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Access to the odor world: olfactory receptors and their role for signal transduction in insects

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Abstract

The sense of smell enables insects to recognize and discriminate a broad range of volatile chemicals in their environment originating from prey, host plants and conspecifics. These olfactory cues are received by olfactory sensory neurons (OSNs) that relay information about food sources, oviposition sites and mates to the brain and thus elicit distinct odor-evoked behaviors. Research over the last decades has greatly advanced our knowledge concerning the molecular basis underlying the reception of odorous compounds and the mechanisms of signal transduction in OSNs. The emerging picture clearly indicates that OSNs of insects recognize odorants and pheromones by means of ligand-binding membrane proteins encoded by large and diverse families of receptor genes. In contrast, the mechanisms of the chemo-electrical transduction process are not fully understood; the present status suggests a contribution of ionotropic as well as metabotropic mechanisms. In this review, we will summarize current knowledge on the peripheral mechanisms of odor sensing in insects focusing on olfactory receptors and their specific role in the recognition and transduction of odorant and pheromone signals by OSNs.

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References

  1. Gadenne C, Barrozo RB, Anton S (2016) Plasticity in insect olfaction: to smell or not to smell? Ann Rev Entomol 61:317–333. doi:10.1146/annurev-ento-010715-023523

    Article  CAS  Google Scholar 

  2. Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72(5):698–711. doi:10.1016/j.neuron.2011.11.003

    Article  CAS  PubMed  Google Scholar 

  3. Schneider D (1969) Insect olfaction: deciphering system for chemical messages. Science 163(3871):1031–1037. doi:10.1126/science.163.3871.1031

    Article  CAS  PubMed  Google Scholar 

  4. Wyatt TD (2014) Pheromones and animal behavior. Cambridge Univ Press, Cambridge

    Google Scholar 

  5. Schneider D (1992) 100 Years of pheromone research—an essay on lepidoptera. Naturwissenschaften 79(6):241–250. doi:10.1007/Bf01175388

    Article  CAS  Google Scholar 

  6. Bentley MD, Day JF (1989) Chemical ecology and behavioral aspects of mosquito oviposition. Ann Rev Entomol 34:401–421. doi:10.1146/annurev.en.34.010189.002153

    Article  CAS  Google Scholar 

  7. Steinbrecht RA (1997) Pore structures in insect olfactory sensilla: a review of data and concepts. Int J Insect Morphol Embryol 26(3–4):229–245. doi:10.1016/S0020-7322(97)00024-X

    Article  Google Scholar 

  8. Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391. doi:10.1146/annurev-ento-120811-153635

    Article  CAS  PubMed  Google Scholar 

  9. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. In: Blomquist G, Vogt RG (eds) Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, London, pp 391–445

    Chapter  Google Scholar 

  10. de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19(11):4520–4532

    PubMed  Google Scholar 

  11. Stensmyr MC, Giordano E, Balloi A, Angioy AM, Hansson BS (2003) Novel natural ligands for Drosophila olfactory receptor neurones. J Exp Biol 206(Pt 4):715–724. doi:10.1242/jeb.00143

    Article  CAS  PubMed  Google Scholar 

  12. 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(3):e32372. doi:10.1371/journal.pone.0032372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19(5):163–171. doi:10.1016/S0166-2236(96)10024-2

    Article  CAS  PubMed  Google Scholar 

  14. Bohbot J, Pitts RJ (2015) The narrowing olfactory landscape of insect odorant receptors. Front Ecol Evol. doi:10.3389/fevo.2015.00039

    Google Scholar 

  15. Suh E, Bohbot J, Zwiebel LJ (2014) Peripheral olfactory signaling in insects. Curr Opin Insect Sci 6:86–92. doi:10.1016/j.cois.2014.10.006

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wicher D (2015) Olfactory signaling in insects. Prog Mol Biol Transl Sci 130:37–54. doi:10.1016/bs.pmbts.2014.11.002

    Article  PubMed  Google Scholar 

  17. 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(2):327–338. doi:10.1016/S0896-6273(00)81093-4

    Article  CAS  PubMed  Google Scholar 

  18. Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60(1):31–39. doi:10.1006/geno.1999.5894

    Article  CAS  PubMed  Google Scholar 

  19. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4(2):e20. doi:10.1371/journal.pbio.0040020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38(8):770–780. doi:10.1016/j.ibmb.2008.05.002

    Article  CAS  PubMed  Google Scholar 

  21. Lundin C, Kall L, Kreher SA, Kapp K, Sonnhammer EL, Carlson JR, Heijne G, Nilsson I (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581(29):5601–5604. doi:10.1016/j.febslet.2007.11.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Missbach C, Dweck HK, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E (2014) Evolution of insect olfactory receptors. Elife 3:e02115. doi:10.7554/eLife.02115

    PubMed  PubMed Central  Google Scholar 

  23. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100:14537–14542. doi:10.1073/pnas.2335847100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452(7190):1002–1006. doi:10.1038/nature06850

    Article  CAS  PubMed  Google Scholar 

  25. 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(7190):1007–1011. doi:10.1038/nature06861

    Article  CAS  PubMed  Google Scholar 

  26. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725–736. doi:10.1016/S0092-8674(00)80582-6

    Article  CAS  PubMed  Google Scholar 

  27. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117(7):965–979. doi:10.1016/j.cell.2004.05.012

    Article  CAS  PubMed  Google Scholar 

  28. Bushdid C, Magnasco MO, Vosshall LB, Keller A (2014) Humans can discriminate more than 1 trillion olfactory stimuli. Science 343:1370–1372. doi:10.1126/science.1249168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Touhara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71:307–332. doi:10.1146/annurev.physiol.010908.163209

    Article  CAS  PubMed  Google Scholar 

  30. Andersson MN, Löfstedt C, Newcomb RD (2015) Insect olfaction and the evolution of receptor tuning. Front Ecol Evol 3(53):1–14. doi:10.3389/fevo.2015.00053

    Google Scholar 

  31. Stensmyr MC, Dweck HK, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, Wicher D, Sachse S, Knaden M, Becher PG, Seki Y, Hansson BS (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151(6):1345–1357. doi:10.1016/j.cell.2012.09.046

    Article  CAS  PubMed  Google Scholar 

  32. Dweck HK, Ebrahim SA, Kromann S, Bown D, Hillbur Y, Sachse S, Hansson BS, Stensmyr MC (2013) Olfactory preference for egg laying on citrus substrates in Drosophila. Curr Biol 23(24):2472–2480. doi:10.1016/j.cub.2013.10.047

    Article  CAS  PubMed  Google Scholar 

  33. Berg BG, Zhao XC, Wang G (2014) Processing of pheromone information in related species of heliothine moths. Insects 5(4):742–761. doi:10.3390/insects5040742

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zhang J, Walker WB, Wang G (2015) Pheromone reception in moths: from molecules to behaviors. Prog Mol Biol Transl Sci 130:109–128. doi:10.1016/bs.pmbts.2014.11.005

    Article  PubMed  Google Scholar 

  35. Kohl J, Huoviala P, Jefferis GS (2015) Pheromone processing in Drosophila. Curr Opin Neurobiol 34:149–157. doi:10.1016/j.conb.2015.06.009

    Article  CAS  PubMed  Google Scholar 

  36. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450(7167):289–293. doi:10.1038/nature06328

    Article  CAS  PubMed  Google Scholar 

  37. 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 7:11866. doi:10.1038/ncomms11866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Jacquin-Joly E, Merlin C (2004) Insect olfactory receptors: contributions of molecular biology to chemical ecology. J Chem Ecol 30(12):2359–2397. doi:10.1007/s10886-004-7941-3

    Article  CAS  PubMed  Google Scholar 

  39. Wang G, Carey AF, Carlson JR, Zwiebel LJ (2010) Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci USA 107(9):4418–4423. doi:10.1073/pnas.0913392107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Montagne N, de Fouchier A, Newcomb RD, Jacquin-Joly E (2015) Advances in the identification and characterization of olfactory receptors in insects. Prog Mol Biol Transl Sci 130:55–80. doi:10.1016/bs.pmbts.2014.11.003

    Article  PubMed  Google Scholar 

  41. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136(1):149–162. doi:10.1016/j.cell.2008.12.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rytz R, Croset V, Benton R (2013) Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol 43(9):888–897. doi:10.1016/j.ibmb.2013.02.007

    Article  CAS  PubMed  Google Scholar 

  43. Olivier V, Monsempes C, Francois MC, Poivet E, Jacquin-Joly E (2011) Candidate chemosensory ionotropic receptors in a Lepidoptera. Insect Mol Biol 20(2):189–199. doi:10.1111/j.1365-2583.2010.01057.x

