Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T12:08:54.614Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and tissue expression profiling of candidate UDP-glycosyltransferase genes expressed in Holotrichia parallela motschulsky antennae

Published online by Cambridge University Press:  05 February 2018

S. Wang ,
Y. Liu ,
J.-J. Zhou ,
J.-K. Yi ,
Y. Pan ,
J. Wang ,
X.-X. Zhang ,
J.-X. Wang ,
S. Yang  and
J.-H. Xi
S. Wang
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
Y. Liu
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
J.-J. Zhou
Affiliation:
Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden AL5 2JQ, UK
J.-K. Yi
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
Y. Pan
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
J. Wang
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
X.-X. Zhang
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
J.-X. Wang
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
S. Yang
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
J.-H. Xi*
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, P.R. China
*
*Author for correspondence Phone: +86-13756072796 Fax: +86-431-87836255 E-mail: jhxi1965@jlu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

It is difficult to control Holotrichia parallela Motschulsky with chemical insecticides due to the larvae's soil-living habit, thus the pest has caused great economic losses in agriculture. In addition, uridine diphosphate-glycosyltransferases (UGTs) catalyze the glycosylation process of a variety of small lipophilic molecules with sugars to produce water-soluble glycosides, and play multiple roles in detoxification, endobiotic modulation, and sequestration in an insect. Some UGTs were found specifically expressed in antennae of Drosophila melanogaster and Spodoptera littoralis, and glucurono-conjugated odorants could not elicit any olfactory signals, suggesting that the UGTs may play roles in odorant inactivation by biotransformation. In the current study, we performed a genome-wide analysis of the candidate UGT family in the dark black chafer, H. parallela. Based on a UGT gene signature and the similarity of these genes to UGT homologs from other organisms, 20 putative H. parallela UGT genes were identified. Bioinformatics analysis was used to predict sequence and structural features of H. parallela UGT proteins, and revealed important domains and residues involved in sugar donor binding and catalysis by comparison with human UGT2B7. Phylogenetic analysis of these 20 UGT protein sequences revealed eight major groups, including both order-specific and conserved groups, which are common to more than one order. Of these 20 UGT genes, HparUGT1265-1, HparUGT3119, and HparUGT8312 were highly (>100-fold change) expressed in antennae, suggesting a possible role in olfactory tissue, and most likely in odorant inactivation and olfactory processing. The remaining UGT genes were expressed in all tissues (head, thorax, abdomen, leg, and wing), indicating that these UGTs likely have different biological functions. This study provides the fundamental basis for determining the function of UGTs in a highly specialized olfactory organ, the H. parallela antenna.

Keywords

UDP-glycosyltransferaseHolotrichia parallelaantennaeolfaction
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 6 , December 2018 , pp. 807 - 816
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

