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Identification of odorant-binding proteins and functional analysis of antenna-specific AplaOBP1 in the emerald ash borer, Agrilus planipennis

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Abstract

Olfaction-based strategies have been successfully applied to monitor the emerald ash borer Agrilus planipennis Fairmaire (Coleoptera: Buprestidae); however, roles of chemosensory-associated proteins in olfactory perception of A. planipennis are rarely reported. Here, we identified 11 odorant-binding proteins (OBPs) from the A. planipennis transcriptome and genome. Sequence and phylogenetic analyses revealed that A. planipennis OBPs (AplaOBPs) could be classified into four subfamilies. The reverse transcription PCR (RT-PCR) analysis showed that all three members of the ABPII, one plus-C OBP, and one minus-C OBP were specifically or predominantly expressed in the antennae of both sexes, indicating their possible involvement in chemoreception. Subsequently, an antenna-specific OBP, AplaOBP1, was investigated through in situ hybridization, immunocytochemistry, and fluorescent competitive binding assays. It was found that the AplaOBP1 gene was detected under the base of the antennal sensilla, and the AplaOBP1 protein was expressed in the lymph of multiparous sensilla basiconica types I and III. In vitro, recombinant AplaOBP1 exhibited high binding affinities (Ki = 3.38–9.25 μM) with nine volatiles including five host-tree terpenes (e.g., myrcene, limonene, nerolidol, α-farnesene, and ocimene), which indicated that AplaOBP1 might be involved in the detection of host volatiles. The electrophysiological activities of all AplaOBP1 ligands were further confirmed using electroantennography, whose results imply that these volatiles may act as putative semiochemicals for A. planipennis. In conclusion, our results provide valuable insights into the molecular basis of olfaction in A. planipennis and help us use OBPs as targets to design novel olfactory regulators for management of A. planipennis.

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References

  • Antony B, Soffan A, Jakše J, Abdelazim MM, Aldosari SA, Aldawood AS, Pain A (2016) Identification of the genes involved in odorant reception and detection in the palm weevil Rhynchophorus ferrugineus, an important quarantine pest, by antennal transcriptome analysis. BMC Genom 17:69

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Bruce TJ, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    CAS  PubMed  Google Scholar 

  • Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    PubMed  Google Scholar 

  • Crook DJ, Kerr LM, Mastro VC (2008a) Distribution and fine structure of antennal sensilla in emerald ash borer (Coleoptera: Buprestidae). Ann Entomol Soc Am 101:1103–1111

    Google Scholar 

  • Crook DJ, Khrimian A, Francese JA, Fraser I, Poland TM, Sawyer AJ, Mastro VC (2008b) Development of a host-based semiochemical lure for trapping emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae). Environ Entomol 37:356–365

    CAS  PubMed  Google Scholar 

  • Cui XN (2018) Behavioral responses of Agrilus mali to host plant volatiles and function of related olfactory genes. Dissertation, Northwest A & F University

  • Dippel S, Oberhofer G, Kahnt J, Gerischer L, Opitz L, Schachtner J, Stanke M, Schütz S, Wimmer EA, Angeli S (2014) Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions. BMC Genom 15:1–14

    Google Scholar 

  • Dweck HK, Ebrahim SA, Thoma M, Mohamed AA, 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 112:2829–2835

    Google Scholar 

  • Ebrahim SA, Dweck HK, Stökl J, Hofferberth JE, Trona F, Weniger K, Rybak J, Seki Y, Stensmyr MC, Sachse S (2015) Drosophila avoids parasitoids by sensing their semiochemicals via a dedicated olfactory circuit. PLoS Biol 13:e1002318

    PubMed  PubMed Central  Google Scholar 

  • Feng SY, Filomena DB, Li QH, Immacolata I, Xiang YS, Yun L, Lea R, Donatella B, Patrizia F, Ling YX (2012) Two odorant-binding proteins mediate the behavioural response of aphids to the alarm pheromone (E)-β-farnesene and structural analogues. PLoS ONE 7:e32759

