Metabolic engineering of flower color pathways using cytochromes P450

Fifty Years of Cytochrome P450 Research

Volumn , Issue , 2014, Pages 207-229

  Tanaka, Yoshikazu ^a   Brugliera, Filippa ^b,c  

^a Soraku   (Japan)

^b Florigene Pty Ltd   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Anthocyanidin; Anthocyanin; Flavone synthase; Flavonoid; Flavonoid 3 , 5 hydroxylase; Flavonoid 3 hydroxylase

Indexed keywords

EID: 84934270557     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-4-431-54992-5_12     Document Type: Chapter

References (87)

1. Abe Y, Tera M, Sasaki N, Okamura M, Umemoto N, Momose M, Kawahara N, Kamakura H, Goda Y, Nagasawa K, Ozeki Y (2008) Detection of 1-O-malylglucose: pelargonidin 3-O-glucose-6''-O-malyltransferase activity in carnation (Dianthus caryophyllus). Biochem Biophys Res Commun 373:473-477
2. Aida R (2008) Torenia fournieri (torenia) as a model plant for transgenic studies. Plant Biotechnol 25:541-545
3. Akashi T, Aoki T, Ayabe S (1998) CYP81E1, a cytochrome P450 cDNA of licorice (Glycyrrhiza echinata L.), encodes isoflavone 2'-hydroxylase. Biochem Biophys Res Commun 251:67-70
4. Akashi T, Aoki T, Ayabe S (1998) Identification of a cytochrome P450 cDNA encoding (2S)-flavanone 2-hydroxylase of licorice (Glycyrrhiza echinata L.; Fabaceae) which represents licodione synthase and flavone synthase II. FEBS Lett 431:287-290
5. Akashi T, Aoki T, Ayabe S (1999) Cloning and functional expression of a cytochrome P450 cDNA encoding 2-hydroxyisoflavanone synthase involved in biosynthesis of the isoflavonoid skeleton in licorice. Plant Physiol 121:821-828
6. Akashi T, Fukuchi-Mizutani M, Aoki T, Ueyama Y, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Ayabe S (1999) Molecular cloning and biochemical characterization of a novel cytochrome P450, flavone synthase II, that catalyzes direct conversion of flavanones to flavones. Plant Cell Physiol 40:1182-1186
7. Anderson NO (2007) Chrysanthemum (Dendrathema x grandiflora Tzelv.). In: Anderson NO (ed) Flower breeding and genetics. Springer, Amsterdam, pp 389-437
8. Berim A, Gang DR (2013) The roles of a flavone-6-hydroxylase and 7-O-demethylation in the flavone biosynthetic network of sweet basil. J Biol Chem 288:1795-1805
9. Boase MR, Lewis DH, Davies KM, Marshall GB, Patel D, Schwinn KE, Deroles SC (2010) Isolation and antisense suppression of flavonoid 3',5'-hydroxylase modifies flower pigments and colour in cyclamen. BMC Plant Biol 10:107
10. Brazier-Hicks M, Evans KE, Gershater MC, Puschmann H, Steel PG, Edwards R (2009) The C-glycosylation of flavonoids in cereals. J Biol Chem 284:17926-17934
11. Brugliera F, Holton TA, Michael MW (1997) Genetic sequences encoding flavonoid pathway enzymes and uses therefore. International Patent Publication Number WO97/32023
12. Brugliera F, Barri-Rewell G, Holton TA, Mason JG (1999) Isolation and characterization of a flavonoid 3'-hydroxylase cDNA clone corresponding to the Ht1 locus of Petunia hybrida. Plant j 19:441-451
13. Brugliera F, Tao GQ, Tems U, Kalc G, Mouradova E, Price K, Stevenson K, Nakamura N, Stacey I, Katsumoto Y, Tanaka Y, Mason JG (2013) Violet/blue chrysanthemums-metabolic engineering of the anthocyanin biosynthetic pathway results in novel petal colors. Plant Cell Physiol 54:1696-1710
14. Chandler SF, Senior M, Nakamura N, Tsuda S, Tanaka Y (2013) Expression of flavonoid 3',5'-hydroxylase and acetolactate synthase genes in transgenic carnation: assessing the safety of a nonfood plant. J Agric Food Chem 61:11711-11720
