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Identification of the chitinase genes from the diamondback moth, Plutella xylostella

Published online by Cambridge University Press:  15 July 2016

Z.H. Liao
Affiliation:
Department of Life Science, National Central University, Chung-Li, Taoyuan, Taiwan 320, ROC
T.C. Kuo
Affiliation:
Department of Biochemistry, Taipei Medical University, 250 Wu-Hsing Street, Taipei 110, Taiwan
C.H. Kao
Affiliation:
Applied Zoology Division, Taiwan Agricultural Research Institute, Council of Agriculture, Executive Yua, Wufeng, Taichung 41362, Taiwan
T.M. Chou
Affiliation:
Applied Zoology Division, Taiwan Agricultural Research Institute, Council of Agriculture, Executive Yua, Wufeng, Taichung 41362, Taiwan
Y.H. Kao*
Affiliation:
Department of Life Science, National Central University, Chung-Li, Taoyuan, Taiwan 320, ROC
R.N. Huang*
Affiliation:
Department of Entomology, College of Bioresources and Agriculture, National Taiwan University, Taipei 106, Taiwan Research Center for Plant-Medicine, National Taiwan University, Taipei 106, Taiwan
*
*Author for correspondence Tel: 886-2-33665570 and 886-3-4260839 Fax: 886-2-27325017 and 886-3-4228482 E-mail: rongent@ntu.edu.tw; ykao@cc.ncu.edu.tw
*Author for correspondence Tel: 886-2-33665570 and 886-3-4260839 Fax: 886-2-27325017 and 886-3-4228482 E-mail: rongent@ntu.edu.tw; ykao@cc.ncu.edu.tw

Abstract

Chitinases have an indispensable function in chitin metabolism and are well characterized in numerous insect species. Although the diamondback moth (DBM) Plutella xylostella, which has a high reproductive potential, short generation time, and characteristic adaptation to adverse environments, has become one of the most serious pests of cruciferous plants worldwide, the information on the chitinases of the moth is presently limited. In the present study, using degenerated polymerase chain reaction (PCR) and rapid amplification of cDNA ends-PCR strategies, four chitinase genes of P. xylostella were cloned, and an exhaustive search was conducted for chitinase-like sequences from the P. xylostella genome and transcriptomic database. Based on the domain analysis of the deduced amino acid sequences and the phylogenetic analysis of the catalytic domain sequences, we identified 15 chitinase genes from P. xylostella. Two of the gut-specific chitinases did not cluster with any of the known phylogenetic groups of chitinases and might be in a new group of the chitinase family. Moreover, in our study, group VIII chitinase was not identified. The structures, classifications and expression patterns of the chitinases of P. xylostella were further delineated, and with this information, further investigations on the functions of chitinase genes in DBM could be facilitated.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Abdel-Banat, B.M. & Koga, D. (2001) A genomic clone for a chitinase gene from the silkworm, Bombyx mori: structural organization identifies functional motifs. Insect Biochemistry and Molecular Biology 31, 497508.CrossRefGoogle ScholarPubMed
Abdel-Banat, B.M. & Koga, D. (2002) Alternative splicing of the primary transcript generates heterogeneity within the products of the gene for Bombyx mori chitinase. Journal of Biological Chemistry 277, 3052430534.CrossRefGoogle ScholarPubMed
Ahmad, T., Rajagopal, R. & Bhatnagar, R.K. (2003) Molecular characterization of chitinase from polyphagous pest Helicoverpa armigera . Biochemical and Biophysical Research Communications 310, 188195.Google Scholar
Arakane, Y. & Muthukrishnan, S. (2010) Insect chitinase and chitinase-like proteins. Celluar and Molecular Life Sciences 67, 201216.Google Scholar
