Sequence similarity and functional comparisons of pheromone receptor orthologs in two closely related Helicoverpa species

Insect Biochemistry and Molecular Biology

Volumn 48, Issue 1, 2014, Pages 63-74

  Jiang, Xiao Jing ^a,b   Guo, Hao ^a   Di, Chang ^a   Yu, Shanlin ^b   Zhu, Ligui ^b   Huang, Ling Qiao ^a   Wang, Chen Zhu ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b SHANDONG PEANUT RESEARCH INSTITUTE   (China)

Author keywords

Functional evolution; Helicoverpa armigera; Helicoverpa assulta; Odorant receptor; Pheromone receptor

Indexed keywords

PHEROMONE RECEPTOR; SEX PHEROMONE;

AMINO ACID SEQUENCE; ANIMAL; ANTENNA (ORGAN); ELECTROPHYSIOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; MOTH; ODOR; REPRODUCTIVE ISOLATION; SPECIES DIFFERENTIATION;

AMINO ACID SEQUENCE; ANIMALS; ARTHROPOD ANTENNAE; ELECTROPHYSIOLOGICAL PHENOMENA; GENE EXPRESSION; GENETIC SPECIATION; MOTHS; RECEPTORS, PHEROMONE; REPRODUCTIVE ISOLATION; SEX ATTRACTANTS; SMELL;

EID: 84897881285     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.02.010     Document Type: Article

References (46)

