Skip to main content
Log in

Three Chemosensory Proteins Involved in Chemoreception of Oedaleus asiaticus (Orthopera: Acridoidea)

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

Abstract

Chemosensory proteins (CSPs) are thought to play roles in the insect olfactory system by binding and carrying hydrophobic odorants across the aqueous sensillar lymph. The band-winged grasshopper, Oedaleus asiaticus Bei-Bienko, is one of the most important grasshopper pests in northern China, but there is little information about its olfactory system. In order to investigate the olfactory functions of CSPs in this pest, three CSP genes (OasiCSP4, OasiCSP11 and OasiCSP12) were expressed in Escherichia coli, and the binding affinities of the three recombinant CSP proteins were measured for 16 volatiles from the host plant (Stipa krylovii), fecal material and body of live adult O. asiaticus using fluorescence competitive binding assays. To further verify their olfactory functions, RNA interference (RNAi) and electrophysiological recording were conducted. The three recombinant proteins displayed different degrees of binding to various volatiles in ligand-binding assays, with OasiCSP12 having higher binding affinities for more volatiles than OasiCSP4 and OasiCSP11. OasiCSP12 exhibited strong binding affinities (Ki < 20 μΜ) for five host plant volatiles and one volatile from the live body of adult O. asiaticus. The transcript levels of the three OasiCSP genes were significantly lower after silencing the individual genes by RNAi, which in turn reduced the EAG responses in adults of both sexes to most tested compounds. Our study indicates that these three OasiCSPs are involved in the detection of volatile semiochemicals, and may play important roles in finding host plants and in aggregation in O. asiaticus.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Angeli S, Ceron F, Scaloni A, Monti M, Monteforti G, Minnocci PR, Pelosi P (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262:745–754

    Article  CAS  PubMed  Google Scholar 

  • Ban L, Scaloni A, Brandazza A, Angeli S, Zhang L, Yan Y, Pelosi P (2003) Chemosensory proteins of Locusta migratoria. Insect Mol Biol 12:125–134

    Article  CAS  PubMed  Google Scholar 

  • Benton R (2008) Chemical sensing in Drosophila. Curr Opin Neurobiol 18:357–363

    Article  CAS  PubMed  Google Scholar 

  • Briand L, Swasdipan N, Nespoulous C, Bezirard V, Blon F, Huet JC, Ebert P, Penollet JC (2002) Characterization of a chemosensory protein (ASP3c) from honeybee (Apis mellifera L.) as a brood pheromone carrier. Eur J Biochem 269:4586–4596

    Article  CAS  PubMed  Google Scholar 

  • Campanacci V, Krieger J, Bette S, Sturgis JN, Lartigue A, Cambillau C, Breer H, Tegoni M (2001) Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. J Biol Chem 276:20078–20084

    Article  CAS  PubMed  Google Scholar 

  • Campanacci V, Lartigue A, Hallberg BM, Jones TA, Giudici-Orticoni MT, Tegoni M, Cambillau C (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. PNAS 100:5069–5074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cease AJ, Hao S, Kang L, Elser JJ, Harrison JF (2010) Are color or high rearing density related to migratory polyphenism in the band-winged grasshopper, Oedaleus asiaticus? J Insect Physiol 56:926–936

    Article  CAS  PubMed  Google Scholar 

  • Chen HH, Kang L (2000) Olfactory responses of two species of grasshoppers to plant odours. Entomol Exp Appl 95:129–134

    Article  Google Scholar 

  • Chen H, Zhao Y, Kang L (2004) Comparison of the olfactory sensitivity of two sympatric steppe grasshopper species (Orthoptera: Acrididae) to plant volatile compounds. Science in China C: Life Sci 47:115–123

    Article  CAS  Google Scholar 

  • Cheng D, Lu Y, Zeng L, Liang G, He X (2015) Si-CSP9 regulates the integument and moulting process of larvae in the red imported fire ant, Solenopsis invicta. Sci Rep 5:9245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das A, Lee SH, Hyun TK, Kim SW, Kim JY (2013) Plant volatiles as method of communication. Plant Biotech Rep 7:9–26

    Article  Google Scholar 

  • Dong Z, Li HX, Meng RX, Shi L, Feng SJ, Meng HW (2011) Electrophysiological responses in the grasshopper Oedaleus asiaticus (Orthoptera: Acrididae) to volatiles from female adult feces. Acta Agric Boreali-Sin 26:124–128

