The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family

Genome Research

Volumn 16, Issue 11, 2006, Pages 1395-1403

  Robertson, Hugh M ^a   Wanner, Kevin W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHEROMONE;

ANOPHELES GAMBIAE; ARTICLE; CHEMORECEPTOR; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE SEQUENCE; HONEYBEE; KIN SELECTION; MOLECULAR EVOLUTION; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; SPECIES COMPARISON; TASTE BUD;

ANIMALS; BEES; CHEMORECEPTORS; DROSOPHILA MELANOGASTER; FEMALE; GENES, INSECT; INSECT PROTEINS; MALE; MULTIGENE FAMILY; PHYLOGENY; RECEPTORS, CELL SURFACE; RECEPTORS, ODORANT; SPECIES SPECIFICITY;

ANOPHELES GAMBIAE; APIS MELLIFERA; APOIDEA; DROSOPHILA MELANOGASTER; INSECTA;

EID: 33750500530     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.5057506     Document Type: Article

References (53)

1. Ai, H. and Kanzaki, R. 2004. Modular organization of the silkmoth antennal lobe macroglomerular complex revealed by voltage-sensitive dye imaging. J. Exp. Biol. 207: 633-644.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Benton, R., Sachse, S., Michnick, S.W., and Vosshall, L.B. 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4: e20.
4. Berg, B.G., Galizia, C.G., Brandt, R., and Mustaparta, H. 2002. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J. Comp. Neurol. 446: 123-134.
5. Brockmann, A. and Brückner, D. 2001. Structural differences in the drone olfactory system of two phylogenetically distant Apis species, A. florea and A. mellifera. Naturwissenschaften 88: 78-81.
6. Chyb, S., Dahanukar, A., Wickens, A., and Carlson, J.R. 2003. Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl. Acad. Sci. 100: 14526-14530.
7. Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J., and Carlson, J.R. 1999. A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron 22: 327-338.
8. Clyne, P.J., Warr, C.G., and Carlson, J.R. 2000. Candidate taste receptors in Drosophila. Science 287: 1830-1834.
9. 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.
10. Fishilevich, E. and Vosshall, L.B. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15: 1548-1553.
11. 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.
12. Galizia, C.G. and Menzel, R. 2001. The role of glomeruli in the neural representation of odours: Results from optical recording studies. J. Insect Physiol. 47: 115-130.
13. Gao, Q. and Chess, A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60: 31-39.
14. Goldman, A.L., Van der Goes van Naters, W., Lessing, D., Warr, C.G., and Carlson, J.R. 2005. Coexpression of two functional odor receptors in one neuron. Neuron 45: 661-666.
15. Goodman, L. 2003. Form and function in the honey bee. (eds. R.J. Cooter and P.A. Munn). International Bee Research Association, Cardiff, UK.
16. Hallem, E.A., Ho, M.G., and Carlson, J.R. 2004. The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965-979.
17. Hallem, E.A., Dahanukar, A., and Carlson, J.R. 2006. Insect odor and taste receptors. Annu. Rev. Entomol. 51: 113-135.
18. Hill, C.A., Fox, A.N., Pitts, R.J., Kent, L.B., Tan, P.L., Chrystal, M.A., Cravchik, A.F., Collins, H., Robertson, H.M., and Zwiebel, L.J. 2002. G-protein-coupled receptors in Anopheles gambiae. Science 298: 176-178.
19. The Honey Bee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honey bee Apis mellifera. Nature (in press).
20. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403-405.
21. Jones, W.D., Nguyen, T.A., Kloss, B., Lee, K.J., and Vosshall, L.B. 2005. Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr. Biol. 15: R119-R121.
22. 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.
23. Krieger, J., Raming, K., Dewer, Y.M., Bette, S., Conzelmann, S., and Breer, H. 2002. A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 16: 619-628.
24. Krieger, J., Klink, O., Mohl, C., Raming, K., and Breer, H. 2003. 2003. A candidate olfactory receptor subtype highly conserved across different insect orders. J. Comp. Physiol. A Neuroethol. Sens Neural. Behav Physiol. 189: 519-526.