    Google Scholar 

  • Forêt S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16:1404–1413

    PubMed  PubMed Central  Google Scholar 

  • Gitau CW, Bashford R, Carnegie AJ, Gurr GM (2013) A review of semiochemicals associated with bark beetle (Coleoptera: Curculionidae: Scolytinae) pests of coniferous trees: a focus on beetle interactions with other pests and their associates. For Ecol Manage 297:1–14

    Google Scholar 

  • 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:e1001546

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Genom 10:332

    Google Scholar 

  • Gong Y, Tang H, Bohne C, Plettner E (2010) Binding conformation and kinetics of two pheromone-binding proteins from the Gypsy moth Lymantria dispar with biological and nonbiological ligands. Biochemistry 49:793–801

    CAS  PubMed  Google Scholar 

  • Grant GG, Ryall KL, Lyons DB, Abouzaid MM (2010) Differential response of male and female emerald ash borers (Col., Buprestidae) to (Z)-3-hexenol and manuka oil. J Appl Entomol 134:26–33

    CAS  Google Scholar 

  • Grant GG, Poland TM, Tina C, Barry Lyons D, Jones GC (2011) Comparison of male and female emerald ash borer (Coleoptera: Buprestidae) responses to phoebe oil and (Z)-3-hexenol lures in light green prism traps. J Econ Entomol 104:173

    CAS  PubMed  Google Scholar 

  • Gu XC, Zhang YN, Kang K, Dong SL, Zhang LW (2015) Antennal transcriptome analysis of odorant reception genes in the red turpentine beetle (RTB), Dendroctonus valens. PLoS ONE 10:e0125159

    PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711

    CAS  PubMed  Google Scholar 

  • 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 12:1357–1369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30

    CAS  PubMed  Google Scholar 

  • Huang GZ, Liu JT, Zhou JJ, Wang Q, Dong JZ, Zhang YJ, Li XC, Li J, Gu SH (2018) Expressional and functional comparisons of two general odorant binding proteins in Agrotis ipsilon. Insect Biochem Mol Biol 98:34–47

    CAS  PubMed  Google Scholar 

  • Jiang X, Ryl M, Krieger J, Breer H, Pregitzer P (2018) Odorant binding proteins of the desert locust Schistocerca gregaria (Orthoptera, Acrididae): topographic expression patterns in the antennae. Front Physiol 9:417

    PubMed  PubMed Central  Google Scholar 

  • Jun D, Tim L, Daniel D, Michel C, Kees V, Omprakash M, Krell PJ, Guoxing Q (2015) Transcriptome analysis of the emerald ash borer (EAB), Agrilus planipennis: de novo assembly, functional annotation and comparative analysis. PLoS ONE 10:e0134824

    Google Scholar 

  • Kaissling KE, Hildebrand JG, Tumlinson JH (1989) Pheromone receptor cells in the male moth Manduca sexta. Arch Insect Biochem Physiol 10:273–279

    CAS  Google Scholar 

  • Krieger J, von Nickisch-Rosenegk E, Mameli M, Pelosi P, Breer H (1996) Binding proteins from the antennae of Bombyx mori. Insect Biochem Mol Biol 26:297–307

    CAS  PubMed  Google Scholar 

  • Larter NK, Sun JS, Carlson JR (2016) Organization and function of Drosophila odorant binding proteins. eLife 5:e20242

    PubMed  PubMed Central  Google Scholar 

  • Laue M, Steinbrecht R, Ziegelberger G (1994) Immunocytochemical localization of general odorant-binding protein in olfactory sensilla of the silkmoth Antheraea polyphemus. Naturwissenschaften 81:178–180

    CAS  Google Scholar 

  • Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391

    CAS  PubMed  Google Scholar 

  • Leal WS, Chen AM, Ishida Y, Chiang VP, Erickson ML, Morgan TI, Tsuruda JM (2005) Kinetics and molecular properties of pheromone binding and release. Proc Natl Acad Sci USA 102:5386–5391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li KM, Wang SN, Zhang K, Ren LY, Ali A, Zhang YJ, Zhou JJ, Guo YY (2014) Odorant binding characteristics of three recombinant odorant binding proteins in Microplitis mediator (Hymenoptera: Braconidae). J Chem Ecol 40:541–548

