Insects as chemosensors of humans and crops

Nature

Volumn 444, Issue 7117, 2006, Pages 302-307

  Van Der Goes Van Naters, Wynand ^a   Carlson, John R ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURAL PRODUCTS; CHEMICAL SENSORS; CROPS; DISEASE CONTROL; HEALTH CARE;

CHEMOSENSATION; INSECTS; OLFACTION; TASTE;

BIOSENSORS;

INSECT PROTEIN; PHEROMONE;

CHEMORECEPTION; CROP; DISEASE TRANSMISSION; HOST PLANT; INSECT; OLFACTION; TASTE;

AGRICULTURE; CHEMORECEPTOR; CHEMOSENSITIVITY; CROP; DISEASE CARRIER; DISEASE TRANSMISSION; HEALTH HAZARD; INSECT; INSECT CONTROL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMELLING; TASTE;

HEXAPODA; INSECTA;

EID: 33751107175     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature05403     Document Type: Review

References (79)

1. Snow, R. W., Guerra, A. A., Noor, A. M., Myint, H. Y. & Hay, S. I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214-217 (2005).
2. WHO & UNICEF World Malaria Report 2005 [online] (2005).
3. Smallegange, R. C., Qiu, Y. T., Van Loon, J. J. A. & Takken, W. Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chem. Senses 30, 145-152 (2005).
4. Qiu, Y. T., Smallegange, R. C., van Loon, J. J. A. & Takken, W. Interindividual variation in odour-mediated attractiveness of human odours to the malaria mosquito Anopheles gambiae. Med. Vet. Entomol. 20, 280-287 (2006).
5. Schreck, C. E., Kline, D. L. & Carlson, D. A. Mosquito attraction to substances from the skin of different humans. J. Am. Mosquito Control Assoc. 6, 406-410 (1990).
6. White, G. B. Anopheles gambiae complex and disease transmission in Africa. Trans. R. Soc. Trop. Med. Hyg. 68, 278-299 (1974).
7. Pates, H. V., Takken, W., Stuke, K. & Curtis, C. F. Differential behaviour of Anopheles gambiae sensu stricto (Diptera: Culicidae) to human and cow odours in the laboratory. Bull. Entomol. Res. 91, 289-296 (2001).
8. Pimentel, D. Diversification of biological control strategies in agriculture. Crop Protection 10, 243-253 (1991).
9. Haney, P. B. in Boll Weevil Eradication in the United States through 1999 (eds Dickerson, W. A. et al.) 7-24 (The Cotton Foundation Publisher, Memphis, 2001).
10. Harris, K. F. & Maramorosch, K. (eds) Vectors of Plant Pathogens (Academic, New York, 1980).
11. Judd, J. G. R. & Borden, J. Distant olfactory response of the onion fly, Delia antiqua, to host-plant odour in the field. Physiol. Entomol. 14, 429-441 (1989).
12. Zhang, A. et al. Identification of a new blend of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. J. Chem. Ecol. 25, 1221-1231 (1999).
13. Glendinning, J. I., Davis, A. & Ramaswamy, S. Contribution of different taste cells and signaling pathways to the discrimination of 'bitter' taste stimuli by an insect. J. Neurosci. 22, 7281-7287 (2002).
14. Del Campo, M. L. et al. Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411, 186-189 (2001).
15. Fraenkel, G. S. The raison d'être of secondary plant substances. Science 129, 1466-1470 (1959).
16. Metcalf, R. L., Metcalf, R. A. & Rhodes, A. M. Cucurbitacins as kairomones for diabroticite beetles. Proc. Natl Acad. Sci. USA 77, 3769-3772 (1980).
17. Witzgall, P., Lindblom, T., Bengtsson, M. & Tóth, M. The Pherolist Phero Net [online] (2004).
18. Mustaparta, H. in Insect Pheromone Research: New Directions (eds Cardé, R. T. & Minks, A. K.) 144-163 (Chapman & Hall, New York, 1997).
19. Butenandt, A., Beckmann, R., Stamm, D. & Hecker, E. Uber den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z. Naturforsch. 14, 283-284 (1959).
20. Shields, V. D. C. & Hildebrand, J. G. Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J. Comp. Physiol. A 186, 1135-1151 (2001).
21. De Bruyne, M., Clyne, P. J. & Carlson, J. R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520-4532 (1999).