15. Du Y, Chu H, Chu IK, Lo C (2010) CYP93G2 is a flavanone 2-hydroxylase required for C-glycosylflavone biosynthesis in rice. Plant Physiol 154:324-333
16. Fleigmann J, Furtwangler R, Malterer G, Cantarello C, Schuler G, Ebel J, Mithofer A (2010) Flavone synthase II (CYP93B16) from soybean (Glycine max L.). Phytochem 71:508-514
17. Forkman G, Ruhnau B (1987) Distinct substrate specificity of dihydroflavonol 4-reductase from flowers of Petunia hybrida. Z Naturforsch 42c:1146-1148
18. Fukuchi-Mizutani M, Akagi M, Ishiguro K, Katsumoto Y, Fukui Y, Togami J, Nakamura N, Tanaka Y (2011) Biochemical and molecular characterization of anthocyanidin/flavonol 3-glucosylation pathways in Rosa x hybrida. Plant Biotechnol 28:239-244
19. Fukui Y, Tanaka Y, Kusumi T, Iwashita T, Nomoto K (2003) A rationale for the shift in colour towards blue in transgenic carnation flowers expressing the flavonoid 3',5'-hydroxylase gene. Phytochemistry 63:15-23
20. Fukushima EO, Seki H, Muranaka T (2014) Plant cytochrome P450s in triterpenoid biosynthesis: diversity and application to combinatorial biosynthesis
21. Hamberger B, Bak S (2013) Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos Trans R Soc Lond B Biol Sci 368:2012-2026
22. Hatlestad GJ, Sunnadeniya RM, Akhavan NA, Gonzalez A, Goldman IL, McGrath JM, Lloyd AM (2012) The beet R locus encodes a new cytochrome P450 required for red betalain production. Nat Genet 44:816-820
23. Helariutta Y, Elomaa P, Kotilainen H, Seppanen P, Teeri TH (1993) Cloning of cDNA for dihydroflavonol 4-reductase (DFR) and charaterization of dfr expression in the corollas of Gerbera hybrida var. Regina (Compositae). Plant Mol Biol 22:183-193
24. Holton TA, Brugliera F, Lester DR, Tanaka Y, Hyland CD, Menting JG, Lu CY, Farcy E, Stevenson TW, Cornish EC (1993) Cloning and expression of cytochrome P450 genes controlling flower colour. Nature (Lond) 366:276-279
25. Ishiguro K, Masumi T, Tanaka Y (2012) Functional analysis of Antirrhinum kelloggii flavonoid 3'-hydroxylase and flavonoid 3',5'-hydroxylase genes; critical role in flower color and evolution in the genus Antirrhinum. J Plant Res 124:451-456
26. Jung W, Yu O, Lau SM, O’Keefe DP, Odell J, Fader G, McGonigle B (2000) Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nat Biotechnol 18:208-212
27. Katsumoto Y, Mizutani M, Fukui Y, Brugliera F, Holton T, Karan M, Nakamura N, Yonekura- Sakakibara K, Togami J, Pigeaire A, Tao G-Q, Nehra N, Lu C-Y, Dyson B, Tsuda S, Ashikari T, Kusumi T, Mason J, Tanaka Y (2007) Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin. Plant Cell Physiol 48:1589-1600
28. Kim J, DellaPenna D (2006) Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. Proc Natl Acad Sci USA 103:3474-3479
29. Martens S, Forkmann G (1999) Cloning and expression of flavone synthase II from Gerbera hybrids. Plant J 20:611-618
30. Martens S, Forkmann G, Britsch L, Wellmann F, Matem U, Lukacin R (2003) Divergent evolution of flavonoid 2-oxoglutarate-dependent dioxygenases in parsley. FEBS Lett 544:93-98
31. Matsuba Y, Sasaki N, Tera M, Okamura M, Abe Y, Okamoto E, Nakamura H, Funabashi H, Takatsu M, Saito M, Matsuoka H, Nagasawa K, Ozeki Y (2010) A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 22:3374-3389
32. Meyer P, Heidemann I, Forkmann G, Saedler H (1987) A new petunia flower colour generated by transformation of a mutant with a maze gene. Nature (Lond) 330:677-678
33. Mii M (2012) Interspecific hybridization, somatic hybridization and genetic transformation. Acta Hortic 953:43-54
34. Mikanagi Y, Yokoi M, Ueda Y, Saito N (1995) Flower flavonol and anthocyanin distribution in subgenus Rosa. Biochem Syst Ecol 23:183-200
