Dual mechanism for bitter avoidance in drosophila

Journal of Neuroscience

Volumn 35, Issue 9, 2015, Pages 3990-4004

  Sarah French, Alice ^a,b,g   Sellier, Marie Jeanne ^a,b   Agha Moutaz, Ali ^a,g   Guigue, Alexandra ^a,b   Chabaud, Marie Ange ^a   Reeb, Pablo D ^c   Mitra, Aniruddha ^g   Grau, Yves ^d,e,f   Soustelle, Laurent ^d,e,f   Marion Poll, Fréd É Ric ^a,b,g  

^a UPMC University Paris 06   (France)

^b AGROPARISTECH   (France)

^c UNIVERSIDAD NACIONAL DEL COMAHUE   (Argentina)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^e INSERM   (France)

^f UNIV MONTPELLIER   (France)

^g France and University of Paris Sud   (France)

Author keywords

Behavior; Bitter; Drosophila; Electrophysiology; Mixture interaction; Sweet

Indexed keywords

CANAVANINE; RHODOPSIN; STRYCHNINE; SUCROSE; SYNAPTOBREVIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; BITTER TASTE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; DIPTERA; DROSOPHILA; ELECTRICAL STIMULUS TEST; ELECTROPHYSIOLOGICAL PROCEDURES; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; MULTIPLE CHOICE CAPILLARY FEEDER TEST; NERVE CELL INHIBITION; NERVE STIMULATION; NEUROTRANSMISSION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; SENSILLUM; STIMULATION; SYNAPSE; TWO CHOICE FEEDING TEST; ANIMAL; ANIMAL BEHAVIOR; DROSOPHILA MELANOGASTER; INNERVATION; LIMB; PHYSIOLOGY; SENSORY NERVE CELL; TASTE;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; EXTREMITIES; FEMALE; OPTOGENETICS; RHODOPSIN; SENSILLA; SENSORY RECEPTOR CELLS; STIMULATION, CHEMICAL; TASTE;

EID: 84924794752     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1312-14.2015     Document Type: Article

References (96)

