Cellular and Molecular Life Sciences

, Volume 75, Issue 3, pp 485–508 | Cite as

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

  • Joerg Fleischer
  • Pablo Pregitzer
  • Heinz Breer
  • Jürgen KriegerEmail author


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.


Chemosensation Gustatory receptor (GR) Ionotropic receptor (IR) Odorant receptor (OR) Olfaction Pheromone receptor (PR) 



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


  1. 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 CrossRefGoogle Scholar
  2. 2.
    Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72(5):698–711. doi: 10.1016/j.neuron.2011.11.003 PubMedCrossRefGoogle Scholar
  3. 3.
    Schneider D (1969) Insect olfaction: deciphering system for chemical messages. Science 163(3871):1031–1037. doi: 10.1126/science.163.3871.1031 PubMedCrossRefGoogle Scholar
  4. 4.
    Wyatt TD (2014) Pheromones and animal behavior. Cambridge Univ Press, CambridgeGoogle Scholar
  5. 5.
    Schneider D (1992) 100 Years of pheromone research—an essay on lepidoptera. Naturwissenschaften 79(6):241–250. doi: 10.1007/Bf01175388 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 PubMedCrossRefGoogle Scholar
  9. 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 391–445CrossRefGoogle Scholar
  10. 10.
    de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19(11):4520–4532PubMedGoogle Scholar
  11. 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 PubMedCrossRefGoogle Scholar
  12. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 PubMedCrossRefGoogle Scholar
  14. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Wicher D (2015) Olfactory signaling in insects. Prog Mol Biol Transl Sci 130:37–54. doi: 10.1016/bs.pmbts.2014.11.002 PubMedCrossRefGoogle Scholar
  17. 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 PubMedCrossRefGoogle Scholar
  18. 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 PubMedCrossRefGoogle Scholar
  19. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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 PubMedCrossRefGoogle Scholar
  21. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 PubMedPubMedCentralGoogle Scholar
  23. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 PubMedCrossRefGoogle Scholar
  25. 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 PubMedCrossRefGoogle Scholar
  26. 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 PubMedCrossRefGoogle Scholar
  27. 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 PubMedCrossRefGoogle Scholar
  28. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  29. 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 PubMedCrossRefGoogle Scholar
  30. 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. 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 PubMedCrossRefGoogle Scholar
  32. 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 PubMedCrossRefGoogle Scholar
  33. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 PubMedCrossRefGoogle Scholar
  35. 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 PubMedCrossRefGoogle Scholar
  36. 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 PubMedCrossRefGoogle Scholar
  37. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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 PubMedCrossRefGoogle Scholar
  39. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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 PubMedCrossRefGoogle Scholar
  41. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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 PubMedCrossRefGoogle Scholar
  43. 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 PubMedCrossRefGoogle Scholar
  44. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  45. 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 PubMedPubMedCentralGoogle Scholar
  46. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 PubMedCrossRefGoogle Scholar
  48. 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 PubMedCrossRefGoogle Scholar
  49. 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 PubMedCrossRefGoogle Scholar
  50. 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 PubMedCrossRefGoogle Scholar
  51. 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 PubMedCrossRefGoogle Scholar
  52. 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 PubMedCrossRefGoogle Scholar
  53. 53.
    Vosshall LB (2001) The molecular logic of olfaction in Drosophila. Chem Senses 26(2):207–213. doi: 10.1093/chemse/26.2.207 PubMedCrossRefGoogle Scholar
  54. 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 PubMedCrossRefGoogle Scholar
  55. 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 PubMedCrossRefGoogle Scholar
  56. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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 PubMedCrossRefGoogle Scholar
  58. 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 PubMedCrossRefGoogle Scholar
  59. 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 PubMedCrossRefGoogle Scholar
  60. 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 PubMedCrossRefGoogle Scholar
  61. 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 PubMedCrossRefGoogle Scholar
  62. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  63. 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 PubMedCrossRefGoogle Scholar
  64. 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 PubMedCrossRefGoogle Scholar
  65. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 PubMedCrossRefGoogle Scholar
  67. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  69. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  70. 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 PubMedCrossRefGoogle Scholar
  71. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  73. 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 PubMedCrossRefGoogle Scholar
  74. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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 PubMedCrossRefGoogle Scholar
  79. 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 PubMedCrossRefGoogle Scholar
  80. 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 PubMedCrossRefGoogle Scholar
  81. 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 PubMedCrossRefGoogle Scholar
  82. 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 PubMedCrossRefGoogle Scholar
  83. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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 PubMedCrossRefGoogle Scholar
  87. 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 PubMedCrossRefGoogle Scholar
  88. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 PubMedPubMedCentralGoogle Scholar
  90. 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 PubMedCrossRefGoogle Scholar
  91. 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 PubMedCrossRefGoogle Scholar
  92. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 PubMedCrossRefGoogle Scholar
  94. 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. 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 PubMedCrossRefGoogle Scholar
  96. 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 PubMedCrossRefGoogle Scholar
  97. 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 PubMedPubMedCentralGoogle Scholar
  98. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Rodriguez I (2013) Singular expression of olfactory receptor genes. Cell 155(2):274–277. doi: 10.1016/j.cell.2013.09.032 PubMedCrossRefGoogle Scholar
