A Single Sex Pheromone Receptor Determines Chemical Response Specificity of Sexual Behavior in the Silkmoth

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In insects and other animals, intraspecific communication between individuals of the opposite sex is mediated in part by chemical signals called sex pheromones. In most moth species, male moths rely heavily on species-specific sex pheromones emitted by female moths to identify and orient towards an appropriate mating partner among a large number of sympatric insect species. The silkmoth, Bombyx mori, utilizes the simplest possible pheromone system, in which a single pheromone component, (E, Z)-10,12-hexadecadienol (bombykol), is sufficient to elicit full sexual behavior. We have previously shown that the sex pheromone receptor BmOR1 mediates specific detection of bombykol in the antennae of male silkmoths. However, it is unclear whether the sex pheromone receptor is the minimally sufficient determination factor that triggers initiation of orientation behavior towards a potential mate. Using transgenic silkmoths expressing the sex pheromone receptor PxOR1 of the diamondback moth Plutella xylostella in BmOR1-expressing neurons, we show that the selectivity of the sex pheromone receptor determines the chemical response specificity of sexual behavior in the silkmoth. Bombykol receptor neurons expressing PxOR1 responded to its specific ligand, (Z)-11-hexadecenal (Z11-16:Ald), in a dose-dependent manner. Male moths expressing PxOR1 exhibited typical pheromone orientation behavior and copulation attempts in response to Z11-16:Ald and to females of P. xylostella. Transformation of the bombykol receptor neurons had no effect on their projections in the antennal lobe. These results indicate that activation of bombykol receptor neurons alone is sufficient to trigger full sexual behavior. Thus, a single gene defines behavioral selectivity in sex pheromone communication in the silkmoth. Our findings show that a single molecular determinant can not only function as a modulator of behavior but also as an all-or-nothing initiator of a complex species-specific behavioral sequence.

Vyšlo v časopise: A Single Sex Pheromone Receptor Determines Chemical Response Specificity of Sexual Behavior in the Silkmoth. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002115
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002115

Souhrn

Zdroje

1. SchneiderD 1992 100 years of pheromone research: An essay on Lepidoptera. Naturwissenschaften 79 241 250

2. RoelofsWLCardéRT 1974 Sex pheromones in the reproductive isolation of lepidopterous species. BirchMC Pheromones Amsterdam North-Holland 96 114

3. BakerTC 2008 Balanced olfactory antagonism as a concept for understanding evolutionary shifts in moth sex pheromone blends. J Chem Ecol 34 971 981

4. DomingueMJMustoCJLinnCEJrRoelofsWLBakerTC 2007 Altered olfactory receptor neuron responsiveness in rare Ostrinia nubilalis males attracted to the O. furnacalis pheromone blend. J Insect Physiol 53 1063 1071

5. DomingueMJHaynesKFToddJLBakerTC 2009 Altered olfactory receptor neuron responsiveness is correlated with a shift in behavioral response in an evolved colony of the cabbage looper moth, Trichoplusia ni. J Chem Ecol 35 405 415

6. KárpátiZDekkerTHanssonBS 2008 Reversed functional topology in the antennal lobe of the male European corn borer. J Exp Biol 211 2841 2848

7. HallemEADahanukarACarlsonJR 2006 Insect odor and taste receptors. Annu Rev Entomol 51 113 135

8. TouharaKVosshallLB 2009 Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71 307 332

9. NakagawaTSakuraiTNishiokaTTouharaK 2005 Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307 1638 1642

10. MitsunoHSakuraiTMuraiMYasudaTKugimiyaS 2008 Identification of receptors of main sex-pheromone components of three lepidopteran species. Eur J Neurosci 28 893 902

11. MiuraNNakagawaTTatsukiSTouharaKIshikawaY 2009 A male-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int J Biol Sci 5 319 330

12. WannerKWNicholsASAllenJEBungerPLGarczynskiSF 2010 Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE 5 e8685 doi:10.1371/journal.pone.0008685

13. SyedZIshidaYTaylorKKimbrellDALealWS 2006 Pheromone reception in fruit flies expressing a moth's odorant receptor. Proc Natl Acad Sci U S A 103 16538 16543

14. KurtovicAWidmerADicksonBJ 2007 A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446 542 546

15. GouldFEstockMHillierNKPowellBGrootAT 2010 Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. Proc Natl Acad Sci U S A 107 8660 8665

16. ButenandtABeckmannRStammDHeckerE 1959 Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b 283 284

17. KramerE 1975 Orientation of the male silkmoth to the sex attractant bombykol. DentonDACoghlanJP Olfaction and Taste vol. 5 New York Academic Press 329 335

18. KaisslingK-E 1987 R. H. Wright Lectures on Insect Olfaction. ColbowK Burnaby Simon Fraser Univ 107

19. KaisslingK-EKasangGBestmannHJStranskyWVostrowskyO 1978 A new pheromone of the silkworm moth Bombyx mori. Sensory pathway and behavioral effect. Naturwissenschaften 65 382 384

20. SakuraiTNakagawaTMitsunoHMoriHEndoY 2004 Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101 16653 16658

21. TamakiYKawasakiKYamadaHKoshiharaTOsakiN 1977 (Z)-11-hexadecenal and (Z)-11-hexadecenyl acetate: sex-pheromone components of the diamondback moth (Lepidoptera: Plutellidae). Appl Entomol Zool 12 208 210

