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Binding Interactions, Structure-Activity Relationships and Blend Effects in Pheromone and Host Olfactory Detection of Herbivorous Lepidoptera

  • Mailyn Terrado
  • Govardhana R. Pinnelli
  • Jürgen Sanes
  • Erika PlettnerEmail author
Chapter

Abstract

Herbivorous moths (Lepidoptera) use their chemical senses (olfaction and gustation) for choosing their food (during larval stages) and for finding a mate (during adult life). Insects use chemosensory sensilla, hollow cuticular hairs that are innervated, for sensing chemical stimuli in their environment. These chemical stimuli (host plant odorants and pheromones) interact with the molecular components of the sensilla, which include: odorant-binding proteins (OBPs), odorant receptors (ORs) with their co-receptor (ORCO) and ionotropic receptors (IRs). Here we review the structures of moth pheromones and general odorants, as well as structural analogs, and how these molecules interact with OBPs, the structurally best characterized molecular components of insect chemosensory systems. We also review structure-activity relationships that have been obtained with systematically varied odorants. The activities that have been monitored include electrophysiological and behavioral responses.

References

  1. Abraham D, Löfstedt C, Picimbon JF (2005) Molecular evolution and characterization of pheromone binding protein genes in Agrotis moths. Insect Biochem Mol Biol 35:1100–1111CrossRefPubMedGoogle Scholar
  2. Adachi Y, Do ND, Kinjo SD, Yamakawa M, Mori K, Ando T (2010) Positions and stereochemistry of methyl branches in the novel sex pheromone components produced by a lichen moth. Lyclene dharma dharma. J Chem Ecol 36:814–823CrossRefPubMedGoogle Scholar
  3. Akhtar Y, Isman MB, Paduraru PM, Nagabandi S, Nair R, Plettner E (2007) Screening of dialkoxy benzenes and disubstituted cyclopentene derivatives against a noctuid caterpillar Trichoplusia ni, for the discovery of new feeding and oviposition deterrents. J Agric Food Chem 55:10323–10330CrossRefPubMedGoogle Scholar
  4. Akhtar Y, Yu Y, Isman MB, Plettner E (2010) Dialkoxybenzene and dialkoxy-allylbenzene feeding and oviposition deterrents against the cabbage looper, Trichoplusia ni: potential insect behavior control agents. J Agric Food Chem 58:4983–4991CrossRefPubMedGoogle Scholar
  5. Anderson AR, Wanner KW, Trowell SC, Warr CG, Jaquin-Joly E, Zagatti P, Robertson H, Newcomb RD (2009) Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem Mol Biol 39:189–197CrossRefPubMedGoogle Scholar
  6. Ando T, Inomata S, Yamamoto M (2004) Lepidopteran sex pheromones. Top Curr Chem 239:51–96CrossRefPubMedGoogle Scholar
  7. Ban L, Zhang L, Yan Y, Pelosi P (2002) Binding properties of a locust’s chemosensory protein. Biochem Biophys Res Commun 293:50–54CrossRefPubMedGoogle Scholar
  8. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20CrossRefPubMedPubMedCentralGoogle Scholar
  9. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–293CrossRefGoogle Scholar
  10. Bierl B, Beroza M, Collier C (1970) Potent sex attractant of the gypsy moth: its isolation, identification, and synthesis. Science 170:87–89CrossRefPubMedGoogle Scholar
  11. Bouwer M, Slippers B, Degefu D, Wingfield M, Lawson S, Rohwer E (2015) Identification of the sex pheromone of the tree infesting cossid moth Coryphodema tristis (Lepidoptera: Cossidae). PLoS One 10:e0118575CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274CrossRefPubMedGoogle Scholar
  13. Burger H, Ayasse M, Dötterl S, Kreissl S, Galizia CG (2013) Perception of floral volatiles involved in host-plant finding behaviour: comparison of a bee specialist and generalist. J Comp Physiol 199:751–761CrossRefGoogle Scholar
  14. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b:283–284Google Scholar
  15. Cameron LM, Rogers M, Aalhus M, Seward B, Yu Y, Plettner E (2014) Feeding deterrence of cabbage looper (Lepidoptera: Noctuidae) by 1-allyloxy-4-propoxybenzene, alone and blended with neem extract. J Econ Entomol 107:2119–2129CrossRefPubMedGoogle Scholar
  16. Camps F, Gasol V, Guerrero A, Hernández R, Montoya R (1990) Inhibition of the processionary moth sex pheromone by some haloacetate analogues. Pestic Sci 29:123–134CrossRefGoogle Scholar
