Structural and Phylogenetic Analysis of Laccases from Trichoderma: A Bioinformatic Approach

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Cázares García, Saila Viridiana ^a   Vázquez Garcidueñas, Ma Soledad ^a   Vázquez Marrufo, Gerardo ^a  

^a UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENZYME; EXTRACELLULAR ISOENZYME; ISOENZYME; LACCASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CELL ACTIVITY; CELL DIFFERENTIATION; COMPUTER MODEL; ENZYME ANALYSIS; EXON; FUNGAL GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE TRANSFER; GENETIC CONSERVATION; HYPOCREA JECORINA; HYPOCREA LIXII; HYPOCREA VIRENS; INTRON; MYCOPARASITE; NONHUMAN; PHYLOGENY; PROTEIN MOTIF; SENSU STRICTO; STRUCTURE ANALYSIS; TRICHODERMA; TRICHODERMA ASPERELLUM; TRICHODERMA ATROVIRIDE;

AMINO ACID MOTIFS; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE COMPONENTS; LACCASE; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TRICHODERMA;

EID: 84873165224     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055295     Document Type: Article

References (68)

1. Quintanar L, Stoj C, Taylor AB, Hart PJ, Kosman DJ, et al. (2007) Shall we dance? How a multicopper oxidase chooses its electron transfer partner. Acc Chem Res 40: 445-452.
2. Giardiana P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, et al. (2010) Laccases: a never-ending story. Cell Mol Life Sci 67: 369-385.
3. Baldrian P, (2006) Fungal laccases - occurrence and properties. FEMS Microbiol Rev 30: 215-242.
4. Schouten A, Wagemakers L, Stefanato FL, van der Kaaij RM, van Kan JAL, (2002) Resveratrol acts as a natural profungicide and induces self-intoxication by a specific laccase. Mol Microbiol 43: 883-894.
5. Maté D, García-Ruíz E, Camarero S, Alcalde M, (2011) Directed evolution of fungal laccases. Curr Genomics 12: 113-122.
6. Shraddha, Shekher R, Sehgal S, Kamthania M, Kumar A (2011) Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res doi:10.4061/2011/217861.
7. Tetsch L, Bend J, Hölker U, (2006) Molecular and enzymatic characterization of extra- and intracellular laccases from the acidophilic ascomycete Hortaea acidophila. Anton Leeuw 90: 183-194.
8. Tamayo-Ramos JA, Barends S, Verhaert RMD, de Graaff LH, (2011) The Aspergillus niger multicopper oxidase family: analysis and overexpression of laccase-like encoding genes. Microb Cell Fact 10: 78.
9. Hoshida H, Nakao M, Kanazawa H, Kubo K, Hakukawa T, et al. (2001) Isolation of five laccase gene sequences from the white-rot fungus Trametes sanguinea by PCR, and cloning, characterization and expression of the laccase cDNA in yeast. J Biosci Bioeng 92: 372-380.
10. Cordoba CD, Roncero MIG, (2008) Functional analyses of laccase genes from Fusarium oxysporum. Mycology 98: 509-518.
11. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, et al. (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182: 736-750.
12. Pöggeler S, (2011) Evolution of multicopper oxidase genes in coprophilous and non-coprophilous members of the order sordariales. Curr Genomics 12: 95-103.
13. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U, (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273: 2308-2326.
14. Kilaru S, Hoegger PJ, Kües U, (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50: 45-60.
15. Lettera V, Piscitelli A, Leo G, Birolo L, Pezzella C, et al. (2010) Identification of a new member of Pleurotus ostreatus laccase family from mature fruiting body. Fungal Biol 114: 724-730.
16. Kubicek CP, Bissett J, Druzhinina I, Kullnig-Gradinger C, Szakacs G, (2003) Genetic and metabolic diversity of Trichoderma: a case study on South-East Asian isolates. Fungal Genet Biol 38: 310-319.
17. Schuster A, Schmoll M, (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87: 787-799.
18. Assavanig A, Amornkitticharoen B, Ekpaisal N, Meevootisom V, Flegel TW, (1992) Isolation, characterization and function of laccase from Trichoderma. Appl Microbiol Biotechnol 38: 198-202.
19. Krastanov AI, Gochev VK, Girova TD, (2007) Nutritive medium dependent biosynthesis of extracellular laccase from Trichoderma spp. Bulg J Agric Sci 13: 349-355.
20. Gochev VK, Krastanov AI, (2007) Isolation of laccase producing Trichoderma spp. Bulg J Agric Sci 13: 171-176.
