Achievements and perspectives in biochemistry concerning anthocyanin modification for blue flower coloration

Plant and Cell Physiology

Volumn 56, Issue 1, 2015, Pages 28-40

  Sasaki, Nobuhiro ^a   Nakayama, Toru ^b  

^a IWATE BIOTECHNOLOGY RESEARCH CENTER   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Acyltransferase; Anthocyanin; Blue flower coloration; Chrysanthemum; Delphinium; Glycosyltransferase; Polyacylation

Indexed keywords

CHRYSANTHEMUM; DELPHINIUM; DELPHINIUM GRANDIFLORUM; ROSA;

ACYLTRANSFERASE; ANTHOCYANIN; CYTOCHROME P450; DELPHINIDIN; FLAVONOID 3',5'-HYDROXYLASE; GLUCOSYLTRANSFERASE; VEGETABLE PROTEIN;

CHEMISTRY; CHRYSANTHEMUM; COLOR; DNA SHUFFLING; ENZYMOLOGY; FLOWER; GENETIC ENGINEERING; GENETICS; LARKSPUR; METABOLISM; PIGMENTATION; ROSE; TRANSGENIC PLANT;

ACYLTRANSFERASES; ANTHOCYANINS; CHRYSANTHEMUM; COLOR; CYTOCHROME P-450 ENZYME SYSTEM; DELPHINIUM; DNA SHUFFLING; FLOWERS; GENETIC ENGINEERING; GLUCOSYLTRANSFERASES; PIGMENTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; ROSA;

EID: 84922603191     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu097     Document Type: Review

References (82)

