Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T18:15:24.984Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional characterization of a pheromone-binding protein from rice leaffolder Cnaphalocrocis medinalis in detecting pheromones and host plant volatiles

Published online by Cambridge University Press:  07 July 2016

X. Sun ,
Z.-F. Zhao ,
F.-F. Zeng ,
A. Zhang ,
Z.-X. Lu  and
M.-Q. Wang
X. Sun
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China Key Laboratory of Invasive Ecology, College of Life Sciences, Henan University, Kaifeng, Henan, People's Republic of China
Z.-F. Zhao
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China
F.-F. Zeng
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China
A. Zhang
Affiliation:
Invasive Insect Biocontrol and Behavior Laboratory, BARC-West, USDA-ARS, Beltsville, MD 20705-2350, USA
Z.-X. Lu
Affiliation:
Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 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, People's Republic of China
*
*Author for correspondence E-mail: mqwang@mail.hzau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Pheromone-binding proteins (PBPs) are believed to be involved in the recognition of semiochemicals. In the present study, western blot analysis, fluorescence-binding characteristics and immunolocalization of CmedPBP4 from the rice leaffolder, Cnaphalocrocis medinalis, were investigated. Western blot analysis revealed that CmedPBP4 showed obvious antenna-specific expression patterns in female and male antenna, and made a clearly different sex-biased expression. Immunocytochemical labeling revealed that CmedPBP4 showed specific expression in the trichoid sensilla. Competitive fluorescence binding assays indicated that CmedPBP4 could selectively recognize three sex pheromone components (Z13-18:Ac, Z11-16:Al and Z13-18:OH) and eleven rice plant volatiles, including cyclohexanol, nerolidol, cedrol, dodecanal, ionone, (−)-α-cedrene, (Z)-farnesene, β-myrcene, R-(+)-limonene, (−)-limonene, and (+)-3-carene. Meanwhile the CmedPBP4 detection of sex pheromones and host odorants was pH-dependent. Our results, for the first time, provide further evidence that trichoid sensilla might be play an important role in detecting sex pheromones and host plant volatiles in the C. medinalis moth. Our systematic studies provided further detailed evidence for the function of trichoid sensilla in insect semiochemical perception.

Keywords

Cnaphalocrocis medinalispheromone-binding proteinsimmunocytochemistryfluorescence competitive binding assaystrichoid sensilla
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 6 , December 2016 , pp. 781 - 789
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Abraham, D., Löfstedt, C. & Picimbon, J.F. (2005) Molecular characterization and evolution of pheromone binding protein genes in Agrotis moths. Insect Biochemistry and Molecular Biology 35, 1100–1111.CrossRefGoogle ScholarPubMed
Allen, J.E. & Wanner, K.W. (2011) Asian corn borer pheromone binding protein 3, a candidate for evolving specificity to the 12-tetradecenyl acetate sex pheromone. Insect Biochemistry and Molecular Biology 41, 141–149.CrossRefGoogle Scholar
Campanacci, V., Krieger, J., Bette, S., Sturgis, J.N., 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. Journal of Biological Chemistry 276, 20078–20084.Google Scholar
Cho, J.R., Choi, K.S., Park, H.H., Lee, S., Yum, K.H., Jung, J.K., Seo, B.Y. & Lee, M. (2013) Electroantennogram and field responses of Korean population of the rice leaf folder, Cnaphalocrocis medinalis (Lepidoptera: Crambidae), to sex attractant candidates. Journal of Asia-Pacific Entomology 16, 61–66.Google Scholar
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 . International Journal of Biological Sciences 5, 745–757.Google Scholar