35. Mikanagi Y, Saito N, Yokoi M, Tatsuzawa F (2000) Anthocyanins in flowers of genus Rosa, sections Cinnamomeae (=Rosa), Chinenses, Gallicanae and some modern garden roses. Biochem Syst Ecol 28:887-902
36. Mizutani M (2012) Impacts of diversification of cytochrome P450 on plant metabolism. Biol Pharm Bull 35:824-832
37. Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 61:291-315
38. Mizutani M, Sato F (2011) Unusual P450 reactions in plant secondary metabolism. Arch Biochem Biophys 507:194-203
39. Momose M, Abe Y, Ozeki Y (2010) Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 186:59-66
40. Momose M, Nakayama M, Itoh Y, Umemoto N, Toguri T, Ozeki Y (2013) An active hAT transposable element causing bud mutation of carnation by insertion into the flavonoid 3'-hydroxylase gene. Mol Genet Genomics 288:175-184
41. Moreau C, Ambrose MJ, Turner L, Hill L, Ellis TH, Hofer JM (2012) The B gene of pea encodes a defective flavonoid 3',5'-hydroxylase, and confers pink flower color. Plant Physiol 159:759-768
42. Mori S, Kobayashi H, Hoshi Y, Kondo M, Nakano M (2004) Heterologous expression of the flavonoid 3',5'-hydroxylase gene of Vinca major alters flower color in transgenic Petunia hybrida. Plant Cell Rep 22:415-421
43. Nakamura N, Fukuchi-Mizutani M, Fukui Y, Ishiguro K, Suzuki K, Tanaka Y (2010) Generation of red flower varieties from blue Torenia hybrida by redirection of the flavonoid pathway from delphinidin to pelargonidin. Plant Biotechnol 27:375-383
44. Nakamura N, Fukuchi-Mizutani M, Katsumoto Y, Togami J, Senior M, Matsuda Y, Furuichi K, Yoshimoto M, Matsunaga A, Ishiguro K, Aida M, Tasaka M, Fukui H, Tsuda S, Chandler S, Tanaka Y (2011) Environmental risk assessment and field performance of rose (Rosa x hybrida) genetically modified for delphinidin production. Plant Biotechnol 28:251-261
45. Nakamura N, Tems U, Fukuchi-Mizutani M, Chandler S, Matsuda Y, Takeuchi S, Matsumoto S, Tanaka Y (2011b) Molecular based evidence for a lack of gene-flow between Rosa x hybrida and wild Rosa species in Japan. Plant Biotechnol 28:245-250
46. Nakatsuka T, Nishihara M, Mishiba K, Yamamura S (2006) Heterologous expression of two gentian cytochrome P450 genes can modulate the intensity of flower pigmentation in transgenic tobacco plants. Mol Breed 17:91-99
47. Nakatsuka T, Abe Y, Kakizaki Y, Yamamura S, Nishihara M (2007) Production of red-flowered plants by genetic engineering of multiple flavonoid biosynthetic genes. Plant Cell Rep 26:1951-1959
48. Nakatsuka T, Mishiba K, Abe Y, Kubota A, Kakizaki Y, Yamamura S, Nishihara M (2008) Flower color modification of gentian plants by RNAi-mediated gene silencing. Plant Biotechnol 25:61-68
49. Nakayama M, Koshioka M, Shibata M, Hiradate S, Sugie H, Yamaguchi M (1997) Identification of cyanidin 3-O-(3,6-O-dimalonyl-p-glucopyranoside) as a flower pigment of chrysanthemum (Dendranthema grandiflorum). Biosci Biotechnol Biochem 61:1607-1608
50. Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194-211
51. Nielsen KA, Tattersall DB, Jones PR, Moller BL (2008) Metabolon formation in dhurrin biosynthesis. Phytochemistry 69:88-98
52. Nishihara M, Shimoda T, Nakatsuka T, Arimura G (2013) Frontiers of torenia research: innovative ornamental traits and study of ecological interaction networks through genetic engineering. Plant Methods 9:23
53. Noda N, Aida R, Kishimoto S, Ishiguro K, Fukuchi-Mizutani M, Tanaka Y, Ohmiya A (2013) Genetic engineering of novel bluer-colored chrysanthemums produced by accumulation of delphinidin-based anthocyanins. Plant Cell Physiol 54:1684-1695