Bolognesi, R., Arakane, Y., Muthukrishnan, S., Kramer, K.J., Terra, W.R. & Ferreira, C. (2005) Sequences of cDNAs and expression of genes encoding chitin synthase and chitinase in the midgut of Spodoptera frugiperda . Insect Biochemistry and Molecular Biology 35, 12491259.Google Scholar
Daimon, T., Hamada, K., Mita, K., Okano, K., Suzuki, M.G., Kobayashi, M. & Shimada, T. (2003) A Bombyx mori gene, BmChi-h, encodes a protein homologous to bacterial and baculovirus chitinases. Insect Biochemistry and Molecular Biology 33, 749759.Google Scholar
Daimon, T., Katsuma, S., Iwanaga, M., Kang, W. & Shimada, T. (2005) The BmChi-h gene, a bacterial-type chitinase gene of Bombyx mori, encodes a functional exochitinase that plays a role in the chitin degradation during the molting process. Insect Biochemistry and Molecular Biology 35, 11121123.CrossRefGoogle Scholar
De la Vega, H., Specht, C.A., Liu, Y. & Robbins, P.W. (1998) Chitinases are a multi-gene family in Aedes, Anopheles and Drosophila . Insect Molecular Biology 7, 233239.Google Scholar
Fitches, E., Wilkinson, H., Bell, H., Bown, D.P., Gatehouse, J.A. & Edwards, J.P. (2004) Cloning, expression and functional characterisation of chitinase from larvae of tomato moth (Lacanobia oleracea): a demonstration of the insecticidal activity of insect chitinase. Insect Biochemisty and Molecular Biology 34, 10371050.CrossRefGoogle ScholarPubMed
Funkhouser, J.D. & Aronson, N.N. Jr. (2007) Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evolutionary Biology 7, 96.CrossRefGoogle ScholarPubMed
Hegedus, D., Erlandson, M., Gillott, C. & Toprak, U. (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annual Review of Entomology 54, 285302.Google Scholar
Jouraku, A., Yamamoto, K., Kuwazaki, S., Urio, M., Suetsugu, Y., Narukawa, J., Miyamoto, K., Kurita, K., Kanamori, H., Katayose, Y., Matsumoto, T. & Noda, H. (2013) KONAGAbase: a genomic and transcriptomic database for the diamondback moth, Plutella xylostella . BMC Genomics 14, 464.CrossRefGoogle ScholarPubMed
Kawamura, K., Shibata, T., Saget, O., Peel, D. & Bryant, P.J. (1999) A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development 126, 211219.Google Scholar
Khajuria, C., Buschman, L.L., Chen, M.S., Muthukrishnan, S. & Zhu, K.Y. (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochemistry and Molecular Biology 40, 621629.CrossRefGoogle ScholarPubMed
Kim, M.G., Shin, S.W., Bae, K.S., Kim, S.C. & Park, H.Y. (1998) Molecular cloning of chitinase cDNAs from the silkworm, Bombyx mori and the fall webworm, Hyphantria cunea . Insect Biochemistry and Molecular Biology 28, 163171.CrossRefGoogle ScholarPubMed
Kramer, K.J. & Koga, D. (1986) Insect chitin: physical state, synthesis, degradation and metabolic regulation. Insect Biochemistry 16, 851877.CrossRefGoogle Scholar
Kramer, K.J. & Muthukrishnan, S. (1997) Insect chitinases: molecular biology and potential use as biopesticides. Insect Biochemistry and Molecular Biology 27, 887900.Google Scholar
Kramer, K.J. & Muthukrishnan, S. (2005) 4.3 – Chitin Metabolism in Insects. pp. 111144 in Editors-in-Chief: Lawrence, I. G., Kostas, I. & Sarjeet, S.G. (Eds) Comprehensive Molecular Insect Science. Amsterdam, Elsevier.Google Scholar
Kramer, K.J., Corpuz, L., Choi, H.K. & Muthukrishnan, S. (1993) Sequence of a cDNA and expression of the gene encoding epidermal and gut chitinases of Manduca sexta . Insect Biochemistry and Molecular Biology 23, 691701.CrossRefGoogle ScholarPubMed
Kramer, K.J., Hopkins, T.L. & Schaefer, J. (1995) Applications of solids NMR to the analysis of insect sclerotized structures. Insect Biochemistry and Molecular Biology 25, 10671080.CrossRefGoogle Scholar
Kzhyshkowska, J., Gratchev, A. & Goerdt, S. (2006) Stabilin-1, a homeostatic scavenger receptor with multiple functions. Journal of Cellular and Molecular Medicine 10, 635649.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.Google Scholar
