Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens

Frontiers in Cellular Neuroscience

Volumn , Issue SEPTEMBER, 2012, Pages 1-17

  Pregitzer, Pablo ^a   Schubert, Marco ^b   Breer, Heinz ^a   Hansson, Bill S ^c   Sachse, Silke ^c   Krieger, Jürgen ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Antennal lobe; Olfaction; Pheromone binding protein; Pheromone detection; Pheromone receptor

Indexed keywords

11 HEXADECENAL; CALCIUM; CARYOPHYLLENE; GERANIOL; INSECT PROTEIN; ISOPENTYL ACETATE; LINALOOL; LINALYL ACETATE; PHEROMONE BINDING PROTEIN; PHEROMONE BINDING PROTEIN 2; PHEROMONE RECEPTOR; PLANT MEDICINAL PRODUCT; PROTEIN HR13; SEX PHEROMONE; SOLVENT; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL TISSUE; ANTENNA (ORGAN); ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM SIGNALING; CONTROLLED STUDY; EVOKED RESPONSE; HELIOTHIS VIRESCENS; HORMONE DETERMINATION; IN VIVO STUDY; MALE; MOLECULAR RECOGNITION; MOTH; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY NERVE; PLANT; PROTEIN BINDING; SENSORY NERVE CELL; SIGNAL DETECTION;

EID: 84867060585     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00042     Document Type: Article

References (68)