  17. Cao S, Liu Y, Guo M, Wang G (2016) A conserved odorant receptor tuned to floral volatiles in three heliothinae species. PLoS One 11:e0155029CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chang H, Liu Y, Yang T, Pelosi P, Dong S, Wang G (2015) Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Sci Rep 5:13093CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chang H, Guo M, Wang B, Liu Y, Dong S, Wang G (2016) Sensillar expression and responses of olfactory receptors reveal different peripheral coding in two Helicoverpa species using the same pheromone components. Sci Rep 6:18742CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chen H, Gong Y, Gries RM, Plettner E (2010) Synthesis and biological activity of conformationally restricted gypsy moth pheromone mimics. Bioorg Med Chem 18:2920–2929CrossRefPubMedGoogle Scholar
  21. Cheng ZQ, Xiao JC, Huang XT, Chen DL, Li JQ, He YS, Huang SR, Luo QC, Yang CM, Yang TH (1981) Sex pheromone components isolated from China corn borer,Ostrinia furnacalis, Guenee (Lepidoptera: Pyralidae), (E)- and (Z)-12-tetradecenyl acetates. J Chem Ecol 7:841–851CrossRefPubMedGoogle Scholar
  22. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338CrossRefGoogle Scholar
  23. Cork A, Boo KS, Dunkelblum E, Hall DR, Jee-Rajunga K, Kehat M, Kong Jie E, Park KC, Tepgidagarn P, Xun L (1992) Female sex pheromone of oriental tobacco budworm, Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae): identification and field testing. J Chem Ecol 18:403–418CrossRefPubMedGoogle Scholar
  24. Cunningham JP (2012) Can mechanism help explain insect host choice? J Evol Biol 25:244–251CrossRefPubMedGoogle Scholar
  25. Cunningham JP, Zalucki MP (2014) Understanding heliothine (Lepidoptera: Heliothinae) pests: what is a host plant? J Econ Entomol 107:881–896CrossRefGoogle Scholar
  26. Damberger FF, Ishida Y, Leal WS, Wuthrich K (2007) Structural basis of ligand binding and release in insect pheromone-binding proteins: NMR structure of Antheraea polyphemus PBP1 at pH 4.5. J Mol Biol 373:811–819CrossRefPubMedGoogle Scholar
  27. De Moares CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580CrossRefGoogle Scholar
  28. di Luccio E, Ishida Y, Leal WS, Wilson DK (2013) Crystallographic observation of pH-induced conformational changes in the Amyelois transitella pheromone-binding protein AtraPBP1. PLoS One 8:e53840CrossRefPubMedPubMedCentralGoogle Scholar
  29. Faucheux MJ (1995) Sensilla on the larval antennae and mouthparts of the european sunflower moth, Homoeosoma nebulella Den. and Schiff. (Lepidoptera: Pyralidae). Int J Insect Morphol Embryol 24:391–403CrossRefGoogle Scholar
  30. Feng L, Prestwich GD (1997) Expression and characterization of a lepidopteran general odorant binding protein. Insect Biochem Mol Biol 27:405–412CrossRefPubMedGoogle Scholar
  31. Forstner M, Breer H, 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 5:745–757CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31–39CrossRefGoogle Scholar
  33. Ge X, Zhang T, Wang Z, He K, Bai S (2016) Identification of putative chemosensory receptor genes from yellow peach moth Conogethes punctiferalis (Guenée) antennae transcriptome. Sci Rep 6:32636CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gomez-Diaz C, Bargeton B, Abuin L, Bukar N, Reina JH, Bartoi T, Graf M, Ong H, Ulbrich MH, Masson JF, Benton R (2016) A CD36 ectodomain mediates insect pheromone detection via a putative tunnelling mechanism. Nat Commun 7:11866CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gong Y, Plettner E (2011) Effects of aromatic compounds on antennal responses and on the pheromone-binding proteins of the gypsy moth (Lymantria dispar). Chem Senses 36:291–300CrossRefPubMedGoogle Scholar
  36. Gong Y, Pace TCS, Castillo C, Bohne C, O’Neill MA, Plettner E (2009) Ligand-interaction kinetics of the pheromone-binding protein from the gypsy moth, L. dispar: insights into the mechanism of binding and release. Chem Biol 16:162–172CrossRefPubMedGoogle Scholar
  37. Gong Y, Tang H, Bohne C, Plettner E (2010) Binding conformation and kinetics of two pheromone-binding proteins from the gypsy moth Lymantria dispar with biological and nonbiological ligands. Biochemistry 49:793–801CrossRefPubMedGoogle Scholar
  38. Grosse-Wilde E, Svatos A, Krieger J (2006) A pheromone-binding protein mediates the Bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31:547–555CrossRefPubMedGoogle Scholar
  39. Grosse-Wilde E, Gohl T, Bouche E, Breer H, Krieger J (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25:2364–2373CrossRefPubMedGoogle Scholar