54. Ogata J, Itoh Y, Ishida M, Yoshida H, Ozeki Y (2004) Cloning and heterologous expression of a cDNA encoding flavonoid glucosyltransferases from Dianthus caryophyllus. Plant Biotechnol 2003
55. Ogo Y, Ozawa K, Ishimaru T, Murayama T, Takaiwa F (2013) Transgenic rice seed synthesizing diverse flavonoids at high levels: a new platform for flavonoid production with associated health benefits. Plant Biotechnol J 11:734-746
56. Okinaka Y, Shimada Y, Nakano-Shimada R, Ohbayashi M, Kiyokawa S, Kikuchi Y (2003) Selective accumulation of delphinidin derivatives in tobacco using a putative flavonoid 3',5'-hydroxylase cDNA from Campanula medium. Biosci Biotechnol Biochem 67:161-165
57. Qi Y, Lou Q, Quan Y, Liu Y, Wang Y (2013) Flower-specific expression of the Phalaenopsis flavonoid 3',5'-hydoxylase modifies flower color pigmentation in Petunia and Lilium. Plant Cell Tissue Organ Cult 115:263-273
58. Sasaki N, Matsuba Y, Abea Y, Okamura M, Momose M, Umemoto N, Nakayama M, Itoh Y, Ozekia Y (2013) Recent advances in understanding the anthocyanin modification steps in carnation flowers. Sci Hortic 163:37-45
59. Satoh J, Kato K, Shinmyo A (2004) The 5'-untranslated region of the tobacco alcohol dehydrogenase gene functions as an effective translational enhancer in plant. J Biosci Bioeng 98:1-8
60. Schlangen K, Miosic S, Halbwirth H (2010) Allelic variants from Dahlia variabilis encode flavonoid 3'-hydroxylases with functional differences in chalcone 3-hydroxylase activity. Arch Biochem Biophys 494:40-45
61. Schwinn KE, Markham KR, Giveno N (1994) Floral flavonoids and the potential for pelargonidin biosynthesis in commercial chrysanthemum cultivars. Phytochemistry 35:145-150
62. Seitz C, Eder C, Deiml B, Kellner S, Martens S, Forkmann G (2006) Cloning, functional identification and sequence analysis of flavonoid 3'-hydroxylase and flavonoid 3',5'-hydroxylase cDNAs reveals independent evolution of flavonoid 3',5'-hydroxylase in the Asteraceae family. Plant Mol Biol 61:365-381
63. Seitz C, Ameres S, Forkmann G (2007) Identification of the molecular basis for the functional difference between flavonoid 3'-hydroxylase and flavonoid 3',5'-hydroxylase. FEBS Lett 581:3429-3434
64. Shimada Y, Nakano-Shimada R, Ohbayashi M, Okinaka Y, Kiyokawa S, Kikuchi Y (1999) Expression of chimeric P450 genes encoding flavonoid-3', 5'-hydroxylase in transgenic tobacco and petunia plants. FEBS Lett 461:241-245
65. Sonderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates: gene discovery and beyond. Trends Plant Sci 15:283-290
66. Stotz G, Forkmann G (1981) Hydroxylation of the B-ring of flavonoids in the 3- and 5-position with enzyme extracts from flowers of Verbena hybrida. Z Naturforsch 37c:19-23
67. Suzuki K, Xue H, Tanaka Y, Fukui Y, Fukuchi-Mizutani M, Murakami Y, Katsumoto Y, Tsuda S, Kusumi T (2000) Flower color modifications of Torenia hybrida by cosuppression of antho- cyanin biosynthesis genes. Mol Breed 6:239-246
68. Takatsu Y, Hayashi M, Sakumao F (2000) Transgene inactivation in Agrobacterium-mediated chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura) transformants. Plant Biotechnol 17:241-245
69. Tanaka Y (2006) Flower colour and cytochromes P450. Phyochem Rev 5:283-291
70. Tanaka Y, Brngliera F (2013) Flower colour and cytochromes P450. Philos Trans R Soc Lond B Biol Sci 368:20120432
71. Tanaka Y, Fukui Y, Fukuchi-Mizutani M, Holton TA, Higgins E, Kusumi T (1995) Molecular cloning and characterization of Rosa hybrida dihydroflavonol 4-reductase. Plant Cell Physiol 36:1023-1031