Gong, D.P., Zhang, H.J., Zhao, P., Xia, Q.Y. & Xiang, Z.H. (2009 a) The odorant binding protein gene family from the genome of silkworm, Bombyx mori . BMC Genomics 10, 332.CrossRefGoogle ScholarPubMed
Gong, Z.J., Zhou, W.W., Yu, H.Z., Mao, C.G., Zhang, C.X., Cheng, J.A. & Zhu, Z.R. (2009 b) Cloning, expression and functional analysis of a general odorant-binding protein 2 gene of the rice striped stem borer, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae). Insect Molecular Biology 18, 405–417.Google Scholar
Grater, F., Xu, W., Leal, W. & Grubmuller, H. (2006) Pheromone discrimination by the pheromone-binding protein of Bombyx mori . Structure 14, 1577–1586.Google Scholar
Grobe-Wilde, E., Gohl, T., Bouché, E., Breer, H. & Krieger, J. (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. European Journal of Neuroscience 25, 2364–2373.Google Scholar
Groot, A., Gemeno, C., Brownie, C., Gould, F. & Schal, C. (2005) Male and female antennal responses in Heliothis virescens and H. subflexa to conspecific and heterospecific sex pheromone compounds. Environmental Entomology 34, 256–263.Google Scholar
Grosse-Wilde, E., Svatos, A. & Krieger, J. (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro . Chemical Senses 31, 547–555.Google Scholar
Gu, S.H., Wang, S.P., Zhang, X.Y., Wu, K.M., Guo, Y.Y., Zhou, J.J. & Zhang, Y.J. (2011) Identification and tissue distribution of odorant binding protein genes in the lucerne plant bug Adelphocoris lineolatus (Goeze). Insect Biochemistry and Molecular Biology 41, 254–263.Google Scholar
Gu, S.H., Zhou, J.J., Wang, G.R., Zhang, Y.J. & Guo, Y.Y. (2013) Sex pheromone recognition and immunolocalization of three pheromone binding proteins in the black cutworm moth Agrotis ipsilon . Insect Biochemistry and Molecular Biology 43, 237–251.CrossRefGoogle ScholarPubMed
Guo, H., Huang, L.Q., Pelosi, P. & Wang, C.Z. (2012) Three pheromone-binding proteins help segregation between two Helicoverpa species utilizing the same pheromone components. Insect Biochemistry and Molecular Biology 42, 708–716.CrossRefGoogle ScholarPubMed
Hillier, N. & Vickers, N. (2011) Hairpencil volatiles influence interspecific courtship and mating between two related moth species. Journal of Chemical Ecology 37, 1127–1136.Google Scholar
Hooper, A.M., Dufour, S., He, X., Muck, A., Zhou, J.J., Almeida, R., Field, L.M., Svatoš, A. & Pickett, J.A. (2009) High-throughput ESI-MS analysis of binding between the Bombyx mori pheromone-binding protein BmorPBP1, its pheromone components and some analogues. Chemical Communications 38, 5725–5727.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Inoue, H., Kamiwada, H. & Fukamachi, S. (2004) Seasonal changes in adult density and female mating status of the rice leaf roller Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) in paddy fields of Southern Kyushu, Japan. Applied Entomology and Zoology 48, 177–183.Google Scholar
Jin, J.Y., Li, Z.Q., Zhang, Y.N., Liu, N.Y. & Dong, S.L. (2014) Different roles suggested by sex-biased expression and pheromone binding affinity among three pheromone binding proteins in the pink rice borer, Sesamia inferens (Walker) (Lepidoptera: Noctuidae). Journal of Insect Physiology 66, 71–79.Google Scholar
Jin, X., Brandazza, A., Navarrini, A., Ban, L., Zhang, S., Steinbrecht, R.A., Zhang, L. & Pelosi, P. (2005) Expression and immunolocalisation of odorant-binding and chemosensory proteins in locusts. Cellular and Molecular Life Sciences 62, 1156–1166.CrossRefGoogle ScholarPubMed
Kawazu, K. & Tatsuki, S. (2002) Diel rhythms of calling behavior and temporal change in pheromone production of the rice leaffolder moth, Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Applied Entomology and Zoology 37, 219–224.Google Scholar
Kawazu, K., Hasegawa, J., Honda, H., Ishikawa, Y., Wakamura, S., Sugie, H., Kamiwada, H., Kamimuro, T., Yoshiyasu, Y. & Tatsuki, S. (2000) Geographical variation in female sex pheromones of the rice leaf folder moth, Cnaphalocrocis medinalis: identification of pheromone components in Japan. Entomologia Experimentalis et Applicata 96, 103–109.CrossRefGoogle Scholar
