The flavonoid biosynthetic pathway in Arabidopsis: Structural and genetic diversity

Plant Physiology and Biochemistry

Volumn 72, Issue , 2013, Pages 21-34

  Saito, Kazuki ^a,b   Yonekura Sakakibara, Keiko ^a   Nakabayashi, Ryo ^a   Higashi, Yasuhiro ^a   Yamazaki, Mami ^b   Tohge, Takayuki ^c   Fernie, Alisdair R ^c  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b CHIBA UNIVERSITY   (Japan)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Arabidopsis thaliana; Biosynthesis; Flavonoid; Functional genomics

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

FLAVONOID; FLAVONOL DERIVATIVE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BIOSYNTHESIS; FUNCTIONAL GENOMICS; GENETIC VARIABILITY; GENETICS; GENOMICS; METABOLISM; REVIEW;

ARABIDOPSIS THALIANA; BIOSYNTHESIS; FLAVONOID; FUNCTIONAL GENOMICS;

ARABIDOPSIS; FLAVONOLS; GENETIC VARIATION; GENOMICS;

EID: 84886601440     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.02.001     Document Type: Review

References (168)

1. Haslam E. Shikimic Acid: Metabolism and Metabolites, Shikimic Acid 1993, John Wiley & Sons, Chichester, UK, pp. 156-254.
2. Halliwell B., Rafter J., Jenner A. Health promotion by flavonoids, tocopherols, tocotrienols, and other phenols: direct or indirect effects? Antioxidant or not?. The American Journal of Clinical Nutrition 2005, 81:268S-276S.
3. Wang L., Lee I.-M., Zhang S.M., Blumberg J.B., Buring J.E., Sesso H.D. Dietary intake of selected flavonols, flavones, and flavonoid-rich foods and risk of cancer in middle-aged and older women. The American Journal of Clinical Nutrition 2009, 89:905-912.
4. Jan A.T., Kamli M.R., Murtaza I., Singh J.B., Ali A., Haq Q.M.R. Dietary flavonoid quercetin and associated health benefits-An overview. Food Reviews International 2010, 26:302-317.
5. Bino R.J., Hall R.D., Fiehn O., Kopka J., Saito K., Draper J., Nikolau B.J., Mendes P., Roessner-Tunali U., Beale M.H., Trethewey R.N., Lange B.M., Wurtele E.S., Sumner L.W. Potential of metabolomics as a functional genomics tool. Trends in Plant Science 2004, 9:418-425.
6. Saito K., Matsuda F. Metabolomics for functional genomics, systems biology, and biotechnology. Annual Review of Plant Biology 2010, 61:463-489.
7. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 2001, 126:485-493.
8. Grotewold E. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 2006, 57:761-780.
9. Davies M.K., Schwinn K.E. Molecular biology and biotechnology of flavonoid biosynthesis. Flavonoids Chemistry, Biochemistry and Applications 2006, 143-218. CRC Press, Taylor & Francis, Boca Raton. O.M. Andersen, K.R. Markham (Eds.).
10. Lepiniec L., Debeaujon I., Routaboul J.-M., Baudry A., Pourcel L., Nesi N., Caboche M. Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 2006, 57:405-430.
11. Farag M.A., Huhman D.V., Lei Z., Sumner L.W. Metabolic profiling and systematic identification of flavonoids and isoflavonoids in roots and cell suspension cultures of Medicago truncatula using HPLC-UV-ESI-MS and GC-MS. Phytochemistry 2007, 68:342-354.
12. Suzuki H., Sasaki R., Ogata Y., Nakamura Y., Sakurai N., Kitajima M., Takayama H., Kanaya S., Aoki K., Shibata D., Saito K. Metabolic profiling of flavonoids in Lotus japonicus using liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry. Phytochemistry 2008, 69:99-111.
13. Hosseinian F.S., Li W., Beta T. Measurement of anthocyanins and other phytochemicals in purple wheat. Food Chemistry 2008, 109:916-924.
14. Horai H., Arita M., Kanaya S., Nihei Y., Ikeda T., Suwa K., Ojima Y., Tanaka K., Tanaka S., Aoshima K., Oda Y., Kakazu Y., Kusano M., Tohge T., Matsuda F., Sawada Y., Hirai M.Y., Nakanishi H., Ikeda K., Akimoto N., Maoka T., Takahashi H., Ara T., Sakurai N., Suzuki H., Shibata D., Neumann S., Iida T., Tanaka K., Funatsu K., Matsuura F., Soga T., Taguchi R., Saito K., Nishioka T. MassBank: a public repository for sharing mass spectral data for life sciences. Journal of Mass Spectrometry 2010, 45:703-714.