    Google Scholar 

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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Gao S, Han H, Wang N, Xu L, Liu A, Temuer (2016) Morphometric analyses of gregarious and solitarious phases of Oedaleus asiaticus. Plant Prot 42:89–93

    Google Scholar 

  • Gong DP, Zhang HJ, Zhao P, Lin Y, Xia QY, Xiang ZH (2007) Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Bioch Mol Biol 37:266–277

    Article  CAS  Google Scholar 

  • Gong L, Luo Q, Rizwan-ul-Haq M, Hu MY (2012) Cloning and characterization of three chemosensory proteins from Spodoptera exigua and effects of gene silencing on female survival and reproduction. Bull Entomol Res 102:600–609

    Article  CAS  PubMed  Google Scholar 

  • González D, Zhao Q, McMahan C, Velasquez D, Haskins WE, Sponsel V, Cassill A, Renthal R (2009) The major antennal chemosensory protein of red imported fire ant workers. Insect Mol Biol 18:395–404

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu SH, Wu KM, Guo YY, Pickett JA, Field LM, Zhou JJ, Zhang YJ (2013) Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genomics 14:636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan JQ, Wei ZZ (1989) Determination of food intake in Oedaleus asiaticus. Chin Bull Entom 26:8–10

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hassanali A, Njagi PG, Bashir MO (2005) Chemical ecology of locusts and related acridids. Annu Rev Entomol 50:223–245

    Article  CAS  PubMed  Google Scholar 

  • Huang X, McNeill M, Zhang Z (2016) Quantitative analysis of plant consumption and preference by Oedaleus asiaticus (Acrididae: Oedipodinae) in changed plant communities consisting of three grass species. Environ Entomol 45:163–170

    Article  CAS  PubMed  Google Scholar 

  • Huang XB, McNeill MR, Ma JC, Qin XH, Tu XB, Cao GC, Wang GJ, Nong XQ (2017) Biological and ecological evidences suggest Stipa krylovii (Pooideae), contributes to optimal growth performance and population distribution of the grasshopper Oedaleus asiaticus. Bull Entomol Res 107:401–409

    Article  CAS  PubMed  Google Scholar 

  • Iovinella I, Bozza F, Caputo B, Della TA, Pelosi P (2013) Ligand-binding study of Anopheles gambiae chemosensory proteins. Chem Senses 38:409–419

    Article  CAS  PubMed  Google Scholar 

  • Jin X, Zhang S, Zhang L (2006) Expression of odorant-binding and chemosensory proteins and spatial map of chemosensilla on labial palps of Locusta migratoria (Orthoptera: Acrididae). Arthrop Struct Devel 35:47–56

    Article  CAS  Google Scholar 

  • Kaissling KE (2009) Olfactory perireceptor and receptor events in moths: a kinetic model revised. J Comp Physiol A 195:895–922

    Article  CAS  Google Scholar 

  • Kang L, Chen YL (1994) Trophic niche of steppe grasshoppers. Acta Entomol Sin 37:178–189

    Google Scholar 

  • Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li HX, Dong Z, Meng RX, Wei CG, Feng SJ, Meng HW (2011) The chemical analysis of volatiles from live adults of Oedaleus asiaticus B.-Bienko (Orthoptera: Acrididae). J Inner Mongolia Agric Univ 32:68–71

    Google Scholar 

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

    Article  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). Devel Genes Evol 217:189–196

    Article  CAS  Google Scholar 

  • Mamta B, Rajam MV (2017) RNAi technology: a new platform for crop pest control. Physiol Mol Biol Plants 23:487–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nomura A, Kawasaki K, Kubo T, Natori S (1992) Purification and localization of p10, a novel protein that increases in nymphal regenerating legs of Periplaneta americana American cockroach. Int J Devel Biol 36:391–398

    CAS  Google Scholar 

  • Obeng-Ofori D, Torto B, Njagi PGN, Hassanali A, Amiani H (1996) Fecal volatile as part of the aggregation pheromone complex of the desert locust, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). J Chem Ecol 20:2077–2087

    Article  Google Scholar 

  • Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and nonnestmate discrimination by a chemosensory sensillum. Science 309:311–314

    Article  CAS  PubMed  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

    Article  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

    Article  CAS  Google Scholar 

  • Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63:1658–1676

    Article  CAS  PubMed  Google Scholar 

  • Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR (2017) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev Camb Phil Soc 93:184–200