    Article  CAS  PubMed  Google Scholar 

  44. Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA 104(9):3574–3578. doi:10.1073/pnas.0700079104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Robertson HM, Kent LB (2009) Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J Insect Sci 9:19. doi:10.1673/031.009.1901

    PubMed  PubMed Central  Google Scholar 

  46. Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon HW, Pitts RJ, van Loon JJ, Takken W, Carlson JR, Zwiebel LJ (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol 17(18):1533–1544. doi:10.1016/j.cub.2007.07.062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65(1):175–187. doi:10.1016/0092-8674(91)90418-X

    Article  CAS  PubMed  Google Scholar 

  48. Ben-Arie N, Lancet D, Taylor C, Khen M, Walker N, Ledbetter DH, Carrozzo R, Patel K, Sheer D, Lehrach H et al (1994) Olfactory receptor gene cluster on human chromosome 17: possible duplication of an ancestral receptor repertoire. Hum Mol Genet 3(2):229–235. doi:10.1093/hmg/3.2.229

    Article  CAS  PubMed  Google Scholar 

  49. Ngai J, Dowling MM, Buck L, Axel R, Chess A (1993) The family of genes encoding odorant receptors in the channel catfish. Cell 72(5):657–666. doi:10.1016/0092-8674(93)90395-7

    Article  CAS  PubMed  Google Scholar 

  50. Nef S, Allaman I, Fiumelli H, De Castro E, Nef P (1996) Olfaction in birds: differential embryonic expression of nine putative odorant receptor genes in the avian olfactory system. Mech Dev 55(1):65–77. doi:10.1016/0925-4773(95)00491-2

    Article  CAS  PubMed  Google Scholar 

  51. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83(2):207–218. doi:10.1016/0092-8674(95)90162-0

    Article  CAS  PubMed  Google Scholar 

  52. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Siden-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, WoodageT Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287(5461):2185–2195. doi:10.1126/science.287.5461.2185

    Article  PubMed  Google Scholar 

  53. Vosshall LB (2001) The molecular logic of olfaction in Drosophila. Chem Senses 26(2):207–213. doi:10.1093/chemse/26.2.207

    Article  CAS  PubMed  Google Scholar 

  54. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125(1):143–160. doi:10.1016/j.cell.2006.01.050

    Article  CAS  PubMed  Google Scholar 

  55. Kim J, Moriyama EN, Warr CG, Clyne PJ, Carlson JR (2000) Identification of novel multi-transmembrane proteins from genomic databases using quasi-periodic structural properties. Bioinformatics 16(9):767–775. doi:10.1093/bioinformatics/16.9.767

    Article  CAS  PubMed  Google Scholar 

  56. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ (2001) Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc Natl Acad Sci USA 98(25):14693–14697. doi:10.1073/pnas.261432998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002) G protein-coupled receptors in Anopheles gambiae. Science 298(5591):176–178. doi:10.1126/science.1076196

    Article  CAS  PubMed  Google Scholar 

  58. 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(5):703–714. doi:10.1016/j.neuron.2004.08.019

    Article  CAS  PubMed  Google Scholar 

  59. Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36(6):497–498. doi:10.1093/chemse/bjr022

    Article  PubMed  Google Scholar 

  60. Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189(7):519–526. doi:10.1007/s00359-003-0427-x

    Article  CAS  PubMed  Google Scholar 

  61. Jones WD, Nguyen TAT, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol 15(4):R119–R121. doi:10.1016/j.cub.2005.02.007

    Article  CAS  PubMed  Google Scholar 

  62. Pitts RJ, Fox AN, Zwiebel LJ (2004) A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 101(14):5058–5063. doi:10.1073/pnas.0308146101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Yang Y, Krieger J, Zhang L, Breer H (2012) The olfactory co-receptor Orco from the migratory locust (Locusta migratoria) and the desert locust (Schistocerca gregaria): identification and expression pattern. Int J Biol Sci 8(2):159–170. doi:10.7150/ijbs.8.159

    Article  CAS  PubMed  Google Scholar 

  64. Smadja C, Shi P, Butlin RK, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid. Acyrthosiphon pisum. Mol Biol Evol 26(9):2073–2086. doi:10.1093/molbev/msp116

    Article  CAS  PubMed  Google Scholar 

  65. Pask GM, Jones PL, Rutzler M, Rinker DC, Zwiebel LJ (2011) Heteromeric anopheline odorant receptors exhibit distinct channel properties. PLoS ONE 6(12):e28774. doi:10.1371/journal.pone.0028774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Neuhaus EM, Gisselmann G, Zhang WY, Dooley R, Stortkuhl K, Hatt H (2005) Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 8(1):15–17. doi:10.1038/nn1371

    Article  CAS  PubMed  Google Scholar 

  67. Zhou X, Slone JD, Rokas A, Berger SL, Liebig J, Ray A, Reinberg D, Zwiebel LJ (2012) Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet 8(8):e1002930. doi:10.1371/journal.pgen.1002930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Nozawa M, Nei M (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104(17):7122–7127. doi:10.1073/pnas.0702133104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubio JM, Ribeiro JM, Rozas J, Johnston JS, Reese JT, Popadic A, Tojo M, Raoult D, Reed DL, Tomoyasu Y, Kraus E, Mittapalli O, Margam VM, Li HM, Meyer JM, Johnson RM, Romero-Severson J, Vanzee JP, Alvarez-Ponce D, Vieira FG, Aguade M, Guirao-Rico S, Anzola JM, Yoon KS, Strycharz JP, Unger MF, Christley S, Lobo NF, Seufferheld MJ, Wang N, Dasch GA, Struchiner CJ, Madey G, Hannick LI, Bidwell S, Joardar V, Caler E, Shao R, Barker SC, Cameron S, Bruggner RV, Regier A, Johnson J, Viswanathan L, Utterback TR, Sutton GG, Lawson D, Waterhouse RM, Venter JC, Strausberg RL, Berenbaum MR, Collins FH, Zdobnov EM, Pittendrigh BR (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107(27):12168–12173. doi:10.1073/pnas.1003379107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Koenig C, Hirsh A, Bucks S, Klinner C, Vogel H, Shukla A, Mansfield JH, Morton B, Hansson BS, Grosse-Wilde E (2015) A reference gene set for chemosensory receptor genes of Manduca sexta. Insect Biochem Mol Biol 66:51–63. doi:10.1016/j.ibmb.2015.09.007

    Article  CAS  PubMed  Google Scholar 

  71. de Fouchier A, Walker WB 3rd, Montagne N, Steiner C, Binyameen M, Schlyter F, Chertemps T, Maria A, Francois MC, Monsempes C, Anderson P, Hansson BS, Larsson MC, Jacquin-Joly E (2017) Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nat Commun 8:15709. doi:10.1038/ncomms15709

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16(11):1395–1403. doi:10.1101/gr.5057506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Engsontia P, Sanderson AP, Cobb M, Walden KK, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38(4):387–397. doi:10.1016/j.ibmb.2007.10.005

    Article  CAS  PubMed  Google Scholar 

  74. Dippel S, Kollmann M, Oberhofer G, Montino A, Knoll C, Krala M, Rexer KH, Frank S, Kumpf R, Schachtner J, Wimmer EA (2016) Morphological and transcriptomic analysis of a beetle chemosensory system reveals a gnathal olfactory center. BMC Biol 14(1):90. doi:10.1186/s12915-016-0304-z

    Article  PubMed  PubMed Central  Google Scholar 

  75. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6(8):e1001064. doi:10.1371/journal.pgen.1001064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Penalva-Arana DC, Lynch M, Robertson HM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evol Biol 9:79. doi:10.1186/1471-2148-9-79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Evans JD, Brown SJ, Hackett KJ, Robinson G, Richards S, Lawson D, Elsik C, Coddington J, Edwards O, Emrich S, Gabaldon T, Goldsmith M, Hanes G, Misof B, Munoz-Torres M, Niehuis O, Papanicolaou A, Pfrender M, Poelchau M, Purcell-Miramontes M, Robertson HM, Ryder O, Tagu D, Torres T, Zdobnov E, Zhang GJ, Zhou X, Consortium iK (2013) The i5 K initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment i5 K CONSORTIUM. J Heredity 104(5):595–600. doi:10.1093/jhered/est050

    Article  Google Scholar 

  78. Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46(3):445–456. doi:10.1016/j.neuron.2005.04.007

    Article  CAS  PubMed  Google Scholar 

  79. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15(17):1535–1547. doi:10.1016/j.cub.2005.07.034

    Article  CAS  PubMed  Google Scholar 

  80. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102(2):147–159. doi:10.1016/S0092-8674(00)00021-0

