Skip to main content
SpringerLink
Log in

Expression Profiles and Biochemical Analysis of Chemosensory Protein 3 from Nilaparvata lugens (Hemiptera: Delphacidae)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Insects have evolved highly sensitive olfactory sensory systems to detect plant hosts and mates, with plant volatiles playing an important role in informing insect behavior. Chemosensory proteins (CSPs) are thought to play a key role in this process, but in this respect, there is limited information on brown planthopper Nilaparvata lugens, one of the most destructive pests of rice. To expand our understanding of CSP function in N. lugens we explored expression profiles and binding characteristics of NlugCSP3. The ligands with higher binding affinity were also validated by molecular docking and behavioral assays. NlugCSP3 mRNA was expressed at relatively higher levels in antennae and abdomen of 3-day-old unmated macropterous males as well as in antennae of 3-day mated macropterous and brachypterous females. Fluorescence competitive binding assays revealed that 5 out of 25 candidate volatiles are strong binders (Ki < 10 μM). Behavioral assays revealed that nonadecane and 2-tridecanone, which have high binding affinities in fluorescence competition-binding assays, displayed strong attractiveness to N. lugens. Pursuing this further, molecular docking analysis identified key amino acid residues involved in binding volatile compounds. Overall, our data provide a base for further investigation of the potential physiological functions of CSP3 in Nilaparvata lugens, and extend the function of NlugCSP3 in chemoreception of N. lugens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 33:10741–10749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Angeli S et al (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262:745–754

    CAS  PubMed  Google Scholar 

  • Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl 123:1–11

    Google Scholar 

  • Ban L, Scaloni A, D’Ambrosio C, Zhang L, Yan Y, Pelosi P (2003) Biochemical characterization and bacterial expression of an odorant binding protein from Locusta migratoria. Cell Mol Life Sci 60:390–400

    CAS  PubMed  Google Scholar 

  • Bos JI, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus Persicae (Green Peach Aphid). PLoS Genet 6:e1001216

    PubMed  PubMed Central  Google Scholar 

  • Bottrell DG, Schoenly KG (2012) Resurrecting the ghost of green revolutions past: the brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J Asia Pac Entomol 15:122–140

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cheng XL, Zhu L, He G (2013) Towards understanding of molecular interactions between rice and the brown planthopper. Mol Plant 6:621–634

    CAS  PubMed  Google Scholar 

  • Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338

    CAS  PubMed  Google Scholar 

  • Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830–1834

    CAS  PubMed  Google Scholar 

  • Dani FR et al (2011) Odorant-binding proteins and chemosensory proteins in pheromone detection and release in the silkmoth Bombyx mori. Chem Senses 36:335–344

    CAS  PubMed  Google Scholar 

  • Duan SG, Li DZ, Wang MQ (2019) Chemosensory protein used as target for screening behaviourally active compounds in rice pest Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Insect Mol Biol 28:123–135

    CAS  PubMed  Google Scholar 

  • Forêt S, Wanner KW, Maleszka R (2007) Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochem Mol Biol 37:19–28

    PubMed  Google Scholar 

  • Frati F, Salerno G, Conti E, Bin F (2008) Role of the plant conspecific complex in host location and intra-specific communication of Lygus rugulipennis. Physiol Entomol 33:129–137

    Google Scholar 

  • Gadenne C, Dufour MC, Anton S (2001) Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect. Proc R Soc Lond B 268:1631–1635

    CAS  Google Scholar 

  • Gadenne C, Barrozo RB, Anton S (2016) Plasticity in insect olfaction: to smell or not to smell? Annu Rev Entomol 61:317–333

    CAS  PubMed  Google Scholar 

  • Gholizadeh S et al (2015) The Anopheles stephensi odorant binding protein 1 (AsteOBP1) gene: a new molecular marker for biological forms diagnosis. Acta Trop 146:101–113

    CAS  PubMed  Google Scholar 

  • Hanwell MD, Curtis DE, Lonie DC, Vandermeersch T, Zurek E, Hutchison GR (2012) Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J Cheminform 4:17

    CAS  PubMed  PubMed Central  Google Scholar 

  • He P, Zhang J, Liu NY, Zhang YN, Yang K, Dong SL (2011) Distinct expression profiles and different functions of odorant binding proteins in Nilaparvata lugens Stal. PLoS One 6:e28921

    CAS  PubMed  PubMed Central  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 

