The cytochromes P450 of Grosmannia clavigera: Genome organization, phylogeny, and expression in response to pine host chemicals

Fungal Genetics and Biology

Volumn 50, Issue 1, 2013, Pages 72-81

  Lah, Ljerka ^a,c   Haridas, Sajeet ^a   Bohlmann, Joerg ^b   Breuil, Colette ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

CYP; Cytochrome P450; Fatty acid; Grosmannia clavigera; Lodgepole pine; Monoterpene

Indexed keywords

CYTOCHROME P450; OLEIC ACID; TERPENE; TRANSCRIPTOME; TRIACYLGLYCEROL;

ARTICLE; ASCOMYCETES; CARBON SOURCE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CYTOCHROME P450 GENE; DETOXIFICATION; FUNGAL GENE; FUNGAL GENOME; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE CLUSTER; GENE EXPRESSION REGULATION; GENOME ANALYSIS; GROSMANNIA CLAVIGERA; HOST PATHOGEN INTERACTION; HOST RESISTANCE; METABOLITE; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHLOEM; PINE; PINUS CONTORTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; UPREGULATION;

BIOTRANSFORMATION; CYTOCHROME P-450 ENZYME SYSTEM; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE ORDER; GENOME, FUNGAL; METABOLIC NETWORKS AND PATHWAYS; MULTIGENE FAMILY; OPHIOSTOMATALES; PHYLOGENY; PINUS; PLANT EXTRACTS;

CLAVIGERA; DENDROCTONUS PONDEROSAE; PINUS CONTORTA;

EID: 84871363792     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.10.002     Document Type: Article

References (76)

1. Alamouti S.M., Wang V., Diguistini S., Six D.L., Bohlmann J., Hamelin R.C., Feau N., Breuil C. Gene genealogies reveal cryptic species and host preferences for the pine fungal pathogen Grosmannia clavigera. Molecular Ecology 2011, 20:2581-2602.
2. Altschul S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997, 25:3389-3402.
3. Balibar C.J., Walsh C.T. GliP, a multimodular nonribosomal peptide synthetase in Aspergillus fumigatus, makes the diketopiperazine scaffold of gliotoxin. Biochemistry 2006, 45:15029-15038.
4. Bolstad B.M., Irizarry R., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193.
5. Boone C.K., Aukema B.H., Bohlmann J., Carroll A.L., Raffa K.F. Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Canadian Journal of Forest Research 2011, 41:1174-1188.
6. Chiang Y.-M., Szewczyk E., Davidson A.D., Entwistle R., Keller N.P., Wang C.C.C., Oakley B.R. Characterization of the Aspergillus nidulans monodictyphenone gene cluster. Applied and Environmental Microbiology 2010, 76:2067-2074.
7. Clark E.L., Carroll A.L., Huber D.P.W. Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle. The Canadian Entomologist 2010, 142:557-573.
8. Clark E.L., Huber D.P.W., Carroll A.L. The legacy of attack: implications of high phloem resin monoterpene levels in lodgepole pines following mass attack by mountain pine beetle, Dendroctonus ponderosae Hopkins. Environmental Entomology 2012, 41:392-398.
9. Cresnar B., Petric S. Cytochrome P450 enzymes in the fungal kingdom. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2011, 1814:29-35.
10. Dalmais B., Schumacher J., Moraga J., Le Pêcheur P., Tudzynski B., Collado I.G., Viaud M. The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence with botrydial. Molecular Plant Pathology 2011, 12(6):564-579.
11. Davies P.J. Plant Hormones 2010, Springer, Netherlands, Dordrecht.
12. Demain A., Fang A. The Natural Functions of Secondary Metabolites History of Modern Biotechnology I 2000, Springer, Berlin, Heidelberg.
13. Diguistini S., Liao N.Y., Platt D., Robertson G., Seidel M., Chan S.K., Docking T.R., Birol I., Holt R.A., Hirst M., Mardis E., Marra M.A., Hamelin R.C., Bohlmann J., Breuil C., Jones S.J. De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biology 2009, 10:R94.
14. DiGuistini S., Wang Y., Liao N.Y., Taylor G., Tanguay P., Feau N., Henrissat B., Chan S.K., Hesse-Orce U., Alamouti S.M., Tsui C.K.M., Docking R.T., Levasseur A., Haridas S., Robertson G., Birol I., Holt R.A., Marra M.A., Hamelin R.C., Hirst M., Jones S.J.M., Bohlmann J., Breuil C. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:2504-2509.
15. Driggers E., Brakhage A. Metabolites and Fungal Virulence Metabolome Analyses: Strategies for Systems Biology 2005, Springer-Verlag, New York.
16. Duetz W.A., Bouwmeester H., van Beilen J.B., Witholt B. Biotransformation of limonene by bacteria, fungi, yeasts, and plants. Applied Microbiology and Biotechnology 2003, 61:269-277.
17. Faber B.W., van Gorcom R.F.M., Duine J.A. Purification and characterization of benzoate-para-hydroxylase, a cytochrome P450 (CYP53A1), from Aspergillus niger. Archives of Biochemistry and Biophysics 2001, 394:245-254.
18. Ferrer-Sevillano F., Fernández-Cañón J.M. Novel phacB-encoded cytochrome P450 monooxygenase from Aspergillus nidulans with 3-hydroxyphenylacetate 6-hydroxylase and 3,4-dihydroxyphenylacetate 6-hydroxylase activities. Eukaryotic Cell 2007, 6:514-520.
19. Fujii T., Nakamura K., Shibuya K., Tanase S., Gotoh O., Ogawa T., Fukuda H. Structural characterization of the gene and corresponding cDNA for the cytochrome P450rm from Rhodotorula minuta which catalyzes formation of isobutene and 4-hydroxylation of benzoate. Molecular and General Genetics MGG 1997, 256:115-120.
20. Fukuda H., Nakamura K., Sukita E., Ogawa T., Fujii T. Cytochrome P450rm from Rhodotorula minuta catalyzes 4-hydroxylation of benzoate. Journal of Biochemistry 1996, 119:314-318.
21. Georgianna D.R., Fedorova N.D., Burroughs J.L., Dolezal A.L., Bok J.W., Horowitz-Brown S., Woloshuk C.P., Yu J., Keller N.P., Payne G.A. Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters. Molecular Plant Pathology 2010, 11:213-226.
22. Hesse-Orce U., DiGuistini S., Keeling C.I., Wang Y., Li M., Henderson H., Docking T.R., Liao N.Y., Robertson G., Holt R.A., Jones S.J.M., Bohlmann J., Breuil C. Gene discovery for the bark beetle-vectored fungal tree pathogen Grosmannia clavigera. BMC Genomics 2010, 11:536.
23. Hofstetter R.W., Mahfouz J.B., Klepzig K.D., Ayres M.P. Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. Journal of Chemical Ecology 2005, 31:539-560.
24. Hwang B.K., Lim S.W., Kim B.S., Lee J.Y., Moon S.S. Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Applied and Environmental Microbiology 2001, 67:3739-3745.