21. Hölker H, Dohse J, Höfer M, (2002) Extracellular laccases in ascomycetes Trichoderma atroviride and Trichoderma harzianum. Folia Microbiol 47: 423-427.
22. Pokorný R, Vargovič P, Hölker U, Janssen M, Bend J, et al. (2005) Developmental changes in Trichoderma viride enzymes abundant in conidia and the light-induced conidiation signalling pathway. J Basic Microbiol 45: 219-229.
23. Sadhasivam S, Savitha S, Swwaminathan K, (2009) Redox-mediated decolorization of recalcitrant textile dyes by Trichoderma harzianum WL1 laccase. World J Microbiol Biotechnol 25: 1733-1741.
24. Chakroun H, Mechichi T, Martinez MJ, Dhouib A, Sayadi S, (2010) Trichoderma atroviride: application on bioremediation of phenolic compounds. Process Biochem 45: 507-513.
25. Levasseur A, Saloheimo M, Navarro D, Andberg M, Pontarotti P, et al. (2010) Exploring laccase-like multicopper oxidase genes from the ascomycete Trichoderma reesei: a functional, phylogenetic and evolutionary study. BMC Biochem 11: 32.
26. Catalano V, Vergara M, Hauzenberger JR, Seiboth B, Sarrocco S, et al. (2011) Use a non-homologous end-joining-deficient strain (delta-ku70) of the biocontrol fungus Trichoderma virens to investigate the function of the laccase gene lcc1 in sclerotia degradation. Curr Genet 57: 13-23.
27. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martínez DA, Druzhinina IS, et al. (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style for Trichoderma. Genome Biol 12: R40.
28. Martínez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, et al. (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: 553-560.
29. Kumar S, Phale P, Durani S, Wangikar PP, (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83: 386-394.
30. Hakulinen N, Andberg M, Kallio J, Koivula A, Kruus K, et al. (2008) A near atomic resolution structure of a Melanocarpus albomyces laccase. J Struct Biol 162: 29-39.
31. Hakulinen N, Kiiskinen LL, Kruus K, Saloheimo M, Paananen A, et al. (2002) Crystal structure of a laccase from Melanocarpus albomyces with an intact trinuclear copper site. Nature Struct Biol 9: 601-605.
32. Eggert C, LaFayette PR, Temp U, Eriksson KEL, Dean JFD, (1998) Molecular analysis of a laccase gene from the white rot fungus Pycnoporus cinnabarinus. Appl Environ Microbiol 64: 1766-1772.
33. Litvintseva AP, Henson JM, (2002) Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the take-all fungus. Appl Environ Microbiol 68: 1305-1311.
34. Martin C, Pecyna M, Kellner H, Jehmlich N, Junghanns C, et al. (2007) Purification and biochemical characterization of a laccase from the aquatic fungus Myrioconium sp. UHH 1-13-18-4 and molecular analysis of the laccase-encoding gene. Appl Microbiol Biotechnol 77: 613-624.
35. Fernández LJ, Stahl U, (1996) Isolation and characterization of a laccase gene from Podospora anserina. Mol Gen Genet 252: 539-551.
36. Choi GH, Larson TG, Nuss DL, (1992) Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol Plant Microbe Interact 5: 119-128.
37. Shapiro MB, Senepathy P, (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15: 7155-7174.
38. Chung HJ, Kwon BR, Kim JM, Park SM, Park JK, et al. (2008) A tannic acid-inducible and hypoviral-regulated laccase3 contributes to the virulence of the chestnut blight fungus Cryphonectria parasitica. Mol Plant Microbe In 21: 1582-1590.
39. Garavaglia S, Cambria MT, Miglio M, Ragusa S, Lacobazzi V, et al. (2002) The structure of Rigidoporus lignosus laccase containing a full complement of copper ions, reveals an asymmetrical arrangement for the T3 copper pair. J Mol Biol 342: 1519-1531.
40. Piontek K, Antorini M, Choinowsky T, (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-Å resolution containing a full complement of coppers. J Biol Chem 277: 37663-37669.
41. Li H, Webb SP, Ivanic J, Jensen JH, (2004) Determinants of the reactive reduction potentials of type-1 copper sites in proteins. J Am Chem Soc 126: 8010-8019.
42. Kallio JP, Gasparetti C, Andberg M, Boer H, Koivula A, et al. (2011) Crystal structure of an ascomycete fungal laccase from Thielavia arenaria - common structural features of asco-laccases. FEBS J 278: 2283-2295.
43. Ge H, Gao Y, Hong Y, Zhang M, Xiao Y, et al. (2010) Structure of native laccase B from Trametes sp. AH28-2. Acta Cryst F66: 254-258.