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shi WP, Sun HL, Edward N, Yan YH (2011) Fecal volatile components elicit aggregation in the oriental migratory locust, Locusta migratoria manilensis (Orthoptera: Acrididae). Insect Sci 18:166–174

    Article  CAS  Google Scholar 

  • Sun H, Guan L, Feng H, Yin J, Cao Y, Xi J, Li K (2014) Functional characterization of chemosensory proteins in the scarab beetle, Holotrichia oblita Faldermann (Coleoptera: Scarabaeida). PLoS One 9:e107059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Torto B, Obeng-Ofori D, Njagi PGN, Hassanali A, Amiani H (1994) Aggregation pheromone system of adult gregarious desert locust, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). J Chem Ecol 20:1749–1762

    Article  CAS  PubMed  Google Scholar 

  • Torto B, Njagi PGN, Hassanali A, Amiani H (1996) Aggregation pheromone system of nymphal gregarious desert locust, Schistocerca gregaria (Forskal). J Chem Ecol 22:2273–2281

    Article  CAS  PubMed  Google Scholar 

  • Vogt RG, Rogers ME, Franco MD, Sun M (2002) A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J Exp Biol 205:719–744

    Article  CAS  PubMed  Google Scholar 

  • Waris MI, Younas A, ul Qamar MT, Hao L, Ameen A, Ali S, Abdelnabby HE, Zeng FF, Wang MQ (2018) Silencing of chemosensory protein gene NlugCSP8 by RNAi induces declining behavioral responses of Nilaparvata lugens. Front Physiol 9:379

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang RN, Li DZ, Yu G, Yi SC, Zhang Y, Kong DX, Wang MQ (2017) Structural transformation detection contributes to screening of behaviorally active compounds: dynamic binding process analysis of DhelOBP21 from Dastarcus helophoroides. J Chem Ecol 43:1033–1045

    Article  CAS  PubMed  Google Scholar 

  • Yi X, Wang P, Wang Z, Cai J, Hu M, Zhong G (2014) Involvement of a specific chemosensory protein from Bactrocera dorsalis in perceiving host plant volatiles. J Chem Ecol 40:267–275

    Article  CAS  PubMed  Google Scholar 

  • Younas A, Waris MI, ul Qamar MT, Shaaban M, Prager SM, Wang MQ (2018a) Functional analysis of the chemosensory protein MsepCSP8 from the oriental armyworm Mythimna separata. Front Physiol 9:872

    Article  PubMed  PubMed Central  Google Scholar 

  • Younas A, Waris MI, Chang XQ, Shaaban M, Abdelnabby H, ul Qamar MT, Wang MQ (2018b) A chemosensory protein MsepCSP5 involved in chemoreception of oriental armyworm Mythimna separata. Int J Biol Sci 14:1935–1949

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZK, Lei ZR (2015) Identification, expression profiling and fluorescence-based binding assays of a chemosensory protein gene from the western flower thrips, Frankliniella occidentalis. PLoS One 10:e0117726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang TT, Wang WX, Zhang ZD, Zhang YJ, Guo YY (2013) Functional characteristics of a novel chemosensory protein in the cotton bollworm Helicoverpa armigera (Hübner). J Integr Agric 12:853–861

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Pang B, Zhang L (2015) Novel odorant-binding proteins and their expression patterns in grasshopper, Oedaleus asiaticus. Biochem Biophys Res Comm 460:274–280

    Article  CAS  PubMed  Google Scholar 

  • Zhang LW, Li HW, Zhang L (2017) Two olfactory pathways to detect aldehydes on locust mouthpart. Int J Biol Sci 13:759–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou YT, Li L, Pang BP, Shan YM, Zhang ZR (2019) Antennal transcriptome analysis and expression profiling of chemosensory protein genes in Oedaleus asiaticus (Orthoptera: Acrididae). Acta Entomol Sin 62:21–32

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (NSFC) (No. 31760517).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bao-Ping Pang.

Electronic supplementary material

Table S1

(DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, YT., Li, L., Zhou, XR. et al. Three Chemosensory Proteins Involved in Chemoreception of Oedaleus asiaticus (Orthopera: Acridoidea). J Chem Ecol 46, 138–149 (2020). https://doi.org/10.1007/s10886-019-01138-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-019-01138-5

Keywords

Navigation