Bacterial origin of a diverse family of UDP-glycosyltransferase genes in the Tetranychus urticae genome

Insect Biochemistry and Molecular Biology

Volumn 50, Issue 1, 2014, Pages 43-57

  Ahn, Seung Joon ^a,b   Dermauw, Wannes ^c   Wybouw, Nicky ^c   Heckel, David G ^a   Van Leeuwen, Thomas ^c,d  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b Rural Development Administration   (South Korea)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Arthropoda; Chelicerata; Detoxification; Horizontal gene transfer; Tetranychus urticae; UDP glycosyltransferase

Indexed keywords

GLYCOSYLTRANSFERASE; XENOBIOTIC AGENT;

ANIMAL; ARTHROPOD; BACTERIAL GENE; CLADOCERA; CRAYFISH; ENZYMOLOGY; GENETICS; GENOME; HORIZONTAL GENE TRANSFER; INTRON; METABOLISM; PHYLOGENY; TETRANYCHIDAE;

ANIMALS; ARTHROPODS; ASTACOIDEA; CLADOCERA; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENOME; GLYCOSYLTRANSFERASES; INTRONS; PHYLOGENY; TETRANYCHIDAE; XENOBIOTICS;

EID: 84900028173     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.04.003     Document Type: Article

References (69)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Acuña R., Padilla B.E., Flórez-Ramos C.P., Rubio J.D., Herrera J.C., Benavides P., Lee S.-J., Yeats T.H., Egan A.N., Doyle J.J., Rose J.K.C. Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc. Natl. Acad. Sci. USA 2012, 109:4197-4202.
3. Ahn S.-J., Badenes-Pérez F.R., Reichelt M., Svatoš A., Schneider B., Gershenzon J., Heckel D.G. Metabolic detoxification of capsaicin by UDP-glycosyltransferase in three Helicoverpa species. Arch. Insect Biochem. Physiol. 2011, 78:104-118.
4. Ahn S.-J., Vogel H., Heckel D.G. Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochem. Mol. Biol. 2012, 42:133-147.
5. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
6. Andersson J.O. Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 2005, 62:1182-1197.
7. Bock K.W. Vertebrate UDP-glucuronosyltransferases: functional and evolutionary aspects. Biochem. Pharmacol. 2003, 66:691-696.
8. Boucher Y., Douady C.J., Papke R.T., Walsh D.A., Boudreau M.E.R., Nesbø C.L., Case R.J., Doolittle W.F. Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 2003, 37:283-328.
9. Bowles D., Isayenkova J., Lim E.-K., Poppenberger B. Glycosyltransferases: managers of small molecules. Curr. Opin. Plant. Biol. 2005, 8:254-263.
10. Brattsten L.B. Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. J.Chem. Ecol. 1988, 14:1919-1939.
11. Bryon A., Wybouw N., Dermauw W., Tirry L., Van Leeuwen T. Genome wide gene-expression analysis of facultative reproductive diapause in the two-spotted spider mite Tetranychus urticae. BMC Genomics 2013, 14:815.
12. Caputi L., Malnoy M., Goremykin V., Nikiforova S., Martens S. Agenome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J. 2012, 69:1030-1042.
13. Crooks G.E., Hon G., Chandonia J.-M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
14. Daimon T., Hirayama C., Kanai M., Ruike Y., Meng Y., Kosegawa E., Nakamura M., Tsujimoto G., Katsuma S., Shimada T. The silkworm Green b locus encodes a quercetin 5-O-glucosyltransferase that produces green cocoons with UV-shielding properties. Proc. Natl. Acad. Sci. USA 2010, 107:11471-11476.
15. Danchin E.G.J., Rosso M.-N., Vieira P., de Almeida-Engler J., Coutinho P.M., Henrissat B., Abad P. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. USA 2010, 107:17651-17656.
16. Dermauw W., Osborne E., Clark R., Grbić M., Tirry L., Van Leeuwen T. Aburst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics 2013, 14:317.
17. Dermauw W., Wybouw N., Rombauts S., Menten B., Vontas J., Grbić M., Clark R.M., Feyereisen R., Van Leeuwen T. Alink between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc. Natl. Acad. Sci. U.S.A 2013, 110:E113-E122.
18. Després L., David J.-P., Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 2007, 22:298-307.
19. Dunning Hotopp J.C. Horizontal gene transfer between bacteria and animals. Trends Genet. 2011, 27:157-163.
20. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
21. Erb A., Weiß H., Härle J., Bechthold A. Abacterial glycosyltransferase gene toolbox: generation and applications. Phytochemistry 2009, 70:1812-1821.