1. Almaas, T. J., and Mustaparta, H. (1991). Heliothis virescens: Response characteristics of receptor neurons in sensilla trichodea type 1 and type 2. J. Chem. Ecol. 17, 953-972.
2. Anton, S., Löfstedt, C., and Hansson, B. (1997). Central nervous processing of sex pheromones in two strains of the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J. exp. Biol. 200, 1073-1087.
3. Baker, T. C., Ochieng, S. A., Cosse, A. A., Lee, S. G., Todd, J. L., Quero, C., and Vickers, N. J. (2004). A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. J. Comp. Physiol. A 190, 155-165.
4. Ban, L., Scaloni, A., D'Ambrosio, C., Zhang, L., Yahn, Y., and Pelosi, P. (2003). Biochemical characterization and bacterial expression of an odorant-binding protein from Locusta migratoria. Cell. Mol. Life Sci. 60, 390-400.
5. Berg, B. G., Almaas, T. J., Bjaalie, J. G., and Mustaparta, H. (1998). The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J. Comp. Physiol. A 183, 669-682.
6. Bisch-Knaden, S., Carlsson, M. A., Sugimoto, Y., Schubert, M., Missbach, C., Sachse, S., and Hansson, B. S. (2012). Olfactory coding in five moth species from two families. J. exp. Biol. 215, 1542-1551.
7. Bohbot, J. D., and Dickens, J. C. (2010). Insect repellents: modulators of mosquito odorant receptor activity. PLoS ONE 5, e12138.
8. Bohbot, J. D., and Dickens, J. C. (2012). Odorant receptor modulation: ternary paradigm for mode of action of insect repellents. Neuropharmacol. 62, 2086-2095.
9. Bohbot, J. D., Fu, L., Le, T. C., Chauhan, K. R., Cantrell, C. L., and Dickens, J. C. (2011). Multiple activities of insect repellents on odorant receptors in mosquitoes. Med. Vet. Entomol. 25, 436-444.
10. Campanacci, V., Krieger, J., Bette, S., Sturgis, J. N., Lartigue, A., Cambillau, C., Breer, H., and Tegoni, M. (2001). Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. J. Biol. Chem. 276, 20078-20084.
11. Carde, R. T., and Willis, M. A. (2008). Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 34, 854-866.
12. Carey, A. F., and Carlson, J. R. (2011). Insect olfaction from model systems to disease control. Proc. Natl. Acad. Sci. U. S. A 108, 14849-14854.
13. Chaffiol, A., Kropf, J., Barrozo, R. B., Gadenne, C., Rospars, J. P., and Anton, S. (2012). Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth. J. exp. Biol. 215, 1670-1680.
14. Christensen, T. A., Waldrop, B. R., Harrow, I. D., and Hildebrand, J. G. (1993). Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A 173, 385-399.
15. David, C. T., Kennedy, J. S., and Ludlow, A. R. (1983). Finding of a pheromone source by gypsy moths released in the field. Nature 303, 804-806.
16. De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. (2001). Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577-580.
17. Deisig, N., Kropf, J., Vitecek, S., Pevergne, D., Rouyar, A., Sandoz, J. C., Lucas, P., Gadenne, C., Anton, S., and Barrozo, R. (2012). Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth. PLoS ONE 7, e33159.
18. Ditzen, M., Pellegrino, M., and Vosshall, L. B. (2008). Insect odorant receptors are molecular targets of the insect repellent DEET. Science 319, 1838-1842.
19. Forstner, M., Breer, H., and Krieger, J. (2009). A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int. J. Biol. Sci. 5, 745-757.
20. Galizia, C. G., and Menzel, R. (2000). Odour perception in honeybees: coding information in glomerular pattern. Curr. Opin. Neurobiol. 10, 504-510.
21. Galizia, C. G., Sachse, S., and Mustaparta, H. (2000). Calcium responses to pheromones and plant odours in the antennal lobe of the male and female moth Heliothis virescens. J. Comp. Physiol. A 186, 1049-1063.
22. Grosse-Wilde, E., Gohl, T., Bouche, E., Breer, H., and Krieger, J. (2007). Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur. J. Neurosci. 25, 2364-2373.
23. Grosse-Wilde, E., Stieber, R., Forstner, M., Krieger, J., Wicher, D., and Hansson, B. S. (2010). Sex-specific odorant receptors of the tobacco hornworm Manduca sexta. Front. Cell. Neurosci. 4.
24. Grosse-Wilde, E., Svatos, A., and Krieger, J. (2006). A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 31, 547-555.
25. Hallem, E. A., and Carlson, J. R. (2006). Coding of odors by a receptor repertoire. Cell 125, 143-160.
26. Hansson, B. S. (1995). Olfaction in Lepidoptera. Experientia 51, 1003-1027.
27. Hansson, B. S., and Anton, S. (2000). Function and morphology of the antennal lobe: new developments. Annu. Rev. Entomol. 45, 203-231.
28. Hansson, B. S., Carlsson, M. A., and Kalinova, B. (2003). Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta. J. Comp. Physiol. A-Neuroethol. Sens. Neural. and Behav. Physiol. 189, 301-308.
29. Hansson, B. S., Ljungberg, H., Hallberg, E., and Lofstedt, C. (1992). Functional specialization of olfactory glomeruli in a moth. Science 256, 1313-1315.
30. Hansson, B. S., and Stensmyr, M. C. (2011). Evolution of insect olfaction. Neuron 72, 698-711.
31. Hillier, N. K., Kleineidam, C., and Vickers, N. J. (2005). Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera: Noctuidae) responsive to behaviorally relevant odors. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 192, 199-219.
32. Hillier, N. K., and Vickers, N. J. (2007). Physiology and antennal lobe projections of olfactory receptor neurons from sexually isomorphic sensilla on male Heliothis virescens. J Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 193, 649-663.
33. Hillier, N. K., and Vickers, N. J. (2011). Mixture interactions in moth olfactory physiology: examining the effects of odorant mixture, concentration, distal stimulation, and antennal nerve transection on sensillar responses. Chem. Senses 36, 93-108.
34. Kesselmeier, J., and Staudt, M. (1997). Biogenic volatile organic compounds (VOC) an overview on emission, physiology and ecology. J. Atmos. Chem. 33, 22-88.