1. 00-O-malyltransferase activity in carnation (Dianthus caryophyllus). Biochem. Biophys. Res. Commun. 373: 473-477.
2. Anonymous. (2009) Lilac-the new blue? Nat. Biotechnol. 27: 1069.
3. Beld, M., Martin, C., Huits, H., Stuitje, A.R. and Gerats, A.G.M. (1989) Flavonoid synthesis in Petunia hybrida: partial characterization of dihydroflavonol-4-reductase genes. Plant Mol. Biol. 13: 491-502.
4. Boller, T. and Kende, H. (1979) Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol. 63: 1123-1132.
5. Brugliera, F., Tao, G.Q., Tems, U., Kalc, G., Mouradova, E., Price, K. et al. (2013) Violet/blue chrysanthemums-metabolic engineering of the anthocyanin biosynthetic pathway results in novel petal colors. Plant Cell Physiol. 54: 1696-1710.
6. Burbulis, I.E. and Winkel-Shirley, B. (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA 96: 12929-12934.
7. Chandler, S. and Tanaka, Y. (2007) Genetic modification in floriculture. Crit. Rev. Plant Sci. 26: 169-197.
8. D'Auria, J.C. (2006) Acyltransferases in plants: a good time to be BAHD. Curr. Opin. Plant Biol. 9: 331-340.
9. Davies, K.M. and Schwinn, K.E. (2005) Molecular biology and biotechnology of flavonoid biosynthesis. In Flavonoids: Chemistry, Biochemistry and Applications. Edited by Andersen, Ø.M. and Markham, K.R pp. 143-218. Taylor & Francis, Boca Raton, FL.
10. Eudes, A., Bozzo, G.G., Waller, J.C., Naponelli, V., Lim, E.-K., Bowles, D.J. et al. (2008) Metabolism of the folate precursor p-aminobenzoate in plants: glucose ester formation and vacuolar storage. J. Biol. Chem. 283: 15451-15459.
11. Fujiwara, H., Tanaka, Y., Fukui, Y., Nakao, M., Ashikari, T. and Kusumi, T. (1997) Anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Purification, characterization and its role in anthocyanin biosynthesis. Eur. J. Biochem. 249: 45-51.
12. Fujiwara, H., Tanaka, Y., Yonekura-Sakakibara, K., Fukuchi-Mizutani, M., Nakao, M., Fukui, Y. et al. (1998) cDNA cloning, gene expression, and subcellular localization of anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Plant J. 16: 421-431.
13. Fukuchi-Mizutani, M., Okuhara, H., Fukui, Y., Nakao, M., Katsumoto, Y., Yonekura-Sakakibara, K. et al. (2003) Biochemical and molecular characterization of a novel UDP-glucose:anthocyanin 3-O-glucosyltransfer-ase, a key enzyme for blue anthocyanin biosynthesis, from gentian. Plant Physiol. 132: 1652-1663.
14. Fukui, Y., Tanaka, Y., Kusumi, T., Iwashita, T. and 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.
15. Gläßgen, W.E. and Seitz, H.U. (1992) Acylation of anthocyanins with hydroxycinnamic acids via 1-O-acylglucosides by protein preparations from cell cultures of Daucus carota L. Planta 186: 582-585.
16. Goto, T. and Kondo, T. (1991) Structure and molecular stacking of anthocyanins: flower color variation. Angew. Chem. Int. Ed. Engl. 30: 17-33.
17. Hause, B., Meyer, K., Viitanen, P.V., Chapple, C. and Strack, D. (2002) Immunolocalization of 1-O-sinapoylglucose:malate sinapoyltransferase in Arabidopsis thaliana. Planta 215: 26-32.
18. He, H., Ke, H., Keting, H., Qiaoyan, X. and Silan, D. (2013) Flower colour modification of chrysanthemum by suppression of F3H and overex-pression of the exogenous Senecio cruentus F35H gene. PLoS One 8: e74395.
19. Honda, T. and Saito, N. (2002) Recent progress in the chemistry of poly-acylated anthocyanins as flower color pigments. Heterocycles 56: 633-692.
20. Ishiguro, K., Taniguchi, M. and 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. 125: 451-456.
21. Johnson, E.T., Ryu, S., Yi, H., Shin, B., Cheong, H. and Choi, G. (2001) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J. 25: 325-333.