25. Krieger, J., Grosse-Wilde, E., Gohl, T., Dewer, Y.M., Raming, K., and Breer, H. 2004. Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. 101: 11845-11850.
26. Krieger, J., Grosse-Wilde, E., Gohl, T., and Breer, H. 2005. Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci. 21: 2167-2176.
27. Laissue, P.P., Reiter, C., Hiesinger, P.R., Halter, S., Fischbach, K.F., and Stocker, R.F. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405: 543-552.
28. 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.
29. -ΔΔC(T) method. Methods 25: 402-408.
30. Menzel, R. and Erber, J. 1978. Learning and memory in bees. Sci. Am. 239: 102-108.
31. Michener, C.D. 1974. The social behavior of bees: A comparative study. Harvard University Press, Cambridge, MA.
32. Nakagawa, T., Sakurai, T., Nishioka, T., and Touhara, K. 2005. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307: 1638-1642.
33. Pitts, R.J., Fox, A.N., and Zwiebel, L.J. 2004. A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. 101: 5058-5063.
34. Raven, P.H. and Axelrod, D.I. 1974. Angiosperm biogeography and past continental movements. Ann. Mo. Bot. Gard. 61: 539-673.
35. Robertson, H.M. 1998. Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. Genome Res. 8: 449-463.
36. Robertson, H.M. 2000. The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. Genome Res. 10: 192-203.
37. Robertson, H.M. and Thomas, J.H. 2006. The putative chemoreceptor families of C. elegans (Jan. 6, 2006), In WormBook (ed. The C. elegans Research Community). http://www.wormbook.org.
38. Robertson, H.M., Warr, C.G., and Carlson, J.R. 2003. Molecular evolution of the insect chemoreceptor superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. 100: 14537-14542.
39. Rutzler, M. and Zwiebel, L.J. 2005. Molecular biology of insect olfaction: Recent progress and conceptual models. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191: 777-790.
40. Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., and Nishioka, T. 2004. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci. 101: 16653-16658.
41. Schmidt, H.A., Strimmer, K., Vingron, M., and von Haeseler, A. 2002. TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
42. 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.
43. Skiri, H.T., Ro, H., Berg, B.G., and Mustaparta, H. 2005. Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J. Comp. Neurol. 491: 367-380.
44. 2O and Xe. J. Comp. Physiol. 86: 139-158.
45. Stewart, M.K., Clark, N.L., Merrihew, G., Galloway, E.M., and Thomas, J.H. 2005. High genetic diversity in the chemoreceptor superfamily of Caenorhabditis elegans. Genetics 169: 1985-1996.
46. Suh, G.S., Wong, A.M., Hergarden, A.C., Wang, J.W., Simon, A.F., Benzer, S., Axel, R., and Anderson, D.J. 2004. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431: 854-859.
47. Swofford, D.L. 2001. PAUP*: Phylogenetic analysis using parsimony and other methods, version 4. Sinauer Press, New York.
48. von Frisch, K. 1927. Versuche uber den Geschmacksinn der Bienen. Naturwissenschaften 14: 1-20.
49. von Lacher, V. 1964. Elektrophysiologische Unter-suchungen an einzelnen Rezeptoren für Geruch, Kohlendioxid, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifera L.). Z. Vergl. Physiol. 48: 587-623.
50. 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.
51. Vosshall, L.B., Wong, A.M., and Axel, R. 2000. An olfactory sensory map in the fly brain. Cell 102: 147-159.
52. Wright, G.A., Skinner, B.D., and Smith, B.H. 2002. Ability of honeybee, Apis mellifera, to detect and discriminate odors of varieties of canola (Brassica rapa and B. napus) and snapdragon flowers (Antirrhinium majus). J. Chem. Ecol. 28: 721-740.
53. Young, J.M. and Trask, B.J. 2002. The sense of smell: Genomics of vertebrate odorant receptors. Hum. Mol. Genet. 11: 1153-1160.