Kawazu, K., Setokuchi, O., Kohno, K., Takahashi, K., Yoshiyasu, Y. & Tatsuki, S. (2001) Sex pheromone of the rice leaffolder moth. Cnaphalocrocis medinalis (Lepidoptera: Crambidae): synthetic Indian and Philippine blends are not attractive to male C. medinalis, but are attractive to C. pilosa in the South-Western islands in Japan. Applied Entomology and Zoology 36, 471–474.CrossRefGoogle Scholar
Khan, Z.R., Barrion, A.T., Litsinger, J.A., Castilla, N.P. & Joshi, R.C. (1988) A bibliography of rice leaffolders (Lepidoptera: Pyralidae). Insect Science 9, 129–174.Google Scholar
Krieger, J. & Breer, H. 1999. Olfactory reception in invertebrates. Science 286, 720–723.Google Scholar
Krieger, J., von Nickisch-Rosenegk, E., Mameli, M., Pelosi, P. & Breer, H. (1996) Binding proteins from the antennae of Bombyx mori . Insect Biochemistry and Molecular Biology 26, 297–307.Google Scholar
Leal, W.S. (2003) Proteins that make sense. pp. 447–476 in Blomquist, G.J. & Vogt, R.G. (Eds) Insect Pheromone Biochemistry and Molecular Biology, the Biosynthesis and Detection of Pheromone and Plant Volatiles. London, Elsevier Academic Press.Google Scholar
Leal, W.S., Chen, A.M., Ishida, Y., Chiang, V.P., Erickson, M.L., Morgan, T.I. & Tsuruda, J.M. (2005) Kinetics and molecular properties of pheromone binding and release. Proceedings of the National Academy of Sciences of the United States of America 102, 5386–5391.CrossRefGoogle ScholarPubMed
Liu, N.Y., He, P. & Dong, S.L. (2012) Binding properties of pheromone-binding protein 1 from the common cutworm Spodoptera litura . Comparative Biochemistry and Physiology – Part B: Biochemistry & Molecular Biology 161, 295–302.CrossRefGoogle ScholarPubMed
Lou, Y.G., Ma, B. & Cheng, J.A. (2005) Attraction of the parasitoid Anagrus nilaparvatae to rice volatiles induced by the rice brown planthopper Nilaparvata lugens . Journal of Chemical Ecology 31, 2357–2372.CrossRefGoogle ScholarPubMed
Maida, R., Ziegelberger, G. & Kaissling, K.E. (2003) Ligand binding to six recombinant pheromone-binding proteins of Antheraea polyphemus and Antheraea pernyi . Journal of Comparative Physiology B 173, 565–573.Google Scholar
Michel, E., Damberger, F.F., Ishida, Y., Fiorito, F., Lee, D., Leal, W.S. & Wuthrich, K. (2011) Dynamic conformational equilibria in the physiological function of the Bombyx mori pheromone-binding protein. Journal of Molecular Biology 408, 922–931.Google Scholar
Mohl, C., Breer, H. & Krieger, J. (2002) Species-specific pheromonal compounds induce distinct conformational changes of pheromone binding protein subtypes from Antheraea polyphemus . Invertebrates Neuroscience 4, 165–174.CrossRefGoogle ScholarPubMed
Nathan, S.S., Chung, P.G. & Murugan, K. (2004) Effect of botanical insecticides and bacterial toxins on the gut enzyme of the rice leaffolder Cnaphalocrocis medinalis . Phytoparasitica 32, 433–443.CrossRefGoogle Scholar
Pelosi, P. (1994) Odorant-binding proteins. Critical Reviews in Biochemistry and Molecular Biology 29, 199–228.Google Scholar
Pelosi, P. & Maida, R. (1990) Odorant-binding proteins in vertebrates and insects: similarities and possible common function. Chemical Senses 15, 205–215.CrossRefGoogle Scholar
Picimbon, J.F. & Gadenne, C. (2002) Evolution of noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon . Insect Biochemistry and Molecular Biology 32, 839–846.Google Scholar
Prestwich, G.D., Du, G. & LaForest, S. (1995) How is pheromone specificity encoded in proteins? Chemical Senses 20, 461–469.Google Scholar
Roelofs, W.L. (1995) Chemistry of sex attraction. Proceedings of the National Academy of Sciences of the United States of America 92, 44–49.Google Scholar
Schneider, D. (1964) Insect antennae. Annual Review of Entomology 9, 103–122.Google Scholar
