounds of hops (Humulus lupulus L.) and beer. Chemosens. Percept. 2, 118–132 (2009).

    Article  Google Scholar 

  18. Larsson, M.C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004).

    Article  CAS  Google Scholar 

  19. Benton, R., Sachse, S., Michnick, S.W. & Vosshall, L.B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006).

    Article  Google Scholar 

  20. Benton, R., Vannice, K.S., Gomez-Diaz, C. & Vosshall, L.B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162 (2009).

    Article  CAS  Google Scholar 

  21. Abuin, L. et al. Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69, 44–60 (2011).

    Article  CAS  Google Scholar 

  22. Li, X. et al. Pseudogenization of a sweet-receptor gene accounts for cats' indifference toward sugar. PLoS Genet. 1, 27–35 (2005).

    Article  CAS  Google Scholar 

  23. Robertson, H.M. The insect chemoreceptor superfamily in Drosophila pseudoobscura: molecular evolution of ecologically relevant genes over 25 million years. J. Insect Sci. 9, 1–18 (2009).

    Google Scholar 

  24. Stocker, R.F. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3–26 (1994).

    Article  CAS  Google Scholar 

  25. Falk, R., Bleiser-Avivi, N. & Atidia, J. Labellar taste organs of Drosophila melanogaster. J. Morphol. 150, 327–341 (1976).

    Article  Google Scholar 

  26. André, L., Hemming, A. & Adler, L. Osmoregulation in Saccharomyces cerevisiae. Studies on the osmotic induction of glycerol production and glycerol-3-phosphate dehydrogenase (NAD+). FEBS Lett. 286, 13–17 (1991).

    Article  Google Scholar 

  27. Dethier, V.G. The physiology and histology of the contact chemoreceptors of the blowfly. Q. Rev. Biol. 30, 348–371 (1955).

    Article  CAS  Google Scholar 

  28. Koseki, T., Koganezawa, M., Furuyama, A., Isono, K. & Shimada, I. A specific receptor site for glycerol, a new sweet tastant for Drosophila: structure-taste relationship of glycerol in the labellar sugar receptor cell. Chem. Senses 29, 703–711 (2004).

    Article  CAS  Google Scholar 

  29. Koseki, T., Koganezawa, M., Furuyama, A., Isono, K. & Shimada, I. Stereospecificity of the receptor site for glycerol, a new sweetener, in a labellar sugar receptor cell of Drosophila. Chem. Senses 30 (suppl. 1, i277–i278 (2005).

    Article  CAS  Google Scholar 

  30. Hiroi, M., Marion-Poll, F. & Tanimura, T. Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog. Sci. 19, 1009–1018 (2002).

    Article  Google Scholar 

  31. Hiroi, M., Meunier, N., Marion-Poll, F. & Tanimura, T. Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333–342 (2004).

    Article  Google Scholar 

  32. Wieczorek, H. & Wolff, G. The labellar sugar receptor of Drosophila. J. Comp. Physiol. [A] 164, 825–834 (1989).

    Article  Google Scholar 

  33. de Bruyne, M., Foster, K. & Carlson, J.R. Odor coding in the Drosophila antenna. Neuron 30, 537–552 (2001).

    Article  CAS  Google Scholar 

  34. Jones, W.D., Cayirlioglu, P., Kadow, I.G. & Vosshall, L.B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86–90 (2007).

    Article  CAS  Google Scholar 

  35. Kwon, J.Y., Dahanukar, A., Weiss, L.A. & Carlson, J.R. The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. USA 104, 3574–3578 (2007).

    Article  CAS  Google Scholar 

  36. Montell, C. A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19, 345–353 (2009).

    Article  CAS  Google Scholar 

  37. Lee, Y., Moon, S.J. & Montell, C. Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106, 4495–4500 (2009).

    Article  CAS  Google Scholar 

  38. Lee, Y., Kim, S.H. & Montell, C. Avoiding DEET through insect gustatory receptors. Neuron 67, 555–561 (2010).

    Article  CAS  Google Scholar 

  39. Yarmolinsky, D.A., Zuker, C.S. & Ryba, N.J. Common sense about taste: from mammals to insects. Cell 139, 234–244 (2009).

