All Title Author
Keywords Abstract

PLOS ONE  2008 

Hedonic Taste in Drosophila Revealed by Olfactory Receptors Expressed in Taste Neurons

DOI: 10.1371/journal.pone.0002610

Full-Text   Cite this paper   Add to My Lib


Taste and olfaction are each tuned to a unique set of chemicals in the outside world, and their corresponding sensory spaces are mapped in different areas in the brain. This dichotomy matches categories of receptors detecting molecules either in the gaseous or in the liquid phase in terrestrial animals. However, in Drosophila olfactory and gustatory neurons express receptors which belong to the same family of 7-transmembrane domain proteins. Striking overlaps exist in their sequence structure and in their expression pattern, suggesting that there might be some functional commonalities between them. In this work, we tested the assumption that Drosophila olfactory receptor proteins are compatible with taste neurons by ectopically expressing an olfactory receptor (OR22a and OR83b) for which ligands are known. Using electrophysiological recordings, we show that the transformed taste neurons are excited by odor ligands as by their cognate tastants. The wiring of these neurons to the brain seems unchanged and no additional connections to the antennal lobe were detected. The odor ligands detected by the olfactory receptor acquire a new hedonic value, inducing appetitive or aversive behaviors depending on the categories of taste neurons in which they are expressed i.e. sugar- or bitter-sensing cells expressing either Gr5a or Gr66a receptors. Taste neurons expressing ectopic olfactory receptors can sense odors at close range either in the aerial phase or by contact, in a lipophilic phase. The responses of the transformed taste neurons to the odorant are similar to those obtained with tastants. The hedonic value attributed to tastants is directly linked to the taste neurons in which their receptors are expressed.


