Impacts of diversification of cytochrome P450 on plant metabolism

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 6, 2012, Pages 824-832

  Mizutani, Masaharu ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

Metabolic engineering; P450; Phytohormone; Terpenoid

Indexed keywords

ALKALOID; BISBENZYLISOQUINOLINE ALKALOID; CYTOCHROME P450; GLYCYRRHIZIC ACID; PACLITAXEL; PHYTOHORMONE; PLANT MEDICINAL PRODUCT; SAPONIN; TERPENOID;

CATALYSIS; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE; GENE CLUSTER; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME ANALYSIS; HOMEOSTASIS; HORMONE SYNTHESIS; LARGE SCALE PRODUCTION; METABOLIC ENGINEERING; NONHUMAN; OXYGENATION; P450 GENE; PLANT DEFENSE; PLANT EVOLUTION; PLANT GENOME; PLANT METABOLISM; PROTEIN FAMILY; REVIEW; SPECIES DIFFERENCE;

EID: 84861900283     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.35.824     Document Type: Review

References (84)

1. Nelson D, Werck-Reichhart D. A P450-centric view of plant evolution. Plant J., 66, 194-211 (2011).
2. Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S. Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol., 135, 756-772 (2004).
3. Nelson DR, Ming R, Alam M, Schuler MA. Comparison of cytochrome P450 genes from six plant genomes. Tropical Plant Biol., 1, 216-235 (2008).
4. Mizutani M, Ohta D. Diversification of P450 genes during land plant evolution. Annu. Rev. Plant Biol., 61, 291-315 (2010).
5. Bak S, Kahn RA, Olsen CE, Halkier BA. Cloning and expression in Escherichia coli of the obtusifoliol 14 α-demethylase of Sorghum bicolor (L.) MOENCH, a cytochrome P450 orthologous to the sterol 14 α-demethylases (CYP51) from fungi and mammals. Plant J., 11, 191-201 (1997).
6. Morikawa T, Mizutani M, Aoki N, Watanabe B, Saga H, Saito S, Oikawa A, Suzuki H, Sakurai N, Shibata D, Wadano A, Sakata K, Ohta D. Cytochrome P450 CYP710A encodes the sterol C-22 desaturase in Arabidopsis and tomato. Plant Cell, 18, 1008-1022 (2006).
7. Kim J, DellaPenna D. Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid β-ring hydroxylase CYP97A3. Proc. Natl. Acad. Sci. U.S.A., 103, 3474-3479 (2006).
8. Tian L, Musetti V, Kim J, Magallanes-Lundback M, DellaPenna D. The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid ε-ring hydroxylation activity. Proc. Natl. Acad. Sci. U.S.A., 101, 402-407 (2004).
9. Mizutani M, Ward E, DiMaio J, Ohta D, Ryals J, Sato R. Molecular cloning and sequencing of a cDNA encoding mung bean cytochrome P450 (P450C4H) possessing cinnamate 4-hydroxylase activity. Biochem. Biophys. Res. Commun., 190, 875-880 (1993).
10. Teutsch HG, Hasenfratz MP, Lesot A, Stoltz C, Garnier JM, Jeltsch JM, Durst F, Werck-Reichhart D. Isolation and sequence of a cDNA encoding the Jerusalem artichoke cinnamate 4-hydroxylase, a major plant cytochrome P450 involved in the general phenylpropanoid pathway. Proc. Natl. Acad. Sci. U.S.A., 90, 4102-4106 (1993).
11. Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C. The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J., 30, 33-45 (2002).
12. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D. CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem., 276, 36566-36574 (2001).
13. Pollard M, Beisson F, Li Y, Ohlrogge JB. Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci., 13, 236-246 (2008).
14. Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu. Rev. Plant Biol., 59, 683-707 (2008).
15. Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Yephremov A. Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid ω-hydroxylation in development. Proc. Natl. Acad. Sci. U.S.A., 98, 9694-9699 (2001).
16. Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J., 23, 2903-2913 (2004).
17. Kandel S, Sauveplane V, Olry A, Diss L, Benveniste I, Pinot F. Cytochrome P450-dependent fatty acid hydroxylases in plants. Phytochem. Rev., 5, 359-372 (2006).