    Article  CAS  Google Scholar 

  40. da Cunha, A.B., Dobzhansky, T. & Sokoloff, A. On food preferenes of sympatric species of Drosophila. Evolution 5, 97–101 (1951).

    Article  Google Scholar 

  41. Dobzhansky, T. Differential attraction of species of Drosophila to different species of yeasts. Ecology 37, 544–550 (1956).

    Article  Google Scholar 

  42. da Cunha, A.B., El-Tabey Shehata, A.M. & de Oliveira, W. A study of the diets and nutritional preferences of tropical species of Drosophila. Ecology 38, 98–106 (1957).

    Article  Google Scholar 

  43. Cooper, D.M. Food preferences of larval and adult Drosophila. Evolution 14, 41–55 (1960).

    Article  Google Scholar 

  44. Mattick, L.R. & Rice, A.C. Survey of the glycerol content of New York State wines. Am. J. Enol. Vitic. 21, 213–215 (1970).

    Google Scholar 

  45. Klopper, W.J., Angelino, S.A.G.F., Tunning, B. & Vermeire, H.A. Organic acids and glycerol in beer. J. Inst. Brew. 92, 225–228 (1986).

    Article  CAS  Google Scholar 

  46. Scanes, K.T., Hohmann, S. & Prior, B.A. Glycerol production by the yeast Saccharomyces cerevisiae and its relavance to wine: a review. S. Afr. J. Enol. Viti. 19, 17–24 (1998).

    CAS  Google Scholar 

  47. Brandolini, V. et al. Automated multiple development method for determination of glycerol produced by wine yeasts. World J. Microbiol. Biotechnol. 18, 481–485 (2002).

    Article  CAS  Google Scholar 

  48. Rosini, G., Federici, F. & Martini, A. Yeast flora of grape berries during ripening. Microb. Ecol. 8, 83–89 (1982).

    Article  CAS  Google Scholar 

  49. Romano, P., Suzzi, G., Comi, G., Zironi, R. & Maifreni, M. Glycerol and other fermentation products of apiculate wine yeasts. J. Appl. Microbiol. 82, 615–618 (1997).

    Article  CAS  Google Scholar 

  50. Dobritsa, A.A., van der Goes van Naters, W., Warr, C.G., Steinbrecht, R.A. & Carlson, J.R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827–841 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank W. Tom and A. Ray for help with olfactory single-sensillum recordings, K. Risser for initial behavioral analysis, members of the Dahanukar and Ray laboratories for helpful discussions, and A. Ray, S. Charlu and S. Siemens for comments on the manuscript. This research was supported in part by a Whitehall Foundation Research grant (2010-12-42, to A.D.) and a fellowship from the National Science Foundation Integrated Graduate Education Research and Training Program in Video Bioinformatics (DGE0903667 to E.F.)

Author information

Authors and Affiliations

  1. Interdepartmental Neuroscience Program, University of California, Riverside, California, USA

    Zev Wisotsky & Anupama Dahanukar

  2. Department of Entomology, University of California, Riverside, California, USA

    Adriana Medina & Anupama Dahanukar

  3. Bioengineering Interdepartmental Graduate Program, University of California, Riverside, California, USA

    Erica Freeman & Anupama Dahanukar

Authors
  1. Zev Wisotsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adriana Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erica Freeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anupama Dahanukar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Z.W. performed imaging, taste electrophysiology and behavior experiments. A.M. performed feeding preference experiments and molecular analysis. E.F. performed olfactory recordings. Z.W., A.M., E.F. and A.D. analyzed the data. A.D. supervised the project and wrote the paper with Z.W. and E.F.

Corresponding author

Correspondence to Anupama Dahanukar.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7 (PDF 1381 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wisotsky, Z., Medina, A., Freeman, E. et al. Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nat Neurosci 14, 1534–1541 (2011). https://doi.org/10.1038/nn.2944

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2944

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing