Studying the organization of genes encoding plant cell wall degrading enzymes in Chrysomela tremula provides insights into a leaf beetle genome

Insect Molecular Biology

Volumn 23, Issue 3, 2014, Pages 286-300

  Pauchet, Yannick ^a   Saski, C A ^b   Feltus, F A ^b   Luyten, I ^c   Quesneville, H ^c   Heckel, D G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b CLEMSON UNIVERSITY   (United States)

^c Centre de recherche de Versailles   (France)

Author keywords

BAC library; Chrysomela tremula; Coleoptera; genomics; leaf beetle; plant cell wall degrading enzymes

Indexed keywords

BACTERIA (MICROORGANISMS); CHRYSOMELA TREMULA; CHRYSOMELIDAE; CHRYSOMELOIDEA; COLEOPTERA; CURCULIONOIDEA; HEXAPODA; LEPTINOTARSA DECEMLINEATA; TRIBOLIUM CASTANEUM;

TRANSCRIPTOME;

AMINO ACID SEQUENCE; ANIMAL; BACTERIAL ARTIFICIAL CHROMOSOME; BEETLE; ENZYMOLOGY; GENETICS; GENOME; INSECT GENOME; MOLECULAR GENETICS; PHYLOGENY; SYNTENY;

AMINO ACID SEQUENCE; ANIMALS; BEETLES; CHROMOSOMES, ARTIFICIAL, BACTERIAL; GENOME; GENOME, INSECT; MOLECULAR SEQUENCE DATA; PHYLOGENY; SYNTENY; TRANSCRIPTOME;

EID: 84899937327     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/imb.12081     Document Type: Article

References (55)