    Article  CAS  PubMed  Google Scholar 

  81. Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19(11):881–890. doi:10.1016/j.cub.2009.04.035

    Article  CAS  PubMed  Google Scholar 

  82. Wanner KW, Anderson AR, Trowell SC, Theilmann DA, Robertson HM, Newcomb RD (2007) Female-biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori. Insect Mol Biol 16(1):107–119. doi:10.1111/j.1365-2583.2007.00708.x

    Article  CAS  PubMed  Google Scholar 

  83. Karner T, Schneider I, Schultze A, Breer H, Krieger J (2015) Co-expression of six tightly clustered odorant receptor genes in the antenna of the malaria mosquito. Front Ecol Evol 3(26):1–8. doi:10.3389/fevo.2015.00026

    Google Scholar 

  84. Schymura D, Forstner M, Schultze A, Krober T, Swevers L, Iatrou K, Krieger J (2010) Antennal expression pattern of two olfactory receptors and an odorant binding protein implicated in host odor detection by the malaria vector Anopheles gambiae. Int J Biol Sci 6(7):614–626. doi:10.7150/ijbs.6.614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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 5:11001. doi:10.1038/srep11001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307(5715):1638–1642. doi:10.1126/science.1106267

    Article  CAS  PubMed  Google Scholar 

  87. Krieger J, Grosse-Wilde E, Gohl T, Breer H (2005) Candidate pheromone receptors of the silkmoth Bombyx mori. Eur J Neurosci 21(8):2167–2176. doi:10.1111/j.1460-9568.2005.04058.x

    Article  PubMed  Google Scholar 

  88. 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 USA 101(32):11845–11850. doi:10.1073/pnas.0403052101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Grosse-Wilde E, Stieber R, Forstner M, Krieger J, Wicher D, Hansson BS (2010) Sex-specific odorant receptors of the tobacco hornworm manduca sexta. Front Cell Neurosci. doi:10.3389/fncel.2010.00022

    PubMed  PubMed Central  Google Scholar 

  90. 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(8):2364–2373. doi:10.1111/j.1460-9568.2007.05512.x

    Article  PubMed  Google Scholar 

  91. Patch HM, Velarde RA, Walden KK, Robertson HM (2009) A candidate pheromone receptor and two odorant receptors of the hawkmoth Manduca sexta. Chem Senses 34(4):305–316. doi:10.1093/chemse/bjp002

    Article  CAS  PubMed  Google Scholar 

  92. Miura N, Nakagawa T, Tatsuki S, Touhara K, Ishikawa Y (2009) A male-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int J Biol Sci 5(4):319–330. doi:10.7150/ijbs.5.319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Miura N, Nakagawa T, Touhara K, Ishikawa Y (2010) Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem Mol Biol 40(1):64–73. doi:10.1016/j.ibmb.2009.12.011

    Article  CAS  PubMed  Google Scholar 

  94. Bengtsson JM, Gonzalez F, Cattaneo AM, Montagne N, Walker WB, Bengtsson M, Anfora G, Ignell R, Jacquin-Joly E, Witzgall P (2014) A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester. Front Ecol Evol 2(33):1–11. doi:10.3399/fevo.2014.00033

    Google Scholar 

  95. Dobritsa AA, Naters VDGV, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37(5):827–841. doi:10.1016/S0896-6273(03)00094-1

    Article  CAS  PubMed  Google Scholar 

  96. Iatrou K, Biessmann H (2008) Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem Mol Biol 38(2):268–274. doi:10.1016/j.ibmb.2007.11.008

    Article  CAS  PubMed  Google Scholar 

  97. Bohbot J, Pitts RJ, Kwon HW, Rutzler M, Robertson HM, Zwiebel LJ (2007) Molecular characterization of the Aedes aegypti odorant receptor gene family. Insect Mol Biol 16(5):525–537. doi:10.1111/j.1365-2583.2007.00748.x

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Liu Y, Gu S, Zhang Y, Guo Y, Wang G (2012) Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS ONE 7(10):e48260. doi:10.1371/journal.pone.0048260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. An XK, Sun L, Liu HW, Liu DF, Ding YX, Li LM, Zhang YJ, Guo YY (2016) Identification and expression analysis of an olfactory receptor gene family in green plant bug Apolygus lucorum (Meyer-Dur). Sci Rep 6:37870. doi:10.1038/srep37870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. 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(3):e0152147. doi:10.1371/journal.pone.0152147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Rodriguez I (2013) Singular expression of olfactory receptor genes. Cell 155(2):274–277. doi:10.1016/j.cell.2013.09.032

    Article  CAS  PubMed  Google Scholar 

  102. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96(5):713–723. doi:10.1016/S0092-8674(00)80581-4

    Article  CAS  PubMed  Google Scholar 

  103. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78(5):823–834. doi:10.1016/S0092-8674(94)90562-2

    Article  CAS  PubMed  Google Scholar 

  104. Monahan K, Lomvardas S (2015) Monoallelic expression of olfactory receptors. Ann Rev Cell Develop Biol 31:721–740. doi:10.1146/annurev-cellbio-100814-125308

    Article  CAS  Google Scholar 

  105. Goldman AL, van Naters WV, Lessing D, Warr CG, Carlson JR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45(5):661–666. doi:10.1016/j.neuron.2005.01.025

    Article  CAS  PubMed  Google Scholar 

  106. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15(17):1548–1553. doi:10.1016/j.cub.2005.07.066

    Article  CAS  PubMed  Google Scholar 

  107. Ray A, van Naters WG, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53(3):353–369. doi:10.1016/j.neuron.2006.12.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Koutroumpa FA, Kárpáti Z, Monsempes C, Hill SR, Hansson BS, Jacquin-Joly E, Krieger J, Dekker T (2014) Shifts in sensory neuron identity parallel differences in pheromone preference in the European corn borer. Front Ecol Evol. doi:10.3389/fevo.2014.00065

    Google Scholar 

  109. Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464(7285):66–71. doi:10.1038/nature08834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Slone J, Daniels J, Amrein H (2007) Sugar receptors in Drosophila. Curr Biol 17(20):1809–1816. doi:10.1016/j.cub.2007.09.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Dahanukar A, Lei YT, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56(3):503–516. doi:10.1016/j.neuron.2007.10.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mathew D, Martelli C, Kelley-Swift E, Brusalis C, Gershow M, Samuel AD, Emonet T, Carlson JR (2013) Functional diversity among sensory receptors in a Drosophila olfactory circuit. Proc Natl Acad Sci USA 110(23):2134–2143. doi:10.1073/pnas.1306976110

    Article  Google Scholar 

  113. 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 USA 101(47):16653–16658. doi:10.1073/pnas.0407596101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 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(6):547–555. doi:10.1093/chemse/bjj059

    Article  CAS  PubMed  Google Scholar 

  115. Wang G, Vasquez GM, Schal C, Zwiebel LJ, Gould F (2011) Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol Biol 20(1):125–133. doi:10.1111/j.1365-2583.2010.01045.x

    Article  PubMed  CAS  Google Scholar 

  116. Wanner KW, Nichols AS, Allen JE, Bunger PL, Garczynski SF, Linn CE, Robertson HM, Luetje CW (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS ONE 5(1):e8685. doi:10.1371/journal.pone.0008685

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Montagne N, Chertemps T, Brigaud I, Francois A, Francois MC, de Fouchier A, Lucas P, Larsson MC, Jacquin-Joly E (2012) Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur J Neurosci 36(5):2588–2596. doi:10.1111/j.1460-9568.2012.08183.x

    Article  PubMed  Google Scholar 

  118. Cattaneo AM, Gonzalez F, Bengtsson JM, Corey EA, Jacquin-Joly E, Montagne N, Salvagnin U, Walker WB, Witzgall P, Anfora G, Bobkov YV (2017) Candidate pheromone receptors of codling moth Cydia pomonella respond to pheromones and kairomones. Sci Rep 7:41105. doi:10.1038/srep41105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Gonzalez F, Bengtsson JM, Walker WB, Sousa MFR, Cattaneo AM, Montagne N, de Fouchier A, Anfora G, Jacquin-Joly E, Witzgall P, Ignell R, Bengtsson M (2015) A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth. Front Ecol Evol 3(131):1–12. doi:10.3389/fevo.2015.00131

    Google Scholar 

  120. Wang B, Liu Y, He K, Wang G (2016) Comparison of research methods for functional characterization of insect olfactory receptors. Sci Rep 6:32806. doi:10.1038/srep32806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Gonzalez D, Witzgall P, Walker WB (2016) Protocol for heterologous expression of insect odourant receptors in Drosophila. Front Ecol Evol 4(24):1–5. doi:10.3389/fevo.2016.00024