25. Ide M., Ichinose H., Wariishi H. Molecular identification and functional characterization of cytochrome P450 monooxygenases from the brown-rot basidiomycete Postia placenta. Archives of Microbiology 2012, 194:243-253.
26. Ikeda R., Sugita T., Jacobson E.S., Shinoda T. Effects of melanin upon susceptibility of Cryptococcus to antifungals. Microbiology and Immunology 2003, 47:271-277.
27. Kal A.J., van Zonneveld A.J., Benes V., van den Berg M., Koerkamp M.G., Albermann K., Strack N., Ruijter J.M., Richter A., Dujon B., Ansorge W., Tabak H.F. Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Molecular Biology of the Cell 1999, 10:1859-1872.
28. Kalb V.F., Woods C.W., Turi T.G., Dey C.R., Sutter T.R., Loper J.C. Primary structure of the P450 lanosterol demethylase gene from Saccharomyces cerevisiae. DNA 1987, 6:529-537.
29. Keeling C.I., Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. The New Phytologist 2006, 170:657-675.
30. Keller N.P., Turner G., Bennett J.W. Fungal secondary metabolism - from biochemistry to genomics. Nature Reviews Microbiology 2005, 3:937-947.
31. Kelly S.L., Lamb D.C., Corran A.J., Baldwin B.C., Parks L.W., Kelly D.E. Purification and reconstitution of activity of Saccharomyces cerevisiae P450 61, a sterol delta 22-desaturase. FEBS Letters 1995, 377:217-220.
32. Kelly S.L., Lamb D.C., Cannieux M., Greetham D., Jackson C.J., Marczylo T., Ugochukwu C., Kelly D.E. An old activity in the cytochrome P450 superfamily (CYP51) and a new story of drugs and resistance. Biochemical Society Transactions 2001, 29:122-128.
33. Kelly D.E., Krasevec N., Mullins J., Nelson D.R. The CYPome (Cytochrome P450 complement) of Aspergillus nidulans. Fungal Genetics and Biology: FG & B 2009, 46(Suppl. 1):S53-S61.
34. Kempken F., Rohlfs M. Fungal secondary metabolite biosynthesis - a chemical defence strategy against antagonistic animals?. Fungal Ecology 2010, 3:107-114.
35. Khaldi N., Seifuddin F.T., Turner G., Haft D., Nierman W.C., Wolfe K.H., Fedorova N.D. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genetics and Biology: FG & B 2010, 47:736-741.
36. Kimura M., Tokai T., Takahashi-Ando N., Ohsato S., Fujimura M. Molecular and genetic studies of fusarium trichothecene biosynthesis: pathways, genes, and evolution. Bioscience, Biotechnology, and Biochemistry 2007, 71:2105-2123.
37. 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. The Journal of Biological Chemistry 2000, 275:39734-39740.
38. Kitazume T., Tanaka A., Takaya N., Nakamura A., Matsuyama S., Suzuki T., Shoun H. Kinetic analysis of hydroxylation of saturated fatty acids by recombinant P450foxy produced by an Escherichia coli expression system. European Journal of Biochemistry 2002, 269:2075-2082.
39. Kitazume T., Yamazaki Y., Matsuyama S., Shoun H., Takaya N. Production of hydroxy-fatty acid derivatives from waste oil by Escherichia coli cells producing fungal cytochrome P450foxy. Applied Microbiology and Biotechnology 2008, 79:981-988.
40. Kopper B.J., Illman B.L., Kersten P.J., Klepzig K.D., Raffa K.F. Effects of diterpene acids on components of a conifer bark beetle-fungal interaction: tolerance by ips pini and sensitivity by its associate Ophiostoma ips. Environmental Entomology 2005, 34:486-493.
41. Lah L., Krasevec N., Trontelj P., Komel R. High diversity and complex evolution of fungal cytochrome P450 reductase: cytochrome P450 systems. Fungal Genetics and Biology 2008, 45:446-458.
42. Lah L., Podobnik B., Novak M., KoroŠec B., Berne S., Vogelsang M., KraŠevec N., Zupanec N., Stojan J., Bohlmann J., Komel R. The versatility of the fungal cytochrome P450 monooxygenase system is instrumental in xenobiotic detoxification. Molecular Microbiology 2011, 81:1374-1389.
43. Lee S., Kim J.-J., Breuil C. Pathogenicity of Leptographium longiclavatum associated with Dendroctonus ponderosae to Pinus contorta. Canadian Journal of Forest Research 2006, 36:2864-2872.
44. Li Y., Image I.I., Xu W., Image I., Tang Y. Classification, prediction, and verification of the regioselectivity of fungal polyketide synthase product template domains. The Journal of Biological Chemistry 2010, 285:22764-22773.
45. Massoumi Alamouti S., Tsui C.K.M., Breuil C. Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycological Research 2009, 113:822-835.
46. Matsuzaki F., Wariishi H. Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochemical and Biophysical Research Communications 2005, 334:1184-1190.
47. Matsuzaki F., Shimizu M., Wariishi H. Proteomic and metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. Journal of Proteome Research 2008, 7:2342-2350.
48. Mendonça A.de L., da Silva C.E., de Mesquita F.L.T., Campos R.da S., Do Nascimento R.R., Ximenes E.C.P.de A., Sant'Ana A.E.G. Antimicrobial activities of components of the glandular secretions of leaf cutting ants of the genus Atta. Antonie van Leeuwenhoek 2009, 95:295-303.
49. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 2008, 5:621-628.
