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Reciprocal regulation ofArabidopsis UGT78D2 and BANYULS is critical for regulation of the metabolic flux of anthocyanidins to condensed tannins in developing seed coats

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Abstract

Anthocyanins are major color pigments in plants. Their biosynthetic pathways are well established, and the majority of these biosynthetic enzymes have been identified in model plants such asArabidopsis, maize, and petunia. One exception inArabidopsis is UDP-glucose:flavonoid 3-O-glucosyltransferase (UF3GT). This enzyme is known as Bronze-1 (Bz1 ) in maize, where it converts anthocyanidins to anthocyanins. Phylogenetic sequence analysis of theArabidopsis thaliana UDP-glycosyltransferase (UGT) family previously indicated that UGT78D1, UGT78D2, and UGT78D3 cluster together with UF3GTs from other species. Here, we report thatUGT78D2 encodes a cytosolic UGT that is functionally consistent with maize Bz-1. Biochemically, UGT78D2 catalyzes the glucosylation of both flavonols and anthocyanidins at the 3-OH position. A T-DNA-insertedugt78d2 mutant accumulates very little anthocyanin and lacks 3-O-glucosylated quercetin. Expression analysis indicated thatUGT78D2, in opposite toBANYULS, is highly expressed in anthocyanin-accumulating seedlings but repressed in condensed tannin-accumulating seed coats. This suggests that the reciprocal regulation of these two genes is important in directing the metabolic flux to either anthocyanins or condensed tannins. Consistent with this, the ectopic expression of UGT78D2 produces purple-colored seed coats due to the accumulation of anthocyanins. Taken together, our data indicate thatUGT78D2 encodes an enzyme equivalent to maize Bz1, and that the reciprocal regulation of UGT78D2 and BANYULS is critical for the regulation of metabolic flux of anthocyanidins inArabidopsis.

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Literature Cited

  • Albert S, Delseny M, Devic M (1997) BANYULS, a novel negative regulator of flavonoid biosynthesis inthe Arabidopsis seed coat. Plant J11: 289–299

    Article  PubMed  CAS  Google Scholar 

  • Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell10: 1135–1149

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema Eric, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Gerait M, Hazari N, Horn E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis ofArabidopsis thaliana. Science301: 653–657

    Article  PubMed  Google Scholar 

  • Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control ofArabidopsis development. Mol Cell1: 213–222

    Article  PubMed  CAS  Google Scholar 

  • Beld M, Martin C, Huits H, Stuitje AR, Gerats AG (1989) Flavonoid synthesis inPetunia hybrida: Partial characterization of dihydroflavonol-4-reductase genes. Plant Mol Biol13: 491–502

    Article  PubMed  CAS  Google Scholar 

  • Bloor SJ, Abrahams S (2002) The structure of the major anthocyanin inArabidopsis thaliana. Phytochem59: 343–346

    Article  CAS  Google Scholar 

  • Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell12: 2383–2394

    Article  PubMed  CAS  Google Scholar 

  • Brouillard R (1982) Chemical Structure of Anthocyanins,In P Markakis, ed, Anthocyanins as Food Colors. Academic Press, New York, pp 1–40

    Google Scholar 

  • Cho HS, Lee SS, Kim KD, Hwang I, Lim JS, Park Yl, Pai HS (2004) DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell16: 2665–2682

    Article  PubMed  CAS  Google Scholar 

  • Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M (2001) The TRANSPARENT TESTAI 2 gene ofArabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell13: 853–871

    Article  PubMed  CAS  Google Scholar 

  • Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, Pelletier G, Delseny M (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J19: 387–398

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA, Steele CL (1999) Flavonoids and isoflavonoids -a gold mine for metabolic engineering. Trends Plant Sci4: 394–400

    Article  PubMed  Google Scholar 

  • Elomaa P, Helariutta Y, Griesbach RJ, Kotilainen M, Seppanen P, Teeri TH (1995) Transgene inactivation inPetunia hybrida is influenced by the properties of the foreign gene. Mol Gen Genet248: 649–656