  40. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS (2011) Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci U S A 108:7449–7454CrossRefPubMedPubMedCentralGoogle Scholar
  41. Gu SH, Zhou JJ, Wang GR, Zhang YJ, Guo YY (2013) Sex pheromone recognition and immunolocalization of three pheromone binding proteins in the black cutworm moth Agrotis ipsilon. Insect Biochem Mol Biol 43:237–251CrossRefPubMedGoogle Scholar
  42. Guerrero A, Camps F, Coll J, Riba M, Einhorn J, Descoins C, Lallemand JY (1981) Identification of a potential sex pheromone of the processionary moth Thaumetopoea pityocampa. Tetrahedron Lett 22:2013–2016CrossRefGoogle Scholar
  43. Gullan PJ, Cranston PS (2010) The insects: an outline of entomology, 4th edn. Wiley-Blackwell, Chichester, p 584Google Scholar
  44. Guo H, Huang LQ, Pelosi P, Wang CZ (2012) Three pheromone-binding proteins help segregation between two Helicoverpa species utilizing the same pheromone compounds. Insect Biochem Mol Biol 42:708–716CrossRefPubMedGoogle Scholar
  45. He X, Tzotzos G, Woodcock C, Pickett JA, Hooper T, Field LM, Zhou JJ (2010) Binding of the general odorant binding protein of Bombyx mori BmorGOBP2 to the moth sex pheromone components. J Chem Ecol 36:1293–1305CrossRefPubMedGoogle Scholar
  46. Hill AS, Rings RW, Swier SR, Roelofs WL (1979) Sex pheromone of the black cutworm moth, Agrotis ipsilon. J Chem Ecol 5:439–457CrossRefGoogle Scholar
  47. Hillier N, Kavanagh R (2015) Differential octopaminergic modulation of olfactory receptor neuron responses to sex pheromones in Heliothis virescens. PLoS One 10:e0143179CrossRefPubMedPubMedCentralGoogle Scholar
  48. Honson NS, Plettner E (2006) Disulfide connectivity and reduction in pheromone-binding proteins of the gypsy moth, Lymantria dispar. Naturwissenschaften 93:267–277CrossRefPubMedGoogle Scholar
  49. Honson NS, Johnson MA, Oliver JE, Prestwich GD, Plettner E (2003) Structure-activity studies with pheromone-binding proteins of the gypsy moth, Lymantria dispar. Chem Senses 28:479–489CrossRefPubMedGoogle Scholar
  50. Honson NS, Gong Y, Plettner E (2005) Structure and function of insect odorant and pheromone-binding Proteins (OBPs and PBPs) and chemosensory-specific proteins (CSPs). In: Romeo J (ed) Chemical ecology and phytochemistry of forest ecosystems: proceedings of the Phytochemical Society of North America. Elsevier, Amsterdam, pp 228–268Google Scholar
  51. Ishida Y, Tsuchiya W, Fuji T, Fujimoto Z, Miyazawa M, Ishibashi J, Matsuyama S, Ishikawa Y, Yamazaki T (2014) Niemann-Pick type C2 protein mediating chemical communication in the worker ant. Proc Natl Acad Sci U S A 111:3847–3852CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jin X, Ha TS, Smith DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci U S A 105:10996–11001CrossRefPubMedPubMedCentralGoogle Scholar
  53. Jordan MD, Anderson A, Begum D, Carraher C, Authier A, Marshall SDG, Kiely A, Gatehouse LN, Greenwood DR, Christie DL, Kralicek AV, Trowell SC, Newcomb RD (2009) Odorant receptors from the light brown apple moth (Epiphyas postvittana) recognize important volatile compounds produced by plants. Chem Senses 34:383–394CrossRefPubMedGoogle Scholar
  54. Kaissling KE (2001) Olfactory perireceptor and receptor events in moths: a kinetic model. Chem Senses 26:125–150CrossRefPubMedGoogle Scholar
  55. Kaissling K, Thorson J (1980) Insect olfactory sensilla: structural, chemical and electrical aspects of the functional organization. In: Sattelle D, Hall L, Hildebrand J (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier, Amsterdam, pp 261–282Google Scholar
  56. Kaissling KE, Keil TA, Williams JLD (1991) Pheromone stimulation in perfused sensory hairs of the moth Antheraea polyphemus. J Insect Physiol 37:71–78CrossRefGoogle Scholar
  57. Kanaujia S, Kaissling KE (1985) Interactions of pheromone with moth antennae: adsorption, desorption and transport. J Insect Physiol 31:71–81CrossRefGoogle Scholar
  58. Katre UV, Mazumder S, Prusti RK, Mohanty S (2009) Ligand binding turns moth pheromone-binding protein into a pH sensor, effect on the Antheraea polyphemus PBP1 conformation. J Biol Chem 284:32167–32177CrossRefPubMedPubMedCentralGoogle Scholar
  59. Katre UV, Mazumder S, Mohanty S (2013) Structural insights into the ligand binding and releasing mechanism of Antheraea polyphemus pheromone-binding protein 1: role of the C-terminal tail. Biochemistry 52:1037–1044CrossRefPubMedPubMedCentralGoogle Scholar