    Google Scholar 

  122. 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(7):745–757. doi:10.7150/ijbs.5.745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Pregitzer P, Schubert M, Breer H, Hansson BS, Sachse S, Krieger J (2012) Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Front Cell Neurosci 6:42. doi:10.3389/fncel.2012.00042

    Article  PubMed  PubMed Central  Google Scholar 

  124. Bohbot JD, Jones PL, Wang G, Pitts RJ, Pask GM, Zwiebel LJ (2011) Conservation of indole responsive odorant receptors in mosquitoes reveals an ancient olfactory trait. Chem Senses 36(2):149–160. doi:10.1093/chemse/bjq105

    Article  CAS  PubMed  Google Scholar 

  125. Jones PL, Pask GM, Rinker DC, Zwiebel LJ (2011) Functional agonism of insect odorant receptor ion channels. Proc Natl Acad Sci USA 108(21):8821–8825. doi:10.1073/pnas.1102425108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Corcoran JA, Jordan MD, Carraher C, Newcomb RD (2014) A novel method to study insect olfactory receptor function using HEK293 cells. Insect Biochem Mol Biol 54:22–32. doi:10.1016/j.ibmb.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  127. Jordan MD, Anderson A, Begum D, Carraher C, Authier A, Marshall SD, 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(5):383–394. doi:10.1093/chemse/bjp010

    Article  CAS  PubMed  Google Scholar 

  128. Kiely A, Authier A, Kralicek AV, Warr CG, Newcomb RD (2007) Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J Neurosci Methods 159(2):189–194. doi:10.1016/j.jneumeth.2006.07.005

    Article  CAS  PubMed  Google Scholar 

  129. 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 Molec 39(3):189–197. doi:10.1016/j.ibmb.2008.11.002

    Article  CAS  Google Scholar 

  130. Claudianos C, Lim J, Young M, Yan SZ, Cristino AS, Newcomb RD, Gunasekaran N, Reinhard J (2014) Odor memories regulate olfactory receptor expression in the sensory periphery. Eur J Neurosci 39(10):1642–1654. doi:10.1111/ejn.12539

    Article  PubMed  Google Scholar 

  131. German PF, van der Poel S, Carraher C, Kralicek AV, Newcomb RD (2013) Insights into subunit interactions within the insect olfactory receptor complex using FRET. Insect Biochem Mol Biol 43(2):138–145. doi:10.1016/j.ibmb.2012.11.002

    Article  CAS  PubMed  Google Scholar 

  132. Tsitoura P, Andronopoulou E, Tsikou D, Agalou A, Papakonstantinou MP, Kotzia GA, Labropoulou V, Swevers L, Georgoussi Z, Iatrou K (2010) Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells. PLoS ONE. doi:10.1371/journal.pone.0015428

    Google Scholar 

  133. Zhang DD, Wang HL, Schultze A, Fross H, Francke W, Krieger J, Lofstedt C (2016) Receptor for detection of a Type II sex pheromone in the winter moth Operophtera brumata. Sci Rep 6:18576. doi:10.1038/srep18576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. 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(4):e62098. doi:10.1371/journal.pone.0062098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Zhang J, Yan S, Liu Y, Jacquin-Joly E, Dong S, Wang G (2015) Identification and functional characterization of sex pheromone receptors in the common cutworm (Spodoptera litura). Chem Senses 40(1):7–16. doi:10.1093/chemse/bju052

    Article  PubMed  CAS  Google Scholar 

  136. Liu F, Xiong C, Liu N (2017) Chemoreception to aggregation pheromones in the common bed bug, Cimex lectularius. Insect Biochem Mol Biol 82:62–73. doi:10.1016/j.ibmb.2017.01.012

    Article  CAS  PubMed  Google Scholar 

  137. 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 5:13093. doi:10.1038/srep13093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Papke RL, Stokes C (2010) Working with OpusXpress: methods for high volume oocyte experiments. Methods 51(1):121–133. doi:10.1016/j.ymeth.2010.01.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Schnizler K, Kuster M, Methfessel C, Fejtl M (2003) The roboocyte: automated cDNA/mRNA injection and subsequent TEVC recording on Xenopus oocytes in 96-well microtiter plates. Receptors Channels 9(1):41–48. doi:10.3109/10606820308253

    Article  CAS  PubMed  Google Scholar 

  140. Leisgen C, Kuester M, Methfessel C (2007) The roboocyte: automated electrophysiology based on Xenopus oocytes. Methods Mol Biol 403:87–109. doi:10.1007/978-1-59745-529-9_6

    Article  CAS  PubMed  Google Scholar 

  141. Chen S, Luetje CW (2012) Identification of new agonists and antagonists of the insect odorant receptor co-receptor subunit. PLoS ONE 7(5):e36784. doi:10.1371/journal.pone.0036784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Chen S, Luetje CW (2014) Trace amines inhibit insect odorant receptor function through antagonism of the co-receptor subunit. F1000Res 3:84. doi:10.12688/f1000research.3825.1

    PubMed  PubMed Central  Google Scholar 

  143. Pellegrino M, Nakagawa T, Vosshall LB (2010) Single sensillum recordings in the insects Drosophila melanogaster and Anopheles gambiae. J Vis Exp 36:1–5. doi:10.3791/1725

    Google Scholar 

  144. Hallem EA, Nicole FA, Zwiebel LJ, Carlson JR (2004) Olfaction: mosquito receptor for human-sweat odorant. Nature 427(6971):212–213. doi:10.1038/427212a

    Article  CAS  PubMed  Google Scholar 

  145. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446(7135):542–546. doi:10.1038/nature05672

    Article  CAS  PubMed  Google Scholar 

  146. Jin X, Ha TS, Smith DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci USA 105(31):10996–11001. doi:10.1073/pnas.0803309105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ronderos DS, Lin CC, Potter CJ, Smith DP (2014) Farnesol-detecting olfactory neurons in Drosophila. J Neurosci 34(11):3959–3968. doi:10.1523/JNEUROSCI.4582-13.2014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. You Y, Smith DP, Lv M, Zhang L (2016) A broadly tuned odorant receptor in neurons of trichoid sensilla in locust, Locusta migratoria. Insect Biochem Mol Biol 79:66–72. doi:10.1016/j.ibmb.2016.10.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, Jasinskiene N, James AA, Vosshall LB (2013) orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498(7455):487–491. doi:10.1038/nature12206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Yi X, Zhao H, Wang P, Hu M, Zhong G (2014) Bdor\Orco is important for oviposition-deterring behavior induced by both the volatile and non-volatile repellents in Bactrocera dorsalis (Diptera: Tephritidae). J Insect Physiol 65:51–56. doi:10.1016/j.jinsphys.2014.05.007

    Article  CAS  PubMed  Google Scholar 

  151. Zhou YL, Zhu XQ, Gu SH, Cui HH, Guo YY, Zhou JJ, Zhang YJ (2014) Silencing in Apolygus lucorum of the olfactory coreceptor Orco gene by RNA interference induces EAG response declining to two putative semiochemicals. J Insect Physiol 60:31–39. doi:10.1016/j.jinsphys.2013.10.006

    Article  CAS  PubMed  Google Scholar 

  152. Fan J, Zhang Y, Francis F, Cheng D, Sun J, Chen J (2015) Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae. Insect Biochem Mol Biol 64:16–24. doi:10.1016/j.ibmb.2015.07.006

    Article  CAS  PubMed  Google Scholar 

  153. 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(7):772–780. doi:10.7150/ijbs.11898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Franco TA, Oliveira DS, Moreira MF, Leal WS, Melo AC (2016) Silencing the odorant receptor co-receptor RproOrco affects the physiology and behavior of the Chagas disease vector Rhodnius prolixus. Insect Biochem Mol Biol 69:82–90. doi:10.1016/j.ibmb.2015.02.012

    Article  CAS  PubMed  Google Scholar 

  155. Koutroumpa FA, Monsempes C, Francois MC, de Cian A, Royer C, Concordet JP, Jacquin-Joly E (2016) Heritable genome editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Sci Rep 6:29620. doi:10.1038/srep29620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Li Y, Zhang J, Chen D, Yang P, Jiang F, Wang X, Kang L (2016) CRISPR/Cas9 in locusts: successful establishment of an olfactory deficiency line by targeting the mutagenesis of an odorant receptor co-receptor (Orco). Insect Biochem Mol Biol 79:27–35. doi:10.1016/j.ibmb.2016.10.003

