Taste processing in Drosophila larvae

Frontiers in Integrative Neuroscience

Volumn 9, Issue OCT, 2015, Pages

  Apostolopoulou, Anthi A ^a   Rist, Anna ^a   Thum, Andreas S ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Drosophila melanogaster; Gustation; Larvae; Single cell analysis; Taste processing

Indexed keywords

IONOTROPIC RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ARTICLE; BITTER TASTE; DROSOPHILA; FEEDING BEHAVIOR; GENE; GENE EXPRESSION; GENE FUNCTION; GR GENE; IONOTROPIC RECEPTOR GENE; LARVA; NONHUMAN; PPK GENE; SALTINESS; SWEETNESS; TASTE; TASTE DISCRIMINATION; TRP GENE;

EID: 84944461036     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2015.00050     Document Type: Article

References (64)

1. Alves, G., Sallé, J., Chaudy, S., Dupas, S., and Manière, G. (2014). High-NaCl perception in Drosophila melanogaster. J. Neurosci. 34, 10884–10891. doi: 10.1523/JNEUROSCI.4795-13.2014
2. Apostolopoulou, A. A., Mazija, L., Wust, A., and Thum, A. S. (2014). The neuronal and molecular basis of quinine-dependent bitter taste signaling in Drosophila larvae. Front. Behav. Neurosci. 8:6. doi: 10.3389/fnbeh.2014.00006
3. Ashburner, M., Golic, K. G., and Hawley, R. S. (2005). Drosophila: A Laboratory Handbook, 2nd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
4. Atkinson, W., and Shorrocks, B. (1977). Breeding site specificity in the domestic species of Drosophila. Oecologia 29, 223–232. doi: 10.1007/BF00345697
5. Bandell, M., Macpherson, L. J., and Patapoutian, A. (2007). From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr. Opin. Neurobiol. 17, 490–497. doi: 10.1016/j.conb.2007.07.014
6. Becher, P. G., Flick, G., Rozpêdowska, E., Schmidt, A., Hagman, A., Lebreton, S., et al. (2012). Yeast, not fruit volatiles mediateDrosophila melanogaster attraction, oviposition and development. Functi. Ecol. 26, 822–828. doi: 10.1111/j.1365-2435.2012.02006.x
7. Ben-Shahar, Y. (2011). Sensory functions for degenerin/epithelial sodium channels (DEG/ENaC). Adv. Genet. 76, 1–26. doi: 10.1016/B978-0-12-386481-9.00001-8
8. Benton, R., Vannice, K. S., Gomez-Diaz, C., and Vosshall, L. B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162. doi: 10.1016/j.cell.2008.12.001
9. Bjordal, M., Arquier, N., Kniazeff, J., Pin, J. P., and Léopold, P. (2014). Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell 156, 510–521. doi: 10.1016/j.cell.2013.12.024
10. Bray, S., and Amrein, H. (2003). A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39, 1019–1029. doi: 10.1016/S0896-6273(03)00542-7
11. Chen, Z., Wang, Q., and Wang, Z. (2010). The amiloride-sensitive epithelial Na+ channel PPK28 is essential for Drosophila gustatory water reception. J. Neurosci. 30, 6247–6252. doi: 10.1523/JNEUROSCI.0627-10.2010
12. Chu, I. W., and Axtell, R. C. (1971). Fine structure of the dorsal organ of the house fly larva, Musca domestica L. Z. Zellforsch. Mikrosk. Anat. 117, 17–34. doi: 10.1007/BF00331098
13. Chu-Wang, I. W., and Axtell, R. C. (1972). Fine structure of the terminal organ of the house fly larva, Musca domestica L. Z. Zellforsch. Mikrosk. Anat. 127, 287–305. doi: 10.1007/BF00306874
14. Clyne, P. J., Warr, C. G., and Carlson, J. R. (2000). Candidate taste receptors in Drosophila. Science 287, 1830–1834. doi: 10.1126/science.287.5459.1830
15. Colomb, J., Grillenzoni, N., Ramaekers, A., and Stocker, R. F. (2007). Architecture of the primary taste center of Drosophilamelanogaster larvae. J. Comp. Neurol. 502, 834–847. doi: 10.1002/cne.21312
16. Cooper, D. M. (1960). Food preferences of larval and adult Drosophila. Evolution 14, 41–55. doi: 10.2307/2405921
17. Croset, V., Rytz, R., Cummins, S. F., Budd, A., Brawand, D., Kaessmann, H., et al. (2010). Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 6:e1001064. doi: 10.1371/journal.pgen.1001064
18. 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. doi: 10.1016/j.neuron.2007.10.024
19. Dethier, V. G., and Gelperin, A. (1967). Hyperphagia in the blowfly. J. Exp. Biol. 47, 191–200.
20. El-Keredy, A., Schleyer, M., König, C., Ekim, A., and Gerber, B. (2012). Behavioural analyses of quinine processing in choice, feeding and learning of larval Drosophila. PLoS ONE 7:e40525. doi: 10.1371/journal.pone.0040525