15. Matsuda F., Yonekura-Sakakibara K., Niida R., Kuromori T., Shinozaki K., Saito K. MS/MS spectral tag-based annotation of non-targeted profile of plant secondary metabolites. Plant Journal 2009, 57:555-577.
16. Sawada Y., Nakabayashi R., Yamada Y., Suzuki M., Sato M., Sakata A., Akiyama K., Sakurai T., Matsuda F., Aoki T., Hirai M.Y., Saito K. RIKEN tandem mass spectral database (ReSpect) for phytochemicals: a plant-specific MS/MS-based data resource and database. Phytochemistry 2012, 82:38-45.
17. Graham T.L. Flavonoid and flavonol glycoside metabolism in Arabidopsis. Plant Physiology and Biochemistry 1998, 36:135-144.
18. Veit M., Pauli G.F. Major flavonoids from Arabidopsis thaliana leaves. Journal of Natural Products 1999, 62:1301-1303.
19. Bloor S.J., Abrahams S. The structure of the major anthocyanin in Arabidopsis thaliana. Phytochemistry 2002, 59:343-346.
20. Tohge T., Nishiyama Y., Hirai M.Y., Yano M., Nakajima J., Awazuhara M., Inoue E., Takahashi H., Goodenowe D.B., Kitayama M., Noji M., Yamazaki M., Saito K. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant Journal 2005, 42:218-235.
21. Kerhoas L., Aouak D., Cingoz A., Routaboul J.-M., Lepiniec L., Einhorn J., Birlirakis N. Structural characterization of the major flavonoid glycosides from Arabidopsis thaliana seeds. Journal of Agricultural and Food Chemistry 2006, 54:6603-6612.
22. Routaboul J.M., Kerhoas L., Debeaujon I., Pourcel L., Caboche M., Einhorn J., Lepiniec L. Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 2006, 224:96-107.
23. Stobiecki M., Skirycz A., Kerhoas L., Kachlicki P., Muth D., Einhorn J., Mueller-Roeber B. Profiling of phenolic glycosidic conjugates in leaves of Arabidopsis thaliana using LC/MS. Metabolomics 2006, 2:197-219.
24. Tohge T., Yonekura-Sakakibara K., Niida R., Watanabe-Takahashi A., Saito K. Phytochemical genomics in Arabidopsis thaliana: a case study for functional identification of flavonoid biosynthesis genes. Pure and Applied Chemistry 2007, 79:811-823.
25. Yonekura-Sakakibara K., Tohge T., Matsuda F., Nakabayashi R., Takayama H., Niida R., Watanabe-Takahashi A., Inoue E., Saito K. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 2008, 20:2160-2176.
26. Nakabayashi R., Kusano M., Kobayashi M., Tohge T., Yonekura-Sakakibara K., Kogure N., Yamazaki M., Kitajima M., Saito K., Takayama H. Metabolomics-oriented isolation and structure elucidation of 37 compounds including two anthocyanins from Arabidopsis thaliana. Phytochemistry 2009, 70:1017-1029.
27. Tohge T., Fernie A.R. Web-based resources for mass-spectrometry-based metabolomics: a user's guide. Phytochemistry 2009, 70:450-456.
28. Matsuda F., Hirai M.Y., Sasaki E., Akiyama K., Yonekura-Sakakibara K., Provart N.J., Sakurai T., Shimada Y., Saito K. AtMetExpress development: a phytochemical atlas of Arabidopsis development. Plant Physiology 2010, 152:566-578.
29. Vallabhaneni P., Ray W.K., Winkel B.S.J., Helm R.F. Characterization of flavonol glycosides in individual Arabidopsis root tips by flow injection electrospray mass spectrometry. Phytochemistry 2012, 73:114-118.
30. Rowan D.D., Cao M., Lin-Wang K., Cooney J.M., Jensen D.J., Austin P.T., Hunt M.B., Norling C., Hellens R.P., Schaffer R.J., Allan A.C. Environmental regulation of leaf colour in red 35S: PAP1 Arabidopsis thaliana. New Phytologist 2009, 182:102-115.
31. Stracke R., Jahns O., Keck M., Tohge T., Niehaus K., Fernie A.R., Weisshaar B. Analysis of production of flavonol glycosides-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12-and MYB111-independent flavonol glycoside accumulation. New Phytologist 2010, 188:985-1000.
32. Kitamura S., Matsuda F., Tohge T., Yonekura-Sakakibara K., Yamazaki M., Saito K., Narumi I. Metabolic profiling and cytological analysis of proanthocyanidins in immature seeds of Arabidopsis thaliana flavonoid accumulation mutants. Plant Journal 2010, 62:549-559.