1. Acuna, R., Padilla, B.E., Florez-Ramos, C.P., Rubio, J.D., Herrera, J.C., Benavides, P., et al. (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci U S A 109: 4197-4202.
2. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
3. Aggarwal, R., Benatti, T.R., Gill, N., Zhao, C., Chen, M.S., Fellers, J.P., et al. (2009) A BAC-based physical map of the Hessian fly genome anchored to polytene chromosomes. BMC Genomics 10: 293.
4. d'Alencon, E., Sezutsu, H., Legeai, F., Permal, E., Bernard-Samain, S., Gimenez, S., et al. (2010) Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci U S A 107: 7680-7685.
5. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
6. Bao, Z., and, Eddy, S.R., (2002) Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 12: 1269-1276.
7. Benson, G., (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580.
8. Calderon-Cortes, N., Watanabe, H., Cano-Camacho, H., Zavala-Paramo, G., and, Quesada, M., (2010) cDNA cloning, homology modelling and evolutionary insights into novel endogenous cellulases of the borer beetle Oncideres albomarginata chamela (Cerambycidae). Insect Mol Biol 19: 323-336.
9. Cantarel, B.L., Korf, I., Robb, S.M., Parra, G., Ross, E., Moore, B., et al. (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18: 188-196.
10. Chang, C.J., Wu, C.P., Lu, S.C., Chao, A.L., Ho, T.H., Yu, S.M., et al. (2012) A novel exo-cellulase from white spotted longhorn beetle (Anoplophora malasiaca). Insect Biochem Mol Biol 42: 629-636.
11. Conesa, A., and, Götz, S., (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008: 619832.
12. Cosgrove, D.J., (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850-861.
13. Danchin, E.G., Rosso, M.N., Vieira, P., de Almeida-Engler, J., Coutinho, P.M., Henrissat, B., et al. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci U S A 107: 17651-17656.
14. Davison, A., and, Blaxter, M., (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22: 1273-1284.
15. Drysdale, R., (2008) FlyBase: a database for the Drosophila research community. Methods Mol Biol 420: 45-59.
16. Edgar, R.C., and, Myers, E.W., (2005) PILER: identification and classification of genomic repeats. Bioinformatics 21 (Suppl 1): i152-i158.
17. Ewing, B., and, Green, P., (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
18. Farrell, B.D., (1998) 'Inordinate Fondness' explained: why are there so many beetles? Science 281: 555-559.
19. Flutre, T., Duprat, E., Feuillet, C., and, Quesneville, H., (2011) Considering transposable element diversification in de novo annotation approaches. PLoS One 6: e16526.
20. Gassmann, A.J., Petzold-Maxwell, J.L., Keweshan, R.S., and, Dunbar, M.W., (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS One 6: e22629.
21. Genissel, A., Augustin, S., Courtin, C., Pilate, G., Lorme, P., and, Bourguet, D., (2003) Initial frequency of alleles conferring resistance to Bacillus thuringiensis poplar in a field population of Chrysomela tremulae. Proc R Soc Lond B Biol Sci 270: 791-797.
22. Gladyshev, E.A., Meselson, M., and, Arkhipova, I.R., (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320: 1210-1213.
23. Holt, R.A., Subramanian, G.M., Halpern, A., Sutton, G.G., Charlab, R., Nusskern, D.R., et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.
24. Hunt, T., Bergsten, J., Levkanicova, Z., Papadopoulou, A., John, O.S., Wild, R., et al. (2007) A comprehensive phylogeny ofbeetles reveals the evolutionary origins of a superradiation. Science 318: 1913-1916.
25. Keeling, C.I., Yuen, M.M., Liao, N.Y., Docking, T.R., Chan, S.K., Taylor, G.A., et al. (2013) Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14: R27.
26. Kim, H.S., Murphy, T., Xia, J., Caragea, D., Park, Y., Beeman, R.W., et al. (2010) BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res 38: D437-D442.
27. Kirsch, R., Wielsch, N., Vogel, H., Svatos, A., Heckel, D.G., and, Pauchet, Y., (2012) Combining proteomics and transcriptome sequencing to identify active plant-cell-wall-degrading enzymes in a leaf beetle. BMC Genomics 13: 587.
28. Kohany, O., Gentles, A.J., Hankus, L., and, Jurka, J., (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7: 474.
29. Kolpakov, R., Bana, G., and, Kucherov, G., (2003) mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res 31: 3672-3678.
30. Lee, S.J., Kim, S.R., Yoon, H.J., Kim, I., Lee, K.S., Je, Y.H., et al. (2004) cDNA cloning, expression, and enzymatic activity of a cellulase from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol B Biochem Mol Biol 139: 107-116.
31. Lee, S.J., Lee, K.S., Kim, S.R., Gui, Z.Z., Kim, Y.S., Yoon, H.J., et al. (2005) A novel cellulase gene from the mulberry longicorn beetle, Apriona germari: gene structure, expression, and enzymatic activity. Comp Biochem Physiol B Biochem Mol Biol 140: 551-560.