Ahn, S.J., Badenes-Pérez, F.R., Reichelt, M., Svatoš, A., Schneider, B., Gershenzon, J. & Heckel, D.G. (2011) Metabolic detoxification of capsaicin by UDP-glycosyltransferase in three Helicoverpa species. Archives of Insect Biochemistry and Physiology 78, 104–118.Google Scholar
Ahn, S.J., Vogel, H. & Heckel, D.G. (2012) Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochemistry and Molecular Biology 42, 133–147.Google Scholar
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Barvkar, V.T., Pardeshi, V.C., Kale, S.M., Kadoo, N.Y. & Gupta, V.S. (2012) Phylogenomic analysis of UDP glycosyltransferase 1 multigene family in Linum usitatissimum identified genes with varied expression patterns. BMC Genomics 13, 1471–2164.Google Scholar
Benton, R., Vannice, K.S. & Vosshall, L.B. (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289–293.Google Scholar
Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T.G., Bertoni, M., Bordoli, L. & Schwede, T. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42, W252–W258.Google Scholar
Bock, K.W. (2016) The UDP-glycosyltransferase (UGT) superfamily expressed in humans, insects and plants: animal-plant arms-race and co-evolution. Biochemical Pharmacology 99, 11–17.Google Scholar
Bozzolan, F., Siaussat, D., Maria, A., Durand, N., Pottier, M.A., Chertemps, T. & Maïbèche-Coisne, M. (2014) Antennal uridine diphosphate (UDP)-glycosyltransferases in a pest insect: diversity and putative function in odorant and xenobiotics clearance. Insect Molecular Biology 23, 539–549.Google Scholar
Cartwright, A.M., Lim, E.K., Kleanthous, C. & Bowles, D.J. (2008) A kinetic analysis of regiospecific glucosylation by two glycosyltransferases of Arabidopsis thaliana: domain swapping to introduce new activities. Journal of Biological Chemistry 283, 15724–15731.Google Scholar
Duan, M., Xiong, J., Lu, D., Wang, G. & Ai, H. (2016) Transcriptome sequencing analysis and functional identification of sex differentiation genes from the mosquito parasitic nematode, Romanomermis wuchangensis. PLoS ONE 11, e0163127.Google Scholar
Durand, N., Carot-Sans, G., Chertemps, T., Montagné, N., Jacquin-Joly, E., Debernard, S. & Maïbèche-Coisne, M. (2010) A diversity of putative carboxylesterases are expressed in the antennae of the noctuid moth Spodoptera littoralis. Insect Molecular Biology 19, 87–97.Google Scholar
Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D. & Bairoch, A. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 31, 3784–3788.Google Scholar
Hanser, H.I., Faure, P., Robert-Hazotte, A., Artur, Y., Duchamp-Viret, P., Coureaud, G. & Heydel, J.M. (2017) Odorant-odorant metabolic interaction, a novel actor in olfactory perception and behavioral responsiveness. Scientific Reports 7, 10219.Google Scholar
He, P., Li, Z.Q., Liu, C.C., Liu, S.J. & Dong, S.L. (2014) Two esterases from the genus Spodoptera degrade sex pheromones and plant volatiles. Genome 57, 201–208.Google Scholar
Heydel, J., Leclerc, S., Bernard, P., Pelczar, H., Gradinaru, D., Magdalou, J., Minn, A., Artur, Y. & Goudonnet, H. (2001) Rat olfactory bulb and epithelium UDP-glucuronosyltransferase 2A1 (UGT2A1) expression: in situ mRNA localization and quantitative analysis. Molecular Brain Research 90, 83–92.Google Scholar
Heydel, J.M., Holsztynska, E.J., Legendre, A., Thiebaud, N., Artur, Y. & Le Bon, A.M. (2010) UDP-glucuronosyltransferases (UGTs) in neuro-olfactory tissues: expression, regulation, and function. Drug Metabolism Reviews 42, 74–97.Google Scholar
Heydel, J.M., Coelho, A., Thiebaud, N., Legendre, A., Le Bon, A.M., Faure, P., Neiers, F., Artur, Y., Golebiowski, J. & Briand, L. (2013) Odorant-binding proteins and xenobiotic metabolizing enzymes: implications in olfactory perireceptor events. The Anatomical Record-Advances in Integrative Anatomy and Evolutionary Biology 296, 1333–1345.Google Scholar
Huang, F.F., Chai, C.L., Zhang, Z., Liu, Z.H., Dai, F.Y., Lu, C. & Xiang, Z.H. (2008) The UDP-glucosyltransferase multigene family in Bombyx mori. BMC Genomics 27, 1471–2164.Google Scholar
Ju, Q., Qu, M.J., Wang, Y., Jiang, X.J., Li, X., Dong, S.L. & Han, Z.J. (2012) Molecular and biochemical characterization of two odorant-binding proteins from dark black chafer, Holotrichia parallela. Genome 55, 537–546.Google Scholar
Ju, Q., Li, X., Jiang, X.J., Qu, M.J., Guo, X.Q., Han, Z.J. & Li, F. (2014) Transcriptome and tissue-specific expression analysis of Obp and Csp genes in the dark black chafer. Archives of Insect Biochemistry and Physiology 87, 177–200.Google Scholar
Kojima, W., Fujii, T., Suwa, M., Miyazawa, M. & Ishikawa, Y. (2010) Physiological adaptation of the Asian corn borer Ostrinia furnacalis to chemical defenses of its host plant, maize. Journal of Insect Physiology 56, 1349–1355.Google Scholar
Krempl, C., Sporer, T., Reichelt, M., Ahn, S.J., Heidel-Fischer, H., Vogel, H., Heckel, D.G. & Joußen, N. (2016) Potential detoxification of gossypol by UDP-glycosyltransferases in the two heliothine moth species Helicoverpa armigera and Heliothis virescens. Insect Biochemistry and Molecular Biology 71, 49–57.Google Scholar
Lazard, D., Zupko, K., Poria, Y., Nef, P., Lazarovits, J., Horn, S., Khen, M. & Lancet, D. (1991) Odorant signal termination by olfactory UDP glucuronosyl transferase. Nature 349, 790–793.Google Scholar