  60. Keil TA (1984) Reconstruction and morphometry of silkworm olfactory hairs: a comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and Antheraea pernyi (Insecta, Lepidoptera). Zoomorphology 104:147–156CrossRefGoogle Scholar
  61. Kochansky J, Carde RT, Liebherr J, Roelofs WL (1975) Sex pheromone of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in New york. J Chem Ecol 1:225–231CrossRefGoogle Scholar
  62. Koh YH, Park KC, Boo KS (1995) Antennal sensilla in adult Helicoverpa assulta (Lepidoptera: Noctuidae): morphology, distribution, and ultrastructure. Ann Entomol Soc Am 88:519–530CrossRefGoogle Scholar
  63. Krieger J, Raming K, Dewer YME, Bette S, Conzelmann S, Breer H (2002) A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur J Neurosci 16:619–628CrossRefPubMedGoogle Scholar
  64. Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci U S A 101:11845–11850CrossRefPubMedPubMedCentralGoogle Scholar
  65. Krieger J, Grosse-Wilde E, Gohl T, Breer H (2005) Candidate pheromone receptors of the silkmoth Bombyx mori. Eur J Neursci 21:2167–2176CrossRefGoogle Scholar
  66. Krieger J, Gondensen I, Forstner M, Gohl T, Dewer Y, Breer H (2009) HR11 and HR13 receptor-expressing neurons are housed together in pheromone-responsive sensilla trichodea of male Heliothis virescens. Chem Senses 34:469–477CrossRefPubMedGoogle Scholar
  67. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714CrossRefGoogle Scholar
  68. Leal WS, Chen AM, Ishida Y, Chiang VP, Erickson ML, Morgan TI, Tsuruda JM (2005) Kinetics and molecular properties of pheromone binding and release. Proc Natl Acad Sci U S A 102:5386–5391CrossRefPubMedPubMedCentralGoogle Scholar
  69. Leal WS, Ishida Y, Pelletier J, Xy W, Rayo J, Xu X, Ames JB (2009) Olfactory proteins mediating chemical communication in the navel orangeworm moth, Amyelois transitella. PLoS One 4:e7235CrossRefPubMedPubMedCentralGoogle Scholar
  70. Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE Jr, Macallister IE, Kavanaugh MP, Wanner KW (2012) Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci U S A 109:14081–14086CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lee JK, Strausfeld NJ (1990) Structure, distribution and number of surface sensilla and their receptor cells on the olfactory appendage of the male moth Manduca sexta. J Neurocytol 19:519–538CrossRefPubMedGoogle Scholar
  72. Lee D, Damberger FF, Peng G, Horst R, Guntert P, Nikonova L, Leal WS, Wuthrich K (2002) NMR structure of the unliganded Bombyx mori pheromone-binding protein at physiological pH. FEBS Lett 531:314–318CrossRefPubMedGoogle Scholar
  73. Li G, Chen X, Li B, Zhang G, Li Y, Wu J (2016a) Binding properties of general odorant binding proteins from the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae). PLoS One 11:e0155096CrossRefPubMedPubMedCentralGoogle Scholar
  74. Li G, Zhang Y, Li YP, Wu JX, Xu XL (2016b) Cloning expression and functional analysis of three odorant-binding proteins of the oriental fruit moth Grapholita molesta (Busck) (Lepidoptera: Tortricidae). Arch Insect Biochem Physiol 91:67–87CrossRefPubMedGoogle Scholar
  75. Li PY, Qin YC (2011) Molecular cloning and characterization of sensory neuron membrane protein and expression pattern analysis in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Appl Entomol Zool 46:497–504CrossRefGoogle Scholar
  76. Li Z, Ni JD, Huang J, Montell C (2014) Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genet 10:e1004600CrossRefPubMedPubMedCentralGoogle Scholar
  77. Li ZQ, Zhang S, Luo JY, Cui JJ, Ma Y, Dong SL (2013) Two Minus-C odorant binding proteins from Helicoverpa armigera display higher ligand binding affinity at acidic pH than neutral pH. J Insect Physiol 59:263–272CrossRefPubMedGoogle Scholar
  78. Lin W, Yu Y, Zhou P, Zhang J, Dou L, Hao Q, Chen H, Zhu S (2015) Identification and knockdown of the olfactory receptor (OrCo) in gypsy moth, Lymantria dispar. Int J Biol Sci 11:772–780CrossRefPubMedPubMedCentralGoogle Scholar
  79. Liu NY, Yang F, Yang K, He P, Niu XH, Xu W, Anderson A, Dong SL (2014a) Two subclasses of odorant-binding proteins in Spodoptera exigua display structural conservation and functional divergence. Insect Mol Biol 24:167–182CrossRefPubMedGoogle Scholar
  80. Liu C, Zhang J, Liu Y, Wang G, Dong S (2014b) Expression of SNMP1 and SNMP2 genes in antennal sensilla of Spodoptera exigua (Hubner). Arch Insect Biochem Physiol 85:114–126CrossRefPubMedGoogle Scholar