    CAS  PubMed  Google Scholar 

  • Maida R, Steinbrecht A, Ziegelberger G, Pelosi P (1993) The pheromone binding protein of Bombyx mori: purification, characterization and immunocytochemical localization. Insect Biochem Mol Biol 23:243–253

    CAS  Google Scholar 

  • Maida R, Mameli M, Müller B, Krieger J, Steinbrecht RA (2005) The expression pattern of four odorant-binding proteins in male and female silk moths, Bombyx mori. J Neurocytol 34:149–163

    CAS  PubMed  Google Scholar 

  • Mamidala P, Wijeratne AJ, Wijeratne S, Poland T, Qazi SS, Doucet D, Cusson M, Beliveau C, Mittapalli O (2013) Identification of odor-processing genes in the emerald ash borer, Agrilus planipennis. PLoS ONE 8:e56555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mattiacci L, Dicke M (1995) The parasitoid Cotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its host Pieris brassicae, on the basis of contact cues from frass, silk, and herbivore-damaged leaf tissue. J Insect Behav 8:485–498

    Google Scholar 

  • Metcalf RL, Kogan M (1987) Plant volatiles as insect attractants. Crit Rev Plant Sci 5:251–301

    CAS  Google Scholar 

  • Miller DR (2007) Limonene: attractant kairomone for white pine cone beetles (Coleoptera: Scolytidae) in an eastern white pine seed orchard in western North Carolina. J Econ Entomol 100:815–822

    CAS  PubMed  Google Scholar 

  • Morin RS, Liebhold AM, Pugh SA, Crocker SJ (2017) Regional assessment of emerald ash borer, Agrilus planipennis, impacts in forests of the Eastern United States. Biol Invasions 19:703–711

    Google Scholar 

  • Nunez JA (1982) Food source orientation and activity in Rhodnius prolixus Stal (Hemiptera: Reduviidae). Bull Entomol Res 72:253–262

    Google Scholar 

  • Pelletier J, Guidolin A, Syed Z, Cornel AJ, Leal WS (2010) Knockdown of a mosquito odorant-binding protein involved in the sensitive detection of oviposition attractants. J Chem Ecol 36:245–248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pelosi P, Iovinella I, Felicioli A, Dani FR (2014) Soluble proteins of chemical communication: an overview across arthropods. Front Physiol 5:320

    PubMed  PubMed Central  Google Scholar 

  • Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev Camb Philos Soc 93:184–200

    PubMed  Google Scholar 

  • Pikielny CW, Hasan G, Rouyer F, Rosbash M (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12:35–49

    CAS  PubMed  Google Scholar 

  • Pitts RJ (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genom 12:271

    CAS  Google Scholar 

  • Rigsby CM, Mccartney NB, Herms DA, Tumlinson JH, Cipollini D (2017) Variation in the volatile profiles of black and Manchurian ash in relation to emerald ash borer oviposition preferences. J Chem Ecol 43:831–842

    CAS  PubMed  Google Scholar 

  • Rodriguez-Saona C, Poland TM, Miller JR, Stelinski LL, Grant GG, Groot PD, Buchan L, Macdonald L (2006) Behavioral and electrophysiological responses of the emerald ash borer, Agrilus planipennis, to induced volatiles of Manchurian ash, Fraxinus mandshurica. Chemoecology 16:75–86

    CAS  Google Scholar 

  • Schultze A, Schymura D, Forstner M, Krieger J (2012) Expression pattern of a ‘Plus-C’ class odorant binding protein in the antenna of the malaria vector Anopheles gambiae. Insect Mol Biol 21:187–195

    CAS  PubMed  Google Scholar 

  • Shanbhag SR, Smith DP, Steinbrecht RA (2005) Three odorant-binding proteins are co-expressed in sensilla trichodea of Drosophila melanogaster. Arthropod Struct Dev 34:153–165