33. Tanner G.J., Francki K.T., Abrahams S., Watson J.M., Larkin P.J., Ashton A.R. Proanthocyanidin biosynthesis in plants - purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. Journal of Biological Chemistry 2003, 278:31647-31656.
34. Xie D.Y., Dixon R.A. Proanthocyanidin biosynthesis - still more questions than answers?. Phytochemistry 2005, 66:2127-2144.
35. Pang Y., Peel G.J., Wright E., Wang Z., Dixon R.A. Early steps in proanthocyanidin biosynthesis in the model legume Medicago truncatula. Plant Physiology 2007, 145:601-615.
36. Pollastri S., Tattini M. Flavonols: old compounds for old roles. Annals of Botany 2011, 108:1225-1233.
37. Dixon R.A., Paiva N.L. Stress-induced phenylpropanoid metabolism. Plant Cell 1995, 7:1085-1097.
38. Winkel-Shirley B. Molecular genetics and control of anthocyanin expression. Advances in Botanical Research 2002, 75-94.
39. Taylor L.P., Grotewold E. Flavonoids as developmental regulators. Current Opinion in Plant Biology 2005, 8:317-323.
40. Roberts M.R., Paul N.D. Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytologist 2006, 170:677-699.
41. Falcone Ferreyra M.L., Rius S.P., Casati P. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Frontiers in Plant Science 2012, 3:1-15.
42. Teng S., Keurentjes J., Bentsink L., Koornneef M., Smeekens S. Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiology 2005, 139:1840-1852.
43. Diaz U., Saliba-Colombani V., Loudet O., Belluomo P., Moreau L., Daniel-Vedele F., Morot-Gaudry J.F., Maselaux-Daubresse U. Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant and Cell Physiology 2006, 47:74-83.
44. Korn M., Gaertner T., Erban A., Kopka J., Selbig J., Hincha D.K. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Molecular Plant 2010, 3:224-235.
45. Korn M., Peterek S., Mock H.-P., Heyer A.G., Hincha D.K. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell and Environment 2008, 31:813-827.
46. Matsuda F., Nakabayashi R., Sawada Y., Suzuki M., Hirai M.Y., Kanaya S., Saito K. Mass spectra-based framework for automated structural elucidation of metabolome data to explore phytochemical diversity. Frontiers in Plant Science 2011, 2:40.
47. Martens S., Forkmann G., Britsch L., Wellmann F., Matern U., Lukacin R. Divergent evolution of flavonoid 2-oxoglutarate-dependent dioxygenases in parsley. FEBS Letters 2003, 544:93-98.
48. Caputi L., Malnoy M., Goremykin V., Nikiforova S., Martens S. Agenome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant Journal 2011, 69:1030-1042.
49. Bredebach M., Matern U., Martens S. Three 2-oxoglutarate-dependent dioxygenase activities of Equisetum arvense L. forming flavone and flavonol from (2S)-naringenin. Phytochemistry 2011, 72:557-563.
50. T. Tohge, M. Watanabe, R. Hoefgen, A.R. Fernie, The evolution of phenylpropanoid metabolism in the green lineage, Critical Reviews in Biochemistry and Molecular biology, http://dx.doi.org/10.3109/10409238.2012.758083.
51. Turnbull J.J., Nakajima J.-I., Welford R.W.D., Yamazaki M., Saito K., Schofield C.J. Mechanistic studies on three 2-oxoglutarate-dependent oxygenases of flavonoid biosynthesis: anthocyanidin synthase, flavonol synthase, and flavanone 3β-hydroxylase. Journal of Biological Chemistry 2004, 279:1206-1216.
52. Yonekura-Sakakibara K., Hanada K. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant Journal 2011, 66:182-193.
53. Keurentjes J.J.B., Fu J.Y., de Vos C.H.R., Lommen A., Hall R.D., Bino R.J., van der Plas L.H.W., Jansen R.C., Vreugdenhil D., Koornneef M. The genetics of plant metabolism. Nature Genetics 2006, 38:842-849.
54. Tohge T., Fernie A.R. Combining genetic diversity, informatics and metabolomics to facilitate annotation of plant gene function. Nature Protocols 2010, 5:1210-1227.
55. Routaboul J.-M., Dubos C., Beck G., Marquis C., Bidzinski P., Loudet O., Lepiniec L. Metabolite profiling and quantitative genetics of natural variation for flavonoids in Arabidopsis. Journal of Experimental Botany 2012, 63:3749-3764.
56. Fraser C.M., Chapple C. The phenylpropanoid pathway in Arabidopsis. The Arabidopsis Book 2011, e0152.
57. Maeda H., Dudareva N. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology 2012, 63:73-105.
58. Ohl S., Hedrick S.A., Chory J., Lamb C.J. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 1990, 2:837-848.
59. Shufflebottom D., Edwards K., Schuch W., Bevan M. Transcription of two members of a gene family encoding phenylalanine ammonia-lyase leads to remarkably different cell specificities and induction patterns. Plant Journal 1993, 3:835-845.