  81. Liu S, Zhang YR, Zhou WW, Liang QM, Yuan X, Cheng J, Zhu ZR, Gong ZJ (2013a) Identification and characterization of two sensory neuron membrane proteins from Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Arch Insect Biochem Physiol 82:29–42CrossRefPubMedGoogle Scholar
  82. Liu S, Qiao F, Liang QM, Huang YJ, Zhou WW, Gong ZJ, Cheng J, Zhu ZR (2013b) Molecular characterization of two sensory neuron membrane proteins from Chilo suppressalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am 106:378–384CrossRefGoogle Scholar
  83. Liu YP, Liu Y, Yang T, Gui FR, Wang GR (2015) Identification and characterization of a general odorant receptor gene PxylOR9 in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Acta Entomol Sin 58:507–515Google Scholar
  84. Liu Z, Hua B, Liu L (2011) Ultrastructure of the sensilla on larval antennae and mouthparts in the peach fruit moth, Carposina sasakii Matsumura (Lepidoptera: Carposinidae). Micron 42:478–483CrossRefPubMedGoogle Scholar
  85. Lundin C, Kall L, Kreher SA, Kapp K, Sonnhammer EL, Carlson JR, von Heijne G, Nilsson I (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581:5601–5604CrossRefPubMedPubMedCentralGoogle Scholar
  86. Ma M, Chang MM, Lei CL, Yang FL (2016) A garlic substance disrupts odorant-binding protein recognition of insect pheromones released from adults of the angoumois grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Mol Biol 25:530–540CrossRefPubMedGoogle Scholar
  87. Maida R, Krieger J, Gebauer T, Lange U, Ziegelberger G (2000) Three pheromone-binding proteins in olfactory sensilla of the two silkmoth species Antheraea polyphemus and Antheraea pernyi. Eur J Biochem 267:2899–2908CrossRefPubMedGoogle Scholar
  88. Maida R, Ziegelberger G, Kaissling KE (2003) Ligand binding to six recombinant pheromone-binding proteins of Antheraea polyphemus and Antheraea pernyi. J Comp Physiol B 173:565–573CrossRefPubMedGoogle Scholar
  89. Mitchell C, Brennan RM, Graham J, Karley AJ (2016) Plant defense against herbivorous pests: exploiting resistance and tolerance traints for sustainable crop protection. Front Plant Sci 7:1132CrossRefPubMedPubMedCentralGoogle Scholar
  90. Mohanty S, Zubkov S, Gronenborn AM (2004) The solution NMR of Antheraea polyphemus PBP provides new insight into pheromone recognition by pheromone-binding Proteins. J Mol Biol 337:443–451CrossRefPubMedGoogle Scholar
  91. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19:284–292CrossRefPubMedPubMedCentralGoogle Scholar
  92. Nakagawa T, Pellegrino M, Sato K, Vosshall LB, Touhara K (2012) Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex. PLoS One 7:e32372CrossRefPubMedPubMedCentralGoogle Scholar
  93. Namiki S, Iwabuchi S, 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 194:501–515CrossRefGoogle Scholar
  94. Nardella J, Terrado M, Honson NS, Plettner E (2015) Endogenous fatty acids in olfactory hairs influence pheromone binding protein structure and function in Lymantria dispar. Arch Biochem Biophys 579:73–84CrossRefPubMedGoogle Scholar
  95. Nesbitt BF, Beevor PS, Hall DR, Lester R, Dyck VA (1975) Identification of female sex phermones of moth, Chilo suppresalis. J Insect Physiol 21:1883–1886CrossRefGoogle Scholar
  96. Nesbitt BF, Beevor PS, Hall DR, Lester R (1979) Female sex pheromone components of the cotton bollworm, Heliothis armigera. J Insect Physiol 25:535–541CrossRefGoogle Scholar
  97. Neuhaus EM, Gisselmann G, Zhang W, Dooley R, Stortkuhl K, Hatt H (2005) Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 8:15–17CrossRefGoogle Scholar
  98. Ochieng SA, Park KC, Baker TC (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J Comp Physiol A 188:325–333CrossRefGoogle Scholar
  99. Opler P (1994) Peterson first guide to butterflies and moths. Houghton Mifflin Harcourt, Boston, p 123Google Scholar
  100. Paduraru PM, Nair R, Popoff RTW, Gries R, Gries G, Plettner E (2008) Synthesis of substituted alkoxy benzene minilibraries, for the discovery of new insect olfaction of gustation inhibitors. J Comb Chem 10:123–134CrossRefPubMedGoogle Scholar
  101. Picimbon JF (2003) Evolution and biochemistry of OBP and CSP proteins. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology-the biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, SanDiego/London, pp 385–431Google Scholar
