The smell of love in Drosophila

Frontiers in Physiology

Volumn 4 APR, Issue , 2013, Pages

  Ziegler, Anna B ^a   Berthelot Grosjean, Martine ^a   Grosjean, Yael ^a  

^a CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

11 CIS VACCENYL ACETATE; ACETALDEHYDE; PHENYLACETALDEHYDE; PHENYLACETIC ACID; SEX PHEROMONE; UNCLASSIFIED DRUG;

AGGRESSION; ARTICLE; COPULATION; COURTSHIP; DROSOPHILA MELANOGASTER; MATE CHOICE; NONHUMAN; OLFACTORY RECEPTOR; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SMELLING;

EID: 84883826613     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00072     Document Type: Article

References (67)

1. Abuin, L., Bargeton, B., Ulbrich, M. H., Isacoff, E. Y., Kellenberger, S., and Benton, R. (2011). Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69, 44-60.
2. Ai, M., Min, S., Grosjean, Y., Leblanc, C., Bell, R., Benton, R., et al. (2010). Acid sensing by the Drosophila olfactory system. Nature 468, 691-695.
3. Barata, A., Campo, E., Malfeito-Ferreira, M., Loureiro, V., Cacho, J., and Ferreira, V. (2011). Analytical and sensorial characterization of the aroma of wines produced with sour rotten grapes using GC-O and GC-MS: identification of key aroma compounds. J. Agric. Food Chem. 59, 2543-2553.
4. Bartelt, R. J., Schaner, A. M., and Jackson, L. L. (1985). Cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J. Chem. Ecol. 11, 1747-1756.
5. 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.
6. Benton, R., Vannice, K. S., and Vosshall, L. B. (2007). An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289-293.
7. Billeter, J. C., Atallah, J., Krupp, J. J., Millar, J. G., and Levine, J. D. (2009). Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987-991.
8. 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.
9. Brieger, G., and Butterworth, F. M. (1970). Drosophila melanogaster: identity of male lipid in reproductive system. Science 167, 1262.
10. Butterworth, F. M. (1969). Lipids of Drosophila: a newly detected lipid in the male. Science 163, 1356-1357.
11. Connolly, J. B., and Cook, R. (1973). Rejection responses by female Drosophila melanogaster: their ontogeny, causality and effects upon behaviour of courting male. Behaviour 44, 142-166.
12. Couto, A., Alenius, M., and Dickson, B. J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547.
13. Datta, S. R., Vasconcelos, M. L., Ruta, V., Luo, S., Wong, A., Demir, E., et al. (2008). The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473-477.
14. de Bruyne, M., Clyne, P. J., and Carlson, J. R. (1999). Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520-4532.
15. Ejima, A., Smith, B. P., Lucas, C., van der Goes van Naters, W., Miller, C. J., Carlson, J. R., et al. (2007). Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17, 599-605.
16. Fabre, C. C., Hedwig, B., Conduit, G., Lawrence, P. A., Goodwin, S. F., and Casal, J. (2012). Substrate-borne vibratory communication during courtship in Drosophila melanogaster. Curr. Biol. 22, 2180-2185.
17. Farine, J. P., Ferveur, J. F., and Everaerts, C. (2012). Volatile Drosophila cuticular pheromones are affected by social but not sexual experience. PLoS ONE 7:e40396. doi: 10.1371/journal.pone.0040396
18. Ferveur, J.-F. (2010). Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Curr. Opin. Neurobiol. 20, 764-769.
19. Gailey, D. A., and Hall, J. C. (1989). Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics 121, 773-785.
20. Greenspan, R. J., and Ferveur, J. F. (2000). Courtship in Drosophila. Annu. Rev. Genet. 34, 205-232.
21. Grosjean, Y., Rytz, R., Farine, J. P., Abuin, L., Cortot, J., Jefferis, G. S., et al. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236-240.
22. Ha, T. S., and Smith, D. P. (2006). A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J. Neurosci. 26, 8727-8733.
23. Hall, J. C. (1977). Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav. Genet. 7, 291-312.
24. Hall, J. C. (1994). The mating of a fly. Science 264, 1702-1714.
25. Hallem, E. A., and Carlson, J. R. (2006). Coding of odors by a receptor repertoire. Cell 125, 143-160.
26. Heimbeck, G., Bugnon, V., Gendre, N., Keller, A., and Stocker, R. F. (2001). A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 98, 15336-15341.
27. Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266-275.
28. Ito, H., Fujitani, K., Usui, K., Shimizu-Nishikawa, K., Tanaka, S., and Yamamoto, D. (1996). Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl. Acad. Sci. U.S.A. 93, 9687-9692.
29. Jallon, J. M., Antony, C., and Benamar, O. (1981). Un anti-aphrodisiaque produit par les males de Drosophila melanogaster. C. R. Acad. Sci. Paris 292, 1147-1149.
30. Jefferis, G. S., Potter, C. J., Chan, A. M., Marin, E. C., Rohlfing, T. Maurer, et al. (2007). Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187-1203.
31. Jin, X., Ha, T. S., and Smith, D. P. (2008). SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 10996-11001.
32. Jones, W. D., Cayirlioglu, P., Kadow, I. G., and Vosshall, L. B. (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86-90.
33. Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., et al. (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171.
34. Kim, J., Jeon, C. O., and Park, W. A. (2007). Green fluorescent protein-based whole-cell bioreporter for the detection of phenylacetic acid. J. Microbiol. Biotechnol. 17, 1727-1732.
35. Kondoh, Y., Kaneshiro, K. Y., Kimura, K., and Yamamoto, D. (2003). Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc. Biol. Sci. 270, 1005-1013.
36. Kurtovic, A., Widmer, A., and Dickson, B. J. (2007). A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542-546.
37. Lasbleiz, C., Ferveur, J. F., and Everaerts, C. (2006). Courtship behaviour of Drosophila melanogaster revisited. Anim. Behav. 72, 1001-1012.
38. Laughlin, J. D., Ha, T. S., Jones, D. N., and Smith, D. P. (2008). Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255-1265.
39. Liu, W., Liang, X., Gong, J., Yang, Z., Zhang, Y. H., Zhang, J. X., et al. (2011). Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat. Neurosci. 14, 896-902.
40. Manoli, D. S., Foss, M., Villella, A., Taylor, B. J., Hall, J. C., and Baker, B. S. (2005). Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395-400.
41. Mehren, J. E., Ejima, A., and Griffith, L. C. (2004). Unconventional sex: fresh approaches to courtship learning. Curr. Opin. Neurobiol. 14, 745-750.
42. Mellert, D. J., Robinett, C. C., and Baker, B. S. (2012). Doublesex functions early and late in gustatory sense organ development. PLoS ONE 7:e51489. doi: 10.1371/journal.pone.0051489
43. Nayak, S. V., and Singh, R. N. (1985). Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera, Drosophilidae). Int. J. Insect Morph. Embryol. 14, 115-129.
44. Neckameyer, W. S. (1998). Dopamine and mushroom bodies in Drosophila: experience-dependent and -independent aspects of sexual behavior. Learn. Mem. 5, 157-165.
45. Rezaval, C., Pavlou, H. J., Dornan, A. J., Chan, Y. B., Kravitz, E. A., and Goodwin, S. F. (2012). Neural circuitry underlying Drosophila female postmating behavioral responses. Curr. Biol. 22, 1155-1165.
46. Ryner, L. C., Goodwin, S. F., Castrillon, D. H., Anand, A., Villella, A., Baker, B. S., et al. (1996). Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079-1089.
47. Ruta, V., Datta, S. R., Vasconcelos, M. L., Freeland, J., Looger, L. L., and Axel, R. (2010). A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686-690.
48. Sakai, T., Sato, S., Ishimoto, H., and Kitamoto, T. (2012). Significance of the centrally expressed TRP channel painless in Drosophila courtship memory. Learn. Mem. 20, 34-40.
49. Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L. B., and Touhara, K. (2008). Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002-1006.
50. Savarit, F., Sureau, G., Cobb, M., and Ferveur, J. F. (1999). Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 96, 9015-9020.
51. Silbering, A. F., Rytz, R., Grosjean, Y., Abuin, L., Ramdya, P., Jefferis, G. S., et al. (2011). Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J. Neurosci. 31, 13357-13375.
52. Spieth, H. T. (1952). Mating behavior within the genus Drosophila (Diptera). Bull. Am. Mus. Nat. Hist. 99, 396-474.
53. Spieth, H. T. (1966). Drosophilid mating behavior: the behaviour of decapitated females. Anim. Behav. 14, 226-235.
54. Spieth, H. T. (1974). Courtship behavior in Drosophila. Ann. Rev. Entomol. 19, 385-406.
55. Stocker, R. F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26.
56. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirián, L., and Dickson, B. J. (2005). Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807.
57. Suh, G. S., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., et al. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854-859.
58. Thorne, N., and Amrein, H. (2008). Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J. Comp. Neurol. 506, 548-568.
59. van der Goes van Naters, W., and Carlson, J. R. (2007). Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606-612.
60. Villella, A., and Hall, J. C. (2008). Neurogenetics of courtship and mating in Drosophila. Adv. Genet. 62, 67-184.
61. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A., and Axel, R. (1999). A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736.
62. Wang, L., and Anderson, D. J. (2010). Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231.
63. Wang, L., Han, X., Mehren, J., Hiroi, M., Billeter, J. C., Miyamoto, T., et al. (2011). Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat. Neurosci. 14, 757-762.
64. Wightman, F., and Lighty, D. L. (1982). Identification of phenylacetic acid as a natural auxin in the shoots of higher plants. Physiol. Plant. 55, 17-24.
65. Wolfner, M. F. (1997). Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem. Mol. Biol. 27, 179-192.
66. Wolfner, M. F. (2002). The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85-93.
67. Xu, P., Atkinson, R., Jones, D. N., and Smith, D. P. (2005). Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193-200.