60. Rohde A., Morreel K., Ralph J., Goeminne G., Hostyn V., De Rycke R., Kushnir S., Van Doorsselaere J., Joseleau J.P., Vuylsteke M., Van Driessche G., Van Beeumen J., Messens E., Boerjan W. Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 2004, 16:2749.
61. Raes J., Rohde A., Christensen J.H., Van de Peer Y., Boerjan W. Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiology 2003, 133:1051-1071.
62. Cochrane F.C., Davin L.B., Lewis N.G. The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms. Phytochemistry 2004, 65:1557-1564.
63. Huang J., Gu M., Lai Z., Fan B., Shi K., Zhou Y.H., Yu J.Q., Chen Z. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiology 2010, 153:1526.
64. Mizutani M., Ohta D., Sato R. Isolation of a cDNA and a genomic clone encoding cinnamate 4-hydroxylase from Arabidopsis and its expression manner in planta. Plant Physiology 1997, 113:755-763.
65. Werck-Reichhart D., Bak S., Paquette S. Cytochrome P450 2002, American Society of Plant Biologists.
66. Schilmiller A.L., Stout J., Weng J.-K., Humphreys J., Ruegger M.O., Chapple C. Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant Journal 2009, 60:771-782.
67. Ehlting J., Büttner D., Wang Q., Douglas C.J., Somssich I.E., Kombrink E. Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant Journal 1999, 19:9.
68. Hamberger B., Hahlbrock K. The 4-coumarate: CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:2209-2214.
69. Nikolau B.J., Ohlrogge J.B., Wurtele E.S. Plant biotin-containing carboxylases. Archives of Biochemistry and Biophysics 2003, 414:211-222.
70. Alban C., Job D., Douce R. Biotin metabolism in plants. Annual Review of Plant Physiology and Plant Molecular Biology 2000, 51:17-47.
71. Sasaki Y., Nagano Y. Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Bioscience, Biotechnology, and Biochemistry 2004, 68:1175-1184.
72. Li X., Ilarslan H., Brachova L., Qian H.R., Li L., Che P., Wurtele E.S., Nikolau B.J. Reverse-genetic analysis of the two biotin-containing subunit genes of the heteromeric acetyl-coenzyme A carboxylase in Arabidopsis indicates a unidirectional functional redundancy. Plant Physiology 2011, 155:293-314.
73. Roesler K.R., Shorrosh B.S., Ohlrogge J.B. Structure and expression of an Arabidopsis acetyl-coenzyme A carboxylase gene. Plant Physiology 1994, 105:611-617.
74. Yanai Y., Kawasaki T., Shimada H., Wurtele E.S., Nikolau B.J., Ichikawa N. Genomic organization of 251 kDa acetyl-CoA carboxylase genes in Arabidopsis: tandem gene duplication has made two differentially expressed isozymes. Plant and Cell Physiology 1995, 36:779-787.
75. Babiychuk E., Vandepoele K., Wissing J., Garcia-Diaz M., De Rycke R., Akbari H., Joubes J., Beeckman T., Jansch L., Frentzen M., Van Montagu M.C.E., Kushnir S. Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:6674-6679.
76. Puyaubert J., Denis L., Alban C. Dual targeting of Arabidopsis holocarboxylase synthetase1: a small upstream open reading frame regulates translation initiation and protein targeting. Plant Physiology 2008, 146:478-491.
77. Fatland B.L., Nikolau B.J., Wurtele E.S. Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell 2005, 17:182-203.
78. Baud S., Bellec Y., Miquel M., Bellini C., Caboche M., Lepiniec L., Faure J.D., Rochat C. gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. EMBO Reports 2004, 5:515-520.
79. Amid A., Lytovchenko A., Fernie A.R., Warren G., Thorlby G.J. The sensitive to freezing3 mutation of Arabidopsis thaliana is a cold-sensitive allele of homomeric acetyl-CoA carboxylase that results in cold-induced cuticle deficiencies. Journal of Experimental Botany 2012, 63:5289-5299.
80. Lu S.Y., Zhao H.Y., Parsons E.P., Xu C.C., Kosma D.K., Xu X.J., Chao D., Lohrey G., Bangarusamy D.K., Wang G., Bressan R.A., Jenks M.A. The glossyhead1 allele of ACC1 reveals a principal role for multidomain acetyl-coenzyme A carboxylase in the biosynthesis of cuticular waxes by Arabidopsis. Plant Physiology 2011, 157:1079-1092.