18. Li Y, Beisson F. The biosynthesis of cutin and suberin as an alternative source of enzymes for the production of bio-based chemicals and materials. Biochimie, 91, 685-691 (2009).
19. Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L, Franke R, Pinot F. CYP86B1 is required for very long chain ω-hydroxyacid and α,ω-dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiol., 150, 1831-1843 (2009).
20. Morant M, Jørgensen K, Schaller H, Pinot F, Møller BL, Werck-Reichhart D, Bak S. CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell, 19, 1473-1487 (2007).
21. Takei K, Yamaya T, Sakakibara H. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J. Biol. Chem., 279, 41866-41872 (2004).
22. Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M. Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol., 134, 1439-1449 (2004).
23. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J., 23, 1647-1656 (2004).
24. Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA, Peacock WJ, Dennis ES. Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc. Natl. Acad. Sci. U.S.A., 95, 9019-9024 (1998).
25. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ. The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc. Natl. Acad. Sci. U.S.A., 98, 2065-2070 (2001).
26. Yamaguchi S., A gene encoding steviol synthase and a method for producing steviol. JP2008237110 (2008).
27. Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z. ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell, 18, 442-456 (2006).
28. Zhang Y, Zhang B, Yan D, Dong W, Yang W, Li Q, Zeng L, Wang J, Wang L, Hicks LM, He Z. Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. Plant J., 67, 342-353 (2011).
29. Bishop GJ, Yokota T. Plants steroid hormones, brassinosteroids: current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response. Plant Cell Physiol., 42, 114-120 (2001).
30. Ohnishi T, Yokota T, Mizutani M. Insights into the function and evolution of P450s in plant steroid metabolism. Phytochemistry, 70, 1918-1929 (2009).
31. Bishop GJ, Nomura T, Yokota T, Harrison K, Noguchi T, Fujioka S, Takatsuto S, Jones JD, Kamiya Y. The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc. Natl. Acad. Sci. U.S.A., 96, 1761-1766 (1999).
32. Nomura T, Kushiro T, Yokota T, Kamiya Y, Bishop GJ, Yamaguchi S. The last reaction producing brassinolide is catalyzed by cytochrome P-450s, CYP85A3 in tomato and CYP85A2 in Arabidopsis. J. Biol. Chem., 280, 17873-17879 (2005).
33. Kim TW, Hwang JY, Kim YS, Joo SH, Chang SC, Lee JS, Takatsuto S, Kim SK. Arabidopsis CYP85A2, a cytochrome P450, mediates the Baeyer-Villiger oxidation of castasterone to brassinolide in brassinosteroid biosynthesis. Plant Cell, 17, 2397-2412 (2005).
34. Fujita S, Ohnishi T, Watanabe B, Yokota T, Takatsuto S, Fujioka S, Yoshida S, Sakata K, Mizutani M. Arabidopsis CYP90B1 catalyses the early C-22 hydroxylation of C27, C28 and C29 sterols. Plant J., 45, 765-774 (2006).
35. Ohnishi T, Szatmari AM, Watanabe B, Fujita S, Bancos S, Koncz C, Lafos M, Shibata K, Yokota T, Sakata K, Szekeres M, Mizutani M. C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell, 18, 3275-3288 (2006).
36. Ohnishi T, Watanabe B, Sakata K, Mizutani M. CYP724B2 and CYP90B3 function in the early C-22 hydroxylation steps of brassinosteroid biosynthetic pathway in tomato. Biosci. Biotechnol. Biochem., 70, 2071-2080 (2006).
37. Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol., 24, 105-109 (2006).
38. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, Chory J. BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A., 96, 15316-15323 (1999).
39. Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Wang H, Torres QI, Ward JM, Murthy G, Zhang J, Walker JC, Neff MM. BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J., 42, 23-34 (2005).
40. Ohnishi T, Nomura T, Watanabe B, Ohta D, Yokota T, Miyagawa H, Sakata K, Mizutani M. Tomato cytochrome P450 CYP734A7 functions in brassinosteroid catabolism. Phytochemistry, 67, 1895-1906 (2006).