72. Tanaka Y, Sasaki N, Ohmiya A (2008) Plant pigments for coloration: anthocyanins, betalains and carotenoids. Plant J 54:733-749
73. Tanaka Y, Brugliera F, Chandler S (2009) Recent progress of flower colour modification by biotechnology. Int J Mol Sci 10:5350-5369
74. Tanaka Y, Brugliera F, Kalc G, Senior M, Dyson B, Nakamura N, Katsumoto Y, Chandler S (2010) Flower color modification by engineering of the flavonoid biosynthetic pathway: practical perspectives. Biosci Biotechnol Biochem 74:1760-1769
75. Thill J, Miosic S, Ahmed R, Schlangen K, Muster G, Stich K, Halbwirth H (2012) Le Rouge et le Noir: a decline in flavone formation correlates with the rare color of black dahlia (Dahlia variabilis hort.) flowers. BMC Plant Biol 12:225
76. Thill J, Miosic S, Gotame TP, Mikulic-Petkovsek M, Gosch C, Veberic R, Preuss A, Schwab W, Stampar F, Stich K, Halbwirth H (2013) Differential expression of flavonoid 3'-hydroxylase during fruit development establishes the different B-ring hydroxylation patterns of flavonoids in Fragaria x ananassa and Fragaria vesca. Plant Physiol Biochem 72:72-78
77. Tian L, Musetti V, Kim J, Magallanes-Lundback M, DellaPenna D (2004) The Arabidopsis LUT1 locus encodes a member of the cytochrome p450 family that is required for carotenoid epsilonring hydroxylation activity. Proc Natl Acad Sci USA 101:402-407
78. Togami J, Tamura M, Ishiguro K, Hirose C, Okuhara H, Ueyama Y, Nakamura N, Yonekura- Sakakibara K, Fukuchi-Mizutani M, Suzuki K, Fukui Y, Kusumi T, Tanaka Y (2006) Molecular characterization of the flavonoid biosynthesis of Verbena hybrida and the functional analysis of verbena and Clitoria ternatea F3'5'H genes in transgenic verbena. Plant Biotechnol 23:5-11
79. Tsuda S, Fukui Y, Nakamura N, Katsumoto Y, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Ohira K, Ueyama Y, Ohkawa H, Holton TA, Kusumi T, Tanaka Y (2004) Flower color modification of Petunia hybrida commercial varieties by metabolic engineering. Plant Biotechnol 21:377-386
80. Ueyama U, Suzuki K, Fukuchi-Mizutani M, Fukui Y, Miyazaki K, Ohkawa H, Kusumi T, Tanaka Y (2002) Molecular and biochemical characterization of torenia flavonoid 3'-hydroxylase and flavone synthase II and modification of flower color by modulating the expression of these genes. Plant Sci 163:253-263
81. Wang M-B, Waterhouse PM (2001) Application of gene silencing in plants. Curr Opin Plant Biol 5:146-150
82. Wesley SV, Helliwell CA, Smith NA (2001) Construct design for efficient, effective and high- throughput gene silencing in plants. Plant J 27:581-590
83. Winkel BSJ (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85-107
84. Yabuya T, Nakamura M, Iwashina T, Yamaguchi M, Takehara T (1997) Anthocyanin-flavone copigmentaion in bluish purple flowers of Japanese garden iris (Iris ensata Thunb.). Euphytica 98:163-167
85. Yagi M, Kosugi S, Hirakawa H, Ohmiya A, Tanase K, Harada T, Kishimoto K, Nakayama M, Ichimura K, Onozaki T, Yamaguchi H, Sasaki N, Miyahara T, Nishizaki Y, Ozeki Y, Nakamura N, Suzuki S, Tanaka Y, Sato S, Shirasawa K, Isobe S, Miyamura Y, Watanabe A, Nakayama S, Kishida Y, Kohara M, Tabata S (2013) Sequence analysis of the genome of carnation(Dianthus caryophyllus L.). DNA Res. doi:10.1093/dnares/dst053
86. Yoshida K, Mori M, Kondo T (2009) Blue flower color development by anthocyanins: from chemical structure to cell physiology. Nat Prod Rep 26:884-915
87. Zhang J, Subramanian S, Zhang Y, Yu O (2007) Flavone synthases from Medicago truncatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol 144:741-751