Leclerc, S., Heydel, J.M., Amossé, V., Gradinaru, D., Cattarelli, M., Artur, Y., Goudonnet, H., Magdalou, J., Netter, P., Pelczar, H. & Minn, A. (2002) Glucuronidation of odorant molecules in the rat olfactory system: activity, expression and age-linked modifications of UDP-glucuronosyltransferase isoforms, UGT1A6 and UGT2A1, and relation to mitral cell activity. Molecular Brain Research 107, 201–213.Google Scholar
Lim, E.K., Baldauf, S., Li, Y., Elias, L., Worrall, D., Spencer, S.P., Jackson, R.G., Taguchi, G., Ross, J. & Bowles, D.J. (2003) Evolution of substrate recognition across a multigene family of glycosyltransferases in Arabidopsis. Glycobiology 13, 139–145.Google Scholar
Luque, T., Okano, K. & O'Reilly, D.R. (2002) Characterization of a novel silkworm (Bombyx mori) phenol UDP-glucosyltransferase. European Journal of Biochemistry 269, 819–825.Google Scholar
Mackenzie, P.I., Owens, I.S., Burchell, B., Bock, K.W., Bairoch, A., Bélanger, A., Fournel-Gigleux, S., Green, M., Hum, D.W. & Iyanagi, T. (1997) The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7, 255–269.Google Scholar
Mackenzie, P.I., Bock, K.W., Burchell, B., Guillemette, C., Ikushiro, S., Iyanagi, T., Miners, J.O., Owens, I.S. & Nebert, D.W. (2005) Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenetics and Genomics 15, 677–685.Google Scholar
Magdalou, J., Fournel-Gigleux, S. & Ouzzine, M. (2010) Insights on membrane topology and structure/function of UDP-glucuronosyltransferases. Drug Metabolism Reviews 42, 159–166.Google Scholar
Mayer, U., Ungerer, N., Klimmeck, D., Warnken, U., Schnölzer, M., Frings, S. & Möhrlen, F. (2008) Proteomic analysis of a membrane preparation from rat olfactory sensory cilia. Chemical Senses 33, 145–162.Google Scholar
Miley, M.J., Zielinska, A.K., Keenan, J.E., Bratton, S.M., Radominska-Pandya, A. & Redinbo, M.R. (2007) Crystal structure of the cofactor-binding domain of the human phase II drug-metabolism enzyme UDP-glucuronosyltransferase 2B7. Journal of Molecular Biology 369, 498–511.Google Scholar
Olender, T., Keydar, I., Pinto, J.M., Tatarskyy, P., Alkelai, A., Chien, M.S., Fishilevich, S., Restrepo, D., Matsunami, H., Gilad, Y. & Lancet, D. (2016) The human olfactory transcriptome. BMC Genomics 17, 619.Google Scholar
Osmani, S.A., Bak, S. & Møller, B.L. (2009) Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modelling. Phytochemistry 70, 325–347.Google Scholar
Petersen, T.N., Brunak, S., von Heijne, G. & Nielsen, H. (2011) Signalp 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785–786.Google Scholar
Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Radominska-Pandya, A., Bratton, S.M., Redinbo, M.R. & Miley, M.J. (2010) The crystal structure of human UDP-glucuronosyltransferase 2B7 C-terminal end is the first mammalian UGT target to be revealed: the significance for human UGTs from both the 1A and 2B families. Drug Metabolism Reviews 42, 133–144.Google Scholar
Robertson, H.M., Martos, R., Sears, C.R., Todres, E.Z., Walden, K.K. & Nardi, J.B. (1999) Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antennae. Insect Molecular Biology 8, 501–518.Google Scholar
Rützler, M. & Zwiebel, L.J. (2005) Molecular biology of insect olfaction: recent progress and conceptual models. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 191, 777–790.Google Scholar
Sasai, H., Ishida, M., Murakami, K., Tadokoro, N., Ishihara, A., Nishida, R. & Mori, N. (2009) Species-specific glucosylation of DIMBOA in larvae of the rice Armyworm. Bioscience, Biotechnology, and Biochemistry 73, 1333–1338.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Vogt, R.G. & Riddiford, L.M. (1981) Pheromone binding and inactivation by moth antennae. Nature 293, 161–163.Google Scholar
Wang, Q., Hasan, G. & Pikielny, C.W. (1999) Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. Journal of Biological Chemistry 274, 10309–10315.Google Scholar
Wang, S., Yi, J.K., Yang, S., Liu, Y., Zhang, J.H. & Xi, J.H. (2017) Identification and characterization of microRNAs expressed in antennae of Holotrichia parallela motschulsky and their possible roles in olfactory regulation. Archives of Insect Biochemistry and Physiology 94, e21369.Google Scholar
Younus, F., Chertemps, T., Pearce, S.L., Pandey, G., Bozzolan, F., Coppin, C.W., Russell, R.J., Maïbèche-Coisne, M. & Oakeshott, J.G. (2014) Identification of candidate odorant degrading gene/enzyme systems in the antennal transcriptome of Drosophila melanogaster. Insect Biochemistry and Molecular Biology 53, 30–43.Google Scholar
Zhang, J.H., Wang, S., Yang, S., Yi, J., Liu, Y. & Xi, J.H. (2016) Differential proteome analysis of the male and female antennae from Holotrichia parallela. Archives of Insect Biochemistry and Physiology 92, 274–287.Google Scholar
Zhang, X., Zhang, Q.Y., Liu, D., Su, T., Weng, Y., Ling, G., Chen, Y., Gu, J., Schilling, B. & Ding, X. (2005) Expression of cytochrome p450 and other biotransformation genes in fetal and adult human nasal mucosa. Drug Metabolism and Disposition 33, 1423–1428.Google Scholar
Zhou, J.J. (2010) Odorant-binding proteins in insects. Vitamins and Hormones 83, 241–272.Google Scholar
Zhou, J.J., Field, L.M. & He, X.L. (2010). Insect odorant-binding proteins: do they offer an alternative pest control strategy? Outlooks on Pest Management 21, 31–34.Google Scholar
Supplementary material: File

Wang et al. supplementary material

Wang et al. supplementary material 1

Download Wang et al. supplementary material(File)
File 582.3 KB