Skip to main content
Log in

Diversity in plant red pigments: anthocyanins and betacyanins

Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Plant pigments are of interest for research into questions of basic biology as well as for purposes of applied biology. Red colors in flowers are mainly produced by two types of pigments: anthocyanins and betacyanins. Though anthocyanins are broadly distributed among plants, betacyanins have replaced anthocyanins in the Caryophyllales. Red plant pigments are good indicator metabolites for evolutionary studies of plant diversity as well as for metabolic studies of plant cell growth and differentiation. In this review, we focus on the biosynthesis of anthocyanins and betacyanins and the possible mechanisms underlying the mutual exclusion of betalains and anthocyanins based on the regulation of the biosynthesis of these red pigments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Allegra M, Tesoriere L, Livrea MA (2007) Betanin inhibits the myeloperoxidase/nitrite-induced oxidation of human low density lipoproteins. Free Rad Res 41:335–341

    CAS  Google Scholar 

  • Arias JA, Dixon RA, Lamb CJ (1993) Dissection of the functional architecture of a plant defense gene promoter using a homologous in vitro transcription initiation system. Plant Cell 5:485–496

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bauberger E, Mayer AM (1960) Effect of kinetin on formation of red pigment in seedlings of Amaranthus retroflexus. Science 141:1094–1095

    Google Scholar 

  • Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2 TT8, and TTG1 synergistically specify the expression of BANYULS and, proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380

    CAS  PubMed  Google Scholar 

  • Beld M, Martin C, Huits H, Stuitje AR, Gerats AG (1989) Flavonoid synthesis in Petunia hybrida: partial characterization of dihydroflavonol-4-reductase genes. Plant Mol Biol 13:491–502

    CAS  PubMed  Google Scholar 

  • Bernhardt J, Stich K, Schwarz-Sommer Z, Saedler H, Wienand U (1998) Molecular analysis of a second functional A1 gene (dihydroflavonol 4-reductase) in Zea mays. Plant J 14:483–488

    CAS  PubMed  Google Scholar 

  • Biddington NK, Thomas TH (1973) A modified Amaranthus betacyanin bioassay for the rapid determination of cytokinins in plant extracts. Planta 111:183–186

    CAS  PubMed  Google Scholar 

  • Biddington NK, Thomas TH (1977) Interaction of abscisic acid, cytokinin and gibberellins in the control of betacyanin synthesis in seedlings of Amaranthus caudatus. Physiol Plant 40:312–314

    CAS  Google Scholar 

  • Brockington SF, Walker RH, Glover BJ, Soltis PS, Soltis DE (2011) Complex pigment evolution in the Caryophyllales. New Phytol 190:854–864

    CAS  PubMed  Google Scholar 

  • Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Opin Plant Biol 8:272–279

    CAS  PubMed  Google Scholar 

  • Cai Y, Sun M, Corke H (2003) Antioxidant activity of betalains from plants of the Amaranthaceae. J Agric Food Chem 51:2288–2294

    CAS  PubMed  Google Scholar 

  • Christensen AB, Gregersen PL, Schroder J, Collinge DB (1998) A chalcone synthase with an unusual substrate preference is expressed in barley leaves in response to UV light and pathogen attack. Plant Mol Biol 37:849–857

    CAS  PubMed  Google Scholar 

  • Christensen KY, Naidu A, Parent MÉ, Pintos J, Abrahamowicz M, Siemiatycki J, Koushik A (2012) The risk of lung cancer related to dietary intake of flavonoids. Nutr Cancer 64:964–974

    CAS  PubMed  Google Scholar 

  • Christinet L, Burdet FX, Zaiko M, Hinz U, Zrÿd JP (2004) Characterization and functional identification of a novel plant 4,5-extradiol dioxygenase involved in betalain pigment biosynthesis in Portulaca grandiflora. Plant Physiol 134:265–274

    CAS  PubMed Central  PubMed  Google Scholar 

  • Constabel F, Nassif-Makki H (1971) Betalainbildung in Beta-Calluskulturen. Ber Deutsch Bot Ges 84:629–636