35. Krieger, J., Gaenssle, H., Raming, K., and Breer, H. (1993). Odorant binding proteins of Heliothis virescens. Insect Biochem. Mol. Biol. 23, 449-456.
36. Krieger, J., Grosse-Wilde, E., Gohl, T., Dewer, Y. M. E., Raming, K., and Breer, H. (2004). Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. U. S. A 101, 11845-11850.
37. Kuebler, L. S., Schubert, M., Karpati, Z., Hansson, B. S., and Olsson, S. B. (2012). Antennal lobe processing correlates to moth olfactory behavior. J. Neurosci. 32, 5772-5782.
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. Leal, W. S. (2003). "Proteins that make sense. " Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles, eds. G. Blomquist and R. Vogt (Elsevier Academic Press), 447-476.
40. Lei, H., and Vickers, N. (2008). Central processing of natural odor mixtures in insects. J. Chem. Ecol. 34, 915-927.
41. Maida, R., Mameli, M., Muller, B., Krieger, J., and Steinbrecht, R. A. (2005). The expression pattern of four odorant-binding proteins in male and female silk moths, Bombyx mori. J. Neurocytol. 34, 149-163.
42. Müller, K., Pelzing, M., Gnauk, T., Kappe, A., Teichmann, U., Spindler, G., Haferkorn, S., Jahn, Y., and Hermann, H. (2002). Monoterpene emissions and carbonyl compound air concentration during blooming period of rape (Brassica napus). Chemosphere 49, 1247-1256.
43. 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.
44. Namiki, S., Iwabuchi, S., and Kanzaki, R. (2008). Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 194, 501-515.
45. Ochieng, S. A., Park, K. C., and Baker, T. C. (2002). Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 188, 325-333.
46. Oldham, N. J., Krieger, J., Breer, H., and Svatos, A. (2001). Detection and removal of an artefact fatty acid from the binding site of recombinant Bombyx mori pheromone-binding protein. Chem. Senses 26, 529-531.
47. Party, V., Hanot, C., Said, I., Rochat, D., and Renou, M. (2009). Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. Chem. Senses 34, 763-774.
48. Plettner, E., Lazar, J., Prestwich, E. G., and Prestwich, G. D. (2000). Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar. Biochemistry 39, 8953-8962.
49. Qiao, H., He, X., Schymura, D., Id, L., Dani, F. R., Michelucci, E., Caputo, B., Torre, A. D., Iatrou, K., Zhou, J. J., Krieger, J., and Pelosi, P. (2010). Cooperative interactions between odorant-binding proteins of Anopheles gambiae. Cell. Mol. Life Sci 68, 1799-1813.
50. Rostelien, T., Stranden, M., Borg-Karlson, A. K., and Mustaparta, H. (2005). Olfactory receptor neurons in two Heliothine moth species responding selectively to aliphatic green leaf volatiles, aromatic compounds, monoterpenes and sesquiterpenes of plant origin. Chem. Senses 30, 443-461.
51. Rouyar, A., Party, V., Presern, J., Blejec, A., and Renou, M. (2011). A general odorant background affects the coding of pheromone stimulus intermittency in specialist olfactory receptor neurones. PLoS ONE 6, e26443.
52. Sandler, B. H., Nikonova, L., Leal, W. S., and Clardy, J. (2000). Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem. Biol. 7, 143-151.
53. Schneider, D. (1992). 100 Years of Pheromone Research / An Essay on Lepidoptera. Naturwissenschaften 79, 241-250.
54. Seki, Y., and Kanzaki, R. (2008). Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J. Comp. Neurol. 506, 93-107.
55. Skiri, H. T., Galizia, C. G., and Mustaparta, H. (2004). Representation of primary plant odorants in the antennal lobe of the moth Heliothis virescens using calcium imaging. Chem. Senses 29, 253-267.
56. Steinbrecht, R. A., and Gnatzy, W. (1984). Pheromone receptors in Bombyx mori and Antheraeapernyi. I. Reconstruction of the cellular organization of the sensilla trichodea. Cell Tissue Res. 235, 25-34.
57. Vickers, N. J. (2006). Winging it: moth flight behavior and responses of olfactory neurons are shaped by pheromone plume dynamics. Chem. Senses 31, 155-166.
58. Vickers, N. J., and Baker, T. C. (1997). Flight of Heliothis virescens males in the field in response to sex-pheromone. Physiol. Entomol. 22, 277-285.
59. Vickers, N. J., Christensen, T. A., Mustaparta, H., and Baker, T. C. (1991). Chemical communication in heliothine moths. III. Flight behavior of male Helicoverpa zea and Heliothis virescens in response to varying ratios of intra-and interspecific pheromone compounds. J. Comp. Physiol. A 169, 275-280.
60. Vogt, R. G. (2003). "Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. " Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles, eds. G. Blomquist and R. G. Vogt (Elsevier Academic Press), 391-445.
61. Vogt, R. G., and Riddiford, L. M. (1981). Pheromone binding and inactivation by moth antennae. Nature 293, 161-163.
62. Vosshall, L. B. (2008). Scent of a fly. Neuron 59, 685-689.
63. Wang, G., Carey, A. F., Carlson, J. R., and Zwiebel, L. J. (2010). Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 107, 4418-4423.
64. Wanner, K. W., Nichols, A. S., Allen, J. E., Bunger, P. L., Garczynski, S. F., Linn, C. E., Robertson, H. M., and Luetje, C. W. (2010). Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS. ONE. 5, e8685.
65. Wojtasek, H., and Leal, W. S. (1999). Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J. Biol. Chem. 274, 30950-30956.
66. Zhang, S., Maida, R., and Steinbrecht, R. A. (2001). Immunolocalization of odorant-binding proteins in noctuid moths (Insecta, Lepidoptera). Chem. Senses 26, 885-896.
67. Zhou, J. J., Zhang, G. A., Huang, W., Birkett, M. A., Field, L. M., Pickett, J. A., and Pelosi, P. (2004). Revisiting the odorant-binding protein LUSH of Drosophila melanogaster: evidence for odour recognition and discrimination. FEBS Lett. 558, 23-26.
68. Zwiebel, L. J., and Takken, W. (2004). Olfactory regulation of mosquito-host interactions. Insect Biochem. Mol. Biol. 34, 645-652.