  • Hooper AM et al (2009) High-throughput ESI-MS analysis of binding between the Bombyx mori pheromone-binding protein BmorPBP1, its pheromone components and some analogues. Chem Commun 38:5725–5727

    Google Scholar 

  • Hua JF, Zhang S, Cui JJ, Wang DJ, Wang CY, Luo JY, Lv LM, Ma Y (2013) Functional characterizations of one odorant binding protein and three chemosensory proteins from Apolygus lucorum (Meyer-Dur) (Hemiptera: Miridae) legs. J Insect Phys 59:690–696

  • Jean-François P (2014) Renaming Bombyx mori chemosensory proteins. Int J Bioorg Chem Mol Biol 2:1–4

    Google Scholar 

  • Jiang X, Pregitzer P, Grosse-Wilde E, Breer H, Krieger J (2016) Identification and characterization of two "Sensory Neuron Membrane Proteins" (SNMPs) of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). J Insect Sci 16:33

    PubMed  PubMed Central  Google Scholar 

  • Khoo KM, Chang CF, Schubert J, Wondrak JE, Chng HH (2005) Expression and purification of the recombinant His-tagged GST-CD38 fusion protein using the baculovirus/insect cell expression system. Protein Expr Purif 40:396–403

    CAS  PubMed  Google Scholar 

  • Knecht ZA et al (2017) Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila. eLife 6:e26654

    PubMed  PubMed Central  Google Scholar 

  • Kulmuni J, Havukainen H (2013) Insights into the evolution of the CSP gene family through the integration of evolutionary analysis and comparative protein modeling. PLoS One 8:e63688

    CAS  PubMed  PubMed Central  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 

  • Laughlin JD, Ha TS, Jones DNM, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133:1255–1265

    CAS  PubMed  PubMed Central  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 

  • Li H, Zhang L, Ni C, Shang H, Zhuang S, Li J (2013) Molecular recognition of floral volatile with two olfactory related proteins in the eastern honeybee (Apis cerana). Int J Biol Macromol 56: 114–121

  • Li QL et al (2018a) Optimization of reverse chemical ecology method: false positive binding of Aenasius bambawalei odorant binding protein 1 caused by uncertain binding mechanism. Insect Mol Biol 27:305–318

  • Li ZQ, Zhang S, Luo JY, Cui JJ, Ma Y, Dong SL (2018b) Two minus-C odorant binding proteins from Helicoverpa armigera display higher ligand binding affinity at acidic pH than neutral pH. J Insect Physiol 59:263–272

  • Liu R, He X, Lehane S, Lehane M, Hertz-Fowler C, Berriman M (2012) Expression of chemosensory proteins in the tsetse fly Glossina morsitans morsitans is related to female host-seeking behaviour. Insect Mol Biol 21: 41–48

  • Liu Z, Smagghe G, Lei Z, Wang JJ (2016) Identification of male- and female-specific olfaction genes in antennae of the oriental fruit fly (Bactrocera dorsalis). PLoS One 11:e0147783

    PubMed  PubMed Central  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Ma M, Chang MM, Lei CL, Yang FL (2016) A garlic substance disrupts odorant-binding protein recognition of insect pheromones released from adults of the Angoumois grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Mol Biol 25:530–540

    CAS  PubMed  Google Scholar 

  • Maleszka J, Forêt S, Saint R, Maleszka R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol 217:189–196

    CAS  PubMed  Google Scholar 

  • McKenna M, Hekmat-Scafe D, Gaines P, Carlson J (1994) Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system. J Biol Chem 269:16340–16347

    CAS  PubMed  Google Scholar 

  • Mechaber WL, Capaldo CT, Hildebrand JG (2002) Behavioral responses of adult female tobacco hornworms, Manduca sexta, to host plant volatiles change with age and mating status. J Insect Sci 2:1–8

    Google Scholar 

  • Ming H, Peng H (2014) Molecular characterization, expression profiling, and binding properties of odorant binding protein genes in the whitebacked planthopper, Sogatella furcifera. Comp Biochem Physiol B Biochem Mol Biol 174:1–8

    Google Scholar 

  • Ni L et al (2016) The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila. eLife 5:e13254

    PubMed  PubMed Central  Google Scholar 

  • Obata T, Koh HS, Kim M, Fukami H (1983) Constituents of planthopperattractant in rice plant. Appl Entomol Zool 18:161–169

  • Oduol F, Xu J, Niare O, Natarajan R, Vernick KD (2000) Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria. Proc Natl Acad Sci U S A 97:11397–11402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pelosi P, Calvello M, Ban L (2005) Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem Senses 30:291–292

