Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-22T19:58:04.308Z Has data issue: false hasContentIssue false

Analysis of the workers head transcriptome of the Asian subterranean termite, Coptotermes gestroi

Published online by Cambridge University Press:  21 December 2010

F.C. Leonardo
Affiliation:
Laboratório de Genômica e Expressão, Departamento de Genética Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, CEP: 13083-970, Campinas, São Paulo, Brazil
A.F. da Cunha
Affiliation:
Laboratório de Bioquímica e Biotecnologia molecular, Departamento de Genética e Evolução, Universidade Federal de São Carlos, Via Washington Luis Km 235, CEP:13565-905, São Carlos, São Paulo, Brazil
M.J. da Silva
Affiliation:
Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Avenida Cândido Rondon, 400, CEP: 13083-875, Campinas, São Paulo, Brazil
M.F. Carazzolle
Affiliation:
Laboratório de Genômica e Expressão, Departamento de Genética Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, CEP: 13083-970, Campinas, São Paulo, Brazil Centro Nacional de Processamento de Alto Desempenho em São Paulo, Rua Saturnino Brito, 45, Cidade Universitária, CEP: 13083-889, Universidade Estadual de Campinas, São Paulo, Brazil
A.M. Costa-Leonardo
Affiliation:
Departamento de Biologia, Unesp, Univ. Estadual Paulista, Avenida 24 A Universidade Estadual Paulista, Avenida 24a, Bela Vista, CEP: 13506-900, Rio Claro, São Paulo, Brazil
F.F. Costa
Affiliation:
Centro de Hematologia e Hemoterapia, Faculdade de Ciências Médicas, Universidade Estadual de Campinas, Rua Carlos Chagas, 480, CEP: 13083-878, Campinas, São Paulo, Brazil
G.A. Pereira*
Affiliation:
Laboratório de Genômica e Expressão, Departamento de Genética Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, CEP: 13083-970, Campinas, São Paulo, Brazil
*
*Author for correspondence Fax: 0055-19-35216235 E-mail: [email protected]

Abstract

The lower termite, Coptotermes gestroi (Isoptera: Rhinotermitidae), is originally from Southeast Asia and has become a pest in Brazil. The main goal of this study was to survey C. gestroi transcriptome composition. To accomplish this, we sequenced and analyzed 3003 expressed sequence tags (ESTs) isolated from libraries of worker heads. After assembly, 695 uniESTs were obtained from which 349 have similarity with known sequences. Comparison with insect genomes demonstrated similarity, primarily with genes from Apis mellifera (28%), Tribolium castaneum (28%) and Aedes aegypti (10%). Notably, we identified two endogenous cellulases in the sequences, which may be of interest for biotechnological applications. The results presented in this work represent the first genomic study of the Asian subterranean termite, Coptotermes gestroi.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2010

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

Altschul, S.F., Madden, T.L., Schaffer, 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(17), 33893402.CrossRefGoogle ScholarPubMed
Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinsk, K., Dwight, S.S., Eppig, J.T., Harris, M.A., Hill, D.P., Issel-Tarver, L., Kasarski, A., Lewis, S., Matese, J.C., Richardson, J.E., Ringwald, M., Rubin, G.M. & Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25(1), 2529.CrossRefGoogle ScholarPubMed
Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281297.CrossRefGoogle ScholarPubMed
Colonello-Frattini, N. & Hartfelder, K. (2009) Differential gene expression profiling in mucus glands of honey bee (Apis mellifera) drones during sexual maturation. Apidologie 40, 481495.CrossRefGoogle Scholar
Ewing, B. & Green, P. (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8(3), 186194.CrossRefGoogle ScholarPubMed
Fujita, A., Miura, T. & Matsumoto, T. (2008) Differences in cellulose digestive systems among castes in two termite lineages. Phisiological Entomology 33, 7382.CrossRefGoogle Scholar
Geib, S.M., Filley, T.R., Hatcher, P.G., Hoover, K., Carlson, J.E., del Mar Jimenez-Gasco, M., Nakagawa-Izumi, A., Sleighter, R.L. & Tien, M. (2008) Lignin degradation in wood-feeding insects. Proceedings of the National Academy of Sciences of the United States of America 105, 1293212937.CrossRefGoogle ScholarPubMed
Grassé, P.P. (1949) Ordre des Isoptères ou termites. pp. 408544 in Grassé, P.P. (Ed.) Traité de Zoologie. v. 9, Masson, Paris. Physiological Entomology 33, 73–82.Google Scholar
Huang, X. & Madan, A. (1999) CAP3: A DNA sequence assembly program. Genome Research 9(9), 868877.CrossRefGoogle ScholarPubMed
Iseli, C., Jongeneel, C.V. & Bucher, P. (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. pp. 138148 in Proceedings of the 7th International Conference on Intelligent Systems for Molecular Biology, AAAi Press, Menlo Park, CA, USA.Google Scholar
Jenkins, T.M., Jones, S.C., Lee, C.Y., Forschler, B.T., Chen, Z., Lopez-Martinez, G., Gallagher, N.T., Brown, G., Neal, M., Thistleton, B. & Kleinschmidt, S. (2007) Phylogeography illuminates maternal origins of exotic Coptotermes gestroi (Isoptera: Rhinotermitidae). Molecular Phylogenetics and Evolution 42(3), 612621.CrossRefGoogle ScholarPubMed
Kannan, N., Taylor, S.S., Zhai, Y., Venter, J.C. & Manning, G. (2007) Structural and functional diversity of the microbial kinome. Public Library of Science Biology 5(3), e17.Google ScholarPubMed
Khalturin, K., Hemmrich, G., Fraune, S., Augustin, R. & Bosch, T.C. (2009) More than just orphans: are taxonomically restricted genes important in evolution? Trends in Genetics 25(9), 404413.CrossRefGoogle ScholarPubMed
Kirton, L.G. (2005) The importance of accurate termite taxonomy in the broader perspective of termite management. pp. 17 in Lee, C.-Y. & Robinson, W.H. (Eds) Proceedings of the Fifth International Conference on Urban Pests. P & Y Design Network, Penang, Malaysia.Google Scholar
Korb, J., Weil, T., Hoffmann, K., Foster, K.R. & Rehli, M. (2009) A gene necessary for reproductive suppression in termites. Science 324, 758.CrossRefGoogle ScholarPubMed
Kudo, T. (2009) Termite-Microbe Symbiotic System and Its Efficient Degradation of Lignocellulose. Bioscience Biotechnology and Biochemistry 73(12), 25612567.CrossRefGoogle ScholarPubMed
Mercer, T.R., Dinger, M.E. & Mattick, J.S. (2009) Long non-coding RNAs: insights into functions. Nature Reviews Genetics 10(3), 155159.CrossRefGoogle ScholarPubMed
Nakashima, K., Watanabe, H., Saitoh, H., Tokuda, G. & Azuma, J.I. (2002) Dual cellulose digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochemistry and Molecular Biology 32(7), 777784.CrossRefGoogle ScholarPubMed
Nunes, F.M., Valente, V., Sousa, J.F., Cunha, M.A., Pinheiro, D.G., Maia, R.M., Silva, W.A., Araujo, D.D., Costa, M.C.R., Martins, W.K., Carvalho, A.F., Monesi, N., Nascimento, A.M., Peixoto, P.M.V., Silva, M.F.R., Ramos, R.G.P., Reis, L.F.L., Dias-Neto, E., Souza, S.J., Simpson, A.J.G., Zago, M.A., Soares, A.E.E., Bitondi, M.M.G., Espreafico, E.M., Espindola, F.S., Paco-Larson, L., Simoes, Z.L.P., Hartfelder, K. & Silva, W.A. (2004) The use of Open Reading frame ESTs (ORESTES) for analysis of the honey bee transcriptome. BioMed Central Genomics 5(1), 84–1.Google ScholarPubMed
Ohkuma, M. (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends in Microbiology 16(7), 345352.CrossRefGoogle ScholarPubMed
Ronaghi, M. (2001) Pyrosequencing sheds light on DNA sequencing. Genome Research 11(1), 311.CrossRefGoogle ScholarPubMed