    Article  PubMed  CAS  Google Scholar 

  • Ford CM, Boss PK, Hoj PB (1998) Cloning and characterization ofVitis vinifera UDP glucose: Flavonoid 3-O-glu-cosyltransferase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidinsin vivo. J Biol Chem273: 9224–9233

    Article  PubMed  CAS  Google Scholar 

  • Forkmann G, Martens S (2001) Metabolic engineering and applications of flavonoids. Curr Opin Biotechnol12: 155–160

    Article  PubMed  CAS  Google Scholar 

  • Forkmann G, Ruhnau B (1987) Distinct substrate specificity of dihydroflavonol 4 reductase from flowers ofPetunia hybrida. Z Naturforsch42: 1146–1148

    CAS  Google Scholar 

  • Gerats AG, Vlaming P, Doodeman M, Al B, Schram AW (1982) Genetic control of the conversion of dihydroflavonols into flavonols and anthocyanins in flowers ofPetunia hybrida. Planta155: 364–368

    Article  CAS  Google Scholar 

  • Gong Z, Yamazaki M, Sugiyama M, Tanaka Y, Saito K (1997) Cloning and molecular analysis of structural genes involved in anthocyanin biosynthesis and expressed in a forma-specific manner inPerilla frutescens. Plant Mol Biol35: 915–927

    Article  PubMed  CAS  Google Scholar 

  • Holton TA (1995) Modification of flower colour via manipulation of P450 gene expression in transgenic plants. Drug Metabol Drug Interact12: 359–368

    PubMed  CAS  Google Scholar 

  • Holton TA (1996) Transgenic plants exhibiting altered flower color and methods for producing the same. US Patent 6080920

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell7: 1071–1083

    Article  PubMed  CAS  Google Scholar 

  • Holton TA, Tanaka Y (1999) Transgenic plants having altered anthocyanin levels. US Patent 5948955

  • Hundle BS, O’Brien DA, Alberti M, Beyer P, Hearst JE (1992) Functional expression of zeaxanthin glucosyl-transferase fromErwinia herbicola and a proposed uridine diphosphate binding site. Proc Natl Acad Sci USA89: 9321–9325

    Article  PubMed  CAS  Google Scholar 

  • Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I (2001) A new dynamin like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole inArabidopsis. Plant Cell13: 1511–1526

    Article  PubMed  CAS  Google Scholar 

  • Johnson ET, Ryu S, Yi H, Shin B, Cheong H, Choi G (2001) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J25: 325–333

    Article  PubMed  CAS  Google Scholar 

  • Johnson ET, Yi H, Shin B, Oh BJ, Cheong H, Choi G (1999)Cymbidium hybrida dihydroflavonol 4-reductase does not efficiently reduce dihydrokaempferol to produce orange pelargonidin-type anthocyanins. Plant J19: 81–85

    Article  PubMed  CAS  Google Scholar 

  • Jones P, Messner B, Nakajima J, Schaffner AR, Saito K (2003) UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis inArabidopsis thaliana. J Biol Chem278: 43910–43918

    Article  PubMed  CAS  Google Scholar 

  • Kang SG, Jin JB, Piao HL, Pih KT, Jang HJ, Lim JH, Hwang I (1998) Molecular cloning of anArabidopsis cDNA encoding a dynamin-like protein that is localized to plastids. Plant Mol Biol38: 437–447

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov D, Yu RK (1999) Conserved domains of glycosyltransferases. Glycobiology9: 961–978

    Article  PubMed  CAS  Google Scholar 

  • Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins inArabidopsis. Plant J37: 104–114

    Article  PubMed  CAS  Google Scholar 

  • Kubasek WL, Shirley BW, McKillop A, Goodman HM, Briggs W, Ausubel FM (1992) Regulation of flavonoid biosynthetic genes in germinatingArabidopsis seedlings. Plant Cell4: 1229–1236

    Article  PubMed  CAS  Google Scholar 

  • Kubasek WL, Ausubel FM, Shirley BW (1998) A light-independent developmental mechanism potentiates flavonoid gene expression inArabidopsis seedlings. Plant Mol Biol37: 217–223