1. Baker T.C., Ochieng' S.A., Cosse A.A., Lee S.G., Todd J.L., Quero C., Vickers N.J. Acomparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. J.Comp. Physiol. 2004, 190:155-165.
2. Bengtsson J.M., Trona F., Montagné N., Anfora G., Ignell R., Witzgall P., Jacquin-Joly E. Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptiome analysis. PLoS ONE 2012, 7:e31620.
3. Berg B.G., Mustaparta H. The significance of major pheromone components and interspecific signals as expressed by receptor neurons in the Oriental tobacco budworm moth, Helicoverpa assulta. J.Comp. Physiol. A. 1995, 177:683-694.
4. Berg B.G., Almaas T.J., Bjaalie J.G., Mustaparta H. Projections of male-specific receptor neurons in the antennal lobe of the oriental tobacco budworm moth, Helicoverpa assulta: a unique glomerular organization among related species. J.Comp. Neurol. 2005, 486:209-220.
5. Boo K.S., Park K.C., Hall D.R., Cork A., Berg B.G., Mustaparta H. (Z)-9-tetradecenal: a potent inhibitor of pheromone-mediated communication in the oriental tobacco budworm moth, Helicoverpa assulta. J.Comp. Physiol. A. 1995, 177:695-699.
6. Cork A., Boo K.S., Dunkelblom E., Hall D.R., Jee-Rajunga K., Kehat M., Kong J.E., Park K.C., Tepidagarm D., Liu X. Female sex pheromone of Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae): identification and field testing. J.Chem. Ecol. 1992, 18:403-418.
7. Gould F., Estock M., Hillier N.K. Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. Proc. Natl. Acad. Sci. U S A 2010, 107:8660-8665.
8. Grosse-Wilde E., Gohl T., Bouche E., Breer H., Krieger J. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromone compounds. Eur. J. Neurosci. 2007, 25:2364-2373.
9. Grosse-Wilde E., Kuebler L.S., Bucks S., Vogel H., Wicher D., Hansson B.S. Antennal transcriptome of Manduca sexta. Proc. Natl. Acad. Sci. U S A. 2011, 108:7449-7454.
10. Hallem E.A., Carlson J.R. Coding of odors by a receptor repertoire. Cell 2006, 125:143-160.
11. Hasson B.S., Stensmyr M.C. Evolution of insect olfaction. Neuron 2011, 72:698-711.
12. Howlett N., Dauber K.L., Shukla A., Morton B., Glendinning J.I., Brent E. Identification of chemosensory receptor genes in Manduca sexta and knockdown by RNA interference. BMC Genomics 2012, 13:211.
13. Jacquin-Joly E., Legeai F., Montagné N., Monsempes C., François M.C., Poulain J. Candidate chemosensory genes in female antennae of the Noctuid moth Spodoptera littoralis. Int. J. Biol. Sci. 2012, 8:1036-1050.
14. Kehat M., Dunkelblum E. Behavioral response of male Heliothis armigera (Lepidoptera: Noctuidae) moths in a flight tunnel to combinations of component identified from female sex pheromone glands. J.Insect Behav. 1990, 3:75-83.
15. Krieger J., Raming K., Dewer Y.M., Bette S., Conzelmann S., Breer H. Adivergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 2002, 16:619-628.
16. Krieger J., Grosse-Wilde E., Gohl T., Dewer Y.M., Raming K., Breer H. Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. U S A 2004, 101:11845-11850.
17. Leal W.S. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol. 2013, 58:373-391.
18. Leary G.P., Allen J.E., Bunger P.L., Luginbill J.B., Linn C.E., Macallister I.E., Kavanaugh M.P., Wanner K.W. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc. Natl. Acad. Sci. U S A 2012, 109(35):14081-14086.
19. Lee S.G., Vickers N.J., Baker T.C. Glomerular targets of Heliothis subflexa male olfactory receptor neurons housed within long trichoid sensilla. Chem. Senses 2006, 31:821-834.
20. Legeai F., Malpel S., Montagné N., Monsempes C., Cousserans F., Merlin C. An expressed sequence tag collection from the male antennae of the Noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genomics 2011, 12:86.
21. Liu Y., Gu S., Zhang Y., Guo Y., Wang G. Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS ONE 2012, 7(10):e48260.
22. Liu C., Liu Y., Walker W.B., Dong S., Wang G. Identification and functional characterization of sex pheromone receptors in beet armyworm Spodoptera exigua (HÜbner). Insect Biochem. Mol. Biol. 2013, 43:747-754.
23. Liu Y., Liu C., Lin K., Wang G. Functional specificity of sex pheromone receptors in the cotton bollworm Helicoverpa armigera. PLoS ONE 2013, 8(4):e62094.
24. -δδCT method. Methods 2001, 25:402-408.
25. Mitsuno H., Sakurai T., Murai M., Yasuda T., Kugimiya S., Ozawa R., Toyohara H., Takabayashi J., Miyoshi H., Nishioka T. Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur. J. Neurosci. 2008, 28:893-902.
26. Miura N., Nakagawa T., Tatsuki S., Touhara K., Ishikawa Y. Amale-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int. J. Bio. Sci. 2009, 5:319-330.
27. Miura N., Nakagawa T., Touhara K., Ishikawa Y. Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem. Mol. Biol. 2010, 40:64-73.
28. Montagné N., Chertemps T., Brigaud I., François A., François M.C., Fouchier A. Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur. J. Neurosci. 2012, 36:2588-2596.
29. Nakagawa T., Sakurai T., Nishioka T., Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 2005, 307:1638-1642.
30. Sakurai T., Nakagawa T., Mitsuno H., Mori H., Endo Y., Tanoue S., Yasukochi Y., Touhara K., Nishioka T. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci. U S A 2004, 101:16653-16658.
31. Sato K., Tanaka K., Touhara K. Sugar-regulated cation channel formed by an insect gustatory receptor. Proc. Natl. Acad. Sci. U S A 2011, 108:11680-11685.
32. T method. Nat. Protoc. 2008, 3(6):1101-1108.
33. Semmelhack J.L., Wang J.W. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 2009, 459:218-223.
34. Sun M., Liu Y., Walker W.B., Liu C., Lin K., Gu S., Zhang Y., Zhou J., Wang G. Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth, Plutella xyllostella. PLoS ONE 2013, 8(4):e62098.
35. Syed Z., Kopp A., Kimbrell D.A., Leal W.S. Bombykol receptors in the silkworm moth and the fruit fly. Proc. Natl. Acad. Sci. U S A 2010, 107(20):9436-9439.
36. Tanaka K., Uda Y., Ono Y., Nakagawa T., Suwa M., Yamaoka R., Touhara K. Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr. Biol. 2009, 19:881-890.
37. Vetter R.S., Baker T.C. Behavioral responses of male Heliothis virescens in a sustained-flight tunnel to combinations of seven compounds identified from female sex pheromone glands. J.Chem. Ecol. 1983, 9:747-759.
38. Vickers N.J., Baker T.C. Chemical communication in Heliothine moths. VII. Correlation between diminished responses to point-source plumes and single filaments similarly tainted with a behavioral antagonist. J.Comp. Physiol. A. 1997, 180:523-536.
39. Wang G., Vásquez G.M., Schal C., Zwiebel L.J., Gould F. Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol. Biol. 2010, 20:125-133.
40. Wang H.L., Zhao C.H., Wang C.Z. Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochem. Mol. Biol. 2005, 35:575-583.
41. Wanner K.W., Nichols A.S., Allen J.E., Bunger P.L., Garczynski S.F., Linn C.E., Robertson H.M., Luetje C.W. Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE 2010, 5(1):e8685.
42. Wanner K.W., Robertson H.M. The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single linerage of putative bitter receptors. Insect Mol. Biol. 2008, 17:621-629.
43. Wu D., Yan Y., Cui J. Sex pheromone components of Helicoverpa armigera: chemical analysis and field tests. Insect Sci. 1997, 4:350-356.
44. Wu H., Hou C., Huang L.Q., Yan F.S., Wang C.Z. Peripheral coding of sex pheromone blends with reverse ratios in two Helicoverpa species. PLoS ONE 2013, 8(7):e70078.
45. Zhang D.D., Zhu K.Y., Wang C.Z. Sequencing and characterization of six cDNAs putatively encoding three pairs of pheromone receptors in two sibling species, Helicoverpa armigera and Helicoverpa assulta. J.Insect Physiol. 2010, 56:586-593.
46. Zhang J.P., Salcedo C., Fang Y.L., Zhang R.J., Zhang Z.N. An overlooked component: (Z)-9-tetradecenal as a sex pheromone in Helicoverpa armigera. J.Insect Physiol. 2012, 58:1209-1216.