81. White A.J., Hanley S.Z., Elborough K.M., Slabas A.R. Physiological and biochemical consequences of down regulation, using antisense, of the high molecular weight form of acetyl CoA carboxylase in Brassica napus. Advances in Plant Lipid Research 1998, 63-66. Universidad de Sevilla, Sevilla. J. Sanchez, E. Cerda-Olmedo, E. Martinez-Force (Eds.).
82. Baud S., Guyon V., Kronenberger J., Wuilleme S., Miquel M., Caboche M., Lepiniec L., Rochat C. Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant Journal 2003, 33:75-86.
83. Ebel J., Hahlbrock K. Enzymes of flavone and flavonol-glycoside biosynthesis. Coordinated and selective induction in cell-suspension cultures of Petroselinum hortense. European Journal of Biochemistry 1977, 75:201-209.
84. Shorrosh B.S., Dixon R.A., Ohlrogge J.B. Molecular cloning, characterization, and elicitation of acetyl-CoA carboxylase from alfalfa. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:4323-4327.
85. Kusano M., Tohge T., Fukushima A., Kobayashi M., Hayashi N., Otsuki H., Kondou Y., Goto H., Kawashima M., et al. Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. Plant Journal 2011, 67:354-369.
86. Konishi T., Kamoi T., Matsuno R., Sasaki Y. Induction of cytosolic acetyl-coenzyme A carboxylase in pea leaves by ultraviolet-B irradiation. Plant and Cell Physiology 1996, 37:1197-1200.
87. Austin M.B., Noel J.P. The chalcone synthase superfamily of type III polyketide synthases. Natural Product Reports 2003, 20:79-110.
88. Shirley B.W., Kubasek W.L., Storz G., Bruggemann E., Koornneef M., Ausubel F.M., Goodman H.M. Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant Journal 1995, 8:659-671.
89. Kim S.S., Grienenberger E., Lallemand B., Colpitts C.C., Kim S.Y., Souza Cde A., Geoffroy P., Heintz D., Krahn D., Kaiser M., Kombrink E., Heitz T., Suh D.Y., Legrand M., Douglas C.J. LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl alpha-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 2010, 22:4045-4066.
90. Dobritsa A.A., Lei Z., Nishikawa S., Urbanczyk-Wochniak E., Huhman D.V., Preuss D., Sumner L.W. LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiology 2010, 153:937-955.
91. Ngaki M.N., Louie G.V., Philippe R.N., Manning G., Pojer F., Bowman M.E., Li L., Larsen E., Wurtele E.S., Noel J.P. Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis. Nature 2012, 485:530-533.
92. Pelletier M.K., Shirley B.W. Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings - coordinate regulation with chalcone synthase and chalcone isomerase. Plant Physiology 1996, 111:339-345.
93. Owens D.K., Crosby K.C., Runac J., Howard B.A., Winkel B.S.J. Biochemical and genetic characterization of Arabidopsis flavanone 3β-hydroxylase. Plant Physiology and Biochemistry 2008, 46:833-843.
94. Schoenbohm C., Martens S., Eder C., Forkmann G., Weisshaar B. Identification of the Arabidopsis thaliana flavonoid 3'-hydroxylase gene and functional expression of the encoded P450 enzyme. Biological Chemistry 2000, 381:749-753.
95. Pelletier M.K., Murrell J.R., Shirley B.W. Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis - further evidence for differential regulation of 'early' and 'late' genes. Plant Physiology 1997, 113:1437-1445.
96. Prescott A.G., Stamford N.P.J., Wheeler G., Firmin J.L. Invitro properties of a recombinant flavonol synthase from Arabidopsis thaliana. Phytochemistry 2002, 60:589-593.
97. Wisman E., Hartmann U., Sagasser M., Baumann E., Palme K., Hahlbrock K., Saedler H., Weisshaar B. Knock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate phenylpropanoid biosynthesis phenotypes. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:12432-12437.
98. Owens D.K., Alerding A.B., Crosby K.C., Bandara A.B., Westwood J.H., Winkel B.S.J. Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiology 2008, 147:1046-1061.
99. Stracke R., De Vos R., Bartelniewoehner L., Ishihara H., Sagasser M., Martens S., Weisshaar B. Metabolomic and genetic analyses of flavonol synthesis in Arabidopsis thaliana support the invivo involvement of leucoanthocyanidin dioxygenase. Planta 2009, 229:427-445.
100. Preuß A., Stracke R., Weisshaar B., Hillebrecht A., Matern U., Martens S. Arabidopsis thaliana expresses a second functional flavonol synthase. FEBS Letters 2009, 583:1981-1986.
101. Shirley B.W., Hanley S., Goodman H.M. Effects of ionizing-radiation on a plant genome - analysis of 2 Arabidopsis transparent-testa mutations. Plant Cell 1992, 4:333-347.