1. Bjordal M, Arquier N, Kniazeff J, Pin JP, Leopold P (2014) Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell 156:510–521.
2. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.
3. Burke CJ, Waddell S (2011) Remembering nutrient quality of sugar in Drosophila. Curr Biol 21:746–750.
4. Cameron P, Hiroi M, Ngai J, Scott K (2010) The molecular basis for water taste in Drosophila. Nature 465:91–95.
5. Cao Y, Zhao FL, Kolli T, Hivley R, Herness S (2009) GABA expression in the mammalian taste bud functions as a route of inhibitory cell-to-cell communication. Proc Natl Acad Sci U S A 106:4006–4011.
6. Chandrashekar J, Hoon MA, Ryba NJP, Zuker CS (2006) The receptors and cells for mammalian taste. Nature 444:288–294.
7. Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48:455–484.
8. Chapman RF, Ascoli-Christensen A, White PR (1991) Sensory coding for feeding deterrence in the grasshopper Schistocerca americana. J Exp Biol 158:241–259.
9. Charlu S, Wisotsky Z, Medina A, Dahanukar A (2013) Acid sensing by sweet and bitter taste neurons in Drosophila melanogaster. Nat Commun 4:2042.
10. Chen Y, Amrein H (2014) Enhancing perception of contaminated food through acid-mediated modulation of taste neuron responses. Curr Biol 24:1969–1977.
11. Chen Z, Wang Q, Wang Z (2010) The amiloride-sensitive epithelial Na + channel PPK28 is essential for Drosophila gustatory water reception. J Neurosci 30:6247–6252.
12. Dahanukar A, Lei YT, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56:503–516.
13. Dando R, Roper SD (2009) Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. J Physiol 587:5899–5906.
14. de Brito Sanchez MG (2011) Taste perception in honey bees. Chem Senses 36:675–692.
15. Dethier VG (1980) Evolution ofreceptor sensitivity to secondary plant substances with special reference to deterrents. Am Naturalist 115:45–66.
16. Dethier VG (1987) Discriminative taste inhibitors affecting insects. Chem Senses 12:251–263.
17. Dethier VG, Bowdan E (1989) The effect ofalkaloids on sugar receptors and the feeding behaviour of the blowfly. Physiol Entomol 14:127–136.
18. Dethier VG, Bowdan E (1992) Effects ofalkaloids on feeding by Phormia regina confirm the critical role of sensory inhibition. Physiol Entomol 17:325–330.
19. Devambez I, Ali Agha M, Mitri C, Bockaert J, Parmentier ML, Marion-Poll F, Grau Y, Soustelle L (2013) Gao is required for L-canavanine detection in Drosophila. PLoS One 8:e63484.
20. Dong D, Jones G, Zhang S (2009) Dynamic evolution of bitter taste receptor genes in vertebrates. BMC Evol Biol 9:12.
21. Dus M, Min S, Keene AC, Lee GY, Suh GSB (2011) Taste-independent detection of the caloric content of sugar in Drosophila. Proc Natl Acad Sci USA 108:11644–11649.
22. Engsontia P, Sangket U, Chotigeat W, Satasook C (2014) Molecular evolution of the odorant and gustatory receptor genes in Lepidopteran insects: implications for their adaptation and speciation. J Mol Evol 79:21–39.
23. Formaker BK, MacKinnon BI, Hettinger TP, Frank ME (1997) Opponent effects of quinine and sucrose on single fiber taste responses of the chorda tympani nerve. Brain Res 772:239–242.
24. Frank ME, Formaker BK, Hettinger TP (2003) Taste responses to mixtures: analytic processing of quality. Behav Neurosci 117:228–235.
25. Frank ME, Formaker BK, Hettinger TP (2005) Peripheral gustatory processing of sweet stimuli by golden hamsters. Brain Res Bull 66:70–84.
26. Fujishiro N, Kijima H, Morita H (1984) Impulse frequency and action potential amplitude in the labellar chemosensory neurones of Drosophila melanogaster. J Insect Physiol 30:317–325.
27. Fujita M, Tanimura T (2011) Drosophilaevaluates and learns the nutritional value of sugars. Curr Biol 21:751–755.
28. Galindo-Cuspinera V, Winnig M, Bufe B, Meyerhof W, Breslin PAS (2006) A TAS1R receptor-based explanation of sweet “water-taste.” Nature 441: 354–357.
29. Glendinning JI (1996) Is chemosensory input essential for the rapid rejection of toxic foods? J Exp Biol 199:1523–1534.
30. Glendinning JI (2002) How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol Exp Appl 104:15–25.
31. Glendinning JI (2007) How do predators cope with chemically defended foods? Biol Bull 213:252–266.
32. Gomez-Diaz C, Reina JH, Cambillau C, Benton R (2013) Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins. PLoS Biol 11:e1001546.
33. Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61:373–384.
34. Green BG, Lim J, Osterhoff F, Blacher K, Nachtigal D (2010) Taste mixture interactions: suppression, additivity, and the predominance of sweetness. Physiol Behav 101:731–737.
35. Gruber F, Knapek S, Fujita M, Matsuo K, Bräcker L, Shinzato N, Siwanowicz I, Tanimura T, Tanimoto H (2013) Suppression of conditioned odor approach by feeding is independent of taste and nutritional value in Dro-sophila. Curr Biol 23:507–514.
36. Herness S, Zhao FL (2009) The neuropeptides CCK and NPY and the changing view of cell-to-cell communication in the taste bud. Physiol Behav 97:581–591.
37. Hiroi M, Marion-Poll F, Tanimura T (2002) Differentiated response to sugars among labellar chemosensilla in Drosophila. Zool Sci 19:1009–1018.
38. 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.
39. Hiroi M, Tanimura T, Marion-Poll F (2008) Hedonic taste in Drosophila revealed by olfactory receptors expressed in taste neurons. PLoS One 3:e2610.
40. Hong W, Zhao HB (2014) Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats. Proc R Soc 281: 20141079.
41. Hornstein NJ, Pulver SR, Griffith LC (2009) Channelrhodopsin2 mediated stimulationof synaptic potentials at Drosophila neuromuscular junctions. J Vis Exp 25:e1133.
42. Imada T, Misaka T, Fujiwara S, Okada S, Fukuda Y, Abe K (2010) Amiloride reduces the sweet taste intensity by inhibiting the human sweet taste receptor. Biochem Biophys Res Commun 397:220–225.
43. Jeong YT, Shim J, Oh SR, Yoon HI, Kim CH, Moon SJ, Montell C (2013) An odorant-binding protein required for suppression of sweet taste by bitter chemicals. Neuron 79:725–737.
44. Jiang P, Josue J, Li X, Glaser D, Li W, Brand JG, Margolskee RF, Reed DR, Beauchamp GK (2012) Major taste loss in carnivorous mammals. Proc Natl Acad Sci U S A 109:4956–4961.
45. Keast SJR, Breslin PAS (2002) Anoverviewofbinary taste-taste interactions. Food Qual Prefer 14:111–124.
46. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubío JM, Ribeiro JM, Rozas J, etal. (2010) Genome sequencesof the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci U S A 107:12168–12173.
47. König C, Schleyer M, Leibiger J, El-Keredy A, Gerber B (2014) Bitter-sweet processing in larval Drosophila. Chem Senses 39:489–505.
48. Kool O (2005) Insect antifeedants. Boca Raton, FL: CRC.
49. Laughlin JD, Ha TS, Jones DNM, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133:1255–1265.
50. Lee Y, Kim SH, Montell C (2010) Avoiding DEET through insect gustatory receptors. Neuron 67:555–561.
51. Lee Y, Kang MJ, Shim J, Cheong CU, Moon SJ, Montell C (2012) Gustatory receptors required for avoiding the insecticide L-canavanine. J Neurosci 32:1429–1435.
52. Li D, Zhang J (2014) Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire. Mol Biol Evol 31:303–309.
53. Ling F, Dahanukar A, Weiss LA, Kwon JY, Carlson JR (2014) The molecular and cellular basis of taste coding in the legs of Drosophila. J Neurosci 34:7148–7164.
54. Maillet EL, Margolskee RF, Mosinger B (2009) Phenoxy herbicides and fi-brates potently inhibit the human chemosensory receptor subunit T1R3. J Med Chem 52:6931–6935.
55. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285–295.
56. Marion-Poll F, van der Pers J (1996) Un-filtered recordings from insect taste sensilla. Entomol Exp Appl 80:113–115.
57. Martin TL, Shields VDC (2012) An electrophysiological analysis of the effect of phagostimulant mixtures on the responses of a deterrent-sensitive cell of gypsy moth larvae, Lymantria dispar (L.). Arthrop Plant Interact 6:259–267.
58. Masek P, Scott K (2010) Limited taste discrimination in Drosophila. Proc Natl Acad Sci U S A 107:14833–14838.
59. McBride CS, Arguello JR, O’Meara BC (2007) Five drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416.
60. Meunier N, Marion-Poll F, Rospars JP, Tanimura T (2003a) Peripheral coding of bitter taste i Drosophila. J Neurobiol 56:139–152.
61. Meunier N, Marion-Poll F, Lansky P, Rospars JP (2003b) Estimation of the individual firing frequencies of two neurons recorded with a single electrode. Chem Senses 28:671–679.
62. Milligan G, Smith NJ (2007) Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol Sci 28:615–620.
63. Mitri C, Soustelle L, Framery B, Bockaert J, Parmentier ML, Grau Y (2009) Plant insecticide L-canavanine repels Drosophila via the insect orphan GPCR DmX. PLoS Biol 7:e1000147.