    CAS  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25:173–199

    CAS  PubMed  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726–738

    PubMed  Google Scholar 

  • Elliott DC (1979a) Analysis of variability in the Amaranthus bioassay for cytokinins: effects of water stress on benzyladenine- and fusicoccin-dependent responses. Plant Physiol 63:269–273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elliott DC (1979b) Analysis of variability in the Amaranthus bioassay for cytokinins: effects of “aging” excised cotyledons. Plant Physiol 63:274–276

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elliott DC (1979c) Temperature-dependent expression of betacyanin synthesis in Amaranthus seedlings. Plant Physiol 63:277–279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elliott DC (1979d) Temperature-sensitive responses of red light-dependent betacyanin synthesis. Plant Physiol 64:521–524

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elliott DC (1983) Accumulation of cytokinin-induced betacyanin in specific cells of Amaranthus tricolor seedlings. J Exp Bot 34:67–73

    CAS  Google Scholar 

  • Endress R (1976) Betacyan-Akkumulation in Kallus von Portulaca grandiflora var. JR unter dem Einfluss von Phytohormonen und Cu2+-Ionen auf unterschiedlichen Grundmedium. Biochem Physiol Pflanzen 169:87–98

    CAS  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116

    CAS  PubMed  Google Scholar 

  • Fischer N, Dreiding AS (1972) Biosynthesis of betaleins. On the cleavage of the aromatic ring during enzymic transformation of dopa into betalamic acid. Helv Chem Acta 55:649–658

    CAS  Google Scholar 

  • Forkmann G, Martens S (2001) Metabolic engineering and applications of flavonoids. Curr Opin Biotechnol 12:155–160

    CAS  PubMed  Google Scholar 

  • Fracassetti D, Del Bo’ C, Simonetti P, Gardana C, Klimis-Zacas D, Ciappellano S (2013) Effect of time and storage temperature on anthocyanin decay and antioxidant activity in wild blueberry (Vaccinium angustifolium) powder. J Agric Food Chem 27:2999–3005

    Google Scholar 

  • Gandía-Herrero F, García-Carmona F (2012) Characterization of recombinant Beta vulgaris 4,5-DOPA-extradiol-dioxygenase active in the biosynthesis of betalains. Planta 236:91–100

    PubMed  Google Scholar 

  • Gandía-Herrero F, García-Carmona F (2013) Biosynthesis of betalains: yellow and violet plant pigments. Trends Plant Sci 18:334–343

    PubMed  Google Scholar 

  • Garay AS, Towers GHN (1966) Studies on the biosynthesis of amaranthin. Can J Bot 44:231–236

    CAS  Google Scholar 

  • Girod PA, Zrÿd JP (1991) Biogenesis of betalains: purification and partial characterization of Dopa 4,5-dioxygenase from Amanita muscaria. Phytochemistry 30:169–174

    CAS  Google Scholar 

  • Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433:481–487

    CAS  PubMed  Google Scholar 

  • Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827

    CAS  PubMed  Google Scholar 

  • Guruprasad KN, Laloraya MM (1980) Dissimilarity in the inhibition of betacyanin synthesis caused by gibberellic acid and abscisic acid. Biochem Physiol Pflanzen 175:582–586

    Google Scholar 

  • Hahlblock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40:347–369

    Google Scholar 

  • Harborne JB (1996) The evolution of flavonoid pigments in plants. In: Swain T (ed) Comparative phytochemistry. Academic Press, London, pp 271–295

    Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:6481–6504

    Google Scholar 

  • Harris NN, Javellana J, Davies KM, Lewis DH, Jameson PE, Deroles SC, Calcott KE, Gould KS, Schwinn KE (2012) Betalain production is possible in anthocyanin-producing plant species given the presence of DOPA-dioxygenase and l-DOPA. BMC Plant Biol 12:34