102. Bowerman P., Ramirez M., Moore M., Helm R., Winkel B. Analysis of T-DNA alleles of flavonoid biosynthesis genes in Arabidopsis ecotype Columbia. BMC Research Notes 2012, 5:485.
103. Abrahams S., Lee E., Walker A.R., Tanner G.J., Larkin P.J., Ashton A.R. The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant Journal 2003, 35:624-636.
104. Nakajima J.-I., Tanaka Y., Yamazaki M., Saito K. Reaction mechanism from leucoanthocyanidin to anthocyanidin 3-glucoside, a key reaction for coloring in anthocyanin biosynthesis. Journal of Biological Chemistry 2001, 276:25797-25803.
105. Welford R.W., Turnbull J.J., Claridge T.D., Prescott A.G., Schofield C.J. Evidence for oxidation at C-3 of the flavonoid C-ring during anthocyanin biosynthesis. Chemical Communications (Cambridge) 2001, 1828-1829.
106. Saito K., Kobayashi M., Gong Z., Tanaka Y., Yamazaki M. Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependent oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens. Plant Journal 1999, 17:181-189.
107. Martens S., Preuß A., Matern U. Multifunctional flavonoid dioxygenases: flavonol and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry 2010, 71:1040-1049.
108. Nakajima J.-i., Sato Y., Hoshino T., Yamazaki M., Saito K. Mechanistic study on the oxidation of anthocyanidin synthase by quantum mechanical calculation. Journal of Biological Chemistry 2006, 281:21387-21398.
109. Devic M., Guilleminot J., Debeaujon I., Bechtold N., Bensaude E., Koornneef M., Pelletier G., Delseny M. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant Journal 1999, 19:387-398.
110. Xie D.-Y., Sharma S.B., Dixon R.A. Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana. Archives of Biochemistry and Biophysics 2004, 422:91-102.
111. Xie D.Y., Sharma S.B., Paiva N.L., Ferreira D., Dixon R.A. Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 2003, 299:396-399.
112. Bogs J., Downey M.O., Harvey J.S., Ashton A.R., Tanner G.J., Robinson S.P. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiology 2005, 139:652-663.
113. Yuan L., Wang L., Han Z., Jiang Y., Zhao L., Liu H., Yang L., Luo K. Molecular cloning and characterization of PtrLAR3, a gene encoding leucoanthocyanidin reductase from Populus trichocarpa, and its constitutive expression enhances fungal resistance in transgenic plants. Journal of Experimental Botany 2012, 63:2513-2524.
114. Pourcel L., Routaboul J.M., Kerhoas L., Caboche M., Lepiniec L., Debeaujon I. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 2005, 17:2966-2980.
115. Pourcel L., Routaboul J.-M., Cheynier V., Lepiniec L., Debeaujon I. Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends in Plant Science 2007, 12:29-36.
116. Li Y., Baldauf S., Lim E.K., Bowles D.J. Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. Journal of Biological Chemistry 2001, 276:4338-4343.
117. D'Auria J.C., Gershenzon J. The secondary metabolism of Arabidopsis thaliana: growing like a weed. Current Opinion in Plant Biology 2005, 8:308-316.
118. Jones P., Messner B., Nakajima J., Schaffner A.R., Saito K. UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. Journal of Biological Chemistry 2003, 278:43910-43918.
119. Yonekura-Sakakibara K., Tohge T., Niida R., Saito K. Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. Journal of Biological Chemistry 2007, 282:14932-14941.
120. Yonekura-Sakakibara K., Fukushima A., Nakabayashi R., Hanada K., Matsuda F., Sugawara S., Inoue E., Kuromori T., Ito T., et al. Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. Plant Journal 2012, 69:154-167.
121. 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. Anovel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 2010, 22:3374-3389.
122. Miyahara T., Takahashi M., Ozeki Y., Sasaki N. Isolation of an acyl-glucose-dependent anthocyanin 7-O-glucosyltransferase from the monocot Agapanthus africanus. Journal of Plant Physiology 2012, 169:1321-1326.
123. T. Miyahara, R. Sakiyama, Y. Ozeki, N. Sasaki, Acyl-glucose-dependent glucosyltransferase catalyzes the final step of anthocyanin formation in Arabidopsis, Journal of Plant Physiology, http://dx.doi.org/10.1016/j.jplph.2012.12.001.
124. Yonekura-Sakakibara K., Nakayama T., Yamazaki M., Saito K. Modification and stabilization of anthocyanins. Anthocyanins. Biosynthesis, Functions, and Applications 2008, 169-190. Springer, New York. K. Gould, K. Davies, C. Winefield (Eds.).