22. Johnson, E.T., Yi, H., Shin, B., Oh, B.-J., Cheong, H. and Choi, G. (1999) Cymbidium hybrida dihydroflavonol 4-reductase does not efficiently reduce dihydrokaempferol to produce orange pelargonidin-type antho-cyanins. Plant J. 19: 81-85.
23. Katsumoto, Y., Fukuchi-Mizutani, M., Fukui, Y., Brugliera, F., Holton, T.A., Karan, M. et al. (2007) Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphi-nidin. Plant Cell Physiol. 48: 1589-1600.
24. Kawai, Y., Ono, E. and Mizutani, M. (2014) Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant J. 78: 328-343.
25. Kogawa, K., Kato, N., Kazuma, K., Noda, N. and Suzuki, M. (2007) Purification and characterization of UDP-glucose:anthocyanin 3, 5-O-glucosyltransferase from Clitoria ternatea. Planta 226: 1501-1509.
26. Kroon, J., Souer, E., de Graaff, A., Xue, Y., Mol, J. and Koes, R. (1994) Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. Plant J. 5: 69-80.
27. Lim, E.K. and Bowles, D.J. (2004) A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J. 23: 2915-2922.
28. Luang, S., Cho, J.I., Mahong, B., Opassiri, R., Akiyama, T., Phasai, K. et al. (2013) Rice Os9BGlu31 is a transglucosidase with the capacity to equilibrate phenylpropanoid, flavonoid, and phytohormone glycoconjugates. J. Biol. Chem. 288: 10111-10123.
29. Luo, J., Nishiyama, Y., Fuell, C., Taguchi, G., Elliott, K., Hill, L. et al. (2007) Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J. 50: 678-695.
30. Martens, S., Teeri, T. and Forkmann, G. (2002) Heterologous expression of dihydroflavonol 4-reductases from various plants. FEBS Lett. 531: 453-458.
31. Matsuba, Y., Sasaki, N., Tera, M., Okamura, M., Abe, Y., Okamoto, E. et al. (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., Heidmann, I., Forkmann, G. and Saedler, H. (1987) A new petunia flower colour generated by transformation of a mutant with a maize gene. Nature 330: 677-678.
33. Milkowski, C. and Strack, D. (2010) Sinapate esters in brassicaceous plants: biochemistry, molecular biology, evolution and metabolic engineering. Planta 232: 19-35.
34. Miyahara, T., Sakiyama, R., Ozeki, Y. and Sasaki, N. (2013) Acyl-glucose-dependent glucosyltransferase catalyzes the final step of anthocyanin formation in Arabidopsis. J. Plant Physiol. 170: 619-624.
35. Miyahara, T., Takahashi, M., Ozeki, Y. and Sasaki, N. (2012) Isolation of an acyl-glucose-dependent anthocyanin 7-O-glucosyltransferase from the monocot Agapanthus africanus. J. Plant Phisiol. 169: 1321-1326.
36. Mizutani, M., Katsumoto, Y., Fukui, Y., Togami, J., Nakamura, N., Okuhara, H. et al. (2006) An acyltransferase involved in biosynthesis of polyacylated anthocyanin. Plant Cell Physiol 47s: s198.
37. Mock, H.-P. and Strack, D. (1993) Energetics of the uridine 5-diphospho-glucose: hydroxycinnamic acid acyl-glucosyltransferase reaction. Phytochemistry 32: 515-519.
38. Montefiori, M., Espley, R.V., Stevenson, D., Cooney, J., Datson, P.M., Saiz, A. et al. (2011) Identification and characterisation of F3GT1 and F3GGT1, two glycosyltransferases responsible for anthocyanin biosynthesis in red-fleshed kiwifruit (Actinidia chinensis). Plant J. 65: 106-118.
39. Nakatsuka, T. and Nishihara, M. (2010) UDP-glucose:3-deoxyanthocyani-din 5-O-glucosyltransferase from Sinningia cardinalis. Planta 232: 383-392.
40. 00-O-dimalo-nyl-b-glucopyranoside) as a flower pigment of chrysanthemum (Dendranthema grandiflorum). Biosci. Biotechnol. Biochem. 61: 1607-1608.
41. Nakayama, T., Suzuki, H. and Nishino, T. (2003) Anthocyanin acyltrans-ferases: specificities, mechanism, phylogenetics, and applications. J. Mol. Cat. B: Enzymatic 23: 117-132.
42. Nishizaki, Y., Sasaki, N., Yasunaga, M., Miyahara, T., Okamoto, E., Okamoto, M. et al. (2014) Identification of the glucosyltransferase gene that supplies the p-hydroxybenzoyl-glucose for 7-polyacylation of anthocyanin in delphinium. J. Exp. Bot. 65: 2495-2506.