    Article  CAS  PubMed  Google Scholar 

  157. Zhang R, Gao G, Chen H (2016) Silencing of the olfactory co-receptor gene in Dendroctonus armandi leads to EAG response declining to major host volatiles. Sci Rep 6:23136. doi:10.1038/srep23136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Liu Q, Liu W, Zeng B, Wang G, Hao D, Huang Y (2017) Deletion of the Bombyx mori odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms. Insect Biochem Mol Biol 86:58–67. doi:10.1016/j.ibmb.2017.05.007

    Article  CAS  PubMed  Google Scholar 

  159. Carey AF, Carlson JR (2011) Insect olfaction from model systems to disease control. Proc Natl Acad Sci USA 108(32):14849–14854. doi:10.1073/pnas.1103472108

    Article  PubMed  PubMed Central  Google Scholar 

  160. Almaas TJ, Mustaparta H (1991) Heliothis virescens: response characteristics of receptor neurons in sensilla trichodea type 1 and type 2. J Chem Ecol 17(5):953–972. doi:10.1007/BF01395602

    Article  CAS  PubMed  Google Scholar 

  161. Baker TC, Ochieng SA, Cosse AA, Lee SG, Todd JL, Quero C, Vickers NJ (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(2):155–165. doi:10.1007/s00359-003-0483-2

    Article  CAS  Google Scholar 

  162. Kaissling K-E, Kasang G, Bestmann HJ, Stransky W, Vostrowsky O (1978) A new pheromone of the silkworm moth Bombyx mori. Naturwissenschaften 65:382–384. doi:10.1007/BF00439702

    Article  CAS  Google Scholar 

  163. Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T (2008) Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur J Neurosci 28(5):893–902. doi:10.1111/j.1460-9568.2008.06429.x

    Article  PubMed  Google Scholar 

  164. Legeai F, Malpel S, Montagne N, Monsempes C, Cousserans F, Merlin C, Francois MC, Maibeche-Coisne M, Gavory F, Poulain J, Jacquin-Joly E (2011) 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 12:86. doi:10.1186/1471-2164-12-86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Bengtsson JM, Trona F, Montagne N, Anfora G, Ignell R, Witzgall P, Jacquin-Joly E (2012) Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS ONE 7(2):e31620. doi:10.1371/journal.pone.0031620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Engsontia P, Sangket U, Chotigeat W, Satasook C (2014) Molecular evolution of the odorant and gustatory receptor genes in lepidopteran insects: implications for their adaptation and speciation. J Mol Evol 79(1–2):21–39. doi:10.1007/s00239-014-9633-0

    Article  CAS  PubMed  Google Scholar 

  167. Steinwender B, Thrimawithana AH, Crowhurst RN, Newcomb RD (2015) Pheromone receptor evolution in the cryptic leafroller species, Ctenopseustis obliquana and C. herana. J Mol Evol 80(1):42–56. doi:10.1007/s00239-014-9650-z

    Article  CAS  PubMed  Google Scholar 

  168. Dong J, Song Y, Li W, Shi J, Wang Z (2016) Identification of putative chemosensory receptor genes from the Athetis dissimilis antennal transcriptome. PLoS ONE 11(1):e0147768. doi:10.1371/journal.pone.0147768

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  169. Yew JY, Chung H (2015) Insect pheromones: an overview of function, form, and discovery. Prog Lipid Res 59:88–105. doi:10.1016/j.plipres.2015.06.001

    Article  CAS  PubMed  Google Scholar 

  170. Wanner KW, Nichols AS, Walden KK, Brockmann A, Luetje CW, Robertson HM (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci USA 104(36):14383–14388. doi:10.1073/pnas.0705459104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463(7278):227–231. doi:10.1038/nature08678

    Article  CAS  PubMed  Google Scholar 

  172. Naters VDGV, Carlson JR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17(7):606–612. doi:10.1016/j.cub.2007.02.043

    Article  CAS  Google Scholar 

  173. Liu W, Liang X, Gong J, Yang Z, Zhang YH, Zhang JX, Rao Y (2011) Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 14(7):896–902. doi:10.1038/nn.2836

    Article  CAS  PubMed  Google Scholar 

  174. Ha TS, Smith DP (2006) A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 26(34):8727–8733. doi:10.1523/JNEUROSCI.0876-06.2006

    Article  CAS  PubMed  Google Scholar 

  175. Ejima A, Smith BP, Lucas C, Naters VDGV, Miller CJ, Carlson JR, Levine JD, Griffith LC (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17(7):599–605. doi:10.1016/j.cub.2007.01.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Pitts S, Pelser E, Meeks J, Smith D (2016) Odorant responses and courtship behaviors influenced by at4 neurons in Drosophila. PLoS ONE 11(9):e0162761. doi:10.1371/journal.pone.0162761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  177. Lin CC, Prokop-Prigge KA, Preti G, Potter CJ (2015) Food odors trigger Drosophila males to deposit a pheromone that guides aggregation and female oviposition decisions. Elife. doi:10.7554/eLife.08688

    Google Scholar 

  178. Dweck HKM, Ebrahim SAM, Thoma M, Mohamed AAM, Keesey IW, Trona F, Lavista-Llanos S, Svatos A, Sachse S, Knaden M, Hansson BS (2015) Pheromones mediating copulation and attraction in Drosophila. Proc Natl Acad Sci USA 112(21):2829–2835. doi:10.1073/pnas.1504527112

    Article  CAS  Google Scholar 

  179. Larter NK, Sun JS, Carlson JR (2016) Organization and function of Drosophila odorant binding proteins. Elife. doi:10.7554/eLife.20242

    PubMed  PubMed Central  Google Scholar 

  180. Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63(14):1658–1676. doi:10.1007/s00018-005-5607-0

    Article  CAS  PubMed  Google Scholar 

  181. Schultze A, Pregitzer P, Walter MF, Woods DF, Marinotti O, Breer H, Krieger J (2013) The co-expression pattern of odorant binding proteins and olfactory receptors identify distinct trichoid sensilla on the antenna of the malaria mosquito Anopheles gambiae. PLoS ONE 8(7):e69412. doi:10.1371/journal.pone.0069412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Qiao H, He X, Schymura D, Ban L, Dani FR, Michelucci E, Caputo B, Torre AD, Iatrou K, Zhou JJ, Krieger J, Pelosi P (2010) Cooperative interactions between odorant-binding proteins of Anopheles gambiae. Cell Mol Life Sci 68:1799–1813. doi:10.1007/s00018-010-0539-8

    Article  PubMed  CAS  Google Scholar 

  183. Guo H, Huang LQ, Pelosi P, Wang CZ (2012) Three pheromone-binding proteins help segregation between two Helicoverpa species utilizing the same pheromone components. Insect Biochem Mol Biol 42(9):708–716. doi:10.1016/j.ibmb.2012.06.004

    Article  CAS  PubMed  Google Scholar 

  184. Swarup S, Williams TI, Anholt RR (2011) Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10(6):648–657. doi:10.1111/j.1601-183X.2011.00704.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Nordström KJ, Sallman Almen M, Edstam MM, Fredriksson R, Schioth HB (2011) Independent HHsearch, Needleman–Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families. Mol Biol Evol 28(9):2471–2480. doi:10.1093/molbev/msr061

    Article  PubMed  CAS  Google Scholar 

  186. Wistrand M, Kall L, Sonnhammer EL (2006) A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci 15(3):509–521. doi:10.1110/ps.051745906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Guo S, Kim J (2010) Dissecting the molecular mechanism of Drosophila odorant receptors through activity modeling and comparative analysis. Proteins 78(2):381–399. doi:10.1002/prot.22556

    Article  CAS  PubMed  Google Scholar 

  188. Olafson PU (2013) Molecular characterization and immunolocalization of the olfactory co-receptor Orco from two blood-feeding muscid flies, the stable fly (Stomoxys calcitrans, L.) and the horn fly (Haematobia irritans irritans, L.). Insect Mol Biol 22(2):131–142. doi:10.1111/imb.12009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Hull JJ, Hoffmann EJ, Perera OP, Snodgrass GL (2012) Identification of the western tarnished plant bug (Lygus hesperus) olfactory co-receptor Orco: expression profile and confirmation of atypical membrane topology. Arch Insect Biochem Physiol 81(4):179–198. doi:10.1002/arch.21042

    Article  CAS  PubMed  Google Scholar 

  190. Miller R, Tu ZJ (2008) Odorant receptor c-terminal motifs in divergent insect species. J Insect Sci 8(53):1–10. doi:10.1673/031.008.5301

    Article  PubMed  Google Scholar 

  191. Elmore T, Ignell R, Carlson JR, Smith DP (2003) Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum. J Neurosci 23(30):9906–9912