  102. Picimbon JF, Gadenne C (2002) Evolution of noctuid Pheromone Binding Proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochem Mol Biol 32:839–846CrossRefPubMedGoogle Scholar
  103. Picimbon JF, Gadenne C, Bécard JM, Clément JL, Sreng L (1997) Sex pheromone of the French black cutworm moth, Agrotis ipsilon (Lepidoptera: Noctuidae): identication and regulation of a multicomponent blend. J Chem Ecol 23:211–230CrossRefGoogle Scholar
  104. Plettner E (2002) Insect pheromone olfaction: new targets for the design of species-selective pest control agents. Curr Med Chem 9:1075–1085CrossRefPubMedGoogle Scholar
  105. Plettner E, Gries R (2010) Agonists and antagonists of antennal responses of gypsy moth (Lymantria dispar) to the pheromone (+)-disparlure and other odorants. J Agric Food Chem 58:3708–3719CrossRefPubMedGoogle Scholar
  106. Plettner E, Lazar J, Prestwich EG, Prestwich GD (2000) Discrimination of pheromone enantiomers by two Pheromone Binding Proteins from the gypsy moth Lymantria dispar. Biochemistry 39:8953–8962CrossRefPubMedGoogle Scholar
  107. Poivet E, Rharrabe K, Monsempes C, Glaser N, Rochat D, Renou M, Marion-Poll F, Jacquin-Joly E (2012) The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars. Nat Commun 3:1047CrossRefPubMedGoogle Scholar
  108. Pophof B (2002) Moth pheromone binding proteins contribute to the excitation of olfactory receptor cells. Naturwissenschaften 89:515–518CrossRefPubMedGoogle Scholar
  109. Pophof B (2004) Pheromone-binding proteins contribute to the activation of olfactory receptor neurons in the silkmoths Antheraea poyphemus and Bombyx mori. Chem Senses 29:117–125CrossRefPubMedGoogle Scholar
  110. Pregitzer P, Greschista M, Breer H, Krieger J (2014) The sensory neuron membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Mol Biol 23:733–742CrossRefPubMedGoogle Scholar
  111. Raina AK, Kingan TG, Mattoo AK (1992) Chemical signals from host plant and sexual behavior in a moth. Science 255:592–594CrossRefPubMedGoogle Scholar
  112. Rajapakse CNK, Walter GH, Moore CJ, Hull CD, Cribb BW (2006) Host recognition by a polyphagous lepidopteran (Helicoverpa armigera): primary host plants, host produced bolatiles and neurosensory stimulation. Physiol Entomol 31:270–277CrossRefGoogle Scholar
  113. Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261CrossRefPubMedPubMedCentralGoogle Scholar
  114. Reimer S, Van Klei C, Yu Y, Plettner E, Weinberg N (2011) Partition coefficients of disparlure at hydrophobic/aqueous interfaces: a comparative experimental and theoretical study. Can J Chem 89:568–572CrossRefGoogle Scholar
  115. Roelofs WL, Hill AS, Linn CE, Meinwald J, Jain SC, Herbert HJ, Smith RF (1982) Sex pheromone of the winter moth, a geometrid with unusually low-temperature pre-copulatory responses. Science 217:657–659CrossRefPubMedGoogle Scholar
  116. Rogers ME, Sun M, Lerner MR, Vogt RG (1997) Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the family of membrane proteins. J Biol Chem 272:14792–14799CrossRefPubMedGoogle Scholar
  117. Røstelien T, Stranden M, Borg-Karlson AK, 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 30:443–461CrossRefPubMedGoogle Scholar
  118. Ryan MF (2002) The chemoreceptive organs: structural aspects. In: Ryan MF (ed) Insect chemoreception: fundamental and applied. Springer, Dordrecht, pp 113–139Google Scholar
  119. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101:16653–16658CrossRefPubMedPubMedCentralGoogle Scholar
  120. Sakurai T, Mitsuno H, Mikami A, Uchino K, Tabuchi M, Zhang F, Sezutsu H, Kanzaki R (2015) Targeted disruption of a single sex pheromone receptor gene completely abolishes in vivo pheromone response in the silkmoth. Sci Rep 5:11001CrossRefPubMedPubMedCentralGoogle Scholar
  121. Sandler BH, Nikonova L, Leal WS, Clardy J (2000) Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem Biol 7:143–151CrossRefPubMedGoogle Scholar
  122. Sanes J, Hildebrand JG (1976) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51:282–299CrossRefGoogle Scholar
  123. Sanes JT, Plettner E (2016) Gypsy moth pheromone-binding protein-ligand interactions: pH profiles and simulations as tools for detecting polar interactions. Arch Biochem Biophys 606:53–63CrossRefPubMedGoogle Scholar
  124. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1007CrossRefPubMedGoogle Scholar
  125. Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122CrossRefGoogle Scholar
