Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Gustatory Receptors Required for Avoiding the Toxic Compound Coumarin in Drosophila melanogaster

  • Poudel, Seeta (Department of Bio and Fermentation Convergence Technology, BK21 PLUS Project, Kookmin University) ;
  • Lee, Youngseok (Department of Bio and Fermentation Convergence Technology, BK21 PLUS Project, Kookmin University)
  • Received : 2015.09.25
  • Accepted : 2015.12.17
  • Published : 2016.04.30
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Abstract

Coumarin is a phenolic compound that mainly affects the liver due to its metabolization into a toxic compound. The deterrent and ovicidal activities of coumarin in insect models such as Drosophila melanogaster have been reported. Here we explore the molecular mechanisms by which these insects protect themselves and their eggs from this toxic plant metabolite. Coumarin was fatal to the flies in a dosage-dependent manner. However, coumarin feeding could be inhibited through activation of the aversive gustatory receptor neurons (GRNs), but not the olfactory receptor neurons. Furthermore, three gustatory receptors, GR33a, GR66a, and GR93a, functioned together in coumarin detection by the proboscis. However, GR33a, but not GR66a and GR93a, was required to avoid coumarin during oviposition, with a choice of the same substrates provided as in binary food choice assay. Taken together, these findings suggest that anti-feeding activity and oviposition to avoid coumarin occur via separate mechanisms.