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Heinekamp T, Kuhlmann M, Lenk A, Strathmann A, Dröge-Laser W (2002) The tobacco bZIP transcription factor BZI-1 binds to G-box elements in the promoters of phenylpropanoid pathway genes in vitro, but it is not involved in their regulation in vivo. Mol Genet Genomics 267:16–26

    CAS  PubMed  Google Scholar 

  • Helariutta Y, Elomaa P, Kotilainen M, Seppanen P, Teeri TH (1993) Cloning of cDNA coding for dihydroflavonol-4-reductase (DFR) and characterization of dfr expression in the corollas of Gerbera hybrida var. Regina (Compositae). Plant Mol Biol 22:183–193

    CAS  PubMed  Google Scholar 

  • Heuer S, Strack D (1992) Synthesis of betanin from betanidin and UDP-glucose by a protein preparation from cell suspension cultures of Dorotheanthus bellidiformis (Burm.f.) N. E. Br. Planta 186:626–628

    CAS  PubMed  Google Scholar 

  • Hinz UG, Fivaz J, Girod PA, Zrÿd JP (1997) The gene coding for the DOPA dioxygenase involved in betalain biosynthesis in Amanita muscaria and its regulation. Mol Gen Genet 256:1–6

    CAS  PubMed  Google Scholar 

  • Hirano H, Komamine A (1994) Correlation of betacyanin synthesis with cell division in cell suspension cultures of Phytolacca americana. Physiol Plant 90:239–245

    CAS  Google Scholar 

  • Hirano H, Sakuta M, Komamine A (1996) Inhibition of betacyanin accumulation by abscisic acid in suspension cultures of Phytolacca americana. Z Naturforsch C 51:818–822

    CAS  Google Scholar 

  • Hobbs DA, Kaffa N, George TW, Methven L, Lovegrove JA (2012) Blood pressure-lowering effects of beetroot juice and novel beetroot-enriched bread products in normotensive male subjects. Br J Nutr 108:2066–2074

    CAS  PubMed  Google Scholar 

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083

    CAS  PubMed Central  PubMed  Google Scholar 

  • Impellizzeri G, Piattelli M (1972) Biosynthesis of indicaxanthin in Opuntia ficus-indica fruit. Phytochemistry 11:2499–2502

    CAS  Google Scholar 

  • Inagaki Y, Johzuka-Hisatomi Y, Mori T, Takahashi S, Hayakawa Y, Peyachoknagul S, Ozeki Y, Iida S (1999) Genomic organization of the genes encoding dihydroflavonol 4-reductase for flower pigmentation in the Japanese and common morning glories. Gene 226:181–188

    CAS  PubMed  Google Scholar 

  • Itoh Y, Higeta D, Suzuki A, Yoshida H, Ozeki Y (2002) Excision of transposable elements from the chalcone isomerase and dihydroflavonol 4-reductase genes may contribute to the variegation of the yellow-flowered carnation (Dianthus caryophyllus). Plant Cell Physiol 43:578–585

    CAS  PubMed  Google Scholar 

  • Iwashina T (2001) Flavonoids and their distribution in plant families containing the betalain pigments. Ann Tsukuba Bot Gard 20:11–74

    Google Scholar 

  • Iwashina T, Ootani S, Hayashi K (1988) On the pigmentation spherical bodies and crystals in tepals of Cactaceous species in reference to the nature of betalains or flavonols. Bot Mag Tokyo 101:175–184

    CAS  Google Scholar 

  • Joy RW 4th, Sugiyama M, Fukuda H, Komamine A (1995) Cloning and characterization of polyphenol oxidase cDNAs of Phytolacca americana. Plant Physiol 107:1083–1089

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kircher S, Ledger S, Hayashi H, Weisshaar B, Schafer E, Rohnmeyer H (1998) CPRF4a, a novel plant bZIP protein of the CPRF family: comparative analyses of light-dependent expression, post-transcriptional regulation, nuclear import and heterodimerisation. Mol Gen Genet 257:595–605