  126. Schneider D (1969) Insect olfaction: deciphering system for chemical messages. Science 163:1031–1037CrossRefPubMedGoogle Scholar
  127. Silbering AF, Benton R (2010) Ionotropic and metabotropic mechanisms in chemoreception: ‘chance or design’? EMBO Rep 11:173–179CrossRefPubMedPubMedCentralGoogle Scholar
  128. Solari P, Cerboneschi A, Masala C, Crnjar R, Liscia A (2002) Chemoreception in larvae of the moth Lymantria dispar. Ital J Zool 69:305–312CrossRefGoogle Scholar
  129. Song YQ, Sun HZ, Wu JX (2014) Morphology of the sensilla of larval antennae and mouthparts of the oriental fruit moth, Grapholita molesta. B Insectol 67:193–198Google Scholar
  130. Starratt AN, Dahm KH, Allen N, Hildebrand JG, Payne TL, Roller H (1979) Bombykal, a sex pheromone of the sphinx moth, Manduca sexta. Z Naturforsch 34:9–12CrossRefGoogle Scholar
  131. Steinbrecht RA (1996) Structure and function of insect olfactory sensilla. CIBA Found Symp 200:158–177PubMedGoogle Scholar
  132. Steinbrecht RA, Laue M, Ziegelberger G (1995) Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res 282:203–217CrossRefGoogle Scholar
  133. Steinwender B, Thrimawithana AH, Crowhurst R, Newcomb RD (2016) Odorant receptors of the New Zealand endemic leafroller moth species Planotortrix octo and P. excessana. PLoS One 11:e0152147CrossRefPubMedPubMedCentralGoogle Scholar
  134. Stengl M, Funk NW (2013) The role of the coreceptor Orco in insect olfactory transduction. J Comp Physiol A 199:897–909CrossRefGoogle Scholar
  135. Sugie H, Tamaki Y, Sato R, Kumakura M (1984) Sex pheromone of the peach leafminer moth, Lyonetia clerkella: isolation and identification. Appl Entomol Zool 19:323–330CrossRefGoogle Scholar
  136. Sun M, Liu Y, Walker WB, Liu C, Lin K, Gu S, Zhang Y, Zhou J, Wang G (2013) Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth, Plutella xyllostella. PLoS One 8:e62098CrossRefPubMedPubMedCentralGoogle Scholar
  137. Tamaki Y, Kawasaki K, Yamada H, Koshihara T, Osaki N, Ando T, Yoshida S, Kakinohana H (1977) Z-ll-hexadecenal and Z-l 1-hexadecenayl acetate: sex pheromone components of the diamondback moth (Lepidoptera: Plutellidae). Appl Entomol Zool 12:208–210CrossRefGoogle Scholar
  138. Tang QB, Hong ZZ, Cao H, Yan FM, Zhao XC (2015) Characteristics of morphology, electrophysiology, and central projections of two sensilla styloconica in Helicoverpa assulta larvae. Neuroreport 26:703–711CrossRefPubMedGoogle Scholar
  139. Tatsuki S, Kurihara M, Usui K, Ohguchi Y, Uchiumi K, Fukami J, Arai K, Yabuki S, Tanaka F (1983) Sex-pheromone of the rice stem borer Chilo suppressalis (Walker) (Lepidoptera: Pyralidae), the 3rd component. Z-9-hex-adecenal. Appl Entomol Zool 18:443–446CrossRefGoogle Scholar
  140. Terrado M, Yu Y, Plettner E (2018) Correlation of pheromone-binding protein-ligand equilibrium dissociation constants with electroantennogram response patterns. Can J Chem 96:168–177CrossRefGoogle Scholar
  141. Tian Z, Liu J, Zhang Y (2016) Structural insights into Cydia pomonella pheromone binding protein 2 mediated prediction of potentiallly active semiochemicals. Sci Rep 6:22336CrossRefPubMedPubMedCentralGoogle Scholar
  142. Toth M, Buser HR, Pena A, Arn H, Mori K, Takeuchi T, Nikolaeve LN, Kovalev BG (1989) Identification of (3Z,6Z)-1,3,6-9,10-epoxyhenicosatriene and (3Z,6Z)-1,3,6- 9,10-epoxycosatriene in the sex pheromone of Hyphantria cunea. Tetrahedron Lett 30:3405–3408CrossRefGoogle Scholar
  143. Tumlinson JH, Hendricks PE, Mitchell ER, Doolittle RE, Brennan MM (1975) Isolation, identification and synthesis of the sex pheromone of the tobacco budworm. J Chem Ecol 1:203–214CrossRefGoogle Scholar
  144. Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos BE, Baumhover AH, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10:255–271CrossRefGoogle Scholar
  145. Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163CrossRefGoogle Scholar
  146. Vogt RG, Köhne AC, Dubnau JT, Prestwich GD (1989) Expression of pheromone binding proteins during antennal development in the gypsy moth Lymantria dispar. J Neurosci 9:3332–3346CrossRefPubMedGoogle Scholar
  147. Vogt RG, Rybczynski R, Lerner MR (1991) Molecular cloning and sequencing of General Odorant Binding Protein GOBP1 and GOBP2 from tobacco hawk moth, Manduca sexta: comparisons with other insect OBPs and their signal peptides. J Neurosci 11:2972–2984CrossRefPubMedGoogle Scholar