  102. 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 PubMedCrossRefGoogle Scholar
  103. 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 PubMedCrossRefGoogle Scholar
  104. 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 CrossRefGoogle Scholar
  105. 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 PubMedCrossRefGoogle Scholar
  106. 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 PubMedCrossRefGoogle Scholar
  107. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 CrossRefGoogle Scholar
  113. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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 PubMedCrossRefGoogle Scholar
  115. 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 PubMedCrossRefGoogle Scholar
  116. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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 PubMedCrossRefGoogle Scholar
  118. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  119. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  121. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 PubMedCrossRefGoogle Scholar
  125. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  126. 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 PubMedCrossRefGoogle Scholar
  127. 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 PubMedCrossRefGoogle Scholar
  128. 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 PubMedCrossRefGoogle Scholar
  129. 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 CrossRefGoogle Scholar
  130. 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 PubMedCrossRefGoogle Scholar
  131. 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 PubMedCrossRefGoogle Scholar
  132. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  134. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  135. 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 PubMedCrossRefGoogle Scholar
  136. 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 PubMedCrossRefGoogle Scholar
  137. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  138. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  139. 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 PubMedCrossRefGoogle Scholar
  140. 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 PubMedCrossRefGoogle Scholar
  141. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  142. 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 PubMedPubMedCentralGoogle Scholar
  143. 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. 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 PubMedCrossRefGoogle Scholar
  145. 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 PubMedCrossRefGoogle Scholar
  146. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  147. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  148. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  149. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  150. 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 PubMedCrossRefGoogle Scholar
  151. 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 PubMedCrossRefGoogle Scholar
  152. 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 PubMedCrossRefGoogle Scholar
  153. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  154. 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 PubMedCrossRefGoogle Scholar
  155. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  156. 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 PubMedCrossRefGoogle Scholar
  157. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  158. 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 PubMedCrossRefGoogle Scholar
  159. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  160. 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 PubMedCrossRefGoogle Scholar
  161. 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 CrossRefGoogle Scholar
  162. 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 CrossRefGoogle Scholar
  163. 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 PubMedCrossRefGoogle Scholar
  164. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  165. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  166. 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 PubMedCrossRefGoogle Scholar
  167. 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 PubMedCrossRefGoogle Scholar
  168. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  169. 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 PubMedCrossRefGoogle Scholar
  170. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  171. 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 PubMedCrossRefGoogle Scholar
  172. 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 CrossRefGoogle Scholar
  173. 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 PubMedCrossRefGoogle Scholar
  174. 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 PubMedCrossRefGoogle Scholar
  175. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  176. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  177. 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. 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 CrossRefGoogle Scholar
  179. 179.
    Larter NK, Sun JS, Carlson JR (2016) Organization and function of Drosophila odorant binding proteins. Elife. doi: 10.7554/eLife.20242 PubMedPubMedCentralGoogle Scholar
  180. 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 PubMedCrossRefGoogle Scholar
  181. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  182. 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 PubMedCrossRefGoogle Scholar
  183. 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 PubMedCrossRefGoogle Scholar
  184. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  185. 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 PubMedCrossRefGoogle Scholar
  186. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  187. 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 PubMedCrossRefGoogle Scholar
  188. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  189. 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 PubMedCrossRefGoogle Scholar
  190. 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 PubMedCrossRefGoogle Scholar
  191. 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):9906–9912PubMedGoogle Scholar
  192. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  193. 193.
    Bahk S, Jones WD (2016) Insect odorant receptor trafficking requires calmodulin. BMC Biol. doi: 10.1186/s12915-016-0306-x PubMedPubMedCentralGoogle Scholar
  194. 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 PubMedCrossRefGoogle Scholar
  195. 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 PubMedPubMedCentralGoogle Scholar
  196. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  197. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  198. 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 PubMedCrossRefGoogle Scholar
  199. 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 PubMedCrossRefGoogle Scholar
  200. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  201. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  202. 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 PubMedCrossRefGoogle Scholar
  203. 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 PubMedCrossRefGoogle Scholar
  204. 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 PubMedCrossRefGoogle Scholar
  205. 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 PubMedCrossRefGoogle Scholar
  206. 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 PubMedCrossRefGoogle Scholar