    CAS  PubMed  Google Scholar 

  • Kircher S, Wellmer F, Nick P, Rugner A, Schafer E, Harter K (1999) Nuclear import of the parsley bZIP transcription factor CPRF2 is regulated by phytochrome photoreceptors. J Cell Biol 144:201–211

    CAS  PubMed  Google Scholar 

  • Kochhar HK (1972a) Action of inhibitors of protein and nucleic acid synthesis on light-dependent and kinetin-stimulated betacyanin synthesis. Phytochemistry 11:127–132

    Google Scholar 

  • Kochhar HK (1972b) Phytocontrol of betacyanin synthesis in Amaranthus caudatus seedlings in the presence of kinetin. Phytochemistry 11:133–137

    Google Scholar 

  • Kochhar HK, Kochhar S, Mohr H (1981) Action of light and kinetin on betalain synthesis in seedlings of Amaranthus caudatus: a two-factor analysis. Ber Deutsch Bot Ges 94:27–34

    CAS  Google Scholar 

  • Koes R, Quattrocchio F, Mol J (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16:123–132

    CAS  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242

    CAS  PubMed  Google Scholar 

  • Komamine A (1962) Metabolism of aromatic amino acids in plants I. On 3,4-dihydroxyphenylalanine in Stizolobium hassjoo. Bot Mag Tokyo 75:228–236

    CAS  Google Scholar 

  • Komamine A, Sakuta M, Hirose M, Hirano H, Takagi T, Kakegawa K, Ozeki Y (1989) Regulation of secondary metabolism in relation to growth and differentiation. In: Kurz WGW (ed) Primary and secondary metabolism of plant cell cultures II. Springer-Verlag, Berlin, pp 49–52

    Google Scholar 

  • Kujala T, Loponen J, Pihlaja K (2001) Betalains and phenolics in red beetroot (Beta vulgaris) peel extracts: extraction and characterisation. Z Naturforsch C 56:343–348

    CAS  PubMed  Google Scholar 

  • Lawson CG, Djordjevic MA, Weinman JJ, Rolfe BG (1994) Rhizobium inoculation and physical wounding result in the rapid induction of the same chalcone synthase copy in Trifolium subterraneum. Mol Plant Microbe Interact 7:498–507

    CAS  PubMed  Google Scholar 

  • Lee CH, Wettasinghe M, Bolling BW, Ji LL, Parkin KL (2005) Betalains, phase II enzyme-inducing components from red beetroot (Beta vulgaris L.) extracts. Nutr Cancer 53:91–103

    CAS  PubMed  Google Scholar 

  • Li C, Feng J, Huang WY, An XT (2013) Composition of polyphenols and antioxidant activity of rabbiteye blueberry (Vaccinium ashei) in Nanjing. J Agric Food Chem 23:523–531

    Google Scholar 

  • Loake GJ, Faktor O, Lamb CJ, Dixon RA (1992) Combination of H-box [CCTACC(N)7CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc Natl Acad Sci USA 89:9230–9234

    CAS  PubMed  Google Scholar 

  • Logemann E, Tavernaro A, Schulz W, Somssich IE, Hahlbrock K (2000) UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc Natl Acad Sci USA 97:1903–1907

    CAS  PubMed  Google Scholar 

  • Mabry TJ (1980) Betalains. In: Bell EA, Charlwood BV (eds) Secondary plant products. Encyclopedia of plant physiology, vol 8. Springer-Verlag, Berlin, pp 513–533

    Google Scholar 

  • Martin C, Prescott A, Mackay S, Bartlett J, Vrijlandt E (1991) Control of anthocyanin biosynthesis in flowers of Antirrhinum majus. Plant J 1:37–49

    CAS  PubMed  Google Scholar 

  • Miller HE, Rosler H, Wohlpart A, Wyler H, Wilcox ME, Frohofer H, Mabry TJ, Dreiding AS (1968) Biogenese der betalaine. Biotransformation von Dopa und tyrosin in den betalaminsaureteil des betanins. Vorläufige Mitteilung. Helv Chim Acta 51:1470–1474