[1]  Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci U S A 101: 2584–2589.
[2]  Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, et al. (2005) The receptors and coding logic for bitter taste. Nature 434: 225–229.
[3]  Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, et al. (2003) The receptors for mammalian sweet and umami taste. Cell 115: 255–266.
[4]  Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, et al. (2006) The cells and logic for mammalian sour taste detection. Nature 442: 934–938.
[5]  Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, et al. (2006) Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci U S A 103: 12569–12574.
[6]  Accolla R, Bathellier B, Petersen CCH, Carleton A (2007) Differential spatial representation of taste modalities in the rat gustatory cortex. J Neurosci 27: 1396–1404.
[7]  Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4: e20.
[8]  Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595–631.
[9]  Ray A, van der Goes van Naters W, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53: 353–369.
[10]  Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102: 147–159.
[11]  Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965–979.
[12]  Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48: 455–484.
[13]  Rogers SM, Newland PL (2003) The neurobiology of taste in insects. Adv Insect Physiol 31: 141–204.
[14]  Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51: 113–135.
[15]  Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, et al. (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104: 661–673.
[16]  Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14: 1065–1079.
[17]  Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117: 981–991.
[18]  Moon SJ, Kottgen M, Jiao YC, Xu H, Montell C (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16: 1812–1817.
[19]  Chyb S, Dahanukar A, Wickens A, Carlson JR (2003) Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci U S A 100: 14526–14530.
[20]  Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35: 279–295.
[21]  Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, et al. (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 2: e661.
[22]  Tsuchihara K, Fujikawa K, Ishiguro M, Yamada T, Tada C, et al. (2005) An odorant-binding protein facilitates odorant transfer from air to hydrophilic surroundings in the blowfly. Chem Senses 30: 559–564.
[23]  Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40: 171–194.
[24]  Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5: e118.
[25]  Koganezawa M, Shimada I (2002) Novel odorant-binding proteins expressed in the taste tissue of the fly. Chem Senses 27: 319–332.
[26]  Galindo K, Smith DP (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159: 1059–1072.
[27]  Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Gen Res 12: 1357–1369.
[28]  Ozaki M, Takahara T, Kawahara Y, Wada-Katsumata A, Seno K, et al. (2003) Perception of noxious compounds by contact chemoreceptors of the blowfly, Phormia regina: putative role of an odorant-binding protein. Chem Senses 28: 349–359.
[29]  Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100: 14537–14542.
[30]  Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63: 1256–1272.
[31]  Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51: 505–517.
[32]  Lundin C, Kall L, Kreher SA, Kapp K, Sonnhammer EL, et al. (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581: 5601–5604.
[33]  Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, et al. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452: 1002–U1009.
[34]  Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, et al. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452: 1007–U1010.
[35]  Neuhaus EM, Gisselmann G, Zhang WY, Dooley R, St?rtkuhl K, et al. (2005) Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 8: 15–17.
[36]  Hodgson ES, Roeder KD (1954) Electrical response of insect chemosensory neurons to normal stimuli. Anat Rec 120: 718.
[37]  Falk R, Atidia J (1975) Mutation affecting taste perception in Drosophila melanogaster. Nature 254: 325–326.
[38]  Shanbhag SR, Park SK, Pikielny CW, Steinbrecht RA (2001) Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorant-binding protein PBPRP2. Cell Tissue Res 304: 423–437.
[39]  Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster - a review. Cell Tissue Res 275: 3–26.
[40]  Hiroi M, Meunier N, Marion-Poll F, Tanimura T (2004) Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J Neurobiol 61: 333–342.
[41]  de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30: 537–552.
[42]  Dahanukar A, Lei Y-T, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56: 503–516.
[43]  Ueno K, Ohta M, Morita H, Mikuni Y, Nakajima S, et al. (2001) Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol 11: 1451–1455.
[44]  Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.
[45]  Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, et al. (2005) Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol 15: 2086–2096.
[46]  de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19: 4520–4532.
[47]  Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci U S A 104: 3574–3578.
[48]  Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo- and hygroreceptors and its functional significance. Int Rev Cytol 67: 69–139.
[49]  Haupt S (2007) Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee. J Comp Physiol A 193: 523–535.
[50]  Jorgensen K, Kvello P, Almaas TJ, Mustaparta H (2006) Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens. J Comp Neurol 496: 121–134.
[51]  Nishino H, Nishikawa M, Yokohari F, Mizunami M (2005) Dual, multilayered somatosensory maps formed by antennal tactile and contact chemosensory afferents in an insect brain. J Comp Neurol 493: 291–308.
[52]  Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, et al. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43: 703–714.
[53]  St?dler E, Hanson FE (1975) Olfactory capabilities of the ‘gustatory’ chemoreceptors of the tobacco hornworm larvae. J Comp Physiol A 104: 97–102.
[54]  Mitchell BK, McCashin BG (1994) Tasting green leaf volatiles by larvae and adults of Colorado potato beetle, Leptinotarsa decemlineata. J Chem Ecol 20: 753–769.
[55]  Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307: 1638–1642.
[56]  Kain P, Chakraborty TS, Sundaram S, Siddiqi O, Rodrigues V, et al. (2008) Reduced odor responses from antennal neurons of Gqα, phospholipase Cβ, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J Neurosci 28: 4745–4755.
[57]  Murakami M, Kijima H (2000) Transduction ion channels directly gated by sugars on the insect taste cell. J Gen Physiol 115: 455–466.
[58]  Ahamed A, Tsurumi S, Ozaki M, Amakawa T (2001) An artificial sweetener stimulates the sweet taste in insect: dual effects of glycyrrhizin in Phormia regina. Chem Senses 26: 507–515.
[59]  Jiao Y, Moon SJ, Montell C (2007) A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A 104: 14110–14115.
[60]  Slone J, Daniels J, Amrein H (2007) Sugar receptors in Drosophila. Curr Biol 17: 1809–1816.
[61]  Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, et al. (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49: 285–295.
[62]  Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11: 822–835.
[63]  Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, et al. (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112: 293–301.
[64]  Glendinning JI, Brown H, Capoor M, Davis A, Gbedemah A, et al. (2001) A peripheral mechanism for behavioral adaptation to specific “bitter” taste stimuli in an insect. J Neurosci 21: 3688–3696.
[65]  del Campo ML, Miles CI, Schroeder FC, Mueller C, Booker R, et al. (2001) Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411: 186–189.
[66]  Silverman J, Selbach H (1998) Feeding behavior and survival of glucose-averse Blattella germanica (Orthoptera : Blattoidea : Blattellidae) provided glucose as a sole food source. J Insect Behav 11: 93–102.
[67]  Yang C-h, Belawat P, Hafen E, Jan LY, Jan Y-N (2008) Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319: 1679–1683.


comments powered by Disqus