21. Fishilevich, E., Domingos, A. I., Asahina, K., Naef, F., Vosshall, L. B., and Louis, M. (2005). Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15, 2086–2096. doi: 10.1016/j.cub.2005.11.016
22. Fowler, M. A., and Montell, C. (2013). Drosophila TRP channels and animal behavior. Life Sci. 92, 394–403. doi: 10.1016/j.lfs.2012.07.029
23. Gendre, N., Lüer, K., Friche, S., Grillenzoni, N., Ramaekers, A., Technau, G. M., et al. (2004). Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131, 83–92. doi: 10.1242/dev.00879
24. Gerber, B., and Stocker, R. F. (2007). The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review.Chem. Senses 32, 65–89. doi: 10.1093/chemse/bjl030
25. Green, C. H., Burnet, B., and Connolly, K. J. (1983). Organization and patterns of inter- and intraspecific variation in the behaviour ofDrosophila larvae. Anim. Behav. 31, 282–291. doi: 10.1016/S0003-3472(83)80198-5
26. Heimbeck, G., Bugnon, V., Gendre, N., Häberlin, C., and Stocker, R. F. (1999). Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J. Neurosci. 19, 6599–6609.
27. Huang, A. L., Chen, X., Hoon, M. A., Chandrashekar, J., Guo, W., Tränkner, D., et al. (2006). The cells and logic for mammalian sour taste detection. Nature 442, 934–938. doi: 10.1038/nature05084
28. Klein, M., Afonso, B., Vonner, A. J., Hernandez-Nunez, L., Berck, M., Tabone, C. J., et al. (2015). Sensory determinants of behavioral dynamics in Drosophila thermotaxis. Proc. Natl. Acad. Sci. U.S.A. 112, E220–E229. doi: 10.1073/pnas.1416212112
29. König, C., Schleyer, M., Leibiger, J., El-Keredy, A., and Gerber, B. (2015). Bitter-sweet processing in larval Drosophila. Chem. Senses 40, 445. doi: 10.1093/chemse/bju071
30. Kreher, S. A., Kwon, J. Y., and Carlson, J. R. (2005). The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445–456. doi: 10.1016/j.neuron.2005.04.007
31. Kwon, J. Y., Dahanukar, A., Weiss, L. A., and Carlson, J. R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 104, 3574–3578. doi: 10.1073/pnas.0700079104
32. Kwon, J. Y., Dahanukar, A., Weiss, L. A., and Carlson, J. R. (2011). Molecular and cellular organization of the taste system in theDrosophila larva. J. Neurosci. 31, 15300–15309. doi: 10.1523/JNEUROSCI.3363-11.2011
33. Liu, L., Johnson, W. A., and Welsh, M. J. (2003a). Drosophila DEG/ENaC pickpocket genes are expressed in the tracheal system, where they may be involved in liquid clearance. Proc. Natl. Acad. Sci. U.S.A. 100, 2128–2133. doi: 10.1073/pnas.252785099
34. Liu, L., Leonard, A. S., Motto, D. G., Feller, M. A., Price, M. P., Johnson, W. A., et al. (2003b). Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39, 133–146. doi: 10.1016/S0896-6273(03)00394-5
35. Liu, L., Li, Y., Wang, R., Yin, C., Dong, Q., Hing, H., et al. (2007). Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450, 294–298. doi: 10.1038/nature06223
36. Mast, J. D., De Moraes, C. M., Alborn, H. T., Lavis, L. D., and Stern, D. L. (2014). Evolved differences in larval social behavior mediated by novel pheromones. Elife 3:e04205. doi: 10.7554/eLife.04205
37. Mishra, D., Miyamoto, T., Rezenom, Y. H., Broussard, A., Yavuz, A., Slone, J., et al. (2013). The molecular basis of sugar sensing inDrosophila larvae. Curr. Biol. 23, 1466–1471. doi: 10.1016/j.cub.2013.06.028
38. Miyakawa, Y. (1982). Behavioural evidence for the existence of sugar, salt and amino acid taste receptor cells and some of their properties in Drosophila larvae. J. Insect Physiol. 28, 405–410. doi: 10.1016/0022-1910(82)90066-X
39. Niewalda, T., Singhal, N., Fiala, A., Saumweber, T., Wegener, S., and Gerber, B. (2008). Salt processing in larval Drosophila: choice, feeding, and learning shift from appetitive to aversive in a concentration-dependent way. Chem. Senses 33, 685–692. doi: 10.1093/chemse/bjn037
40. Oppliger, F. Y., M Guerin, P., and Vlimant, M. (2000). Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. J. Insect Physiol. 46, 135–144. doi: 10.1016/S0022-1910(99)00109-2
41. Park, J.-H., and Kwon, J. Y. (2011). Heterogeneous expression of drosophila gustatory receptors in enteroendocrine cells. PLoS ONE 6:e29022. doi: 10.1371/journal.pone.0029022