Li, D., Zhang, J., Wang, Y., Liu, X., Ma, E., Sun, Y., Li, S. & Zhu, K.Y. (2015) Two chitinase 5 genes from Locusta migratoria: molecular characteristics and functional differentiation. Insect Biochemistry and Molecular Biology 58, 4654.CrossRefGoogle ScholarPubMed
Lu, Y., Zen, K.C., Muthukrishnan, S. & Kramer, K.J. (2002) Site-directed mutagenesis and functional analysis of active site acidic amino acid residues D142, D144 and E146 in Manduca sexta (tobacco hornworm) chitinase. Insect Biochemistry and Molecular Biology 32, 13691382.Google Scholar
Merzendorfer, H. (2006) Insect chitin synthases: a review. Journal of Comparative Physiology B 176, 115.Google Scholar
Merzendorfer, H. & Zimoch, L. (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. Journal of Experimental Biology 206, 43934412.Google Scholar
Mikitani, K., Sugasaki, T., Shimada, T., Kobayashi, M. & Gustafsson, J.A. (2000) The chitinase gene of the silkworm, Bombyx mori, contains a novel Tc-like transposable element. Journal of Biological Chemistry 275, 3772537732.Google Scholar
Nakabachi, A., Shigenobu, S. & Miyagishima, S. (2010) Chitinase-like proteins encoded in the genome of the pea aphid, Acyrthosiphon pisum . Insect Molecular Biology 19 (Suppl 2), 175185.Google Scholar
Pan, Y., Chen, K., Xia, H., Yao, Q., Gao, L., Lu, P., Huojuan, , He, Y. & Wang, L. (2010) Molecular cloning, expression and characterization of BmIDGF gene from Bombyx mori . ZEITSCHRIFT FUR NATURFORSCHUNG SECTION C – A Journal of Bioscience 65, 277283.Google Scholar
Pan, Y., Lu, P., Wang, Y., Yin, L., Ma, H., Ma, G., Chen, K. & He, Y. (2012) In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori, genome. Journal of Insect Science 12, 150.Google Scholar
Royer, V., Fraichard, S. & Bouhin, H. (2002) A novel putative insect chitinase with multiple catalytic domains: hormonal regulation during metamorphosis. Biochemical Journal 366, 921928.Google Scholar
Shinoda, T., Kobayashi, J., Matsui, M. & Chinzei, Y. (2001) Cloning and functional expression of a chitinase cDNA from the common cutworm, Spodoptera litura, using a recombinant baculovirus lacking the virus-encoded chitinase gene. Insect Biochemistry and Molecular Biology 31, 521532.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, 27252729.Google Scholar
Tetreau, G., Cao, X., Chen, Y.R., Muthukrishnan, S., Jiang, H., Blissard, G.W., Kanost, M.R. & Wang, P. (2015) Overview of chitin metabolism enzymes in Manduca sexta: identification, domain organization, phylogenetic analysis and gene expression. Insect Biochemistry and Molecular Biology 62, 114126.Google Scholar
Varela, P.F., Llera, A.S., Mariuzza, R.A. & Tormo, J. (2002) Crystal structure of imaginal disc growth factor-2. A member of a new family of growth-promoting glycoproteins from Drosophila melanogaster . Journal of Biological Chemistry 277, 1322913236.CrossRefGoogle ScholarPubMed
Wang, H.B., Sakudoh, T., Kawasaki, H., Iwanaga, M., Araki, K., Fujimoto, H., Takada, N., Iwano, H. & Tsuchida, K. (2009) Purification and expression analysis of imaginal disc growth factor in the silkworm, Bombyx mori . Journal of Insect Physiology 55, 10651071.Google Scholar
Watanabe, T., Kobori, K., Miyashita, K., Fujii, T., Sakai, H., Uchida, M. & Tanaka, H. (1993) Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. Journal of Biological Chemistry 268, 1856718572.CrossRefGoogle ScholarPubMed
Yan, J., Cheng, Q., Narashimhan, S., Li, C.B. & Aksoy, S. (2002) Cloning and functional expression of a fat body-specific chitinase cDNA from the tsetse fly, Glossina morsitans . Insect Biochemistry and Molecular Biology 32, 979989.CrossRefGoogle ScholarPubMed
