Genome-wide analysis of cytochrome p450s of trichoderma spp.: Annotation and evolutionary relationships

Fungal Biology and Biotechnology

Volumn 5, Issue 1, 2018, Pages 1-15

  Chadha, Sonia ^a   Mehetre, Sayaji T ^a   Bansal, Ravindra ^a   Kuo, Alan ^b   Aerts, Andrea ^b   Grigoriev, Igor V ^b   Druzhinina, Irina S ^c   Mukherjee, Prasun K ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

^b DOE JOINT GENOME INSTITUTE   (United States)

^c VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85068876817     PISSN: None     EISSN: 20543085     Source Type: Journal    
DOI: 10.1186/s40694-018-0056-3     Document Type: Article

References (82)

1. Druzhinina I, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol. 2011;9:749–59.
2. Bissett J, Gams W, Jaklitsch W, Samuels GJ. Accepted Trichoderma names in the year 2015. IMA Fungus. 2015;6:263–95.
3. Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M. Trichoderma in agriculture, industry and medicine: an overview. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M, editors. Trichoderma: biology and applications. Oxfordshire: CABI; 2013. p. 152–72.
4. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM. Trichoderma research in the genome era. Annu Rev Phytopathol. 2013;51:105–29.
5. Hatvani L, Manczinger L, Vágvölgyi C, Kredics L. Trichoderma as a human pathogen. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M, editors. Trichoderma: Biology and Applications. Oxfordshire: CABI; 2013. p. 152–72.
6. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol. 2008;26:553–60.
7. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 2011;12:R40.
8. Schmoll M, Dattenböck C, Carreras-Villaseñor N, Mendoza-Mendoza A, Tisch D, Alemán MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, et al. The genomes of three uneven siblings: footprints of the lifestyles of three Trichoderma species. Microbiol Mol Biol Rev. 2016;80:205–327.
9. Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42(D1):D699–704.
10. Degtyarenko KN. Structural domains of P450-containing monooxygenase systems. Protein Eng. 1995;8:737–47.
11. Klingenberg M. Pigments of rat liver microsomes. Arch Biochem Biophys. 1958;75:376–86.
12. Han Y, Liu X, Benny U, Kistler HC, VanEtten HD. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J. 2001;25:305–14.
13. Siewers V, Viaud M, Jimenez-Teja D, Collado IG, Gronover CS, Pradier JM, Tudzynsk B, Tudzynski P. Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor. MPMI. 2005;18:602–12.
14. Fan J, Urban M, Parker JE, Brewer HC, Kelly SL, Hammond-Kosack KE, Fraaije BA, Liu X, Cools HJ. Characterization of the sterol 14α-demethylases of Fusarium graminearum identifies a novel genus-specific CYP51 function. New Phytol. 2013;198:821–35.
15. Takaoka S, Kurata M, Harimoto Y, Hatta R, Yamamoto M, Akimitsu K, Tsuge T. Complex regulation of secondary metabolism controlling pathogenicity in the phytopathogenic fungus Alternaria alternata. New Phytol. 2014;202:1297–309.
16. Zhang DD, Wang XY, Chen JY, Kong ZQ, Gui YJ, Li NY, Bao YM, Dai XF. Identification and characterization of a pathogenicity-related gene VdCYP1 from Verticillium dahliae. Sci Rep. 2016;6:27979.
17. Bernhardt R. Cytochromes P450 as versatile biocatalysts. J Biotechnol. 2006;124:128–45.
18. Urlacher VB, Eiben S. Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol. 2006;24:324–30.
19. Kizawa H, Tomura D, Oda M, Fukamizu A, Hoshino T, Gotoh O, Yasui T, Shoun H. Nucleotide sequence of the unique nitrate/nitrite inducible cytochrome P450 cDNA from Fusarium oxysporum. J Biol Chem. 1991;266:10632–7.
20. Lamb DC, Skaug T, Song HL, Jackson CJ, Podust LM, Waterman MR, Kell DB, Kelly DE, Kelly SL. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3 (2). J Biol Chem. 2002;277:24000–5.
21. Nelson DR. Cytochrome P450 and the individuality of species. Arch Biochem Biophys. 1999;369:1–10.
22. Nebert D, Adesnik M, Coon MJ, Estabrook RW, Gonzalez FJ, Guengerich FP, Gunsalus IC, Johnson EF, Kemper B, Levin W, et al. The P450 gene superfamily: recommended nomenclature. DNA. 1987;6:1–11.
23. Nelson DR, Koymans L, Kamataki T, Stegeman JJ, Feyereisen R, Waxman DJ, Waterman MR, Gotoh O, Coon MJ, Estabrook RW, Gunsalus IC, Nebert DW. P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenet. 1996;6:1–42.
24. Nelson D, Werck-Reichhart DA. P450-centric view of plant evolution. Plant J. 2011;66(1):194–211.
25. Nelson DR. Metazoan cytochrome P450 evolution. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998;121(1–3):15–22.
26. Deng J, Carbone I, Dean RA. The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes. BMC Evol Biol. 2007;7(1):10–30.