125. D'Auria J.C., Reichelt M., Luck K., Svatos A., Gershenzon J. Identification and characterization of the BAHD acyltransferase malonyl CoA: anthocyanidin 5-O-glucoside-6'-O-malonyltransferase (At5MAT) in Arabidopsis thaliana. FEBS Letters 2007, 581:872-878.
126. Muzac I., Wang J., Anzellotti D., Zhang H., Ibrahim R.K. Functional expression of an Arabidopsis cDNA clone encoding a flavonol 3'-O-methyltransferase and characterization of the gene product. Archives of Biochemistry and Biophysics 2000, 375:385-388.
127. Goujon T., Sibout R., Pollet B., Maba B., Nussaume L., Bechtold N., Lu F., Ralph J., Mila I., Barrière Y., Lapierre C., Jouanin L. Anew Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Molecular Biology 2003, 51:973-989.
128. St-Pierre B., Luca V.D. Chapter nine evolution of acyltransferase genes: origin and diversification fo the BAHD superfamily of acyltransferases involved in secondary metabolism. Recent Advances in Phytochemistry 2000, 285-315. Elsevier. R.I.L.V. John, T. Romeo, L. Vincenzo De (Eds.).
129. Milkowski C., Strack D. Serine carboxypeptidase-like acyltransferases. Phytochemistry 2004, 65:517-524.
130. Luo J., Nishiyama Y., Fuell C., Taguchi G., Elliott K., Hill L., Tanaka Y., Kitayama M., Yamazaki M., Bailey P., Parr A., Michael A.J., Saito K., Martin C. Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant Journal 2007, 50:678-695.
131. Fraser C.M., Thompson M.G., Shirley A.M., Ralph J., Schoenherr J.A., Sinlapadech T., Hall M.C., Chapple C. Related Arabidopsis serine carboxypeptidase-like sinapoylglucose acyltransferases display distinct but overlapping substrate specificities. Plant Physiology 2007, 144:1986-1999.
132. Kubo H., Nawa N., Lupsea S.A. Anthocyaninless1 gene of Arabidopsis thaliana encodes a UDP-glucose:flavonoid-3-O-glucosyltransferase. Journal of Plant Research 2007, 120:445-449.
133. Yamazaki M., Yamagishi E., Gong Z., Fukuchi-Mizutani M., Fukui Y., Tanaka Y., Kusumi T., Yamaguchi M., Saito K. Two flavonoid glucosyltransferases from Petunia hybrida: molecular cloning, biochemical properties and developmentally regulated expression. Plant Molecular Biology 2002, 48:401-411.
134. Yamazaki M., Gong Z., Fukuchi-Mizutani M., Fukui Y., Tanaka Y., Kusumi T., Saito K. Molecular cloning and biochemical characterization of a novel anthocyanin 5-O-glucosyltransferase by mRNA differential display for plant forms regarding anthocyanin. Journal of Biological Chemistry 1999, 274:7405-7411.
135. Lim E.K., Li Y., Parr A., Jackson R., Ashford D.A., Bowles D.J. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. Journal of Biological Chemistry 2001, 276:4344-4349.
136. Morita Y., Hoshino A., Kikuchi Y., Okuhara H., Ono E., Tanaka Y., Fukui Y., Saito N., Nitasaka E., Noguchi H., Iida S. Japanese morning glory dusky mutants displaying reddish-brown or purplish-gray flowers are deficient in a novel glycosylation enzyme for anthocyanin biosynthesis, UDP-glucose:anthocyanidin 3-O-glucoside-2'-O-glucosyltransferase, due to 4-bp insertions in the gene. Plant Journal 2005, 42:353-363.
137. Sawada S., Suzuki H., Ichimaida F., Yamaguchi M.A., Iwashita T., Fukui Y., Hemmi H., Nishino T., Nakayama T. UDP-glucuronic acid:anthocyanin glucuronosyltransferase from red daisy (Bellis perennis) flowers. Enzymology and phylogenetics of a novel glucuronosyltransferase involved in flower pigment biosynthesis. Journal of Biological Chemistry 2005, 280:899-906.
138. Usadel B., Kuschinsky A.M., Rosso M.G., Eckermann N., Pauly M. RHM2 is involved in mucilage pectin synthesis and is required for the development of the seed coat in Arabidopsis. Plant Physiology 2004, 134:286-295.
139. Western T.L., Young D.S., Dean G.H., Tan W.L., Samuels A.L., Haughn G.W. MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat. Plant Physiology 2004, 134:296-306.
140. Oka T., Nemoto T., Jigami Y. Functional analysis of Arabidopsis thaliana RHM2/MUM4, a multidomain protein involved in UDP-D-glucose to UDP-L-rhamnose conversion. Journal of Biological Chemistry 2007, 282:5389-5403.