32. Luo, M., and, Wing, R.A., (2003) An Improved Method for Plant BAC Library Construction, Vol. 236. Humana Press, Inc, Totowa, NJ.
33. Magbanua, Z.V., Ozkan, S., Bartlett, B.D., Chouvarine, P., Saski, C.A., Liston, A., et al. (2011) Adventures in the enormous: a 1.8 million clone BAC library for the 21.7 Gb genome of loblolly pine. PLoS One 6: e16214.
34. McKenna, D.D., and, Farrell, B.D., (2009) Beetles (Coleoptera). In The Timetree of Life (, Hedges, S.B., and, Kumar, S., eds), pp. 278-289. Oxford University Press, New York.
35. Miller, J.R., Delcher, A.L., Koren, S., Venter, E., Walenz, B.P., Brownley, A., et al. (2008) Aggressive assembly of pyrosequencing reads with mates. Bioinformatics 24: 2818-2824.
36. Pauchet, Y., and, Heckel, D.G., (2013) The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proc Biol Sci 280: 20131021.
37. Pauchet, Y., Wilkinson, P., van Munster, M., Augustin, S., Pauron, D., and, Ffrench-Constant, R.H., (2009) Pyrosequencing of the midgut transcriptome of the poplar leaf beetle Chrysomela tremulae reveals new gene families in Coleoptera. Insect Biochem Mol Biol 39: 403-413.
38. Pauchet, Y., Wilkinson, P., Chauhan, R., and, Ffrench-Constant, R.H., (2010) Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One 5: e15635.
39. Petitpierre, E., Segarra, C., and, Juan, C., (1993) Genome size and chromosomal evolution in leaf beetles (Coleoptera, Chrysomelidae). Hereditas 119: 1-6.
40. Quesneville, H., Nouaud, D., and, Anxolabehere, D., (2003) Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes. J Mol Evol 57 (Suppl 1): S50-S59.
41. Quesneville, H., Bergman, C.M., Andrieu, O., Autard, D., Nouaud, D., Ashburner, M., et al. (2005) Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol 1: 166-175.
42. Richards, S., Gibbs, R.A., Weinstock, G.M., Brown, S.J., Denell, R., Beeman, R.W., et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949-955.
43. Shen, Z., Denton, M., Mutti, N., Pappan, K., Kanost, M.R., Reese, J.C., et al. (2003) Polygalacturonase from Sitophilus oryzae: possible horizontal transfer of a pectinase gene from fungi to weevils. J Insect Sci 3: 24.
44. Shen, Z., Pappan, K., Mutti, N.S., He, Q.J., Denton, M., Zhang, Y., et al. (2005) Pectinmethylesterase from the rice weevil, Sitophilus oryzae: cDNA isolation and sequencing, genetic origin, and expression of the recombinant enzyme. J Insect Sci 5: 21.
45. Song, J.M., Nam, K.W., Kang, S.G., Kim, C.G., Kwon, S.T., and, Lee, Y.H., (2008) Molecular cloning and characterization of a novel cold-active beta-1,4-D-mannanase from the Antarctic springtail, Cryptopygus antarcticus. Comp Biochem Physiol B Biochem Mol Biol 151: 32-40.
46. Sugimura, M., Watanabe, H., Lo, N., and, Saito, H., (2003) Purification, characterization, cDNA cloning and nucleotide sequencing of a cellulase from the yellow-spotted longicorn beetle, Psacothea hilaris. Eur J Biochem 270: 3455-3460.
47. Tomkins, J., Fregene, M., Main, D., Kim, H., Wing, R., and, Tohme, J., (2004) Bacterial artificial chromosome (BAC) library resource for positional cloning of pest and disease resistance genes in cassava (Manihot esculenta Crantz). Plant Mol Biol 56: 555-561.
48. Wang, S., Lorenzen, M.D., Beeman, R.W., and, Brown, S.J., (2008) Analysis of repetitive DNA distribution patterns in the Tribolium castaneum genome. Genome Biol 9: R61.
49. Watanabe, H., Noda, H., Tokuda, G., and, Lo, N., (1998) A cellulase gene of termite origin. Nature 394: 330-331.
50. Willis, J.D., Oppert, B., Oppert, C., Klingeman, W.E., and, Jurat-Fuentes, J.L., (2011) Identification, cloning, and expression of a GHF9 cellulase from Tribolium castaneum (Coleoptera: Tenebrionidae). J Insect Physiol 57: 300-306.
51. Wu, C., Proestou, D., Carter, D., Nicholson, E., Santos, F., Zhao, S., et al. (2009) Construction and sequence sampling of deep-coverage, large-insert BAC libraries for three model lepidopteran species. BMC Genomics 10: 283.
52. Xu, B., Hellman, U., Ersson, B., and, Janson, J.C., (2000) Purification, characterization and amino-acid sequence analysis of a thermostable, low molecular mass endo-beta-1,4-glucanase from blue mussel, Mytilus edulis. Eur J Biochem 267: 4970-4977.
53. Xu, B., Hagglund, P., Stalbrand, H., and, Janson, J.C., (2002) endo-beta-1,4-Mannanases from blue mussel, Mytilus edulis: purification, characterization, and mode of action. J Biotechnol 92: 267-277.
54. Yamamoto, K., Nohata, J., Kadono-Okuda, K., Narukawa, J., Sasanuma, M., Sasanuma, S., et al. (2008) A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biol 9: R21.
55. Zhu, S., Saski, C.A., Boerma, H.R., Tomkins, J.P., All, J.N., and, Parrott, W.A., (2009) Construction of a BAC library for a defoliating insect-resistant soybean and identification of candidate clones using a novel approach. Plant Mol Biol Rep 27: 229-235.