Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-22T18:53:40.812Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional characteristics of chemosensory proteins in the sawyer beetle Monochamus alternatus Hope

Published online by Cambridge University Press:  21 February 2018

S. Ali ,
M.Z. Ahmed ,
N. Li ,
S.A.I. Ali  and
M.-Q. Wang
S. Ali
Affiliation:
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
M.Z. Ahmed
Affiliation:
Tropical Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, 18905 SW 280th Street, Homestead, FL 33031, USA
N. Li
Affiliation:
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
S.A.I. Ali
Affiliation:
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
M.-Q. Wang*
Affiliation:
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
*
*Author for correspondence Phone: (0086) 13627126839 Fax: (0086)−27-87280920 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The Japanese pine sawyer, Monochamus alternatus Hope (Coleoptera: Cerambycidae), is a major pest of pines and it is also the key vector of the exotic pinewood nematode in China. In the present study, we cloned, expressed, and purified a chemosensory protein (CSP) in M. alternatus. We surveyed its expression in various developmental stages of male and female adult tissues and determined its binding affinities for different pine volatiles using a competitive binding fluorescence assay. A CSP known as CSP5 in M. alternatus was obtained from an antennal cDNA library and expressed in Escherichia coli. Quantitative reverse transcription polymerase chain reaction results indicated that the CSP5 gene was mainly expressed in male and female antennae. Competitive binding assays were performed to test the binding affinity of recombinant CSP5 to 13 odour molecules of pine volatiles. The results showed that CSP5 showed very strong binding abilities to myrcene, (+)-β-pinene, and (−)-isolongifolene, whereas the volatiles 2-methoxy-4-vinylphenol, p-cymene, and (+)-limonene oxide have relatively weak binding affinity at pH 5.0. Three volatiles myrcene, (+)-β-pinene, and (−)-isolongifolene may play crucial roles in CSP5 binding with ligands but this needs further study for confirmation. The sensitivity of insect to host plant volatiles can effectively be used to control and monitor the population through mass trapping as part of integrated pest management programs.