Steinbrecht, R.A. (1998) Odorant-binding proteins: expression and function. Annals of the New York Academy of Sciences 855, 323–332.Google Scholar
Sun, M., Liu, Y. & Wang, G. (2013 a) Expression patterns and binding properties of three pheromone binding proteins in the diamondback moth, Plutella xyllotella . Journal of Insect Physiology 59, 46–55.CrossRefGoogle ScholarPubMed
Sun, X., Wang, M.Q. & Zhang, G.A. (2011) Ultrastructural observations on antennal sensilla of Cnaphalocrocis medialis (Lepidoptera: Pyralidae). Microscopy Research and Technique 74, 113–121.CrossRefGoogle Scholar
Sun, X., Zhou, W., Liu, H., Zhang, A.J., Ai, C.R., Zhou, S.S., Zhou, C.X. & Wang, M.Q. (2013 b) Transgenic Bt rice does not challenge host preference of the target pest of rice leaffolder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). PLoS ONE 8, e79032.Google Scholar
Sun, X., Liu, Z., Zhang, A., Dong, H., Zeng, F.F., Pan, X.Y., Wang, Y. & Wang, M.Q. (2014) Electrophysiological Responses of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) to synthetic plant volatiles. Journal of Insect Science V14, 70.Google Scholar
Visser, J.H. (1986) Host odor perception in phytophagous insects. Annual Review of Entomology 31, 121–144.Google Scholar
Vogt, R.G. (1987) The molecular basis of pheromone reception: its influence on behavior. pp. 385–431 in Prestwich, G.D. & Blomquist, G.J. (Eds) Pheromone Biochemistry. New York, Academic Press.Google Scholar
Vogt, R.G. & Riddiford, L.M. (1981) Pheromone binding and inactivation by moth antennae. Nature 293, 161–163.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 polyphemus . Proceedings of the National Academy of Sciences of the United States of America 82, 8827–8831.Google Scholar
Vogt, R.G., Prestwich, G.D. & Lerner, M.R. (1991) Odorant-binding-protein subfamilies associate with distinct classes of olfactory receptors neurons in insect. Journal of Neurobiology 22, 74–84.Google Scholar
Vogt, R.G., Rogers, M.E., Franco, M.D. & 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). Journal of Experimental Biology 205, 719–744.Google Scholar
Watanabe, H., Tabunoki, H., Miura, N., Matsui, A., Sato, R. & Ando, T. (2009) Identification of a new pheromone-binding protein in the antennae of a geometrid species and preparation of its antibody to analyze the antennal proteins of moths secreting type II sex pheromone components. Bioscience, Biotechnology & Biochemistry 73, 1443–1446.Google Scholar
Wechgama, K., Laopaiboom, L. & Laopaiboon, P. (2008) Quantitative analysis of main volatile and other compounds in traditional distilled spirits from Thai rice. Biotechnology 7, 718–724.Google Scholar
Weng, C., Fu, Y., Jiang, H., Zhuang, S. & Li, H. (2015) Binding interaction between a queen pheromone component HOB and pheromone binding protein ASP1 of Apis cerana . International Journal of Biological Macromolecules 72, 430–436.Google Scholar
Willett, C.S. & Harrison, R.G. (1999) Pheromone binding proteins in the European and Asian corn borers: no protein change associated with pheromone differences. Insect Biochemistry and Molecular Biology 29, 277–284.Google Scholar
Zeng, F.F., Sun, X., Dong, H.B. & Wang, M.Q. (2013) Analysis of a cDNA library from the antenna of Cnaphalocrocis medinalis and the expression pattern of olfactory genes. Biochemical and Biophysical Research Communications 433, 463–469.Google Scholar
Zhang, S.G., Maida, R. & Steinbrecht, R.A. (2001) Immunolocalization of odorant-binding proteins in noctuid moths (Insecta, Lepidoptera). Chemical Senses 26, 885–896.Google Scholar
Zhang, T.T., Gu, S.H., Wu, K.M., Zhang, Y.J. & Guo, Y.Y. (2011) Construction and analysis of cDNA libraries from the antennae of male and female cotton bollworms Helicoverpa armigera (Hubner) and expression analysis of putative odorant-binding protein genes. Biochemical and Biophysical Research Communications 407, 393–399.CrossRefGoogle ScholarPubMed