50. Nakayama N., Takemae A., Shoun H. Cytochrome P450foxy, a catalytically self-sufficient fatty acid hydroxylase of the fungus Fusarium oxysporum. Journal of Biochemistry 1996, 119:435-440.
51. Nelson D.R. The cytochrome p450 homepage. Human Genomics 2009, 4:59-65.
52. Nelson D.R. Progress in tracing the evolutionary paths of cytochrome P450. Biochimica et Biophysica Acta 2011, 1814:14-18.
53. Perrin R.M., Fedorova N.D., Bok J.W., Cramer R.A., Wortman J.R., Kim H.S., Nierman W.C., Keller N.P. Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathogens 2007, 3:e50.
54. Podobnik B., Stojan J., Lah L., Krasevec N., Seliskar M., Lanisnik Rizner T., Rozman D., Komel R. CYP53A15 of Cochliobolus lunatus, a target for natural antifungal compounds. Journal of Medicinal Chemistry 2008, 51:3480-3486.
55. Porter T.D., Beck T.W., Kasper C.B. NADPH-cytochrome P-450 oxidoreductase gene organization correlates with structural domains of the protein. Biochemistry 1990, 29:9814-9818.
56. Proctor R.H., Brown D.W., Plattner R.D., Desjardins A.E. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genetics and Biology 2003, 38:237-249.
57. Pureswaran D.S., Gries R., Borden J.H. Quantitative variation in monoterpenes in four species of conifers. Biochemical Systematics and Ecology 2004, 32:1109-1136.
58. Raffa K.F., Aukema B.H., Bentz B.J., Carroll A.L., Hicke J.A., Turner M.G., Romme W.H. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 2008, 58:501.
59. Robinson-Jeffrey R., Davidson R.W. Three new Europhium species with Verticicladiella imperfect states on blue-stained pine. Canadian Journal of Botany 1968, 46:1523-1527.
60. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
61. Ruiz B., Chávez A., Forero A., García-Huante Y., Romero A., Sánchez M., Rocha D., Sánchez B., Rodríguez-Sanoja R., Sánchez S., Langley E. Production of microbial secondary metabolites: regulation by the carbon source. Critical Reviews in Microbiology 2010, 36:146-167.
62. Safranyik, L., Carroll, A.L., 2006. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In: Safranyik, L., Wilson, B., (Eds.), The Mountain Pine Beetle a Synthesis of Biology Management and Impacts on Lodgepole Pine. Natural Resources Canada, Victoria, pp. 3-66.
63. Shishova E.Y., Di Costanzo L., Cane D.E., Christianson D.W. X-ray crystal structure of aristolochene synthase from Aspergillus terreus and evolution of templates for the cyclization of farnesyl diphosphate. Biochemistry 2007, 46:1941-1951.
64. Skaggs B.A., Alexander J.F., Pierson C.A., Schweitzer K.S., Chun K.T., 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, 169:105-109.
65. Sono M., Roach M.P., Coulter E.D., Dawson J.H. Heme-containing oxygenases. Chemical Reviews 1996, 96:2841-2888.
66. Strobel H.W., Hodgson A.V., Shen S. Cytochrome P450: Structure, Mechanism, and Biochemistry (Google eBook) 1995, Plenum Press, New York. second ed.
67. Szewczyk E., Chiang Y.-M., Oakley C.E., Davidson A.D., Wang C.C.C., Oakley B.R. Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Applied and Environmental Microbiology 2008, 74:7607-7612.
68. Tanguay P., Loppnau P., Morin C., Bernier L., Breuil C. A spontaneous albino mutant of Ceratocystis resinifera results from a point mutation in the polyketide synthase gene, PKS1. Canadian Journal of Microbiology 2006, 52:501-507.
69. Van Den Brink J.M., Punt P.J., Van Gorcom R.F.M., Van Den Hondel C.A.M.J.J. Regulation of expression of the Aspergillus niger benzoate para-hydroxylase cytochrome P450 system. Molecular and General Genetics MGG 2000, 263:601-609.
70. Van Der Werf M.J., Boot A.M. Metabolism of carveol and dihydrocarveol in Rhodococcus erythropolis DCL14. Microbiology 2000, 146(Pt 5):1129-1141.
71. Van der Werf M.J., Swarts H.J., de Bont J.A.M. Rhodococcus erythropolis DCL14 contains a novel degradation pathway for limonene. Applied and Environmental Microbiology 1999, 65:2092-2102.
72. Wang Y., DiGuistini S., Wang T.-C.T., Bohlmann J., Breuil C. Agrobacterium-meditated gene disruption using split-marker in Grosmannia clavigera, a mountain pine beetle associated pathogen. Current Genetics 2010, 56:297-307.
73. Yamaoka Y., Hiratsuka Y., Maruyama P.J. The ability of Ophiostoma clavigerum to kill mature lodgepolepine trees. Forest Pathology 1995, 25:401-404.
74. Yong G., Tao C., Breuil C. Identification and quantification of nonvolatile lipophilic substances in fresh sapwood and heartwood of lodgepole pine (Pinus contorta Dougl.). Holzforschung 1995, 49:20-28.
75. Yu J.-H., Keller N. Regulation of secondary metabolism in filamentous fungi. Annual Review of Phytopathology 2005, 43:437-458.
76. Yu J., Chang P.-K., Ehrlich K.C., Cary J.W., Bhatnagar D., Cleveland T.E., Payne G.A., Linz J.E., Woloshuk C.P., Bennett J.W. Clustered pathway genes in aflatoxin biosynthesis. Applied and Environmental Microbiology 2004, 70:1253-1262.