41. Sakamoto T, Kawabe A, Tokida-Segawa A, Shimizu B, Takatsuto S, Shimada Y, Fujioka S, Mizutani M. Rice CYP734As function as multisubstrate and multifunctional enzymes in brassinosteroid catabolism. Plant J., 67, 1-12 (2011).
42. Song WC, Funk CD, Brash AR. Molecular cloning of an allene oxide synthase: a cytochrome P450 specialized for the metabolism of fatty acid hydroperoxides. Proc. Natl. Acad. Sci. U.S.A., 90, 8519-8523 (1993).
43. Koo AJ, Cooke TF, Howe GA. Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc. Natl. Acad. Sci. U.S.A., 108, 9298-9303 (2011).
44. Kitaoka N, Matsubara T, Sato M, Takahashi K, Wakuta S, Kawaide H, Matsui H, Nabeta K, Matsuura H. Arabidopsis CYP94B3 encodes jasmonyl-L-isoleucine 12-hydroxylase, a key enzyme in the oxidative catabolism of jasmonate. Plant Cell Physiol., 52, 1757-1765 (2011).
45. Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F. Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of the plant hormone jasmonoyl-isoleucine for catabolic turnover. J. Biol. Chem., M111.316364 (2012)
46. Matsui K, Shibutani M, Hase T, Kajiwara T. Bell pepper fruit fatty acid hydroperoxide lyase is a cytochrome P450 (CYP74B). FEBS Lett., 394, 21-24 (1996).
47. Lee D-S, Nioche P, Hamberg M, Raman CS. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature, 455, 363-368 (2008).
48. Li L, Chang Z, Pan Z, Fu Z-Q, Wang X. Modes of heme binding and substrate access for cytochrome P450 CYP74A revealed by crystal structures of allene oxide synthase. Proc. Natl. Acad. Sci. U.S.A., 105, 13883-13888 (2008).
49. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH. Secondary metabolite signalling in host-parasitic plant interactions. Curr. Opin. Plant Biol., 6, 358-364 (2003).
50. Akiyama K, Matsuzaki K-I, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, 824-827 (2005).
51. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF. Strigolactone inhibition of shoot branching. Nature, 455, 189-194 (2008).
52. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S. Inhibition of shoot branching by new terpenoid plant hormones. Nature, 455, 195-200 (2008).
53. Dun EA, Brewer PB, Beveridge CA. Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci., 14, 364-372 (2009).
54. Schwartz SH, Qin X, Loewen MC. The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J. Biol. Chem., 279, 46940-46945 (2004).
55. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O. MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev. Cell, 8, 443-449 (2005).
56. Kaspera R, Croteau R. Cytochrome P450 oxygenases of Taxol biosynthesis. Phytochem. Rev., 5, 433-444 (2006).
57. Jennewein S, Wildung MR, Chau M, Walker K, Croteau R. Random sequencing of an induced Taxus cell cDNA library for identification of clones involved in Taxol biosynthesis. Proc. Natl. Acad. Sci. U.S.A., 101, 9149-9154 (2004).
58. Kraus PF, Kutchan TM. Molecular cloning and heterologous expression of a cDNA encoding berbamunine synthase, a C-O phenol-coupling cytochrome P450 from the higher plant Berberis stolonifera. Proc. Natl. Acad. Sci. U.S.A., 92, 2071-2075 (1995).
59. Pauli HH, Kutchan TM. Molecular cloning and functional heterologous expression of two alleles encoding (S)-N-methylcoclaurine 3′-hydroxylase (CYP80B1), a new methyl jasmonate-inducible cytochrome P450-dependent monooxygenase of benzylisoquinoline alkaloid biosynthesis. Plant J., 13, 793-801 (1998).
60. Ikezawa N, Iwasa K, Sato F. Molecular cloning and characterization of CYP80G2, a cytochrome P450 that catalyzes an intramolecular C-C phenol coupling of (S)-reticuline in magnoflorine biosynthesis, from cultured Coptis japonica cells. J. Biol. Chem., 283, 8810-8821 (2008).
61. Ikezawa N, Tanaka M, Nagayoshi M, Shinkyo R, Sakaki T, Inouye K, Sato F. Molecular cloning and characterization of CYP719, a methylenedioxy bridge-forming enzyme that belongs to a novel P450 family, from cultured Coptis japonica cells. J. Biol. Chem., 278, 38557-38565 (2003).