Sabater-Muñoz, B., Legeai, F., Rispe, C., Bonhomme, J., Dearden, P., Dossat, C., Duclert, A., Gauthier, J.P., Ducray, D.G., Hunter, W., Dang, P., Kambhampati, S., Martinez-Torres, D., Cortes, T., Moya, A., Nakabachi, A., Philippe, C., Prunier-Leterme, N., Rahbé, Y., Simon, J.C., Stern, D.L., Wincker, P. & Tagu, D. (2006) Large-scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera). Genome Biology 7(3), R21.CrossRefGoogle ScholarPubMed
Sawata, M., Takeuchi, H. & Kubo, T. (2004) Identification and analysis of the minimal promoter activity of a novel non coding nuclear RNA gene, AncR-1, from the honeybee (Apis mellifera L.). Rna 10(7), 10471058.CrossRefGoogle Scholar
Scharf, M.E. & Tartar, A. (2008) Termites digestome as sources for novel lignocellulases. Biofuels, Bioproducts and Biorefining 6(2), 540552.CrossRefGoogle Scholar
Scharf, M.E., Wu-Scharf, D., Pittendrigh, B.R. & Bennett, G.W. (2003) Caste- and development-associated gene expression in a lower termite. Genome Biology 4(10), R62.CrossRefGoogle Scholar
Scharf, M.E., Wu-Scharf, D., Zhou, X., Pittendrigh, B.R. & Bennett, G.W. (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Molecular Biology 14(1), 3144.CrossRefGoogle ScholarPubMed
Tartar, A., Wheeler, M.M., Zhou, X., Coy, M.R., Boucias, D.G. & Scharf, M. (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnology for Biofuels 2, 25.CrossRefGoogle ScholarPubMed
Todaka, N., Moriya, S., Saita, K., Hondo, T., Kiuchi, I., Hirotoshi, T., Ohkuma, M., Piero, C., Hayashisaky, Y. & Kudo, T. (2007) Enviromental cDNA analysis og the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. Federation of European Microbiological Societies Microbiology Ecology 59, 592599.CrossRefGoogle Scholar
Tokuda, G., Watanabe, H., Matsumoto, T. & Noda, H. (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-beta-1,4-glucanase. Zoological Science 14(1), 8393.CrossRefGoogle ScholarPubMed
Tokuda, G., Saito, H. & Watanabe, H. (2002) A digestive β-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): distribution, characterization and isolation of its precursor cDNA by 5′- and 3′-RACE amplifications with degenerate primers. Insect Biochemistry and Molecular Biology 32(12), 16811689.CrossRefGoogle ScholarPubMed
Telles, G. & da Silva, F. (2001) Trimming and clustering sugarcane ESTs. Genetics and Molecular Biology 24, 1723.CrossRefGoogle Scholar
Tupy, J.L., Bailey, A.M., Dailey, G., Evans-Holm, M., Siebel, C.W., Misra, S., Celniker, S.E. & Rubin, G.M. (2005) Identification of putative noncoding polyadenylated transcripts in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 102(15), 54955500.CrossRefGoogle ScholarPubMed
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3(7), RESEARCH0034.CrossRefGoogle ScholarPubMed
Warnecke, F., Luginbuhl, P., Ivanova, N., Ghassemian, M., Richardson, T.H., Stege, J.T., Cayouette, M., McHardy, A.C., Djordjevic, G., Aboushadi, N., Sorek, R., Tringe, S.G., Podar, M., Martin, H.G., Kunin, V., Dalevi, D., Madejska, J., Kirton, E., Platt, D., Szeto, E., Salamov, A., Barry, K., Mikhailova, N., Kyrpides, N.C., Matson, E.G., Ottesen, E.A., Zhang, X., Hernández, M., Murillo, C., Acosta, L.G., Rigoutsos, I., Tamayo, G., Green, B.D., Chang, C., Rubin, E.M., Mathur, E.J., Robertson, D.E., Hugenholtz, P. & Leadbetter, P. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450(7169), 560565.CrossRefGoogle ScholarPubMed
Watanabe, H. & Tokuda, G. (2001) Animal cellulases. Cellular and Molecular Life Sciences 58(9), 11671178.CrossRefGoogle ScholarPubMed
Weil, T., Rehli, M. & Korb, J. (2007) Molecular basis for the reproductive division of labour in a lower termite. BMC Genomics 8, 198.CrossRefGoogle Scholar
Wilson, G.A., Bertrand, N., Patel, Y., Hughes, J.B., Feil, E.J. & Field, D. (2005) Orphans as taxonomically restricted and ecologically important genes. Microbiology 151, 24992501.CrossRefGoogle ScholarPubMed
Wu-Scharf, D., Scharf, M.E., Pittendrigh, B.R. & Bennett, G.W. (2003) Expressed sequence tags from a polyphenic Reticulitermes flavipes (Isoptera: Rhinotermitidae) cDNA library. Sociobiology 41(2), 479490.Google Scholar
Zhou, X., Oi, F.M. & Scharf, M.E. (2006) Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proceedings of the National Academy of Sciences of the United States of America 103(12), 44994504.CrossRefGoogle Scholar
Zhou, X., Smith, J.A.M., Oi, F.M., Koehler, P.G., Bennett, G.W. & Scharf, M.E. (2007) Correlation of cellulose gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395, 2939.CrossRefGoogle ScholarPubMed