    CAS  PubMed  Google Scholar 

  • Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3:212–217

    Google Scholar 

  • Mueller LA, Hinz U, Uze M, Sautter C, Zrÿd JP (1997a) Biochemical complementation of the betalain biosynthetic pathway in Portulaca grandiflora by a fungal 3,4- dihydroxyphenylalanine dioxygenase. Planta 203:260–263

    CAS  Google Scholar 

  • Mueller LA, Hinz U, Zrÿd JP (1997b) The formation of betalamic acid and muscaflavin by recombinant dopa-dioxygenase from Amanita. Phytochemistry 44:567–569

    CAS  Google Scholar 

  • Nakajima J, Tanaka Y, Yamazaki M, Saito K (2001) Reaction mechanism from leucoanthocyanidin to anthocyanidin 3-glucoside, a key reaction for coloring in anthocyanin biosynthesis. J Biol Chem 276:25797–25803

    CAS  PubMed  Google Scholar 

  • Nassif-Makki H, Constabel F (1972) Zur Bedeutung von tyrosin als vorstufe der betalainsynthese. Z Pflanzenphysiol 67:201–206

    CAS  Google Scholar 

  • Nicola MG, Piattelli M, Amico V (1973a) Phytocontrol of betaxanthin synthesis in Celosia plumosa seedlings. Phytochemistry 12:353–357

    Google Scholar 

  • Nicola MG, Piattelli M, Amico V (1973b) Effect of continuous far red on betaxanthin and betacyanin synthesis. Phytochemistry 12:2163–2166

    Google Scholar 

  • Nicola MG, Amico V, Piattelli M (1974) Effect of white and far-red light on betalain formation. Phytochemistry 13:439–442

    Google Scholar 

  • Ozeki Y, Komamine A (1981) Induction of anthocyanin synthesis in relation to embryogenesis in a carrot suspension culture: correlation of metabolic differentiation with morphological differentiation. Physiol Plant 53:570–577

    CAS  Google Scholar 

  • Ozeki Y, Komamine A (1986) Effects of growth regulators on the induction of anthocyanin synthesis in a carrot suspension culture. Plant Cell Physiol 27:1361–1368

    CAS  Google Scholar 

  • Ozeki Y, Matsuba Y, Abe Y, Umemoto N, Sasaki N (2011) Plant pigments I: anthocyanins. In: Ashihara H, Crozier A, Komamine A (eds) Plant metabolism and biotechnology. Wiley, pp 343–372

  • Piatteri M (1976) Betalains. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments, vol 1. Academic press, New York, pp 560–596

    Google Scholar 

  • Quattrocchio F, Wing JF, Leppen HTC, Mol J, Koes RE (1993) Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5:1497–1512

    CAS  PubMed Central  PubMed  Google Scholar 

  • Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70

    CAS  PubMed  Google Scholar 

  • Ryder TB, Hedrick SA, Bell JN, Liang XW, Clouse SD, Lamb CJ (1987) Organization and differential activation of a gene family encoding the plant defense enzyme chalcone synthase in Phaseolus vulgaris. Mol Gen Genet 210:219–233

    CAS  PubMed  Google Scholar 

  • Saito K, Komamine A (1976) Biosynthesis of stizolobinic acid and stizolobic acid in higher plants: a enzyme system(s) catalyzing the conversion of dihydroxyphenylalanine into stizolobinic acid and stizolobic acid from etiolated seedlings of Stizolobium hassjoo. Eur J Biochem 68:237–243

    CAS  PubMed  Google Scholar 

  • Saito K, Komamine A (1978) Biosynthesis of stizolobinic acid and stizolobic acid in higher plants: stizolobinic acid synthase and stizolobic acid synthase, new enzymes which catalyze the reaction sequences leading to the formation of stizolobinic acid and stizolobic acid from 3,4-dihydroxyphenylalanine in Stizolobium hassjoo. Eur J Biochem 82:385–392