44. Kallio JP, Auer S, Jänis J, Anderberg M, Kruus K, et al. (2009) Structure-function studies of a Melanocarpus albomyces laccase suggest a pathway for oxidation or phenolic compounds. J Mol Biol 392: 895-909.
45. German UA, Muller G, Hunziker PE, Lerch K, (1988) Characterization of two allelic forms of Neurospora crassa laccase amino- and carboxyl-terminal processing of a precursor. J Biol Chem 263: 885-896.
46. Bulter T, Alcalde M, Sieber V, Meinhold P, Schlachtbauer C, et al. (2003) Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microbiol 69: 987-995.
47. Andberg M, Hakulinen N, Auer S, Saloheimo M, Koivula A, et al. (2009) Essential role of the C-terminus in Melanocarpus albomyces laccase for enzyme production, catalytic properties and structure. FEBS J 276: 6285-6300.
48. Pardo I, Vicente AI, Mate DM, Alcalde M, Camareno S (2012) Development of chimeric laccases by directed evolution. Biotechnol Bioeng doi 10.1002/bit.24588.
49. Pezzella C, Autore F, Giardina P, Piscitelli A, Sannia G, et al. (2009) The Pleurotus ostreatus laccase multi-gene family: isolation and heterologous expression of new family members. Curr Genet 55: 45-57.
50. Hoegger PJ, Navarro-González M, Kilaru S, Hoffmann M, Westbrook ED, et al. (2004) The laccase gene family in Coprinopsis cinerea (Coprinus cinereus). Curr Genet 45: 9-18.
51. Nielsen H, Engelbrecht J, Brunak S, von Heijne G, (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
52. Vite-Vallejo O, Palomares LA, Dantán-González E, Ayala-Castro HG, Martínez-Anaya C, et al. (2009) The role of N-glycosylation on the enzymatic activity of a Pycnoporus sanguineus laccase. Enzyme Microb Technol 45: 233-239.
53. Martin F, Laurent P, de Carvalho D, Voiblet C, Balestrini R, et al. (1999) Cell wall proteins of the ectomycorrhizal basidiomycete Pisolithus tinctorius: identification, function and expression in symbiosis. Fungal Genet Biol 27: 161-174.
54. Brandhorst T, Klein B, (2000) Cell wall biogenesis of Blastomyces dermatitidis. Evidence for a novel mechanism of cell surface localization of a virulence-associated adhesin via extracellular release and reassociation with cell wall chitin. J Biol Chem 275: 7925-7934.
55. Soragni E, Bolchi A, Balestrini R, Gambaretto C, Percudani R, et al. (2001) A nutrient-regulated, dual localization phospholipase A2 in the symbiotic fungus Tuber borchii. The EMBO J 20: 5079-5090.
56. Zhu X, Williamson PR, (2004) Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res 5: 1-10.
57. Oda K, Kakizono D, Yamada O, Lefuji H, Akita O, et al. (2006) Proteomic analysis of extracellular proteins from Aspergillus oryzae grown under submerged and solid-state culture conditions. Appl Environ Microbiol 72: 3448-3457.
58. Yogev O, Pines O, (2011) Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim Biophys Acta 1808: 1012-1020.
59. Ben-Menachem R, Tal M, Shadur T, Pines O, (2011) A third of the yeast mitochondrial proteome is dual localized: a question of evolution. Proteomics 11: 4468-4476.
60. Regev-Rudzki N, Karniely S, Ben-Haim NN, Pines O, (2005) Yeast aconitase in two locations and two metabolic pathways: seeing small amounts is believing. Mol Biol Cell 16: 4163-4171.
61. Yogev O, Naamati A, Pines O, (2011) Fumarase: a paradigm of dual targeting and dual localized functions. FEBS J 278: 4230-4242.
62. Vanhee C, Guillon S, Masquelier D, Degand H, Deleu M, et al. (2011) A TSPO-related protein localizes to the early secretory pathway in Arabidopsis, but is targeted to mitochondria when expressed in yeast. J Exp Bot 62: 497-508.
63. Byun-McKay SA, Geeta R, (2007) Protein subcellular relocalization: a new perspective on the origin of novel genes. TRENDS Ecol Evol 22: 338-344.
64. Stohs SJ, Bagchi D, (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18: 321-336.
65. Cobine PA, Ojeda LD, Rigby KM, Winge DR, (2004) Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J Biol Chem 279: 14447-14455.
66. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
67. Fitzpatrick DA, (2012) Horizontal gene transfer in fungi. FEMS Microbiol Lett 329: 1-8.
68. Sprockett DD, Piontkivska H, Blackwood CB, (2011) Evolutionary analysis of glycosyl hydrolase family 28 (GH28) suggests lineage-specific expansions in necrotrophic fungal pathogens. Gene 479: 29-36.