42. Python, F., and Stocker, R. F. (2002). Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445, 374–387. doi: 10.1002/cne.10188
43. Ramaekers, A., Magnenat, E., Marin, E. C., Gendre, N., Jefferis, G. S., Luo, L., et al. (2005). Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15, 982–992. doi: 10.1016/j.cub.2005.04.032
44. Rohwedder, A., Pfitzenmaier, J. E., Ramsperger, N., Apostolopoulou, A. A., Widmann, A., and Thum, A. S. (2012). Nutritional value-dependent and nutritional value-independent effects on Drosophila melanogaster larval behavior. Chem. Senses 37, 711–721. doi: 10.1093/chemse/bjs055
45. Russell, C., Wessnitzer, J., Young, J. M., Armstrong, J. D., and Webb, B. (2011). Dietary salt levels affect salt preference and learning in larval Drosophila. PLoS ONE 6:e20100. doi: 10.1371/journal.pone.0020100
46. Schipanski, A., Yarali, A., Niewalda, T., and Gerber, B. (2008). Behavioral analyses of sugar processing in choice, feeding, and learning in larval Drosophila. Chem. Senses 33, 563–573. doi: 10.1093/chemse/bjn024
47. Schleyer, M., Miura, D., Tanimura, T., and Gerber, B. (2015). Learning the specific quality of taste reinforcement in larval Drosophila. Elife 4:e04711. doi: 10.7554/eLife.04711
48. Schwarz, S., Durisko, Z., and Dukas, R. (2014). Food selection in larval fruit flies: dynamics and effects on larval development. Naturwissenschaften 101, 61–68. doi: 10.1007/s00114-013-1129-z
49. Scott, K., Brady, R., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., et al. 2001. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661–673. doi: 10.1016/S0092-8674(01)00263-X
50. Singh, R. N., and Singh, K. (1984). Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int. J. Insect. Morphol. Embryol. 13, 255–273. doi: 10.1016/0020-7322(84)90001-1
51. Slone, J., Daniels, J., and Amrein, H. (2007). Sugar receptors in Drosophila. Curr. Biol. 17, 1809–1816. doi: 10.1016/j.cub.2007.09.027
52. Sokolowski, M. B. (1980), Foraging strategies of Drosophila melanogaster: a chromosomal analysis. Behav. Genet. 10, 291–302. doi: 10.1007/BF01067774.
53. Sokolowski, M. B., Kent, C., and Wong, J. (1984). Drosophila larval foraging behaviour: developmental stages. Anim. Behav. 32, 645–651. doi: 10.1016/S0003-3472(84)80139-6
54. Spiess, R., Schoofs, A., and Heinzel, H. G. (2008). Anatomy of the stomatogastric nervous system associated with the foregut inDrosophila melanogaster and Calliphora vicina third instar larvae. J. Morphol. 269, 272–282. doi: 10.1002/jmor.10581
55. Stewart, S., Koh, T. W., Ghosh, A. C., and Carlson, J. R. (2015). Candidate ionotropic taste receptors in the Drosophila larva. Proc. Natl. Acad. Sci. U.S.A. 112, 4195–4201. doi: 10.1073/pnas.1503292112
56. Thorne, N., and Amrein, H. (2008). Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J. Comp. Neurol. 506, 548–568. doi: 10.1002/cne.21547
57. Tissot, M., Gendre, N., Hawken, A., Störtkuhl, K. F., and Stocker, R. F. (1997). Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J. Neurobiol. 32, 281–297.
58. Venkatachalam, K., Luo, J., and Montell, C. (2014). Evolutionarily conserved, multitasking TRP channels: lessons from worms and flies. Handb. Exp. Pharmacol. 223, 937–962. doi: 10.1007/978-3-319-05161-1_9
59. Wang, Z., Singhvi, A., Kong, P., and Scott, K. (2004). Taste representations in the Drosophila brain. Cell 117, 981–991. doi: 10.1016/j.cell.2004.06.011
60. 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. doi: 10.1016/j.neuron.2011.01.001
61. Widdowson, E. M., and McCance, R. A. (1935). The available carbohydrate of fruits: determination of glucose, fructose, sucrose and starch. Biochem. J. 29, 151–156. doi: 10.1042/bj0290151
62. Xu, J., Sornborger, A. T., Lee, J. K., and Shen, P. (2008). Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat. Neurosci. 11, 676–682. doi: 10.1038/nn.2119
63. Zhang, Y. V., Ni, J., and Montell, C. (2013). The molecular basis for attractive salt taste coding in Drosophila. Science 340, 1334–1338. doi: 10.1126/science.1234133
64. Zhong, L., Hwang, R. Y., and Tracey, W. D. (2010). Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophilalarvae. Curr. Biol. 20, 429–434. doi: 10.1016/j.cub.2009.12.057