    CAS  PubMed  Google Scholar 

  • Saito K, Kobayashi M, Gong Z, Tanaka Y, Yamazaki M (1999) 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 J 17:181–189

    PubMed  Google Scholar 

  • Sakuta M (2000) Transcriptional control of chalcone synthase by environmental stimuli. J Plant Res 113:327–333

    CAS  Google Scholar 

  • Sakuta M, Komamine A (1987) Cell growth and accumulation of secondary metabolites. In: Constabel F, Vasil IK (eds) Cell culture and somatic genetics of plants, vol 4. Academic Press, San Diego, pp 97–114

    Google Scholar 

  • Sakuta M, Ohmiya A (2011) Plant pigments II: betacyanins and carotenoids. In: Ashihara H, Crozier A, Komamine A (eds) Plant metabolism and biotechnology. Wiley, pp 343–372

  • Sakuta M, Takagi T, Komamine A (1986) Growth related accumulation of betacyanin in suspension cultures of Phytolacca americana L. J Plant Physiol 125:337–343

    CAS  Google Scholar 

  • Sakuta M, Hirano H, Komamine A (1991) Stimulation by 2,4-dichlorophenoxyacetic acid of betacyanin accumulation in suspension cultures of Phytolacca americana. Physiol Plant 83:154–158

    CAS  Google Scholar 

  • Sakuta M, Hirano H, Kakegawa K, Suda J, Hirose M, Joy RV IV, Sugiyama M, Komamine A (1994) Regulatory mechanisms of biosynthesis of betacyanin and anthocyanin in relation to cell division activity in suspension cultures. Plant Cell Tiss Organ Cult 38:167–169

    CAS  Google Scholar 

  • Sasaki N, Adachi T, Koda T, Ozeki Y (2004) Detection of UDP-glucose: cyclo-DOPA 5-O-glucosyltransferase activity in four o’clocks (Mirabilis jalapa L.). FEBS Lett 568:159–162

    CAS  PubMed  Google Scholar 

  • Sasaki N, Abe Y, Wada K, Koda T, Goda Y, Adachi T, Ozeki Y (2005a) Amaranthin in feather cockscombs is synthesized via glucuronylation at the cyclo-DOPA glucoside step in the betacyanin biosynthetic pathway. J Plant Res 118:439–442

    CAS  PubMed  Google Scholar 

  • Sasaki N, Wada K, Koda T, Kasahara K, Adachi T, Ozeki Y (2005b) Isolation and characterization of cDNAs encoding an enzyme with glucosyltransferase activity for cyclo-DOPA from four o’clocks and feather cockscombs. Plant Cell Physiol 46:666–670

    CAS  PubMed  Google Scholar 

  • Sasaki N, Abe Y, Goda Y, Adachi T, Kasahara K, Ozeki Y (2009) Detection of DOPA 4,5-dioxygenase (DOD) activity using recombinant protein prepared from Escherichia coli cells harboring cDNA encoding DOD from Mirabilis jalapa. Plant Cell Physiol 50:1012–1016

    CAS  PubMed  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6:74–78

    CAS  PubMed  Google Scholar 

  • Schliemann W, Kobayashi N, Strack D (1999) The decisive step in betaxanthin biosynthesis is a spontaneous reaction. Plant Physiol 119:1217–1232

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sciuto S, Oriente G, Piatelli M (1972) Betanidin glycosylation in Opuntia dillenii. Phytochemistry 11:2259–2262

    CAS  Google Scholar 

  • Sciuto S, Oriente G, Piattelli M, Impelizzeri G, Amico V (1974) Biosynthesis of amaranthin in Celosia plumosa. Phytochemistry 13:947–951

    CAS  Google Scholar 

  • Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in three spine sticklebacks. Nature 428:717–723