    CAS  Google Scholar 

  • Steinbrecht RA (1997) Pore structures in insect olfactory sensilla: a review of data and concepts. Int J Insect Morphol Embryol 26:229–245

    Google Scholar 

  • Steinbrecht RA, Laue M, Ziegelberger G (1995) Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res 282:203–217

    CAS  Google Scholar 

  • Sun JS, Larter NK, Chahda JS, Rioux D, Gumaste A, Carlson JR (2018) Humidity response depends on the small soluble protein Obp59a in Drosophila. eLife 7:e39249

    PubMed  PubMed Central  Google Scholar 

  • Takken W (1991) The role of olfaction in host-seeking of mosquitoes: a review. Int J Trop Insect Sci 12:287–295

    Google Scholar 

  • Takken W, Knols BG (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44:131–157

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163

    CAS  PubMed  Google Scholar 

  • Vogt RG, Kohne AC, Dubnau JT, Prestwich GD (1989) Expression of pheromone binding proteins during antennal development in the gypsy moth Lymantria dispar. J Neurosci 9:3332–3346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Li DZ, Min SF, Mi F, Zhou SS, Wang MQ (2014) Analysis of chemosensory gene families in the beetle Monochamus alternatus and its parasitoid Dastarcus helophoroides. Comp Biochem Physiol Part D Genomics Proteomics 11:1–8

    PubMed  Google Scholar 

  • Wang SN, Shan S, Zheng Y, Peng Y, Lu ZY, Yang YQ, Li RJ, Zhang YJ, Guo YY (2017) Gene structure and expression characteristic of a novel odorant receptor gene cluster in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae). Insect Mol Biol 26:420–431

    CAS  PubMed  Google Scholar 

  • Wang SN, Shan S, Liu JT, Li RJ, Lu ZY, Dhiloo KH, Khashaveh A, Zhang YJ (2018) Characterization of antennal chemosensilla and associated odorant binding as well as chemosensory proteins in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae). Sci Rep 8:7649

    PubMed  PubMed Central  Google Scholar 

  • Xu PX, Atkinson R, Jones DN, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193–200

    CAS  PubMed  Google Scholar 

  • Ye ZF, Liu XL, Han Q, Liao H, Dong XT, Zhu GH, Dong SL (2017) Functional characterization of PBP1 gene in Helicoverpa armigera (Lepidoptera: Noctuidae) by using the CRISPR/Cas9 system. Sci Rep 7:8470

    PubMed  PubMed Central  Google Scholar 

  • Yin XW, Iovinella I, Marangoni R, Cattonaro F, Flamini G, Sagona S, Zhang L, Pelosi P, Felicioli A (2013) Odorant-binding proteins and olfactory coding in the solitary bee Osmia cornuta. Cell Mol Life Sci 70:3029–3039

    CAS  PubMed  Google Scholar 

  • Zacharuk RY (1980) Ultrastructure and function of insect chemosensilla. Annu Rev Entomol 25:27–47

    Google Scholar 

  • Zhang S, Chen LZ, Gu SH, Cui JJ, Gao XW, Zhang YJ, Guo YY (2011) Binding characterization of recombinant odorant-binding proteins from the parasitic wasp, Microplitis mediator (Hymenoptera: Braconidae). J Chem Ecol 37:189–194

    PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Beijing Natural Science Foundation (6184042), the Beijing Postdoctoral Research Foundation (2017-ZZ-083), and the Promotion and Innovation of Beijing Academy of Agriculture and Forestry Sciences (KJCX20180416).

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Correspondence to Fan Zhang or Yong-Jun Zhang.

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Wang, SN., Shan, S., Yu, GY. et al. Identification of odorant-binding proteins and functional analysis of antenna-specific AplaOBP1 in the emerald ash borer, Agrilus planipennis. J Pest Sci 93, 853–865 (2020). https://doi.org/10.1007/s10340-019-01188-4

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