You, M., Xuan, X., Tsuji, N., Kamio, T., Taylor, D., Suzuki, N. & Fujisaki, K. (2003) Identification and molecular characterization of a chitinase from the hard tick Haemaphysalis longicornis . Journal of Biological Chemistry 278, 85568563.CrossRefGoogle ScholarPubMed
You, M., Yue, Z., He, W., Yang, X., Yang, G., Xie, M., Zhan, D., Baxter, S.W., Vasseur, L., Gurr, G.M., Douglas, C.J., Bai, J., Wang, P., Cui, K., Huang, S., Li, X., Zhou, Q., Wu, Z., Chen, Q., Liu, C., Wang, B., Xu, X., Lu, C., Hu, M., Davey, J.W., Smith, S.M., Chen, M., Xia, X., Tang, W., Ke, F., Zheng, D., Hu, Y., Song, F., You, Y., Ma, X., Peng, L., Zheng, Y., Liang, Y., Chen, Y., Yu, L., Zhang, Y., Liu, Y., Li, G., Fang, L., Li, J., Zhou, X., Luo, Y., Gou, C., Wang, J. & Yang, H. (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nature Genetics 45, 220225.Google Scholar
Zhang, H., Huang, X., Fukamizo, T., Muthukrishnan, S. & Kramer, K.J. (2002) Site-directed mutagenesis and functional analysis of an active site tryptophan of insect chitinase. Insect Biochemistry and Molecular Biology 32, 14771488.CrossRefGoogle ScholarPubMed
Zhang, J., Iwai, S., Tsugehara, T. & Takeda, M. (2006) MbIDGF, a novel member of the imaginal disc growth factor family in Mamestra brassicae, stimulates cell proliferation in two lepidopteran cell lines without insulin. Insect Biochemistry and Molecular Biology 36, 536546.Google Scholar
Zhang, J., Zhang, X., Arakane, Y., Muthukrishnan, S., Kramer, K.J., Ma, E. & Zhu, K.Y. (2011 a) Comparative genomic analysis of chitinase and chitinase-like genes in the African malaria mosquito (Anopheles gambiae). PLoS ONE 6, e19899.CrossRefGoogle ScholarPubMed
Zhang, J., Zhang, X., Arakane, Y., Muthukrishnan, S., Kramer, K.J., Ma, E. & Zhu, K.Y. (2011 b) Identification and characterization of a novel chitinase-like gene cluster (AgCht5) possibly derived from tandem duplications in the African malaria mosquito, Anopheles gambiae . Insect Biochemistry and Molecular Biology 41, 521528.CrossRefGoogle ScholarPubMed
Zhang, D., Chen, J., Yao, Q., Pan, Z. & Zhang, W. (2012) Functional analysis of two chitinase genes during the pupation and eclosion stages of the beet armyworm Spodoptera exigua by RNA interference. Archive of Insect Biochemistry and Physiology 79, 220234.Google Scholar
Zheng, Y., Zheng, S., Cheng, X., Ladd, T., Lingohr, E.J., Krell, P.J., Arif, B.M., Retnakaran, A. & Feng, Q. (2002) A molt-associated chitinase cDNA from the spruce budworm, Choristoneura fumiferana . Insect Biochemistry and Molecular Biology 32, 18131823.Google Scholar
Zhu, Q., Deng, Y., Vanka, P., Brown, S.J., Muthukrishnan, S. & Kramer, K.J. (2004) Computational identification of novel chitinase-like proteins in the Drosophila melanogaster genome. Bioinformatics 20, 161169.CrossRefGoogle ScholarPubMed
Zhu, Q., Arakane, Y., Beeman, R.W., Kramer, K.J. & Muthukrishnan, S. (2008 a) Functional specialization among insect chitinase family genes revealed by RNA interference. Proceedings of the National Academy of Sciences of the United States of America 105, 66506655.CrossRefGoogle ScholarPubMed
Zhu, Q., Arakane, Y., Beeman, R.W., Kramer, K.J. & Muthukrishnan, S. (2008 b) Characterization of recombinant chitinase-like proteins of Drosophila melanogaster and Tribolium castaneum . Insect Biochemistry and Molecular Biology 38, 467477.CrossRefGoogle ScholarPubMed
Zhu, Q., Arakane, Y., Banerjee, D., Beeman, R.W., Kramer, K.J. & Muthukrishnan, S. (2008 c) Domain organization and phylogenetic analysis of the chitinase-like family of proteins in three species of insects. Insect Biochemistry and Molecular Biology 38, 452466.CrossRefGoogle ScholarPubMed
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