62. Gesell A, Rolf M, Ziegler J, Díaz Chávez ML, Huang F-C, Kutchan TM. CYP719B1 is salutaridine synthase, the C-C phenol-coupling enzyme of morphine biosynthesis in opium poppy. J. Biol. Chem., 284, 24432-24442 (2009).
63. Augustin JM, Kuzina V, Andersen SB, Bak S. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry, 72, 435-457 (2011).
64. Zhao CL, Cui XM, Chen YP, Liang Q. Key enzymes of triterpenoid saponin biosynthesis and the induction of their activities and gene expressions in plants. Nat. Prod. Commun., 5, 1147-1158 (2010).
65. Shibuya M, Hoshino M, Katsube Y, Hayashi H, Kushiro T, Ebizuka Y. Identification of β-amyrin and sophoradiol 24-hydroxylase by expressed sequence tag mining and functional expression assay. FEBS J., 273, 948-959 (2006).
66. Seki H, Ohyama K, Sawai S, Mizutani M, Ohnishi T, Sudo H, Akashi T, Aoki T, Saito K, Muranaka T. Licorice β-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc. Natl. Acad. Sci. U.S.A., 105, 14204-14209 (2008).
67. Seki H, Sawai S, Ohyama K, Mizutani M, Ohnishi T, Sudo H, Fukushima EO, Akashi T, Aoki T, Saito K, Muranaka T. Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. Plant Cell, 23, 4112-4123 (2011).
68. Sémon M, Duret L. Evolutionary origin and maintenance of coexpressed gene clusters in mammals. Mol. Biol. Evol., 23, 1715-1723 (2006).
69. Michalak P. Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics, 91, 243-248 (2008).
70. Osbourn AE, Field B. Operons. Cell. Mol. Life Sci., 66, 3755-3775 (2009).
71. Field B, Osbourn AE. Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science, 320, 543-547 (2008).
72. Frey M, Chomet P, Glawischnig E, Stettner C, Grün S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A. Analysis of a chemical plant defense mechanism in grasses. Science, 277, 696-699 (1997).
73. Qi X, Bakht S, Leggett M, Maxwell C, Melton R, Osbourn A. A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Natl. Acad. Sci. U.S.A., 101, 8233-8238 (2004).
74. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. J. Biol. Chem., 284, 26510-26518 (2009).
75. Shimura K, Okada A, Okada K, Jikumaru Y, Ko KW, Toyomasu T, Sassa T, Hasegawa M, Kodama O, Shibuya N, Koga J, Nojiri H, Yamane H. Identification of a biosynthetic gene cluster in rice for momilactones. J. Biol. Chem., 282, 34013-34018 (2007).
76. Ren XY, Stiekema WJ, Nap J-P. Local coexpression domains in the genome of rice show no microsynteny with Arabidopsis domains. Plant Mol. Biol., 65, 205-217 (2007).
77. Williams EJB, Bowles DJ. Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res., 14, 1060-1067 (2004).
78. Fukushima EO, Seki H, Ohyama K, Ono E, Umemoto N, Mizutani M, Saito K, Muranaka T. CYP716A subfamily members are multi-functional oxidases in triterpenoid biosynthesis. Plant Cell Physiol., 52, 2050-2061 (2011).
79. Ajikumar PK, Xiao WH, Tyo KE, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G. Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science, 330, 70-74 (2010).
80. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MC, Withers ST, Shiba Y, Sarpong R, Keasling JD. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature, 440, 940-943 (2006).
81. Chang MC, Eachus RA, Trieu W, Ro DK, Keasling JD. Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nat. Chem. Biol., 3, 274-277 (2007).
82. van Herpen TW, Cankar K, Nogueira M, Bosch D, Bouwmeester HJ, Beekwilder J. Nicotiana benthamiana as a production platform for artemisinin precursors. PLoS ONE, 5, e14222 (2010).
83. Farhi M, Marhevka E, Ben-Ari J, Algamas-Dimantov A, Liang Z, Zeevi V, Edelbaum O, Spitzer-Rimon B, Abeliovich H, Schwartz B, Tzfira T, Vainstein A. Generation of the potent anti-malarial drug artemisinin in tobacco. Nat. Biotechnol., 29, 1072-1074 (2011).
84. Minami H, Kim JS, Ikezawa N, Takemura T, Katayama T, Kumagai H, Sato F. Microbial production of plant benzylisoquinoline alkaloids. Proc. Natl. Acad. Sci. U.S.A., 105, 7393-7398 (2008).