Keywords

olfactory-specific proteinqPCRexpression characteristicscompetitive binding assayvolatiles
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 1 , February 2019 , pp. 34 - 42
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ban, L.P., Zhang, L., Yan, Y.H. & Pelosi, P. (2002) Binding properties of a locust's chemosensory protein. Biochemical and Biophysical Research Communications 293, 50–54.Google Scholar
Benton, R., Vannice, K.S., Gomez-Diaz, C. & Vosshall, L.B. (2009) Variant ionotropic glutamate receptors as chemosensory receptors in drosophila. Cell 136, 149–162.Google Scholar
Breer, H., Raming, K. & Krieger, J. (1994) Signal recognition and transduction in olfactory neurons. Biochimica Et Biophysica Acta-Molecular Cell Research 1224, 277– 287.Google Scholar
Campanacci, V., Krieger, J., Bette, S., Sturgis, J.N., Lartigue, A., Cambillau, C. & Tegoni, M. (2001) Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. Journal of Biological Chemistry 276, 20078–20084.Google Scholar
Campanacci, V., Lartigue, A., Hallberg, B.M., Jones, T.A., Giudici, O.M.T., Tegoni, M. & Cambillau, C. (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proceedings of National Academy of Sciences USA 100: 5069–5074.Google Scholar
Chen, S. (1959) Economic insect fauna of China (Fasc.1) Coleoptera Cerambycidae(I) (Ebook). Economic Insect Fauna of China 120 pages. Retrieved from: https://www.chinascientificbooks.com/economic-insect-fauna-of-china-fasc1-coleoptera-cerambycidaei-ebook-p-10564/.Google Scholar
Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J.H. & Carlson, J.R. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327–338.Google Scholar
Damberger, F., Nikonova, L., Horst, R., Peng, G., Leal, W.S. & Wuthrich, K. (2000) NMR characterization of a pH-dependent equilibrium between two folded solution conformations of the pheromone-binding protein from Bombyx mori. Protein Sciences 9, 1038–1041.Google Scholar
de Santis, F., Francois, M.C., Merlin, C., Pelletier, J., Maibeche-Coisne, M., Conti, E. & Jacquin-Joly, E. (2006) Molecular cloning and in situ expression patterns of two new pheromone-binding proteins from the corn stemborer Sesamia nonagrioides. Journal of Chemical Ecology 32, 1703–1717.Google Scholar
Field, L.M., Pickett, J.A. & Wadhams, L J. (2000) Molecular studies in insect olfaction. Insect Molecular Biology 9, 545–551.Google Scholar
Forêt, S., Wanner, K.W. & Maleszka, R. (2007) Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochemistry and Molecular Biology 37, 19–28.Google Scholar
Gong, D.P., Zhang, H.J., Zhao, P., Lin, Y., Xia, Q.Y. & Xiang, Z.H. (2007) Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 37, 266–277.Google Scholar
Gong, L., Luo, Q., Rizwan-ul-Haq, M. & Hu, M.Y. (2012) Cloning and characterization of three chemosensory proteins from Spodoptera exigua and effects of gene silencing on female survival and reproduction. Bulletin of Entomological Research 102, 600–609.Google Scholar
Gonzalez, D., Zhao, Q., McMahan, C., Velasquez, D., Haskins, W.E., Sponsel, V. & Renthal, R. (2009) The major antennal chemosensory protein of red imported fire ant workers. Insect Molecular Biology 18, 395–404.Google Scholar
Gu, J., Braasch, H., Burgermeister, W. & Zhang, J. (2006) Records of Bursaphelenchus spp. intercepted in imported packaging wood at Ningbo, China. Forest Pathology 36, 323–333.Google Scholar
Gu, S.H., Wang, S.Y., Zhang, X.Y., Ji, P., Liu, J.T., Wang, G.R., Wu, K.M., Guo, Y.Y., Zhou, J.J. & Zhang, Y.J. (2012) Functional characterizations of chemosensory proteins of the Alfalfa plant bug Adelphocoris lineolatus, indicate their involvement in host recognition. PLoS ONE 7(8), e42871.Google Scholar
Guo, W., Wang, X.H., Ma, Z.Y., Xue, L.A., Han, J.Y., Yu, D. & Kang, L. (2011) CSP and takeout genes modulate the switch between attraction and repulsion during behavioral Phase change in the migratory locust. PLoS Genetics 7, e1001291.Google Scholar
Haack, R.A., Herard, F., Sun, J. H. & Turgeon, J.J. (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annual Review of Entomology 55, 521–546.Google Scholar
Horst, R., Damberger, F., Luginbuhl, P., Guntert, P., Peng, G., Nikonova, L., Leal, W.S. & Wuthrich, K. (2001) NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proceedings of the National Academy of Sciences of the United States of America 98, 14374–14379.Google Scholar
Jacquine-Jolly, E., Vogt, R.G., Francois, M.C. & Nagnan-Le Meillour, P. (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chemical Senses 26, 833–844.Google Scholar
Kaissling, K.E., Strausfeld, C.Z. & Rumbo, E.R. (1987) Adaptation processes in insect olfactory receptors. Mechanisms and behavioral significance. Annals of the New York Academy of Sciences 510, 104–112.Google Scholar
Kitabayashi, A.N., Arai, T., Kubo, T. & Natori, S. (1998) Molecular cloning of cDNA for p10, a novel protein that increases in the regenerating legs of Periplaneta americana (American cockroach). Insect Biochemistry and Molecular Biology 28, 785–790.Google Scholar
Kobayashi, F., Yamane, A. & Ikeda, T. (1984) The Japanese pine sawyer beetle as the vector of pine wilt disease. Annual Review of Entomology 29, 115–135.Google Scholar
Kruger, N.J. (2002) The Bradford Method for Protein Quantitation. The Protein Protocols Handbook. 2nd edn. pp. 15–21. Totowa, NJ: Humana Press Inc.Google Scholar
Lartigue, A., Campanacci, V., Roussel, A., Larsson, A.M., Jones, T.A., Tegoni, M. & Cambillau, C. (2002) X-ray structure and ligand binding study of a moth chemosensory protein. Journal of Biological Chemistry 277, 32094–32098.Google Scholar
Li, D.Z., Yu, G.Q., Yi, S.C., Zhang, Y., Kong, D.X. & Wang, M.Q. (2015) Structure based analysis of the ligand-binding mechanism for DhelOBP21, a C minus odorant binding protein, from Dastarcus helophoroides (Fairmaire; Coleoptera: Bothride idae). International Journal of Biological Sciences 11, 1281–1295.Google Scholar