  207. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  208. 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 PubMedCrossRefGoogle Scholar
  209. 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 PubMedCrossRefGoogle Scholar
  210. 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 PubMedCrossRefGoogle Scholar
  211. 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 PubMedPubMedCentralGoogle Scholar
  212. 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 PubMedCrossRefGoogle Scholar
  213. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  214. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  215. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  216. 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 PubMedCrossRefGoogle Scholar
  217. 217.
    Stengl M (2010) Pheromone transduction in moths. Front Cell Neurosci 4:133. doi: 10.3389/fncel.2010.00133 PubMedPubMedCentralCrossRefGoogle Scholar
  218. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  219. 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 PubMedCrossRefGoogle Scholar
  220. 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 Google Scholar
  221. 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):1217–1225PubMedGoogle Scholar
  222. 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):2523–2531PubMedGoogle Scholar
  223. 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 PubMedCrossRefGoogle Scholar
  224. 224.
    Stengl M (1993) Intracellular-messenger-mediated cation channels in cultured olfactory receptor neurons. J Exp Biol 178:125–147PubMedGoogle Scholar
  225. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  226. 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 PubMedCrossRefGoogle Scholar
  227. 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 PubMedPubMedCentralGoogle Scholar
  228. 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 PubMedCrossRefGoogle Scholar
  229. 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 CrossRefGoogle Scholar
  230. 230.
    Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413(6852):186–193. doi: 10.1038/35093002 PubMedCrossRefGoogle Scholar
  231. 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 PubMedCrossRefGoogle Scholar
  232. 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 PubMedCrossRefGoogle Scholar
  233. 233.
    Zhou JJ (2010) Odorant-binding proteins in insects. Vitam Horm 83:241–272. doi: 10.1016/S0083-6729(10)83010-9 PubMedCrossRefGoogle Scholar
  234. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  235. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  236. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  237. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  238. 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 PubMedCrossRefGoogle Scholar
  239. 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 PubMedCrossRefGoogle Scholar
  240. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  241. 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 PubMedCrossRefGoogle Scholar
  242. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  243. 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 PubMedCrossRefGoogle Scholar
  244. 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 PubMedCrossRefGoogle Scholar
  245. 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 PubMedCrossRefGoogle Scholar
  246. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  247. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  248. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  249. 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 PubMedCrossRefGoogle Scholar
  250. 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 PubMedCrossRefGoogle Scholar
  251. 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 PubMedPubMedCentralGoogle Scholar
  252. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  253. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  254. 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 PubMedCrossRefGoogle Scholar
  255. 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 PubMedCrossRefGoogle Scholar
  256. 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 PubMedCrossRefGoogle Scholar
  257. 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 PubMedCrossRefGoogle Scholar
  258. 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 PubMedCrossRefGoogle Scholar
  259. 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 PubMedCrossRefGoogle Scholar
  260. 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 PubMedCrossRefGoogle Scholar
  261. 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 PubMedCrossRefGoogle Scholar
  262. 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 PubMedCrossRefGoogle Scholar
  263. 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 PubMedCrossRefGoogle Scholar
  264. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  265. 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 PubMedCrossRefGoogle Scholar
  266. 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 PubMedCrossRefGoogle Scholar
  267. 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 PubMedCrossRefGoogle Scholar
  268. 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 PubMedCrossRefGoogle Scholar
  269. 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 PubMedCrossRefGoogle Scholar
  270. 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 PubMedCrossRefGoogle Scholar
  271. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  272. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  273. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  274. 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 PubMedCrossRefGoogle Scholar
  275. 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 PubMedCrossRefGoogle Scholar
  276. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  277. 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 PubMedCrossRefGoogle Scholar
  278. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  279. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  280. 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 PubMedCrossRefGoogle Scholar
  281. 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 PubMedCrossRefGoogle Scholar
  282. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  283. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  284. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  285. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  286. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  287. 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 PubMedCrossRefGoogle Scholar
  288. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  289. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  291. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  292. 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 PubMedPubMedCentralGoogle Scholar
  293. 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. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  295. 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 PubMedCrossRefGoogle Scholar
  296. 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 PubMedCrossRefGoogle Scholar
  297. 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

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Animal Physiology, Institute of Biology/ZoologyMartin Luther University Halle-WittenbergHalle (Saale)Germany
  2. 2.Institute of PhysiologyUniversity of HohenheimStuttgartGermany

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