43. Nishizaki, Y., Yasunaga, M., Okamoto, E., Okamoto, M., Hirose, Y., Yamaguchi, M. et al. (2013) p-Hydroxybenzoyl-glucose is a zwitter donor for the biosynthesis of 7-polyacylated anthocyanin in delphinium. Plant Cell 25: 4150-4165.
44. Noda, N., Aida, R., Kishimoto, S., Ishiguro, K., Fukuchi-Mizutani, M., Tanaka, Y. et al. (2013) Genetic engineering of novel bluer-colored chrysanthemums produced by accumulation of delphinidin-based anthocyanins. Plant Cell Physiol. 54: 1684-1695.
45. Noda, N., Kazuma, K., Sasaki, T., Kogawa, K. and Suzuki, M. (2006) Molecular cloning of 1-O-acylglucose dependent anthocyanin aromatic acyltransferase in ternatin biosynthesis of butterfly pea (Clitoria terna-tea). Plant Cell Physiol. 47: S109.
46. Noguchi, A., Horikawa, M., Fukui, Y., Fukuchi-Mizutani, M., Iuchi-Okada, A., Ishiguro, M. et al. (2009) Local differentiation of sugar donor specificity of flavonoid glycosyltransferase in Lamiales. Plant Cell 21: 1556-1572.
47. Ogata, J., Kanno, Y., Itoh, Y., Tsugawa, H. and Suzuki, M. (2005) Plant biochemistry: anthocyanin biosynthesis in roses. Nature 435: 757-758.
48. Ono, E., Homma, Y., Horikawa, M., Kunikane-Doi, S., Imai, H., Takahashi, S. et al. (2010) Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera). Plant Cell 22: 2856-2871.
49. Petit, P., Granier, T., d'Estaintot, B.L, Manigand, C, Bathany, K., Schmitter, J.M. et al. (2007) Crystal structure of grape dihydroflavonol 4-reductase, a key enzyme in flavonoid biosynthesis. J. Mol. Biol. 368: 1345-1357.
50. Rausher, M.D. (2008) Evolutionary transitions in floral color. Int.J. Plant Sci. 169: 7-21.
51. Sawada, S., Suzuki, H., Ichimaida, F., Yamaguchi, M.A., Iwashita, T., Fukui, Y et al. (2005) UDP-glucuronic acid:anthocyanin glucuronosyltransferase from red daisy (Bellis perennis) flowers. Enzymology and phylogenetics of a novel glucuronosyltransferase involved in flower pigment biosynthesis. J. Biol. Chem. 280: 899-906.
52. Schwinn, K.E., Markham, K.R. and Giveno, N. (1994) Floral flavonoids and the potential for pelargonidin biosynthesis in commercial chrysanthemum cultivars. Phytochemistry 35: 145-150.
53. Seitz, C, Eder, C, Deiml, B., Kellner, S., Martens, S. and 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.
54. Shiono, M., Matsugaki, N. and Takeda, K. (2005) Phytochemistry: structure of the blue cornflower pigment. Nature 436: 791.
55. Shoji, K., Miki, N., Nakajima, N., Momonoi, K., Kato, C. and Yoshida, K. (2007) Perianth bottom-specific blue color development in tulip cv. Murasakizuisho requires ferric ions. Plant Cell Physiol. 48: 243-251.
56. Stafford, H.A. (1990) Flavonoid Metabolism pp. 208-215. CRC Press, Boca Raton, FL
57. Stehle, F., Brandt, W., Stubbs, M.T., Milkowski, C. and Strack D. (2009) Sinapoyltransferases in the light of molecular evolution. Phytochemistry 70: 1652-1662.
58. Suzuki, H., Nakayama, T., Yamaguchi, M. and Nishino, T. (2004a) cDNA cloning and characterization of two Dendranthema x morifolium anthocyanin malonyltransferases with different functional activities. Plant Sci. 166: 89-96.
59. Suzuki, H., Sawada, S., Watanabe, K., Nagae, S., Yamaguchi, M.A., Nakayama, T. et al. (2004b) Identification and characterization of a novel anthocyanin malonyltransferase from scarlet sage (Salvia splen-dens) flowers: an enzyme that is phylogenetically separated from other anthocyanin acyltransferases. Plant J. 38: 994-1003.
60. Suzuki, T., Araki, T. and Yuki, S. (2008) Dayflower flavonoid 3, 5-hydroxylase gene. Japanese unexamined patent application JP2008-253250.