    CAS  PubMed  Google Scholar 

  192. Nichols AS, Chen S, Luetje CW (2011) Subunit contributions to insect olfactory receptor function: channel block and odorant recognition. Chem Senses 36(9):781–790. doi:10.1093/chemse/bjr053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Bahk S, Jones WD (2016) Insect odorant receptor trafficking requires calmodulin. BMC Biol. doi:10.1186/s12915-016-0306-x

    PubMed  PubMed Central  Google Scholar 

  194. Mukunda L, Miazzi F, Kaltofen S, Hansson BS, Wicher D (2014) Calmodulin modulates insect odorant receptor function. Cell Calcium 55(4):191–199. doi:10.1016/j.ceca.2014.02.013

    Article  CAS  PubMed  Google Scholar 

  195. Mukunda L, Miazzi F, Sargsyan V, Hansson BS, Wicher D (2016) Calmodulin affects sensitization of Drosophila melanogaster odorant receptors. Front Cell Neurosci. doi:10.3389/fncel.2016.00028

    PubMed  PubMed Central  Google Scholar 

  196. Nolte A, Funk NW, Mukunda L, Gawalek P, Werckenthin A, Hansson BS, Wicher D, Stengl M (2013) In situ tip-recordings found no evidence for an Orco-based ionotropic mechanism of pheromone-transduction in Manduca sexta. PLoS ONE 8(5):e62648. doi:10.1371/journal.pone.0062648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Deng Y, Zhang W, Farhat K, Oberland S, Gisselmann G, Neuhaus EM (2011) The stimulatory Galpha(s) protein is involved in olfactory signal transduction in Drosophila. PLoS ONE 6(4):e18605. doi:10.1371/journal.pone.0018605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Stengl M, Funk NW (2013) The role of the coreceptor Orco in insect olfactory transduction. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199(11):897–909. doi:10.1007/s00359-013-0837-3

    Article  CAS  PubMed  Google Scholar 

  199. Carraher C, Dalziel J, Jordan MD, Christie DL, Newcomb RD, Kralicek AV (2015) Towards an understanding of the structural basis for insect olfaction by odorant receptors. Insect Biochem Mol Biol 66:31–41. doi:10.1016/j.ibmb.2015.09.010

    Article  CAS  PubMed  Google Scholar 

  200. Yao CA, Carlson JR (2010) Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila. J Neurosci 30(13):4562–4572. doi:10.1523/JNEUROSCI.6357-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Talluri S, Bhatt A, Smith DP (1995) Identification of a Drosophila G protein alpha subunit (dGq alpha-3) expressed in chemosensory cells and central neurons. Proc Natl Acad Sci USA 92(25):11475–11479. doi:10.1073/pnas.92.25.11475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Laue M, Maida R, Redkozubov A (1997) G-protein activation, identification and immunolocalization in pheromone-sensitive sensilla trichodea of moths. Cell Tissue Res 288(1):149–158. doi:10.1007/s004410050802

    Article  CAS  PubMed  Google Scholar 

  203. Jacquin-Joly E, Francois MC, Burnet M, Lucas P, Bourrat F, Maida R (2002) Expression pattern in the antennae of a newly isolated lepidopteran Gq protein alpha subunit cDNA. Eur J Biochem 269(8):2133–2142. doi:10.1046/j.1432-1033.2002.02863.x

    Article  CAS  PubMed  Google Scholar 

  204. Kalidas S, Smith DP (2002) Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron 33(2):177–184. doi:10.1016/S0896-6273(02)00560-3

    Article  CAS  PubMed  Google Scholar 

  205. Miura N, Atsumi S, Tabunoki H, Sato R (2005) Expression and localization of three G protein alpha subunits, Go, Gq, and Gs, in adult antennae of the silkmoth (Bombyx mori). J Comp Neurol 485(2):143–152. doi:10.1002/cne.20488

    Article  CAS  PubMed  Google Scholar 

  206. Boto T, Gomez-Diaz C, Alcorta E (2010) Expression analysis of the 3 G-protein subunits, Gα, Gβ, and Gγ, in the olfactory receptor organs of adult Drosophila melanogaster. Chem Senses 35(3):183–193. doi:10.1093/chemse/bjp095

    Article  CAS  PubMed  Google Scholar 

  207. Rutzler M, Lu T, Zwiebel LJ (2006) Galpha encoding gene family of the malaria vector mosquito Anopheles gambiae: expression analysis and immunolocalization of AGαq and AGαo in female antenna. J Comp Neurol 499(4):533–545. doi:10.1002/cne.21083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Gomez-Diaz C, Martin F, Alcorta E (2004) The cAMP transduction cascade mediates olfactory reception in Drosophila melanogaster. Behav Genet 34(4):395–406. doi:10.1023/B:BEGE.0000023645.02710.fe

    Article  PubMed  Google Scholar 

  209. Gomez-Diaz C, Martin F, Alcorta E (2006) The inositol 1,4,5-triphosphate kinase1 gene affects olfactory reception in Drosophila melanogaster. Behav Genet 36(2):309–321. doi:10.1007/s10519-005-9031-x

    Article  PubMed  Google Scholar 

  210. Miazzi F, Hansson BS, Wicher D (2016) Odor-induced cAMP production in Drosophila melanogaster olfactory sensory neurons. J Exp Biol 219(12):1798–1803. doi:10.1242/jeb.137901

    Article  PubMed  Google Scholar 

  211. Sargsyan V, Getahun MN, Llanos SL, Olsson SB, Hansson BS, Wicher D (2011) Phosphorylation via PKC regulates the function of the Drosophila odorant co-receptor. Front Cell Neurosci. doi:10.3389/fncel.2011.00005

    PubMed  PubMed Central  Google Scholar 

  212. Getahun MN, Thoma M, Lavista-Llanos S, Keesey I, Fandino RA, Knaden M, Wicher D, Olsson SB, Hansson BS (2016) Intracellular regulation of the insect chemoreceptor complex impacts odour localization in flying insects. J Exp Biol 219(Pt 21):3428–3438. doi:10.1242/jeb.143396

    Article  PubMed  Google Scholar 

  213. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19(3):284–292. doi:10.1016/j.conb.2009.07.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Getahun MN, Olsson SB, Lavista-Llanos S, Hansson BS, Wicher D (2013) Insect odorant response sensitivity is tuned by metabotropically autoregulated olfactory receptors. PLoS ONE 8(3):e58889. doi:10.1371/journal.pone.0058889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Getahun MN, Wicher D, Hansson BS, Olsson SB (2012) Temporal response dynamics of Drosophila olfactory sensory neurons depends on receptor type and response polarity. Front Cell Neurosci 6:54. doi:10.3389/fncel.2012.00054

    Article  PubMed  PubMed Central  Google Scholar 

  216. Carde RT, Willis MA (2008) Navigational strategies used by insects to find distant, wind-borne sources of odor. J Chem Ecol 34(7):854–866. doi:10.1007/s10886-008-9484-5

    Article  CAS  PubMed  Google Scholar 

  217. Stengl M (2010) Pheromone transduction in moths. Front Cell Neurosci 4:133. doi:10.3389/fncel.2010.00133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  218. Nolte A, Gawalek P, Koerte S, Wei H, Schumann R, Werckenthin A, Krieger J, Stengl M (2016) No evidence for ionotropic pheromone transduction in the hawkmoth Manduca sexta. PLoS ONE 11(11):e0166060. doi:10.1371/journal.pone.0166060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  219. Boekhoff I, Strotmann J, Raming K, Tareilus E, Breer H (1990) Odorant-sensitive phospholipase C in insect antennae. Cell Signal 2(1):49–56. doi:10.1016/0898-6568(90)90032-6

    Article  CAS  PubMed  Google Scholar 

  220. Breer H, Boekhoff I, Strotmann J, Raming K, Tareilus E (1990) Molecular elements of olfactory signal transduction in insect antennae. Nato ASI Series H 39:77–86. doi:10.1007/978-3-642-75127-1_5

    CAS  Google Scholar 

  221. Ziegelberger G, Vandenberg MJ, Kaissling KE, Klumpp S, Schultz JE (1990) Cyclic-GMP levels and guanylate-cyclase activity in pheromone-sensitive antennae of the silkmoths Antheraea polyphemus and Bombyx mori. J Neurosci 10(4):1217–1225

    CAS  PubMed  Google Scholar 

  222. Stengl M, Zufall F, Hatt H, Hildebrand JG (1992) Olfactory receptor neurons from antennae of developing male Manduca sexta respond to components of the species-specific sex pheromone in vitro. J Neurosci 12(7):2523–2531