22. Vogt, R. G. & Riddiford, L. M. Pheromone binding and inactivation by moth antennae. Nature 293, 161-163 (1981).
23. Sandler, B. H., Nikonova, L., Leal, W. S. & Clardy, J. Sexual attraction in the silkworm moth: structure of the pheromone-binding protein-bombykol complex. Chem. Biol. 7, 143-151 (2000).
24. Horst, R. et al. NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proc. Natl Acad. Sci. USA 98, 14374-14379 (2001).
25. Campanacci, V. et al. Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. J. Biol. Chem. 276, 20078-20084 (2001).
26. Maida, R., Krieger, J., Gebauer, T., Lange, U. & Ziegelberger, G. Three pheromone-binding proteins in olfactory sensilla of the two silkmoth species Antheraea polyphemus and Antheraea pernyi. Eur. J. Biochem. 267, 2899-2908 (2000).
27. Kaissling, K.-E. Olfactory perireceptor and receptor events in moths: a kinetic model. Chem. Senses 26, 125-150 (2001).
28. Leal, W. S. Pheromone reception. Top. Curr. Chem. 240, 1-36 (2004).
29. Schoonhoven, L. M., Van Loon, J. J. A. & Dicke, M. Insect-Plant Biology (Oxford Univ. Press, UK, Oxford, 2005).
30. Schoonhoven, L. M., Blaney, W. M. & Simmonds, M. S. J. in Insect-Plant Interactions (ed. Bernays, E. A.) 59-79 (CRC, Boca Raton, 1992).
31. Mitchell, B. K. Physiology of an ATP receptor in labellar sensilla of the tsetse fly Glossina morsitans morsitans Westw. (Diptera: Glossinidae). J. Exp. Biol. 65, 259-271 (1976).
32. Van der Goes van Naters, W. M. & Rinkes, T. H. N. Taste stimuli for tsetse flies on the human skin. Chem. Senses 18, 437-444 (1993).
33. Van der Goes van Naters, W. M. & Den Otter, C. J. Amino acids as taste stimuli for tsetse flies. Physiol. Entomol. 23, 278-284 (1998).
34. Gilbert, I. H., Gouck, H. K. & Smith, C. N. New mosquito repellents. J. Econ. Entomol. 48, 741-743 (1955).
35. Leak, S. G. A. Tsetse Biology and Ecology: Their Role in the Epidemiology and Control of Trypanosomosis (CABI, Wallingford, 1999).
36. Kuhar, T. P., Mori, K. & Dickens, J. C. Potential of a synthetic aggregation pheromone for integrated pest management of Colorado potato beetle. Agric. For. Entomol. 77-81 (2006).
37. Arn, H. & Louis, F. in Insect Pheromone Research: New Directions (eds Cardé, R. T. & Minks, A. K.) 377-382 (Chapman & Hall, New York, 1997).
38. Schmutterer, H. Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annu. Rev. Entomol. 35, 271-297 (1990).
39. Koul, O. Insect Antifeedants (CRC, Boca Raton, 2005).
40. Klun, J. A. et al. Comparative resistance of Anopheles albimanus and Aedes aegypti to N,Ndiethyl-3-methylbenzamide (Deet) and 2-methylpiperidinyl-3- cyclohexen-1-carboxamide (AI3-37220) in laboratory human-volunteer repellent assays. J. Med. Entomol. 41, 418-422 (2004).
41. Mota-Sanchez, D., Hollingworth, R. M., Grafius, E. J. & Moyer, D. D. Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manag. Sci. 62, 30-37 (2006).
42. Glare, T. R. & O'Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety (John Wiley & Sons, Chichester, 2000).
43. Hajek, A. Natural Enemies: An Introduction to Biological Control (Cambridge Univ. Press, Cambridge, UK, 2004).
44. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338 (1999).
45. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736 (1999).
46. Robertson, H. M., Warr, C. G. & Carlson, J. R. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100, 14537-14542 (2003).
47. Stortkuhl, K. F. & Kettler, R. Functional analysis of an olfactory receptor in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 98, 9381-9385 (2001).
48. Wetzel, C. H. et al. Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc. Natl Acad. Sci. USA 98, 9377-9380 (2001).
49. Dobritsa, A. A., Van der Goes van Naters, W., Warr, C. G., Steinbrecht, R. A. & Carlson, J. R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827-841 (2003).
50. Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979 (2004).