61. Takeda, K., Osakabe, A., Saito, S., Furuyama, D., Tomita, A., Kojima, Y. et al. (2005) Components of protocyanin, a blue pigment from the blue flowers of Centaurea cyanus. Phytochemistry 66: 1607-1613.
62. Tanaka, Y. and Brugliera, F. (2013) Flower colour and cytochromes P450. Philos. Trans. R. Soc. B: Biol. Sci 368: 20120432.
63. Tanaka, Y., Brugliera, F. and Chandler, S. (2009) Recent progress of flower colour modification by biotechnology. Int. J. Mol. Sci. 10: 5350-5369.
64. Tanaka, Y., Katsumoto, Y., Brugliera, F. and Mason, J. (2005) Genetic engineering in floriculture. Plant Cell Tiss. Org. Cult. 80: 1-24.
65. Tanaka, Y., Nakamura, N., Kobayashi, H., Okuhara, H., Kondo, M., Koike, Y et al. (2012) Method for producing lilies containing delphinidin in the petals thereof Patent application PCT/JP2011/071271.
66. Tanaka, Y., Sasaki, N. and Ohmiya, A. (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 54: 733-749.
67. Tanaka, Y., Tsuda, S. and Kusumi, T. (1998) Metabolic engineering to modify flower color. Plant Cell Physiol. 39: 1119-1126.
68. Tanikawa, N., Kashiwabara, T., Hokura, A., Abe, T., Shibata, M. and Nakayama, M. (2008) A peculiar yellow flower coloration of camellia using aluminum-flavonoid interaction. Jpn. Soc. Hort. Sci. 77: 402-407.
69. Umemoto, N., Abe, Y., Cano, E.A., Okumyra, M., Sasaki, N., Yoshida, S. et al. (2014) Carnation serine carboxypeptidase-like acyltransferase is important for anthocyanin malyltransferase activity and formation of antho-cyanic vacuolar inclusions. In XXVIIth International Conference on Polyphenols (ICP2014), Nagoya, Japan.
70. Unno, H., Ichimaida, F., Suzuki, H., Takahashi, S., Tanaka, Y., Saito, A. et al. (2007) Structural and mutational studies of anthocyanin malonyltrans-ferases establish the features of BAHD enzyme catalysis. J. Biol. Chem. 282: 15812-15822.
71. Vogt, T. and Jones, P. (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5: 380-386.
72. Weng, J.K. and Noel, J.P. (2012) The remarkable pliability and promiscuity of specialized metabolism. Cold Spring Harb. Symp. Quant. Biol. 77: 309-320.
73. Weng, J.K., Philippe, R.N. and Noel, J.P. (2012) The rise of chemodiversity in plants. Science 336: 1667-1670.
74. Winkel, B.S. (2004) Metabolic channeling in plants. Annu. Rev. Plant Biol. 55: 85-107.
75. Winkel-Shirley, B. (2001) It takes a garden. How work on diverse plant species has contributed to an understanding of flavonoid metabolism. Plant Physiol. 127: 1399-1404.
76. Yazaki, K., Inushima, K., Kataoka, M. and Tabata, M. (1995) Intracellular localization of UDPG:p-hydroxybenzoate glucosyltransferase and its reaction product in Lithospermum cell cultures. Phytochemistry 38: 1127-1130.
77. Yonekura-Sakakibara, K., Fukushima, A., Nakabayashi, R., Hanada, K., Matsuda, F., Sugawara, S. et al. (2012) Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. Plant J. 69: 154-167.
78. Yonekura-Sakakibara, K. and Hanada, K. (2011) An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 66: 182-193.
79. Yoshida, K., Mori, M. and Kondo, T. (2009) Blue flower color development by anthocyanins: from chemical structure to cell physiology. Nat. Prod. Rep. 26: 884-915.
80. Yoshida, K. and Negishi, T. (2013) The identification of a vacuolar iron transporter involved in the blue coloration of cornflower petals. Phytochemistry 94: 60-67.
81. Yoshida, K., Toyama, Y., Kameda, K. and Kondo, T. (2000) Contribution of each caffeoyl residue of the pigment molecule of gentiodelphin to blue color development. Phytochemistry 54: 85-92.
82. Yoshihara, N., Imayama, T., Matsuo, Y., Fukuchi-Mizutani, M., Tanaka, Y., Ino, I. et al. (2006) Characterization of cDNA clones encoding antho-cyanin 3-p-coumaroyltransferase from Iris hollandica. Plant Sci. 171: 632-639.