22. Grbić M., Van Leeuwen T., Clark R.M., Rombauts S., Rouzé P., Grbić V., Osborne E.J., Dermauw W., Thi Ngoc P.C., Ortego F., Hernandez-Crespo P., Diaz I., Martinez M., Navajas M., Sucena É., Magalhães S., Nagy L., Pace R.M., Djuranović S., Smagghe G., Iga M., Christiaens O., Veenstra J.A., Ewer J., Villalobos R.M., Hutter J.L., Hudson S.D., Velez M., Yi S.V., Zeng J., Pires-daSilva A., Roch F., Cazaux M., Navarro M., Zhurov V., Acevedo G., Bjelica A., Fawcett J.A., Bonnet E., Martens C., Baele G., Wissler L., Sanchez-Rodriguez A., Tirry L., Blais C., Demeestere K., Henz S.R., Gregory T.R., Mathieu J., Verdon L., Farinelli L., Schmutz J., Lindquist E., Feyereisen R., Van de Peer Y. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011, 479:487-492.
23. Hacker C.V., Brasier C.M., Buck K.W. Adouble-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J.Gen. Virol. 2005, 86:1561-1570.
24. Halkier B.A., Gershenzon J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 2006, 57:303-333.
25. Hedges S.B., Kumar S. Discovering the Timetree of life 2009, Oxford University Press, New York.
26. Hill C.A. Genome Analysis of Major tick and mite Vectors of Human Pathogens 2010, https://www.vectorbase.org/sites/default/files/ftp/documents/ixs_sequencing_proposal.pdf.
27. Huang H., Wu Q. Cloning and comparative analyses of the zebrafish Ugt repertoire reveal its evolutionary diversity. PLoS ONE 2010, 5:e9144.
28. Hughes A.L. Origin of ecdysosteroid UDP-glycosyltransferases of baculoviruses through horizontal gene transfer from Lepidoptera. Coevolution 2013, 1:1-7.
29. Jeppson L.R., Keifer H.H., Baker E.W. Mites injurious to Economic Plants 1975, University of California Press, Berkeley, Los Angeles.
30. Jobb G., Haeseler A.V., Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol. 2004, 4:18.
31. Kojima W., Fujii T., Suwa M., Miyazawa M., Ishikawa Y. Physiological adaptation of the Asian corn borer Ostrinia furnacalis to chemical defenses of its host plant, maize. J.Insect Physiol. 2010, 56:1349-1355.
32. Lairson L.L., Henrissat B., Davies G.J., Withers S.G. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 2008, 77:521-555.
33. Langmead B., Trapnell C., Pop M., Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
34. 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. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
35. Lee S.-W., Ohta K., Tashiro S., Shono T. Metabolic resistance mechanisms of the housefly (Musca domestica) resistant to pyraclofos. Pestic. Biochem. Physiol. 2006, 85:76-83.
36. Li W., Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659.
37. Liu B., Jiang G., Zhang Y., Li J., Li X., Yue J., Chen F., Liu H., Li H., Zhu S., Wang J., Ran C. Analysis of transcriptome differences between resistant and susceptible strains of the citrus red mite Panonychus citri (Acari: Tetranychidae). PLoS ONE 2011, 6:e28516.
38. Lombard V., Golaconda Ramulu H., Drula E., Coutinho P.M., Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2013, 42:D490-D495.
39. Luzhetskyy A., Bechthold A. Features and applications of bacterial glycosyltransferases: current state and prospects. Appl. Microbiol. Biotechnol. 2008, 80:945-952.
40. Mackenzie P.I., Owens I.S., Burchell B., Bock K.W., Bairoch A., Belanger A., Gigleux S.F., Green M., Hum D.W., Iyanagi T., Lancet D., Louisot P., Magdalou J., Roy Chowdhury J., Ritter J.K., Tephly T.R., Schachter H., Tephly T., Tipton K.F., Nebert D.W. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 1997, 7:255-269.
41. Mackenzie P.I., Walter Bock K., Burchell B., Guillemette C., Ikushiro S.-i., Iyanagi T., Miners J.O., Owens I.S., Nebert D.W. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet. Genomics 2005, 15:677-685.
42. Magdalou J., Fournel-Gigleux S., Ouzzine M. Insights on membrane topology and structure/function of UDP-glucuronosyltransferases. Drug. Metab. Rev. 2010, 42:159-166.
43. Manfrin C., Tom M., De Moro G., Gerdol M., Guarnaccia C., Mosco A., Pallavicini A., Giulianini P.G. Application of D-crustacean hyperglycemic hormone induces peptidases transcription and suppresses glycolysis-related transcripts in the hepatopancreas of the crayfish Pontastacus leptodactylus - results of a transcriptomic study. PLoS ONE 2013, 8:e65176.
44. Meech R., Miners J.O., Lewis B.C., Mackenzie P.I. The glycosidation of xenobiotics and endogenous compounds: versatility and redundancy in the UDP glycosyltransferase superfamily. Pharmacol. Ther. 2012, 134:200-218.