22. AndoTKoshiharaTYamadaHVuMHTakahashiN 1979 Electroantennogram activities of sex pheromone analogues and their synergistic effect on field attraction in the diamondback moth. Appl Entomol Zool 14 362 364

23. SatoKPellegrinoMNakagawaTNakagawaTVosshallLB 2008 Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452 1002 1006

24. WicherDSchäferRBauernfeindRStensmyrMCHellerR 2008 Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452 1007 1011

25. UchinoKImamuraMSezutsuHKobayashiIKojimaK 2006 Evaluating promoter sequences for trapping an enhancer activity in the silkworm Bombyx mori. J Insect Biotechnol Sericol 75 89 97

26. PelosiPZhouJ-JBanLPCalvelloM 2006 Soluble proteins in insect chemical communication. Cell Mol Life Sci 63 1658 1676

27. Große-WildeESvatošAKriegerJ 2006 A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31 547 555

28. Große-WildeEGohlTBouchéEBreerHKriegerJ 2007 Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25 2364 2373

29. ForstnerMBreerHKriegerJ 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

30. ForstnerMGohlTBreerHKriegerJ 2006 Candidate pheromone binding proteins of the silkmoth Bombyx mori. Invert Neurosci 6 177 187

31. ZhouJ-JRobertsonGHeXDufourSHooperAM 2009 Characterisation of Bombyx mori odorant-binding proteins reveals that a general odorant-binding protein discriminates between sex pheromone components. J Mol Biol 389 529 545

32. HeXTzotzosGWoodcockCPickettJAHooperT 2010 Binding of the general odorant binding protein of Bombyx mori BmorGOBP2 to the moth sex pheromone components. J Chem Ecol 36 1293 1305

33. HooperAMDufourSHeXMuckAZhouJ-J 2009 High-throughput ESI-MS analysis of binding between the Bombyx mori pheromone-binding protein BmorPBP1, its pheromone components and some analogues. Chem Comm 14 5725 5727

34. KanzakiRSugiNShibuyaT 1992 Self-generated zigzag turning of Bombyx mori males during pheromone-mediated upwind walking. Zool Sci 9 515 527

35. HildebrandJGShepherdGM 1997 Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20 595 631

36. HanssonBS 1997 Antennal lobe projection patterns of pheromone-specific olfactory receptor neurons in moths. CardéRTMinksAK Insect Pheromone Research. New Directions New York Chapman & Hall 164 183

37. KanzakiRSooKSekiYWadaS 2003 Projections to higher olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silkmoth. Chem Senses 28 113 130

38. KazawaTNamikiSFukushimaRTeradaMSooK 2009 Constancy and variability of glomerular organization in the antennal lobe of the silkmoth. Cell Tissue Res 336 119 136

39. DobritsaAAvan der Goes van NatersWWarrCGSteinbrechtRACarlsonJR 2003 Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37 827 841

40. RonderosDSSmithDP 2010 Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 30 2595 2599

41. VillellaAHallJC 2008 Neurogenetics of courtship and mating in Drosophila. Adv Genet 62 67 184

42. OchiengSAPooleKLinnCEVickersNJRoelofsWL 2003 Unusual pheromone receptor neuron responses in heliothine moth antennae derived from inter-species imaginal disc transplantation. J Comp Physiol A 189 19 28

43. VickersNJPooleKLinnCE 2003 Consequences of interspecies antennal imaginal disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination. J Comp Neurol 466 377 388

44. VickersNJPooleKLinnCE 2005 Plasticity in central olfactory processing and pheromone blend discrimination following interspecies antennal imaginal disc transplantation. J Comp Neurol 491 141 156

45. KikuchiT 1975 Correlation of moth sex pheromone activities with molecular characteristics involved in conformers of bombykol and its derivatives. Proc Natl Acad Sci U S A 72 3337 3341

46. TanakaKUdaYOnoYNakagawaTSuwaM 2009 Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19 1 10

47. LeiHVickersN 2008 Central processing of natural odor mixtures in insects. J Chem Ecol 34 915 927

48. SmadjaCButlinRK 2009 On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102 77 97

49. SakudohTSezutsuHNakashimaTKobayashiIFujimotoH 2007 Carotenoid silk coloration is controlled by a carotenoid-binding protein, a product of the Yellow blood gene. Proc Natl Acad Sci U S A 104 8941 8946

50. TamuraTThibertCRoyerCKandaTAbrahamE 2000 Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18 81 84

51. TamuraTKuwabaraNUchinoKKobayashiIKandaT 2007 An improved DNA injection method for silkworm eggs drastically increases the efficiency of producing transgenic silkworms. J Insect Biotechnol Sericol 76 155 159

52. MounierNGaillardJPrudhommeJ-C 1987 Nucleotide sequence of the coding region of two actin genes in Bombyx mori. Nucleic Acids Res 15 2781

53. TatematsuKIKobayashiIUchinoKSezutsuHIizukaT 2010 Construction of a binary transgenic gene expression system for recombinant protein production in the middle silk gland of the silkworm Bombyx mori. Transgenic Res 19 473 487

54. ShinodaTItoyamaK 2003 Juvelile hormone acid methyltransferase: A key regulatory enzyme for insect metamorphosis. Proc Natl Acad Sci U S A 100 11986 11991

55. SekiYAonumaHKanzakiR 2005 Pheromone processing center in the protocerebrum of Bombyx mori revealed by nitric oxide-induced anti-cGMP immunocytochemistry. J Comp Neurol 481 340 351