    CAS  PubMed  Google Scholar 

  • Shimada S, Takahashi K, Sato Y, Sakuta M (2004) Dihydroflavonol 4-reductase cDNA from non-anthocyanin-producing species in the Caryophyllales. Plant Cell Physiol 45:1290–1298

    CAS  PubMed  Google Scholar 

  • Shimada S, Inoue TY, Sakuta M (2005) Anthocyanidin synthase in non-anthocyanin-producing Caryophyllales species. Plant J 44:950–959

    CAS  PubMed  Google Scholar 

  • Shimada S, Otsuki H, Sakuta M (2007) Transcriptional control of anthocyanin biosynthetic genes in the Caryophyllales. J Exp Bot 58:957–967

    CAS  PubMed  Google Scholar 

  • Shirley BW (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Google Scholar 

  • Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24:743–755

    CAS  PubMed  Google Scholar 

  • Spasic M, Milic B, Obrenovic S (1985) Superoxide dismutase activity versus betacyanin induction under continuous red illumination in Amaranthus seedlings. Biochem Physiol Pflanz 180:319–322

    CAS  Google Scholar 

  • Stafford HA (1990) Flavonoid evolution: an enzymic approach. Plant Physiol 96:680–685

    Google Scholar 

  • Stafford HA (1994) Anthocyanins and betalains: evolution of the mutually exclusive pathways. Plant Sci 101:91–98

    CAS  Google Scholar 

  • Steiner U, Schliemann W, Strack D (1996) Assay for tyrosine hydroxylation activity of tyrosinase from betalain-forming plants and cell cultures. Anal Biochem 238:72–75

    CAS  PubMed  Google Scholar 

  • Steiner U, Schliemann W, Böhm H, Strack D (1999) Tyrosinase involved in betalain biosynthesis of higher plants. Planta 208:114–124

    CAS  Google Scholar 

  • Stintzing FC, Herbach KM, Mosshamme MR, Carle R, Yi W, Sellappan S, Akoh CC, Bunch R, Felker P (2005) Color, betalain pattern, and antioxidant properties of cactus pear (Opuntia spp.) clones. J Agric Food Chem 53:442–451

    CAS  PubMed  Google Scholar 

  • Stobert AK, Kinsman LT (1977) The hormonal control of betacyanin synthesis in Amaranthus caudatus. Phytochemistry 16:137–1142

    Google Scholar 

  • Strack D, Schliemann W (2001) Bifunctional polyphenol oxidases: novel functions in plant pigment biosynthesis. Angew Chem Int Ed 40:3791–3794

    CAS  Google Scholar 

  • Strack D, Vogt T, Schliemann W (2003) Recent advance in betalain research. Phytochemistry 62:247–269

    CAS  PubMed  Google Scholar 

  • Suzuki N, Sakuta M, Shimizu S, Komamine A (1995) Changes in the activity of 3-deoxy-D-arabino-heptulosonate 7-phosphate (DAHP) synthase in suspension cultured cells of Vitis. Physiol Plant 94:591–596

    CAS  Google Scholar 

  • Takahashi K, Takamura E, Sakuta M (2009) Isolation and expression analysis of two DOPA dioxygenases in Phytolacca americana. Z Naturforsch C 64:564–573

    CAS  PubMed  Google Scholar 

  • Tanaka Y, Tsuda S, Kusumi T (1998) Metabolic engineering to modify color. Plant Cell Physiol 39:1119–1126

    CAS  Google Scholar 

  • Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749

    CAS  PubMed  Google Scholar 

  • Tanner GJ, Francki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR (2003) Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. J Biol Chem 278:31647–31656

    CAS  PubMed  Google Scholar 

  • Tesoriere L, Fazzari M, Angileri F, Gentile C, Livrea MA (2008) In vitro digestion of betalainic foods. Stability and bioaccessibility of betaxanthins and betacyanins and antioxidative potential of food digesta. J Agric Food Chem 56:10487–10492

    CAS  PubMed  Google Scholar 

  • Tuteja J, Clough S, Chan W, Vodkin L (2004) Tissue-specific gene silencing mediated by a naturally occurring chalcone synthase gene cluster in Glycine max. Plant Cell 16:819–835