45. Megy K., Emrich S.J., Lawson D., Campbell D., Dialynas E., Hughes D.S.T., Koscielny G., Louis C., MacCallum R.M., Redmond S.N., Sheehan A., Topalis P., Wilson D. VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res. 2012, 40:D729-D734. The VectorBase Consortium.
46. Migeon A., Dorkeld F. Spider Mites web: a Comprehensive Database for the Tetranychidae 2013, http://www.montpellier.inra.fr/CBGP/spmweb.
47. Miley M.J., Zielinska A.K., Keenan J.E., Bratton S.M., Radominska-Pandya A., Redinbo M.R. Crystal structure of the cofactor-binding domain of the human phase II drug-metabolism enzyme UDP-glucuronosyltransferase 2B7. J.Mol. Biol. 2007, 369:498-511.
48. O'Reilly D.R. Baculovirus-encoded ecdysteroid UDP-glucosyltransferases. Insect Biochem. Mol. Biol. 1995, 25:541-550.
49. Paganini J., Campan-Fournier A., Da Rocha M., Gouret P., Pontarotti P., Wajnberg E., Abad P., Danchin E.G.J. Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLoS ONE 2012, 7:e50875.
50. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
51. Radominska-Pandya A., Bratton S.M., Redinbo M.R., Miley M.J. The crystal structure of human UDP-glucuronosyltransferase 2B7 C-termnial end is the first mammalian UGT target to be revealed: the significance for human UGTs from both the 1A and 2B families. Drug. Metab. Rev. 2010, 42:133-144.
52. Ritchie M.E., Silver J., Oshlack A., Holmes M., Diyagama D., Holloway A., Smyth G.K. Acomparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700-2707.
53. Ross J., Li Y., Lim E.-K., Bowles D. Higher plant glycosyltransferases. Genome Biol. 2001, 2. reviews3004.1-reviews3004.6.
54. Sasai H., Ishida M., Murakami K., Tadokoro N., Ishihara A., Nishida R., Mori N. Species-specific glucosylation of DIMBOA in larvae of the rice Armyworm. Biosci. Biotechnol. Biochem. 2009, 73:1333-1338.
55. Schönknecht G., Weber A.P.M., Lercher M.J. Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 2014, 36:9-20.
56. Smith J.N. Detoxication mechanisms. Annu. Rev. Entomol. 1962, 7:465-480.
57. Smyth G., Altman N. Separate-channel analysis of two-channel microarrays: recovering inter-spot information. BMC Bioinforma. 2013, 14:165.
58. Smyth G.K. limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, 397-420. Springer, NewYork. R. Gentleman, V. Carey, W. Huber, R. Irizarry, S. Dudoit, G.K. Smyth (Eds.).
59. Song D., Cho W.K., Park S.-H., Jo Y., Kim K.-H. Evolution of and horizontal gene transfer in the Endornavirus genus. PLoS ONE 2013, 8:e64270.
60. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
61. Van Leeuwen T., Demaeght P., Osborne E.J., Dermauw W., Gohlke S., Nauen R., Grbić M., Tirry L., Merzendorfer H., Clark R.M. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc. Natl. Acad. Sci. USA 2012, 109:4407-4412.
62. Van Leeuwen T., Dermauw W., Grbić M., Tirry L., Feyereisen R. Spider mite control and resistance management: does a genome help?. Pest Manag. Sci. 2012, 69:156-159.
63. Van Leeuwen T., Vontas J., Tsagkarakou A., Dermauw W., Tirry L. Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem. Mol. Biol. 2010, 40:563-572.
64. Wybouw N., Balabanidou V., Ballhorn D.J., Dermauw W., Grbić M., Vontas J., Van Leeuwen T. Ahorizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem. Mol. Biol. 2012, 42:881-889.
65. Yang X., Buschman L.L., Zhu K.Y., Margolies D.C. Susceptibility and detoxifying enzyme activity in two spider mite species (Acari: Tetranychidae) after selection with three insecticides. J.Econ. Entomol. 2002, 95:399-406.
66. Yonekura-Sakakibara K., Hanada K. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 2011, 66:182-193.
67. Zhou Z., Gu J., Li Y.-Q., Wang Y. Genome plasticity and systems evolution in Streptomyces. BMC Bioinforma. 2012, 13:S8.
68. Zhu B., Zhou Q., Xie G., Zhang G., Zhang X., Wang Y., Sun G., Li B., Jin G. Interkingdom gene transfer may contribute to the evolution of phytopathogenicity in Botrytis cinerea. Evol. Bioinforma. 2012, 8:105-117.
69. Zhurov V., Navarro M., Bruinsma K.A., Arbona V., Santamaria E.M., Cazaux M., Wybouw N., Osborne E.J., Ens C., Rioja C., Vermeirssen V., Rubio-Somoza I., Krishna P., Diaz I., Schmid M., Gómez-Cadenas A., Van de Peer Y., Grbić M., Clark R.M., Van Leeuwen T., Grbić V. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol. 2014, 164:384-399.