  148. Vogt RG, Rogers ME, Franco MD, Sun M (2002) A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J Exp Biol 205:719–744PubMedGoogle Scholar
  149. Vogt RG, Große-Wilde E, Zhou JJ (2015) The lepidoptera odorant binding protein gene family: gene and loss within the GOBP/PBP complex of moths and butterflies. Insect Biochem Mol Biol 62:142–153Google Scholar
  150. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736CrossRefGoogle Scholar
  151. Wakamura S, Arakaki N, Yamamoto M, Hiradate S, Yasui H, Yasuda T, Ando T (2001) Posticlure: a novel trans-epoxide as a sex pheromone component of the tussock moth, Orgyia postica (Walker). Tetrahedron Lett 42:687–689CrossRefGoogle Scholar
  152. Wang HL, Svensson GP, Jakobsson J, Jirle EV, Rosenberg O, Francke W, Anderbrant O, Millar JG, Löfstedt C (2014) Sex pheromone of the cloaked pug moth, Eupithecia abietaria (Lepidoptera: Geometridae), a pest of spruce cones. J Appl Entomol 139:352–360CrossRefGoogle Scholar
  153. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1012CrossRefGoogle Scholar
  154. Xu X, Xu W, Rayo J, Ishida Y, Leal WS, Ames JB (2010) NMR structure of navel orangeworm moth pheromone-binding protein (AtraPBP1): implications for pH-sensitive pheromone detection. Biochemistry 49:1469–1476CrossRefPubMedPubMedCentralGoogle Scholar
  155. Xuan N, Bu X, Liu YY, Yang X, Liu GX, Fan ZX, Bi YP, Yang LQ, Lou QN, Rajashekar B, Leppik G, Kasvandik S, Picimbon JF (2014) Molecular evidence of RNA editing in Bombyx chemosensory protein family. PLoS One 9:e86932CrossRefPubMedPubMedCentralGoogle Scholar
  156. Xuan N, Rajashekar B, Kasvandik S, Picimbon JF (2016) Structural components of chemosensory protein mutations in the silkworm moth, Bombyx mori. Agri Gene 2:53–58CrossRefGoogle Scholar
  157. Yamamoto M, Kamata T, Do ND, Adachi Y, Kinjo M, Ando T (2007) A novel lepidopteran sex pheromone produced by females of a Lithosiinae species, Lyclene dharma dharma, in the family of Arctiidae. Biosci Biotechnol Biochem 71:2860–2863CrossRefPubMedGoogle Scholar
  158. Yang B, Ozaki K, Ishikawa Y, Matsuo T (2015) Identification of candidate odorant receptors in Asian corn borer Ostrinia furnacalis. PLoS One 10:e0121261CrossRefPubMedPubMedCentralGoogle Scholar
  159. Yu Y, Plettner E (2013) Enantiomer and conformer recognition of (+) and (−)-disparlure and their analogs by the pheromone binding proteins of the gypsy moth, Lymantria dispar. Bioorg Med Chem 21:1811–1822CrossRefPubMedGoogle Scholar
  160. Yu Y, Ma F, Cao Y, Zhang J, Zhang Y, Duan S, Wei Y, Zhu S, Chen N (2012) Structural and functional difference of pheromone binding proteins in discriminating chemicals in the gypsy moth, Lymantria dispar. Int J Biol Sci 8:979–991CrossRefPubMedPubMedCentralGoogle Scholar
  161. Zhang J, Liu CC, Yan SW, Liu Y, Guo MB, Dong SL, Wang GR (2013) An odorant receptor from the common cutworm (Spodoptera litura) exlusively tuned to the important plant volatile cis-3-Hexenyl acetate. Insect Mol Biol 22:424–432CrossRefPubMedGoogle Scholar
  162. Zhang JP, Salcedo C, Fang YL, Zhang RJ, Zhang ZN (2012) An overlooked component: (Z)-9-tetradecenal as a sex pheromone in Helicoverpa armigera. J Insect Physiol 58:1209–1216CrossRefPubMedGoogle Scholar
  163. Zhang YN, Zhang J, Yan SW, Chang HT, Liu Y, Wang GR, Dong SL (2014) Functional characterization of sex pheromone receptors in the purple stem borer, Sesamia inferens (Walker). Insect Mol Biol 23:611–620CrossRefPubMedGoogle Scholar
  164. Zhang J, Liu Y, Walker WB, Dong SL, Wang GR (2015) Identification and localization of two sensory neuron membrane proteins from Spodoptera litura. Insect Sci 22:399–408CrossRefPubMedGoogle Scholar
  165. Zhang D, Wang H, Schultze A, Froß H, Francke W, Krieger J, Löfstedt C (2016) Receptor for detection of a type II sex pheromone in the winter moth Operophtera brumata. Sci Rep 6:18576CrossRefPubMedPubMedCentralGoogle Scholar
  166. Zhou J, Zhang N, Wang P, Zhang S, Li D, Liu K, Wang G, Wang X, Ai H (2015) Identification of host-plant volatiles and characterization of two novel general odorant-binding proteins from the legume pod borer, Maruca vitrata Fabricius (Lepidoptera: Crambidae). PLoS One 10:e0141208CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mailyn Terrado
    • 1
  • Govardhana R. Pinnelli
    • 1
  • Jürgen Sanes
    • 1
  • Erika Plettner
    • 1
    Email author
  1. 1.Department of ChemistrySimon Fraser UniversityBurnabyCanada

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