64. Moon SJ, Lee Y, Jiao Y, Montell C (2009) A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19:1623–1627.
65. Morita H (1959) Initiation of spike potentials in contact chemosensory hairs of insects. III. D.C. stimulation and generator potential of labellar chemorecep-tor of Calliphora. J Cell Comp Physiol 54:189–204.
66. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100: 13940–13945.
67. Naim M, Seifert R, Nürnberg B, Grünbaum L, Schultz G (1994) Some taste substances are direct activators of G-proteins. Biochem J 297:451–454.
68. Peri I, Mamrud-Brains H, Rodin S, Krizhanovsky V, Shai Y, Nir S, Naim M (2000) Rapid entry of bitter and sweet tastants into liposomes and taste cells: implications for signal transduction. Am J Physiol Cell Physiol 278:C17–C25.
69. Rasband WS, Bright DS (1995) NIH Image—a public domain image-processing program for the MacIntosh. Microbeam Anal 4:137–149.
70. Richards S, Gibbs RA, Wein-Stock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Beeman RW, Brown SJ, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schröder R, Tautz D, Zdobnov EM, Tribolium Genome Sequencing Consortium;. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955.
71. Roper SD (2006) Cell communication in taste buds. Cell Mol Life Sci 63: 1494–1500.
72. Rosenthal GA (2001) L-Canavanine: a higher plant insecticidal allelochemi-cal. Amino Acids 21:319–330.
73. Schoonhoven LM (1982) Biological aspects of antifeedants. Entomol Exp Appl 31:57–69.
74. Schoonhoven LM, Liner L (1994) Multiple mode of action of the feeding deterrent, toosendanin, on the sense of taste in Pieris brassicae larvae. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 175:519–524.
75. Schoonhoven LM, van Loon JJA (2002) An inventory oftaste in caterpillars: Each species its own key. Acta Zool Acad Scient Hung 48:215–263.
76. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16:1741–1747.
77. Sellier MJ, Marion-Poll F (2011) Mixture interactions in taste sensilla of Drosophila melanogaster. Chem Senses 36:E42–E43.
78. Sellier MJ, Reeb P, Marion-Poll F (2011) Consumption of bitter alkaloids in Drosophila melanogaster in multiple-choice test conditions. Chem Senses 36:323–334.
79. 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.
80. Shiraiwa T, Carlson JR (2007) Proboscis extension response (PER) assay in Drosophila. J Vis Exp (3):193.
81. Su CY, Menuz K, Reisert J, Carlson JR (2012) Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492:66–71.
82. Swarup S, Morozova TV, Sridhar S, Nokes M, Anholt RRH (2014) Modulation of feeding behavior by odorant-binding proteins in Drosophila melanogaster. Chem Senses 39:125–132.
83. Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341–351.
84. Talavera K, Yasumatsu K, Yoshida R, Margolskee RF, Voets T, Ninomiya Y, Nilius B (2008) The taste transduction channel TRPM5 is a locus for bitter-sweet taste interactions. FASEB J 22:1343–1355.
85. Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K (2012) Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 149:1140–1151.
86. Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14:1065–1079.
87. Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981–991.
88. Wanner KW, Robertson HM (2008) The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 17:621–629.
89. Weiss LA, Dahanukar A, Kwon JY, Banerjee D, Carlson JR (2011) The molecular and cellular basis ofbitter taste inDrosophila. Neuron 69:258–272.
90. Wieczorek H, Wolff G (1989) The labellar sugar receptor of Drosophila. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 164:825–834.
91. Wooding S (2005) Evolution:a study in bad taste? Curr Biol 15:R805–R807.
92. Wright GA, Mustard JA, Simcock NK, Ross-Taylor AAR, McNicholas LD, Popescu A, Marion-Poll F (2010) Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr Biol 20:2234–2240.
93. Xu H, Staszewski L, Tang H, Adler E, Zoller M, Li X (2004) Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci U S A 101:14258–14263.
94. Yarmolinsky DA, Zuker CS, Ryba NJP (2009) Common sense about taste: from mammals to insects. Cell 139:234–244.
95. Zhang YV, Raghuwanshi RP, Shen WL, Montell C (2013) Food experience-induced taste desensitization modulated bythe DrosophilaTRPL channel. Nat Neurosci 16:1468–1476.
96. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266.