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References

  1. Chyb, S., Dahanukar, A., Wickens, A., and Carlson, J.R. (2003). Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl. Acad. Sci. USA 100, 14526-14530. https://doi.org/10.1073/pnas.2135339100
  2. Dahanukar, A., Foster, K., 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
  3. 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
  4. Dolan, L. C., Matulka, R.A., and Burdock, G.A. (2010). Naturally occurring food toxins. Toxins 2, 2289-2332. https://doi.org/10.3390/toxins2092289
  5. Dunipace, L., Meister, S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835. https://doi.org/10.1016/S0960-9822(01)00258-5
  6. Dweck, H.K., Ebrahim, S.A., Kromann, S., Bown, D., Hillbur, Y., Sachse, S., Hansson, B.S., and Stensmyr, M.C. (2013). Olfactory preference for egg laying on citrus substrates in Drosophila. Curr. Biol. 23, 2472-2480. https://doi.org/10.1016/j.cub.2013.10.047
  7. Hiroi, M., Marion-Poll, F., and Tanimura, T. (2002). Differentiated response to sugars among labellar chemosensilla in Drosophila. Zool. Sci. 19, 1009-1018. https://doi.org/10.2108/zsj.19.1009
  8. Hiroi, M., Meunier, N., Marion-Poll, F., and Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweetsalty and bitter taste in Drosophila. J. Neurobiol. 61, 333-342. https://doi.org/10.1002/neu.20063
  9. 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
  10. 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
  11. Joseph, R. M., and Heberlein, U. (2012). Tissue-specific activation of a single gustatory receptor produces opposing behavioral responses in Drosophila. Genetics 192, 521-532. https://doi.org/10.1534/genetics.112.142455
  12. Kacsoh, B.Z., Lynch, Z.R., Mortimer, N.T., and Schlenke, T.A. (2013). Fruit flies medicate offspring after seeing parasites. Science. 339, 947-950. https://doi.org/10.1126/science.1229625
  13. Lake, B. (1999). Coumarin metabolism, toxicity and carcinogenicity: relevance for human risk assessment. Food Chem. Toxicol. 37, 423-453. https://doi.org/10.1016/S0278-6915(99)00010-1
  14. Larsson, M.C., Domingos, A.I., Jones, W.D., Chiappe, M.E., Amrein, H., and Vosshall, L.B. (2004). Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714. https://doi.org/10.1016/j.neuron.2004.08.019
  15. Lee, Y., Moon, S.J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106, 4495-4500. https://doi.org/10.1073/pnas.0811744106
  16. Lee, Y., Kim, S.H., and Montell, C. (2010). Avoiding DEET through Insect gustatory receptors. Neuron 67, 555-561. https://doi.org/10.1016/j.neuron.2010.07.006
  17. Lee, Y., Kang, M.J., Shim, J., Cheong, C.U., Moon, S.J., and Montell, C. (2012). Gustatory receptors required for avoiding the insecticide L-canavanine. J. Neurosci. 32, 1429-1435. https://doi.org/10.1523/JNEUROSCI.4630-11.2012
  18. Lee, Y., and Poudel, S. (2014). Taste sensation in Drosophila melanoganster. Hanyang Med. Rev. 34, 130-136. https://doi.org/10.7599/hmr.2014.34.3.130
  19. Lee, Y., Moon, S.J., Wang, Y., and Montell, C. (2015). A Dro-sophila gustatory receptor required for strychnine sensation. Chem. Senses 40, 525-533. https://doi.org/10.1093/chemse/bjv038
  20. Meunier, N., Marion-Poll, F., Rospars, J. P., and Tanimura, T. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152. https://doi.org/10.1002/neu.10235
  21. Miyamoto, T., and Amrein, H. (2008). Suppression of male courtship by a Drosophila pheromone receptor. Nat. Neurosci. 11, 874-876. https://doi.org/10.1038/nn.2161
  22. 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
  23. 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
  24. Moon, S.J., Köttgen, M., Jiao, Y., Xu, H., and Montell, C. (2006). A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812-1817. https://doi.org/10.1016/j.cub.2006.07.024
  25. Moon, S.J., Lee, Y., Jiao, Y., and Montell, C. (2009). A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 1623-1627. https://doi.org/10.1016/j.cub.2009.07.061
  26. Nakajima, S., and Kawazu, K. (1980). Coumarin and euponin, two inhibitors for insect development from leaves of Eupatorium japonicum. Agr. Biol. Chem. 44, 2893-2899.
  27. Poudel, S., Kim, Y., Kim, Y.T., and Lee, Y. (2015). Gustatory receptors required for sensing umbelliferone in Drosophila melanogaster. Insect Biochem. Mol. 66, 110-118. https://doi.org/10.1016/j.ibmb.2015.10.010
  28. Robertson, H.M., Warr, C.G., and Carlson, J.R. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100, 14537-14542. https://doi.org/10.1073/pnas.2335847100
  29. Schwartz, N.U., Zhong, L., Bellemer, A., and Tracey, W.D. (2012). Egg laying decisions in Drosophila are consistent with foraging costs of larval progeny. PLoS One 7, e37910. https://doi.org/10.1371/journal.pone.0037910
  30. Scott, K., Brady Jr, R., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., and Axel, R. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673. https://doi.org/10.1016/S0092-8674(01)00263-X
  31. Shim, J., Lee, Y., Jeong, Y.T., Kim, Y., Lee, M.G., Montell, C., and Moon, S.J. (2015). The full repertoire of Drosophila gustatory receptors for detecting an aversive compound. Nat. Commun. 6, 8867. https://doi.org/10.1038/ncomms9867
  32. Singleton, V.L. (1981). Naturally occurring food toxicants: phenolic substances of plant origin common in foods. Adv. Food Res. 27, 149-242. https://doi.org/10.1016/S0065-2628(08)60299-2
  33. Smith, M.T., Yager, J.W., Steinmetz, K.L., and Eastmond, D.A. (1989). Peroxidase-dependent metabolism of Benzene's phenolic metabolites and its potential role in Benzene toxicity and carcinogenicity. Environ. Health Persp. 82, 23-29. https://doi.org/10.1289/ehp.898223
  34. Stocker, R., and Schorderet, M. (1981). Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res. 216, 513-523.
  35. Thorne, N., Chromey, C., Bray, S., and Amrein, H. (2004). Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079. https://doi.org/10.1016/j.cub.2004.05.019
  36. 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
  37. Wang, Z., Singhvi, A., Kong, P., and Scott, K. (2004). Taste representations in the Drosophila brain. Cell 117, 981-991. https://doi.org/10.1016/j.cell.2004.06.011
  38. 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
  39. Yang, C.H., Belawat, P., Hafen, E., Jan, L.Y., and Jan, Y.N. (2008). Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319, 1679-1683. https://doi.org/10.1126/science.1151842

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