51. Kreher, S. A., Kwon, J. Y. & Carlson, J. R. The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445-456 (2005).
52. Goldman, A. L., Van der Goes van Naters, W., Lessing, D., Warr, C. G. & Carlson, J. R. Coexpression of two functional odor receptors in one neuron. Neuron 45, 661-666 (2005).
53. Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143-160 (2006).
54. Fox, A. N., Pitts, R. J., Robertson, H. M., Carlson, J. R. & Zwiebel, L. J. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of downregulation in response to blood feeding. Proc. Natl Acad. Sci. USA 98, 14693-14697 (2001).
55. Hill, C. A. et al. G protein-coupled receptors in Anopheles gambiae. Science 298, 176-178 (2002).
56. Krieger, J. et al. A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 16, 619-628 (2002).
57. Sakurai, T. et al. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl Acad. Sci. USA 101, 16653-16658 (2004).
58. Nakagawa, T., Sakurai, T., Nishioka, T. & Touhara, K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307, 1638-1642 (2005).
59. Jones, W. D., Nguyen, T. A., Kloss, B., Lee, K. J. & Vosshall, L. B. Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr. Biol. 15, R119-R121 (2005).
60. Krieger, J., Klink, O., Mohl, C., Raming, K. & Breer, H. A candidate olfactory receptor subtype highly conserved across different insect orders. J. Comp. Physiol. A 189, 519-526 (2003).
61. Neuhaus, E. M. et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nature Neurosci. 8, 15-17 (2005).
62. Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714 (2004).
63. Clyne, P. J., Warr, C. G. & Carlson, J. R. Candidate taste receptors in Drosophila. Science 287, 1830-1834 (2000).
64. Dahanukar, A., Foster, K., Van der Goes van Naters, W. M. & Carlson, J. R. A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nature Neurosci. 4, 1182-1186 (2001).
65. Scott, K. et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673 (2001).
66. Dunipace, L., Meister, S., McNealy, C. & Amrein, H. Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835 (2001).
67. Bray, S. & Amrein, H. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39, 1019-1029 (2003).
68. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981-991 (2004).
69. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079 (2004).
70. Vogt, R. G., Callahan, F. E., Rogers, M. E. & Dickens, J. C. Odorant binding protein diversity and distribution among the insect orders, as indicated by LAP, an OBP-related protein of the true bug Lygus lineolaris (Hemiptera, Heteroptera). Chem. Senses 24, 481-495 (1999).
71. Hekmat-Scafe, D. S., Scafe, C. R., McKinney, A. J. & Tanouye, M. A. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res. 12, 1357-1369 (2002).
72. Xu, P. X., Zwiebel, L. J. & Smith, D. P. Identification of a distinct family of genes encoding atypical odorant-binding proteins in the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 12, 549-560 (2003).
73. Araneda, R. C., Kini, A. D. & Firestein, S. The molecular receptive range of an odorant receptor. Nature Neurosci. 3, 1248-1255 (2000).
74. Oka, Y., Omura, M., Kataoka, H. & Touhara, K. Olfactory receptor antagonism between odorants. EMBO J. 23, 120-126 (2004).
75. Spehr, M. et al. Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054-2058 (2003).
76. Hallem, E. A., Fox, A. N., Zwiebel, L. J. & Carlson, J. R. Olfaction: mosquito receptor for human-sweat odorant. Nature 427, 212-213 (2004).
77. Xu, P., Atkinson, R., Jones, D. N. & Smith, D. P. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193-200 (2005).
78. Maibeche-Coisne, M., Nikonov, A. A., Ishida, Y., Jacquin-Joly, E. & Leal, W. S. Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proc. Natl Acad. Sci. USA 101, 11459-11464 (2004).
79. De Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537-552 (2001).