    CAS  PubMed  Google Scholar 

  223. Stengl M (1994) Inositol-trisphosphate-dependent calcium currents precede cation currents in insect olfactory receptor neurons in vitro. J Comp Physiol A 174(2):187–194. doi:10.1007/BF00193785

    Article  CAS  PubMed  Google Scholar 

  224. Stengl M (1993) Intracellular-messenger-mediated cation channels in cultured olfactory receptor neurons. J Exp Biol 178:125–147

    CAS  PubMed  Google Scholar 

  225. Ito I, Ong RC, Raman B, Stopfer M (2008) Olfactory learning and spike timing dependent plasticity. Commun Integr Biol 1(2):170–171. doi:10.4161/cib.1.2.7140

    Article  PubMed  PubMed Central  Google Scholar 

  226. Justus KA, Carde RT, French AS (2005) Dynamic properties of antennal responses to pheromone in two moth species. J Neurophysiol 93(4):2233–2239. doi:10.1152/jn.00888.2004

    Article  CAS  PubMed  Google Scholar 

  227. Tripathy SJ, Peters OJ, Staudacher EM, Kalwar FR, Hatfield MN, Daly KC (2010) Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Front Cell Neurosci. doi:10.3389/neuro.03.001.2010

    PubMed  PubMed Central  Google Scholar 

  228. Autrum H (1950) Die Belichtungspotentiale und das Sehen der Insekten (Untersuchungen an Calliphora und Dixippus). Zeitschrift Fur Vergleichende Physiologie 32(3):176–227. doi:10.1007/Bf00344524

    Article  CAS  PubMed  Google Scholar 

  229. Tatler B, O’Carroll DC, Laughlin SB (2000) Temperature and the temporal resolving power of fly photoreceptors. J Comp Physiol A Sens Neural and Behav Physiol 186(4):399–407. doi:10.1007/s003590050439

    Article  CAS  Google Scholar 

  230. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413(6852):186–193. doi:10.1038/35093002

    Article  CAS  PubMed  Google Scholar 

  231. Brito NF, Moreira MF, Melo AC (2016) A look inside odorant-binding proteins in insect chemoreception. J Insect Physiol 95:51–65. doi:10.1016/j.jinsphys.2016.09.008

    Article  CAS  PubMed  Google Scholar 

  232. Fan J, Francis F, Liu Y, Chen JL, Cheng DF (2011) An overview of odorant-binding protein functions in insect peripheral olfactory reception. Genet Mol Res 10(4):3056–3069. doi:10.4238/2011.December.8.2

    Article  CAS  PubMed  Google Scholar 

  233. Zhou JJ (2010) Odorant-binding proteins in insects. Vitam Horm 83:241–272. doi:10.1016/S0083-6729(10)83010-9

    Article  CAS  PubMed  Google Scholar 

  234. Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490. doi:10.1093/gbe/evr033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. Gong DP, Zhang HJ, Zhao P, Xia QY, Xiang ZH (2009) The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics 10:332. doi:10.1186/1471-2164-10-332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  236. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12(9):1357–1369. doi:10.1101/gr.239402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Manoharan M, Ng Fuk CM, Vaitinadapoule A, Frumence E, Sowdhamini R, Offmann B (2013) Comparative genomics of odorant binding proteins in Anopheles gambiae, Aedes aegypti, and Culex quinquefasciatus. Genome Biol Evol 5(1):163–180. doi:10.1093/gbe/evs131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  238. Qiao H, Xiaoli H, Schymura D, Ban L, Field L, Dani FR, Michelucci E, Caputo B, Della Torre A, Iatrou K, Krieger J, Zhou JJ, Pelosi P (2010) Cooparative interactions between odorant-binding proteins of Anopheles gambiae. Cell Mol Life Sci 68:1799–1813. doi:10.1007/s00018-010-0539-8

    Article  PubMed  CAS  Google Scholar 

  239. 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(2):143–151. doi:10.1016/S1074-5521(00)00078-8

    Article  CAS  PubMed  Google Scholar 

  240. Horst R, Damberger F, Luginbuhl P, Guntert P, Peng G, Nikonova L, Leal WS, Wuthrich K (2001) NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proc Natl Acad Sci USA 98(25):14374–14379. doi:10.1073/pnas.251532998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Wojtasek H, Leal WS (1999) Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J Biol Chem 274(43):30950–30956. doi:10.1074/jbc.274.43.30950

    Article  CAS  PubMed  Google Scholar 

  242. Laughlin JD, Ha TS, Jones DN, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133(7):1255–1265. doi:10.1016/j.cell.2008.04.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Pophof B (2004) Pheromone-binding proteins contribute to the activation of olfactory receptor neurons in the silkmoths Antheraea polyphemus and Bombyx mori. Chem Senses 29(2):117–125. doi:10.1093/chemse/bjh012

    Article  PubMed  CAS  Google Scholar 

  244. Pophof B (2002) Moth pheromone binding proteins contribute to the excitation of olfactory receptor cells. Naturwissenschaften 89(11):515–518. doi:10.1007/s00114-002-0364-5

    Article  CAS  PubMed  Google Scholar 

  245. Xu PX, Atkinson R, Jones DNM, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45(2):193–200. doi:10.1016/j.neuron.2004.12.031

    Article  CAS  PubMed  Google Scholar 

  246. Ronderos DS, Smith DP (2010) Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 30(7):2595–2599. doi:10.1523/Jneurosci.4819-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Gomez-Diaz C, Reina JH, Cambillau C, Benton R (2013) Ligands for pheromone-sensing neurons are not conformationally activated odorant binding proteins. PLoS Biol 11(4):e1001546. doi:10.1371/journal.pbio.1001546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. 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(9):e1004600. doi:10.1371/journal.pgen.1004600

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  249. 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 CD36 family of membrane proteins. J Biol Chem 272(23):14792–14799. doi:10.1074/jbc.272.23.14792

    Article  CAS  PubMed  Google Scholar 

  250. Nichols Z, Vogt RG (2008) The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem Mol Biol 38(4):398–415. doi:10.1016/j.ibmb.2007.11.003

    Article  CAS  PubMed  Google Scholar 

  251. Oberland S, Ackelst T, Gaab S, Pelz T, Spehr J, Spehr M, Neuhaus EM (2015) CD36 is involved in oleic acid detection by the murine olfactory system. Front Cell Neurosci. doi:10.3389/fncel.2075.00366

    PubMed  PubMed Central  Google Scholar 

  252. Xavier AM, Ludwig RG, Nagai MH, de Almeida TJ, Watanabe HM, Hirata MY, Rosenstock TR, Papes F, Malnic B, Glezer I (2016) CD36 is expressed in a defined subpopulation of neurons in the olfactory epithelium. Sci Rep 6:25507. doi:10.1038/srep25507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Lee S, Eguchi A, Tsuzuki S, Matsumura S, Inoue K, Iwanaga T, Masuda D, Yamashita S, Fushiki T (2015) Expression of CD36 by olfactory receptor cells and its abundance on the epithelial surface in mice. PLoS ONE 10(7):e0133412. doi:10.1371/journal.pone.0133412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  254. Forstner M, Gohl T, Gondesen I, Raming K, Breer H, Krieger J (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem Senses 33(3):291–299. doi:10.1093/chemse/bjm087

    Article  CAS  PubMed  Google Scholar 

  255. Pregitzer P, Greschista M, Breer H, Krieger J (2014) The sensory neurone membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Mol Biol 23(6):733–742. doi:10.1111/imb.12119

    Article  CAS  PubMed  Google Scholar 

  256. Liu C, Zhang J, Liu Y, Wang G, Dong S (2014) Expression of SNMP1 and SNMP2 genes in antennal sensilla of Spodoptera exigua (Hubner). Arch Insect Biochem Physiol 85(2):114–126. doi:10.1002/arch.21150

    Article  CAS  PubMed  Google Scholar 

  257. Gu SH, Yang RN, Guo MB, Wang GR, Wu KM, Guo YY, Zhou JJ, Zhang YJ (2013) Molecular identification and differential expression of sensory neuron membrane proteins in the antennae of the black cutworm moth Agrotis ipsilon. J Insect Physiol 59(4):430–443. doi:10.1016/j.jinsphys.2013.02.003

    Article  CAS  PubMed  Google Scholar 

  258. Zhang J, Liu Y, Walker WB, Dong SL, Wang GR (2015) Identification and localization of two sensory neuron membrane proteins from Spodoptera litura (Lepidoptera: Noctuidae). Insect Sci 22(3):399–408. doi:10.1111/1744-7917.12131