    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 

  • Pesenti ME et al (2009) Queen bee pheromone binding protein pH induced domain swapping favors pheromone release. J Mol Biol 390:981–990

    CAS  PubMed  Google Scholar 

  • Picimbon JF, Dietrich K, Breer H, Krieger J (2000) Chemosensory proteins of Locusta migratoria (Orthoptera: Acrididae). Insect Biochem Mol Biol 30:233–241

    CAS  PubMed  Google Scholar 

  • Picimbon JF, Dietrich K, Krieger J, Breer H (2001) Identity and expression pattern of chemosensory proteins in Heliothis virescens (Lepidoptera, Noctuidae). Insect Biochem Mol Biol 31:1173–1181

    CAS  PubMed  Google Scholar 

  • Qiao HL, Deng PY, Li DD, Chen M, Jiao ZJ, Liu ZC, Zhang YZ, Kan YC (2013) Expression analysis and binding experiments of chemosensory proteins indicate multiple roles in Bombyx mori. J Insect Physiol 59: 667–675

  • 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 49:47–61

    CAS  PubMed  Google Scholar 

  • Sanchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity 103:208–216

    CAS  PubMed  Google Scholar 

  • Saxena R, Okech S (1985) Role of plant volatiles in resistance of selected rice varieties to brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). J Chem Ecol 11:1601–1616

    CAS  PubMed  Google Scholar 

  • Scaloni A, Monti M, Angeli S, Pelosi P (1999) Structural analysis and disulfide-bridge pairing of two odorant-binding proteins from Bombyx mori. Biochem Biophys Res Commun 266:386–391

    CAS  PubMed  Google Scholar 

  • Sun X et al (2014) Electrophysiological responses of the rice leaf folder, Cnaphalocrocis medinalis, to rice plant volatiles. J Insect Sci 14:70

    PubMed  PubMed Central  Google Scholar 

  • Sun SF, Zeng FF, Yi SC, Wang MQ (2019) Molecular screening of behaviorally active compounds with CmedOBP14 from the rice leaf folder Cnaphalocrocis medinalis. J Chem Ecol. https://doi.org/10.1007/s10886-019-01106

  • Thompson J (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Google Scholar 

  • Tian Z, Zhang Y (2016) Molecular characterization and functional analysis of pheromone binding protein 1 from Cydia pomonella (L.). Insect Mol Biol 25:769–777

    CAS  PubMed  Google Scholar 

  • Tomaselli S et al (2006) Solution structure of a chemosensory protein from the desert locust Schistocerca gregaria. Biochemistry 45:10606–10613

    CAS  PubMed  Google Scholar 

  • Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    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, Prestwich GD (1985) Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea polyphemus. Proc Natl Acad Sci U S A 82:8827–8831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736

    CAS  PubMed  Google Scholar 

  • Waris MI et al (2018a) Silencing of chemosensory protein gene NlugCSP8 by RNAi induces declining behavioral responses of Nilaparvata lugens. Front Physiol 9:379

    PubMed  PubMed Central  Google Scholar 

  • Waris MI et al (2018b) The role of chemosensory protein 10 in the detection of behaviorally active compounds in brown planthopper. Nilaparvata lugens Insect Sci. https://doi.org/10.1111/1744-7917.12659

  • Williams L, Blackmer J, Rodriguez-Saona C, Zhu S (2010) Plant volatiles influence electrophysiological and behavioral responses of Lygus hesperus. J Chem Ecol 36:467–478

    CAS  PubMed  Google Scholar 

  • Xiao S, Sun JS, Carlson JR (2019) Robust olfactory responses in the absence of odorant binding proteins. Elife 8:e51040

    PubMed  PubMed Central  Google Scholar 

  • Xu P, 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 

  • Xu YL et al (2009) Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects. BMC Genomics 10:632

    PubMed  PubMed Central  Google Scholar 

  • Yang K, He P, Dong SL (2014) Different expression profiles suggest functional differentiation among chemosensory proteins in Nilaparvata lugens (Hemiptera: Delphacidae). J Insect Sci 14:270

    PubMed  PubMed Central  Google Scholar 

  • Ye W et al (2017) A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice. Sci Rep 7:40498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yi SY, Li DZ, Zhou CX, Tang YL, Abdelnabby HE, Wang MQ (2018) Screening behaviorally active compounds based on fluorescence quenching in combination with binding mechanism analyses of SspOBP7, an odorant binding protein from Sclerodermus sp. Int J Biol Macromol 107:2667–2678