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vogt T (2002) Substrate specificity and sequence analysis define a polyphyletic origin of betanidin 5- and 6-O-glucosyltransferase from Dorotheanthus bellidiformis. Planta 214:492–495

    CAS  PubMed  Google Scholar 

  • Vogt T, Zimmermann E, Grimm R, Meyer M, Strack D (1997) Are the characteristics of betanidin glucosyltransferases from cell-suspension cultures of Dorotheanthus bellidiformis indicative of their phylogenetic relationship with flavonoid glucosyltransferases? Planta 203:349–361

    CAS  PubMed  Google Scholar 

  • Wallace TC (2011) Anthocyanins in cardiovascular disease. Adv Nutr 2:1–7

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weisshaar B, Armstrong GA, Block A, da Costa e Silva O, Hahlbrock K (1991) Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness. EMBO J 10:1777–1786

    CAS  PubMed  Google Scholar 

  • Wellmer F, Kircher S, Rugner A, Frohnmeyer H, Schafer E, Harter K (1999) Phosphorylation of the parsley bZIP transcription factor CPRF2 is regulated by light. J Biol Chem 274:29476–29482

    CAS  PubMed  Google Scholar 

  • Wellmer F, Schafer E, Harter K (2001) The DNA binding properties of the parsley bZIP transcription factor CPRF4a are regulated by light. J Biol Chem 276:6274–6279

    CAS  PubMed  Google Scholar 

  • Wingender R, Rohrig H, Horicke C, Wing D, Schell J (1989) Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Mol Gen Genet 218:315–322

    CAS  PubMed  Google Scholar 

  • Wyler H, Meuer U, Bauer J, Stravas-Mombelli L (1984) Cyclo dopa glucoside (= (2S)-5-(-β-d-glucopyranosyloxy)-6-hydroxyindoline-2-carboxylic acid) and its occurrence in red beet (Beta vulgaris var. rubra L.). Helv Chim Acta 67:1348–1355

    CAS  Google Scholar 

  • Yamamoto K, Kobayashi N, Yoshitama K, Teramoto S, Komamine A (2001) Isolation and purification of tyrosine hydroxylase from callus cultures of Portulaca grandiflora. Plant Cell Physiol 42:969–975

    CAS  Google Scholar 

  • Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    PubMed  Google Scholar 

  • Yoshida K, Iwasaka R, Kaneko T, Sato S, Tabata S, Sakuta M (2008a) Functional differentiation of Lotus japonicus TT2 s, R2R3-Myb transcription factors comprising a multigene family. Plant Cell Physiol 49:157–169

    CAS  PubMed  Google Scholar 

  • Yoshida K, Wakamatsu S, Sakuta M (2008b) Characterization of SBZ1, a soybean bZIP protein that binds to the chalcone synthase gene promoter. Plant Biotechnol 25:131–140

    CAS  Google Scholar 

  • Yoshida K, Iwasaka R, Shimada N, Ayabe S, Aoki T, Sakuta M (2010a) Transcriptional control of the dihydroflavonol 4-reductase multigene family in Lotus japonicus. J Plant Res 123:801–805

    CAS  PubMed  Google Scholar 

  • Yoshida K, Kume N, Nakaya Y, Yamagami A, Nakano T, Sakuta M (2010b) Comparative analysis of the triplicate proanthocyanidin regulators in Lotus japonicus. Plant Cell Physiol 51:912–922

    CAS  PubMed  Google Scholar 

  • Zeier J, Delledonne M, Mishima T, Severi E, Sonoda M, Lamb C (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol 136:2875–2886

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130:4859–4869

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masaaki Sakuta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sakuta, M. Diversity in plant red pigments: anthocyanins and betacyanins. Plant Biotechnol Rep 8, 37–48 (2014). https://doi.org/10.1007/s11816-013-0294-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-013-0294-z

Keywords

Navigation