    Article  PubMed  CAS  Google Scholar 

  259. Vogt RG, Miller NE, Litvack R, Fandino RA, Sparks J, Staples J, Friedman R, Dickens JC (2009) The insect SNMP gene family. Insect Biochem Mol Biol 39(7):448–456. doi:10.1016/j.ibmb.2009.03.007

    Article  CAS  PubMed  Google Scholar 

  260. Rogers ME, Krieger J, Vogt RG (2001) Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J Neurobiol 49(1):47–61. doi:10.1002/neu.1065

    Article  CAS  PubMed  Google Scholar 

  261. Huang X, Liu L, Fang Y, Feng J (2016) Expression of a sensory neuron membrane protein SNMP2 in olfactory sensilla of codling moth Cydia pomonella (Lepidoptera: Tortricidae). J Econ Entomol 109(4):1907–1913. doi:10.1093/jee/tow098

    Article  PubMed  Google Scholar 

  262. Rogers ME, Steinbrecht RA, Vogt RG (2001) Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell Tissue Res 303(3):433–446. doi:10.1007/s004410000305

    Article  CAS  PubMed  Google Scholar 

  263. Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113–135. doi:10.1146/annurev.ento.51.051705.113646

    Article  CAS  PubMed  Google Scholar 

  264. Montell C (2009) A taste of the Drosophila gustatory receptors. Curr Opin Neurobiol 19(4):345–353. doi:10.1016/j.conb.2009.07.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  265. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104(5):661–673. doi:10.1016/S0092-8674(01)00263-X

    Article  CAS  PubMed  Google Scholar 

  266. Thorne N, Amrein H (2008) Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J Comp Neurol 506(4):548–568. doi:10.1002/cne.21547

    Article  CAS  PubMed  Google Scholar 

  267. Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445(7123):86–90. doi:10.1038/nature05466

    Article  CAS  PubMed  Google Scholar 

  268. Suh GSB, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431(7010):854–859. doi:10.1038/nature02980

    Article  CAS  PubMed  Google Scholar 

  269. Suh GS, Ben-Tabou de Leon S, Tanimoto H, Fiala A, Benzer S, Anderson DJ (2007) Light activation of an innate olfactory avoidance response in Drosophila. Curr Biol 17(10):905–908. doi:10.1016/j.cub.2007.04.046

    Article  CAS  PubMed  Google Scholar 

  270. Faucher C, Forstreuter M, Hilker M, de Bruyne M (2006) Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J Exp Biol 209(Pt 14):2739–2748. doi:10.1242/jeb.02297

    Article  CAS  PubMed  Google Scholar 

  271. Tauxe GM, MacWilliam D, Boyle SM, Guda T, Ray A (2013) Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155(6):1365–1379. doi:10.1016/j.cell.2013.11.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB (2014) Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156(5):1060–1071. doi:10.1016/j.cell.2013.12.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  273. Rodrigues TB, Moriyama EN, Wang H, Khajuria C, Siegfried BD (2016) Carbon dioxide receptor genes and their expression profile in Diabrotica virgifera virgifera. BMC Res Notes 9:18. doi:10.1186/s13104-015-1794-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  274. Ning C, Yang K, Xu M, Huang LQ, Wang CZ (2016) Functional validation of the carbon dioxide receptor in labial palps of Helicoverpa armigera moths. Insect Biochem Mol Biol 73:12–19. doi:10.1016/j.ibmb.2016.04.002

    Article  CAS  PubMed  Google Scholar 

  275. Xu W, Anderson A (2015) Carbon dioxide receptor genes in cotton bollworm Helicoverpa armigera. Naturwissenschaften 102(3–4):11. doi:10.1007/s00114-015-1260-0

    Article  PubMed  CAS  Google Scholar 

  276. Joseph RM, Carlson JR (2015) Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet 31(12):683–695. doi:10.1016/j.tig.2015.09.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. Watanabe K, Toba G, Koganezawa M, Yamamoto D (2011) Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 41(5):746–753. doi:10.1007/s10519-011-9461-6

    Article  PubMed  Google Scholar 

  278. Miyamoto T, Amrein H (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11(8):874–876. doi:10.1038/nn.2161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Moon SJ, Lee Y, Jiao Y, Montell C (2009) A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19(19):1623–1627. doi:10.1016/j.cub.2009.07.061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  280. Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39(6):1019–1029. doi:10.1016/S0896-6273(03)00542-7

    Article  CAS  PubMed  Google Scholar 

  281. Toda H, Zhao X, Dickson BJ (2012) The Drosophila female aphrodisiac pheromone activates ppk23(+) sensory neurons to elicit male courtship behavior. Cell Rep 1(6):599–607. doi:10.1016/j.celrep.2012.05.007

    Article  CAS  PubMed  Google Scholar 

  282. Shankar S, Chua JY, Tan KJ, Calvert ME, Weng R, Ng WC, Mori K, Yew JY (2015) The neuropeptide tachykinin is essential for pheromone detection in a gustatory neural circuit. Elife 4:e06914. doi:10.7554/eLife.06914

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  283. Jeong YT, Shim J, Oh SR, Yoon HI, Kim CH, Moon SJ, Montell C (2013) An odorant-binding protein required for suppression of sweet taste by bitter chemicals. Neuron 79(4):725–737. doi:10.1016/j.neuron.2013.06.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS ONE 6(8):e24111. doi:10.1371/journal.pone.0024111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  285. Liman ER, Zhang YV, Montell C (2014) Peripheral coding of taste. Neuron 81(5):984–1000. doi:10.1016/j.neuron.2014.02.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  286. Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci USA 108(28):11680–11685. doi:10.1073/pnas.1019622108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. Yao CA, Ignell R, Carlson JR (2005) Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25(37):8359–8367. doi:10.1523/JNEUROSCI.2432-05.2005

    Article  CAS  PubMed  Google Scholar 

  288. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69(1):44–60. doi:10.1016/j.neuron.2010.11.042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  289. Chen Q, Man Y, Li J, Pei D, Wu W (2017) Olfactory ionotropic receptors in mosquito Aedes albopictus (Diptera: Culicidae). J Med Entomol. doi:10.1093/jme/tjx063

    Google Scholar 

  290. Guo M, Krieger J, Grosse-Wilde E, Missbach C, Zhang L, Breer H (2013) Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the desert locust (Schistocerca gregaria). Int J Biol Sci 10(1):1–14. doi:10.7150/ijbs.7624

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  291. Mayer ML (2011) Emerging models of glutamate receptor ion channel structure and function. Structure 19(10):1370–1380. doi:10.1016/j.str.2011.08.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  292. Knecht ZA, Silbering AF, Ni L, Klein M, Budelli G, Bell R, Abuin L, Ferrer AJ, Samuel AD, Benton R, Garrity PA (2016) Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife. doi:10.7554/eLife.17879

    PubMed  PubMed Central  Google Scholar 

  293. Ni L, Klein M, Svec KV, Budelli G, Chang EC, Ferrer AJ, Benton R, Samuel AD, Garrity PA (2016) The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife. doi:10.7554/eLife.13254

    Google Scholar 

  294. Ai M, Blais S, Park JY, Min S, Neubert TA, Suh GS (2013) Ionotropic glutamate receptors IR64a and IR8a form a functional odorant receptor complex in vivo in Drosophila. J Neurosci 33(26):10741–10749. doi:10.1523/JNEUROSCI.5419-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  295. Silbering AF, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis GS, Benton R (2011) Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci 31(38):13357–13375. doi:10.1523/JNEUROSCI.2360-11.2011

    Article  CAS  PubMed  Google Scholar 

  296. Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GS, Benton R (2011) An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478(7368):236–240. doi:10.1038/nature10428

    Article  CAS  PubMed  Google Scholar 

  297. Hussain A, Zhang M, Ucpunar HK, Svensson T, Quillery E, Gompel N, Ignell R, Kadow ICG (2016) Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biol. doi:10.1371/journal.pbio.1002454

    Google Scholar 

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Acknowledgements

This work was supported by a grant to J.K. provided by the Deutsche Forschungsgemeinschaft (DFG), priority program SPP1392 (KR1786/4-2).

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  1. Department of Animal Physiology, Institute of Biology/Zoology, Martin Luther University Halle-Wittenberg, 06120, Halle (Saale), Germany

    Joerg Fleischer & Jürgen Krieger

  2. Institute of Physiology, University of Hohenheim, Stuttgart, Germany

    Pablo Pregitzer & Heinz Breer

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  1. Joerg Fleischer
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  2. Pablo Pregitzer
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Fleischer, J., Pregitzer, P., Breer, H. et al. Access to the odor world: olfactory receptors and their role for signal transduction in insects. Cell. Mol. Life Sci. 75, 485–508 (2018). https://doi.org/10.1007/s00018-017-2627-5

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