    CAS  PubMed  Google Scholar 

  • Yoshizawa Y et al (2011) Ligand carrier protein genes expressed in larval chemosensory organs of Bombyx mori. Insect Biochem Mol Biol 41:545–562

    CAS  PubMed  Google Scholar 

  • Younas A et al (2018a) Functional analysis of the chemosensory protein MsepCSP8 from the oriental armyworm Mythimna separate. Front Physiol 9:872

    PubMed  PubMed Central  Google Scholar 

  • Younas A et al (2018b) A chemosensory protein MsepCSP5 involved in chemoreception of oriental armyworm Mythimna separate. Int J Biol Macromol 14:1935–1949

    CAS  Google Scholar 

  • Yu SJ (1995) Allelochemical stimulation of ecdysone 20-monooxygenase in fall armyworm larvae. Arch Int Physiol Biochim 28:365–375

    CAS  Google Scholar 

  • Zeng FF, Liu H, Zhang A, Lu ZX, Leal WS, Abdelnabby H, Wang MQ (2018) Three chemosensory proteins from the rice leaf folder Cnaphalocrocis medinalis involved in host volatile and sex pheromone reception. Insect Mol Biol 27:710-723

    CAS  PubMed  Google Scholar 

  • Zhang ZQ (1983) A study on the development of wing dimorphism in the rice brown planthopper, Nilaparvata lugens Stal. Acta Entomol Sin 26:260–267

    Google Scholar 

  • Zhang YN, Ye ZF, Yang K, Dong SL (2014) Antenna-predominant and male-biased CSP19 of Sesamia inferens is able to bind the female sex pheromones and host plant volatiles. Gene 536:279–286

    CAS  PubMed  Google Scholar 

  • Zhang L, Lu Y, Xiang M, Shang Q, Gao X (2016) The retardant effect of 2-tridecanone, mediated by cytochrome P450, on the development of cotton bollworm, Helicoverpa armigera. BMC Genomics 17:954

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Ding J, Zhang Z, Liu F, Zhou C, Mu W (2018) Sex- and tissue-specific expression profiles of odorant binding protein and chemosensory protein genes in Bradysia odoriphaga (Diptera: Sciaridae). Front Physiol 9:107

    PubMed  PubMed Central  Google Scholar 

  • Zheng ZC, Li DZ, Zhou AM, Yi SC, Liu H, Wang MQ (2016) Predicted structure of a Minus-C OBP from Batocera horsfieldi (Hope) suggests an intermediate structure in evolution of OBPs. Sci Res 6:33981

    CAS  Google Scholar 

  • Zhou S, Sun Z, Ma Z, Chen W, Wang MQ (2014) De novo analysis of the Nilaparvata lugens (Stål) antenna transcriptome and expression patterns of olfactory genes. Comp Biochem Physiol Part D Genomics Proteomics 9:31–39

    CAS  PubMed  Google Scholar 

  • Zhu J et al (2016) Conserved chemosensory proteins in the proboscis and eyes of Lepidoptera. Int J Biol Sci 12:1394–1404

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported and funded by the National Key Research and Development Program (2016YFD0200807), the Special Fund for Agro-scientific Research in the Public Interest of China (201403030), and the Special Technical Innovation of Hubei Province (2017ABA146).

Author information

Authors and Affiliations

  1. Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Muhammad Irfan Waris, Aneela Younas & Man-Qun Wang

  2. Department of Entomology, Faculty of Agriculture, Gomal University, Dera Ismail Khan, Pakistan

    Muhammad Irfan Waris

  3. Department of Agronomy, Faculty of Agriculture, Gomal University, Dera Ismail Khan, Pakistan

    Asif Ameen

  4. National Center for Bioinformatics, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan

    Fatima Rasool

Authors
  1. Muhammad Irfan Waris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aneela Younas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asif Ameen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fatima Rasool
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Man-Qun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Man-Qun Wang.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Electronic supplementary material

ESM 1

(DOCX 21 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Waris, M.I., Younas, A., Ameen, A. et al. Expression Profiles and Biochemical Analysis of Chemosensory Protein 3 from Nilaparvata lugens (Hemiptera: Delphacidae). J Chem Ecol 46, 363–377 (2020). https://doi.org/10.1007/s10886-020-01166-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01166-6

Keywords

Search

Navigation