27. Park J, Choi J, Ahn K, Park B, Park J, Kang S, Lee Y-H. Fungal cytochrome P450 database. BMC Bioinform. 2008;9:402.
28. Hoffmeister D, Keller NP. Natural products of filamentous fungi, enzymes, genes and their regulation. Nat Prod Rep. 2007;24:393–416.
29. Kelly DE, Kraševec N, Mullins J, Nelson DR. The CYPome (cytochrome P450 complement) of Aspergillus nidulans. Fungal Genet Biol. 2009;46:S53–61.
30. Kelly SL, Kelly DE. Microbial cytochromes P450: biodiversity and biotechnology. Where do cytochrome P450 come from, what do they do and what can they do for us? Philos Trans R Soc Lond B Biol Sci. 2013;368(1612):20120476.
31. Ichinose H. Metabolic diversity and cytochromes P450 of fungi. In: Yamazaki H, editor. Fifty years of cytochrome P450 research. Tokyo: Springer; 2014. p. 187–205.
32. Syed K, Yadav JS. P450 monooxygenases (P450ome) of the model white rot fungus Phanerochaete chrysosporium. Crit Rev Microbiol. 2012;38(4):339–63.
33. Newsome AW, Nelson D, Corran A, Kelly SL, Kelly DE. The cytochrome P450 complement (CYPome) of Mycosphaerella graminicola. Biotechnol Appl Biochem. 2013;60:52–64.
34. Lah L, Haridas S, Bohlmann J, Breuil C. The cytochromes P450 of Gros-mannia clavigera: genome organization, phylogeny, and expression in response to pine host chemicals. Fungal Genet Biol. 2013;50:72–81.
35. Chen W, Lee MK, Jefcoate C, Kim SC, Chen F, Yu JH. Fungal cytochrome p450 monooxygenases: their distribution, structure, functions, family expansion, and evolutionary origin. Genome Biol Evol. 2014;6(7):1620–34.
36. Moktali V, Park J, Fedorova-Abrams ND, Park B, Choi J, Lee YH, Kang S. Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes. BMC Genom. 2012;13(1):525.
37. Sirim D, Widmann M, Wagner F, Pleiss J. Prediction and analysis of the modular structure of cytochrome P450 monooxygenases. BMC Struct Biol. 2010;10:34.
38. Sezutsu H, Le Goff G, Feyereisen R. Origins of P450 diversity. Philos Trans R Soc B. 2013;368:20120428.
39. Werck-Reichhart D, Feyereisen R. Cytochromes P450: a success story. Genome Biol. 2000;1:6.
40. Gotoh O. Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J Biol Chem. 1992;267:83–90.
41. Syed K, Mashele SS. Comparative analysis of P450 signature motifs EXXR and CXG in the large and diverse kingdom of fungi: identification of evolutionarily conserved amino acid patterns characteristic of P450 Family. PLoS ONE. 2014;9(4):e95616.
42. Bailey BA, Melnick RL. The endophytic Trichoderma. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M, editors. Trichoderma: biology and applications. Oxfordshire: CABI; 2013. p. 152–72.
43. Komon-Zelazowska M, Bissett J, Zafari D, Hatvani L, Manczinger L, Woo S, Lorito M, Kredics L, Kubicek CP, Druzhinina IS. Genetically closely related but phenotypically divergent Trichoderma species cause green mold disease in oyster mushroom farms worldwide. Appl Environ Microbiol. 2007;73(22):7415–26.
44. Zaidi NW, Singh US. Trichoderma in plant health management. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M, editors. Trichoderma: biology and applications. Oxfordshire: CABI; 2013. p. 152–72.
45. Zeilinger S, Gruber S, Bansal R, Mukherjee PK. Secondary metabolism in Trichoderma—chemistry meets genomics. Fungal Biol Rev. 2016;30(2):74–90.
46. Ramírez-Valdespino CA, Porras-Troncoso MD, Corrales-Escobosa AR, Wro-bel K, Martínez-Hernández P, Olmedo-Monfil V. Functional characterization of TvCyt2, a member of the p450 monooxygenases from Trichoderma virens relevant during the association with plants and mycoparasitism. Mol Plant Microbe Interact. 2018;31:289–98.
47. Ichinose H. Cytochrome P450 of wood-rotting basidiomycetes and biotechnological applications. Biotechnol Appl Biochem. 2013;60:71–81.
48. Bhattacharya SS, Syed K, Shann J, Yadav JS. A novel P450-initiated biphasic process for sustainable biodegradation of benzo[a]pyrene in soil under nutrient-sufficient conditions by the white rot fungus Phanerochaete chrysosporium. J Hazard Mater. 2013;261:675–83.
49. Wang J, Yamamoto R, Yamamoto Y, Tokumoto T, Dong J, Thomas P, Hirai H, Kawagishi H. Hydroxylation of bisphenol A by hyper lignin-degrading fungus Phanerochaete sordida YK-624 under non-ligninolytic condition. Chemosphere. 2013;93:1419–23.
50. Akiyama R, Kajiwara S, Shishido K. Catalytic reaction of basidiomycete Lentinula edodes cytochrome P450, Le. CYP1 enzyme produced in yeast. Biosci Biotechnol Biochem. 2004;68:79–84.
51. Ichinose H, Wariishi H, Tanaka H. Identification and heterologous expression of the cytochrome P450 oxidoreductase from the white-rot basidiomycete Coriolus versicolor. Appl Microbiol Biotechnol. 2002;59:658–64.