141. Shikazono N., Tanaka A., Watanabe H., Tano S. Rearrangements of the DNA in carbon ion-induced mutants of Arabidopsis thaliana. Genetics 2001, 157:379-387.
142. Kitamura S., Shikazono N., Tanaka A. TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant Journal 2004, 37:104-114.
143. Zhao J., Pang Y., Dixon R.A. The mysteries of proanthocyanidin transport and polymerization. Plant Physiology 2010, 153:437-443.
144. Debeaujon I., Peeters A.J.M., Leon-Kloosterziel K.M., Koornneef M. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 2001, 13:853-871.
145. +-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 2007, 19:2023-2038.
146. Thompson E.P., Wilkins C., Demidchik V., Davies J.M., Glover B.J. An Arabidopsis flavonoid transporter is required for anther dehiscence and pollen development. Journal of Experimental Botany 2010, 61:439-451.
147. Marrs K.A., Alfenito M.R., Lloyd A.M., Walbot V. Aglutathione-s-transferase involved in vacuolar transfer encoded by the maize gene bronze-2. Nature 1995, 375:397-400.
148. Wangwattana B., Koyama Y., Nishiyama Y., Kitayama M., Yamazaki M., Saito K. Characterization of PAP1-upregulated Glutathione S-transferase genes in Arabidopsis thaliana. Plant Biotechnology 2008, 25:191-196.
149. Alfenito M.R., Souer E., Goodman C.D., Buell R., Mol J., Koes R., Walbot V. Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 1998, 10:1135-1149.
150. Loyall L., Uchida K., Braun S., Furuya M., Frohnmeyer H. Glutathione and a UV light-induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 2000, 12:1939-1950.
151. Mueller L.A., Goodman C.D., Silady R.A., Walbot V. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiology 2000, 123:1561-1570.
152. Kitamura S., Akita Y., Ishizaka H., Narumi I., Tanaka A. Molecular characterization of an anthocyanin-related glutathione S-transferase gene in cyclamen. Journal of Plant Physiology 2012, 169:636-642.
153. Kitamura S. Transport of flavonoids. Science of Flavonoids 2008, 123-146. E. Grotewold (Ed.).
154. Smith A.P., Nourizadeh S.D., Peer W.A., Xu J.H., Bandyopadhyay A., Murphy A.S., Goldsbrough P.B. Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant Journal 2003, 36:433-442.
155. Zhao J., Dixon R.A. MATE transporters facilitate vacuolar uptake of epicatechin 3'-O-Glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 2009, 21:2323-2340.
156. Sun Y., Li H., Huang J.-R. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Molecular Plant 2012, 5:387-400.
157. +-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:2649-2654.
158. Yonekura-Sakakibara K., Fukushima A., Saito K. Transcriptome data modeling toward plant metabolic engineering. Current Opinion in Biotechnology 2013.
159. R.A. Dixon, C. Liu, J.H. Jun, Metabolic engineering of anthocyanins and condensed tannins in plants, Current Opinion in Biotechnology, http://dx.doi.org/10.1016/j.copbio.2012.07.004.
160. A. Bar-Even, D. Salah Tawfik, Engineering specialized metabolic pathways-is there a room for enzyme improvements?, Current Opinion in Biotechnology, http://dx.doi.org/10.1016/j.copbio.2012.10.006.
161. Yamazaki M., Saito K. Molecular genetic study on the anthocyanin chemotypes of Perilla frutescens var. crispa. Natural Product Communications 2011, 6:423-427.
162. Saito K., Yamazaki M. Biochemistry and molecular biology of the late-stage of biosynthesis of anthocyanin: lessons from Perilla frutescens as a model plant. New Phytologist 2002, 155:9-23.
163. Yonekura-Sakakibara K., Saito K. Functional genomics for plant natural product biosynthesis. Natural Product Reports 2009, 26:1466-1487.
164. Yonekura-Sakakibara K., Saito K. Review: genetically modified plants for the promotion of human health. Biotechnology Letters 2006, 28:1983-1991.
165. Butelli E., Titta L., Giorgio M., Mock H.-P., Matros A., Peterek S., Schijlen E.G.W.M., Hall R.D., Bovy A.G., Luo J., Martin C. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nature Biotechnology 2008, 26:1301-1308.
166. R. Nakabayashi, K. Saito, Metabolomics for unknown plant metabolites, Analytical and Bioanalytical Chemistry, in press.
167. Oikawa A., Saito K. Metabolite analyses of single cells. Plant Journal 2012, 70:30-38.
168. De Luca V., Salim V., Atsumi S.M., Yu F. Mining the biodiversity of plants: a revolution in the making. Science 2012, 336:1658-1661.