Li, Z.Q., Zhang, S., Ma, Y., Luo, J.Y., Wang, C.Y., Lv, L.M. & Cui, J.J. (2013) First transcriptome and digital gene expression analysis in Neuroptera with an emphasis on chemoreception genes in Chrysopa pallens (Rambur). PLoS ONE 8(6), e67151.Google Scholar
Maleszka, J., Foret, 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). Development Genes and Evolution 217, 189–196.Google Scholar
Mamidala, P., Wijeratne, A.J., Wijeratne, S., Poland, T., Qazi, S.S., Doucet, D. & Mittapalli, O. (2013). Identification of odor-processing genes in the emerald ash borer, Agrilus planipennis. PLoS ONE 8(2), e56555.Google Scholar
Mamiya, Y. & Enda, N. (1972) Transmission of Bursaphelenchus lignicolus (Nematoda: Aphelenchoididae) by Monochamus Alternatus (Coleoptera: Cerambycidae). Nematologica 18, 159–162.Google Scholar
Michel, E., Damberger, F.F., Ishida, Y., Fiorito, F., Lee, D., Leal, W.S. & Wüthrich, K. (2011) Dynamic conformational equilibria in the physiological function of the Bombyx mori pheromone-binding protein. Journal of Molecular Biologyl 408, 922–931.Google Scholar
Miles, C.I., del Campo, M.L. & Renwick, J.A.A. (2005) Behavioral and chemosensory responses to a host recognition cue by larvae of Pieris rapae. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 191, 147–155.Google Scholar
Nagnan-Le Meillour, P., Cain, A.H., Jacquin-Joly, E., Francois, M.C., Ramachandran, S., Maida, R. & Steinbrecht, R.A. (2000) Chemosensory proteins from the proboscis of Mamestra brassicae. Chemical Senses 25, 541–553.Google Scholar
Oduol, F., Xu, J.N., Niare, O., Natarajan, R. & Vernick, K.D. (2000) Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria. Proceedings of the National Academy of Sciences of the United States of America 97, 11397–11402.Google Scholar
Pesenti, M.E., Spinelli, S., Bezirard, V., Briand, L., Pernollet, J.C., Campanacci, V., Tegoni, M. & Cambillau, C. (2009) Queen bee pheromone binding protein pH-induced domain swapping favors pheromone release. Journal of Molecular Biology 390, 981–990.Google Scholar
Qiao, H.L., Deng, P.Y., Li, D.D., Chen, M., Jiao, Z.J., Liu, Z.C. & Kan, Y.C. (2013) Expression analysis and binding experiments of chemosensory proteins indicate multiple roles in Bombyx mori. Journal of Insect Physiology 59, 667–675.Google Scholar
Robinet, C., Roques, A., Pan, H.Y., Fang, G.F., Ye, J.R., Zhang, Y.Z. & Sun, J.H. (2009) Role of human-mediated dispersal in the spread of the pinewood nematode in China. PLoS ONE 4(2), e4646.Google Scholar
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C-T method. Nature Protocols 3, 1101–1108.Google Scholar
SFA. (2012) State Forestry Administration. The Bulletin of the State Forestry Administration of China, http://www.forestry.gov.cn/portal/main/govfile/13/govfile_1894.htm.Google Scholar
Singh, V.K., Mangalam, A.K., Dwivedi, S. & Naik, S. (1998) Primer premier: Program for design of degenerate primers from a protein sequence. Biotechniques 24, 318–319.Google Scholar
Tegoni, M., Campanacci, V. & Cambillau, C. (2004) Structural aspects of sexual attraction and chemical communication in insects. Trends in Biochemical Sciences 29, 257–264.Google Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Togashi, K. & Magira, H. (1981) Age-specific survival rate and fecundity of the adult Japanese pine sawyer: Monochamus alternatus HOPE (Coleoptera : Cerambycidae), at different emergence times. Applied Entomology and Zoology 16, 351–361.Google Scholar
Vogt, R.G., Riddiford, L.M. & Prestwich, G.D. (1985) Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea. Proceedings of the National Academy of Sciences of the United States of America 82, 8827–8831.Google Scholar
Vogt, R.G., Miller, N.E., Litvack, R., Fandino, R.A., Sparks, J., Staples, J. & Dickens, J.C. (2009) The insect SNMP gene family. Insect Biochemistry and Molecular Biology 39, 448–456.Google Scholar
Wan, F.H., Guo, J.Y. & Zhang, F. (2009) Research on Biological Invasions in China. 312pp. Science Press, Beijing, China.Google Scholar
Wang, L.P. (2004) Study on the biological characteristic of Monochamus alternatus hope. Journal of Fujian Forestry Science and Technology 31, 23–26.Google Scholar
Wanner, K.W., Willis, L.G., Theilmann, D.A., Isman, M.B., Feng, Q.L. & Plettner, E. (2004) Analysis of the insect OS-D-like gene family. Journal of Chemical Ecology 30, 889–911.Google Scholar
Wei, Y., Brandazza, A. & Pelosi, P. (2008) Binding of polycyclic aromatic hydrocarbons to mutants of odorant-binding protein: A first step towards biosensors for environmental monitoring. Biochimica Et Biophysica Acta-Proteins and Proteomics 1784, 666–671.Google Scholar
Zeng, F.-F., Zhao, Z.-F., Yan, M.-J., Zhou, W., Zhang, Z., Zhang, A., Lu, Z.-X. & Wang, M.-Q. (2015) Identification and comparative expression profiles of chemoreception genes revealed from major chemoreception organs of the rice leaf folder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). PLoS ONE 10, e0144267.Google Scholar
Zhang, T.T., Wang, W.X., Zhang, Z.D., Zhang, Y.J. & Guo, Y.Y. (2013) Functional characteristics of a novel chemosensory protein in the cotton bollworm Helicoverpa armigera (Hubner). Journal of Integrative Agriculture 12, 853–861.Google Scholar
Zhang, Y.N., Ye, Z.F., Yang, K. & Dong, S.L. (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.Google Scholar
Zheng, Z.-C., Li, D.-Z., Zhou, A., Yi, S.-C., Liu, H., & Wang, M.-Q. (2016) Predicted structure of a Minus-C OBP from Batocera horsfieldi (Hope) suggests an intermediate structure in evolution of OBPs. Scientific Reports 6, 33981.Google Scholar
Zhou, J.J., Vieira, F.G., He, X.L., Smadja, C., Liu, R., Rozas, J. & Field, L.M. (2010) Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology 19, 113–122.Google Scholar
Supplementary material: File

Ali et al. supplementary material 1

Supplementary Tables

Download Ali et al. supplementary material 1(File)
File 20.8 KB