52. Mgbeahuruike AC, Kovalchuk A, Ubhayasekera W, Nelson DR, Yadav JS. CYPome of the conifer pathogen Heterobasidion irregulare: inventory, phylogeny, and transcriptional analysis of the response to biocontrol. Fungal Biol. 2017;121:158–71.
53. Eschenfeldt WH, Zhang Y. H, Samaha H, Stols L, Eirich LD, Wilson CR. Donnelly MI. Transformation of fatty acids catalyzed by cytochrome P450 monooxygenase enzymes of Candida tropicalis. Appl Environ Microbiol. 2003;69:5992–9.
54. Skaggs BA, Alexander JF, Pierson CA, Schweitzer KS, Chun KT, Koegel C, Barbuch R, Bard M. Cloning and characterization of the Saccharomyces cerevisiae C-22 sterol desaturase gene, encoding a second cytochrome P-450 involved in ergosterol biosynthesis. Gene. 1996;169:105–9.
55. Becher R, Wirsel SG. Fungal cytochrome P450 sterol 14 alpha-demethy-lase (CYP51) and azole resistance in plant and human pathogens. Appl Microbiol Biotechnol. 2012;95:825–40.
56. Keller G, Turner NP, Bennett JW. Fungal secondary metabolism-from biochemistry to genomics. Nat Rev Microbiol. 2005;3:937–47.
57. Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O’Donnell K. Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc Natl Acad Sci USA. 2002;99:9278–83.
58. Jensen S, Shen L, Liu J. Combining phylogenetic motif discovery and motif clustering to predict co-regulated genes. Bioinformatics. 2005;21:3832–9.
59. Melo NR, Moran GP, Warrilow AGS, Dudley E, Smith SN, Sullivan DJ, Lamb DC, Kelly DE, Coleman DC, Kelly SL. CYP56 (Dit2p) in Candida albicans: characterization and investigation of its role in growth and antifungal drug susceptibility. Antimicrob Agents Chemother. 2008;52:3718–24.
60. Crešnar B, Petrič S. Cytochrome P450 enzymes in the fungal kingdom. Biochim Biophys Acta. 2011;1814:29–35.
61. Briza P, Eckerstorfer M, Breitenbach M. The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble LL-dityrosine-containing precursor of the yeast spore wall. Proc Natl Acad Sci USA. 1994;91(10):4524–8.
62. Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE. Inactivation of a cytochrome PJ450 is a determinant of trichothecene diversity in Fusarium species. Fungal Genet Biol. 2002;36:224–33.
63. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang B, Fang W, Wang S, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia Y, Wang C. Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet. 2011;7(1):e1001264.
64. Kitazume T, Takaya N, Nakayama N, Shoun H. Fusarium oxysporum fatty-acid subterminal hydroxylase (CYP505) is a membrane-bound eukaryotic counterpart of Bacillus megaterium cytochrome P450BM3. J Biol Chem. 2000;275:39734–40.
65. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Oliver SG, Talbot NJ. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE. 2008;3(6):e2300.
66. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E, Gutiérrez S. Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl Environ Microbiol. 2012;78:4856–68.
67. Bansal R, Sherkhane PD, Oulkar D, Khan Z, Banerjee K, Mukherjee PK. The viridin biosynthesis gene cluster of Trichoderma virens and its conserv-ancy in the bat white-nose fungus Pseudogymnoascus destructans. Chem Select. 2018;3:1289–93.
68. Nelson DR. The cytochrome P450 homepage. Hum Genom. 2009;4:59–65.
69. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011;39:225–9.
70. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2017. https://doi.org/10.1093/bib/bbx108.
71. Larsson A. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics. 2014;30:3276–8.
72. Crooks GE, Hon G, Chandoniam JM, Brennerm SE. WebLogo: a sequence logo generator. Genome Res. 2004;2004(14):1188–90.
73. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 2004;5:113.
74. Rzhetsky A, Nei MA. Simple method for estimating and testing minimum evolution trees. Mol Biol Evol. 1992;9:945–67.
75. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91.
76. Zuckerkandl E, Pauling L. Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. Evolving genes and proteins. New York: Academic Press; 1965. p. 97–166.
77. Nei M, Kumar S. Molecular evolution and phylogenetics. New York: Oxford University Press; 2000.
78. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.
79. 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;28:2731–9.
80. Rambaut A. FigTree v1.4.3: Tree figure drawing tool. 2016. http://tree.bio. ed.ac.uk/software/figtree/. Accessed 5 Feb 2018.
81. Bansal R, Mukherjee PK. Identification of novel gene clusters for secondary metabolism in Trichoderma genomes. Microbiology. 2016;85:185–90.
82. Bansal R, Mukherjee PK. The terpenoid biosynthesis toolkit of Trichoderma. Nat Prod Commun. 2016;11:431–4.