    Article  PubMed  CAS  Google Scholar 

  • Kubo A, Arai Y, Nagashima S, Yoshikawa T (2004) Alteration of sugar donor specificities of plant glycosyltransferases by a single point mutation. Arch Biochem Biophys429: 198–203

    Article  PubMed  CAS  Google Scholar 

  • Lee YJ, Kim DH, Kim YW, Hwang I (2001) Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane systemin vivo. Plant Cell13: 2175–2190

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Baldauf S, Lim EK, Bowles DJ (2001) Phylogenetic analysis of the UDP glycosyltransferase multigene familyof Arabidopsis thaliana. J Biol Chem276: 4338–4343

    Article  PubMed  CAS  Google Scholar 

  • Lim EK, Ashford DA, Hou B, Jackson RG, Bowles DJ (2004)Arabidopsis glycosyltransferases as biocatalysts in fermentation for regioselective synthesis of diverse quercetin glucosides. Biotechnol Bioeng87: 623–631

    Article  PubMed  CAS  Google Scholar 

  • Marrs KA, Alfenito MR, Lloyd AM, Walbot V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature375: 397–400

    Article  PubMed  CAS  Google Scholar 

  • Meyer P, Heidmann I, Forkmann G, Saedler H (1987) A new petunia flower colour generated by transformation of a mutant with a maize gene. Nature330: 677–678

    Article  PubMed  CAS  Google Scholar 

  • Mol J, Cornish E, Mason J, Koes R (1999) Novel coloured flowers. Curr Opin Biotechnol10: 198–201

    Article  PubMed  CAS  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) TheArabidopsis HY5 gene encodes a bZIP protein that regulates stimulusinduced development of root and hypocotyl. Genes Dev11: 2983–2995

    Article  PubMed  CAS  Google Scholar 

  • Ralston EJ, English JJ, Dooner HK (1988) Sequence of three bronze alleles of maize and correlation with the genetic fine structure. Genetics119: 185–197

    PubMed  CAS  Google Scholar 

  • Rhoades MM (1952) The effect of thebronze locus on anthocyanin formation in maize. Amer Nat86: 105–108

    Article  CAS  Google Scholar 

  • Ross J, Li Y, Lim E, Bowles DJ (2001) Higher plant giycosyltransferases. Genome Biol 2: Review S3004

  • Schoenbohm C, Martens S, Eder C, Forkmann G, Weisshaar B (2000) Identification of theArabidopsis thaliana flavonoid 3-hydroxylase gene and functional expression of the encoded P450 enzyme. Biol Chem381: 749–753

    Article  PubMed  CAS  Google Scholar 

  • Shirley BW, Hanley S, Goodman HM (1992) Effects of ionizing radiation on a plant genome: Analysis of twoArabidopsis transparent testa mutations. Plant Cell4: 333–347

    Article  PubMed  CAS  Google Scholar 

  • Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM (1995) Analysis ofArabidopsis mutants deficient in flavonoid biosynthesis. Plant J8: 659–671

    Article  PubMed  CAS  Google Scholar 

  • Springob K, Nakajima J, Yamazaki M, Saito K (2003) Recent advances in the biosynthesis and accumulation of anthocyanins. Nat Prod Rep20: 288–303

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Tsuda S, Kusumi T (1998) Metabolic engineering to modify flower color. Plant Cell Physiol39: 1119–1126

    CAS  Google Scholar 

  • Tanaka Y, Yonekura K, Fukuchi-Mizutani M, Fukui Y, Fujiwara H, Ashikari T, Kusumi T (1996) Molecular and biochemical characterization of three anthocyanin synthetic enzymes from Gent/anatriflora. Plant Cell Physiol37: 711–716

    PubMed  CAS  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 Chem278: 31647–31656

    Article  PubMed  CAS  Google Scholar 

  • Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome ofArabidopsis plants over-expressing an MYB transcription factor. Plant J42: 218–235

    Article  PubMed  CAS  Google Scholar 

  • Veit M, Pauli GF (1999) Major flavonoids fromArabidopsis thaliana leaves. J Nat Prod62: 1301–1303

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis: A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol126: 485–493

    Article  PubMed  CAS  Google Scholar 

  • Xie DY, Sharma SB, Dixon RA (2004) Anthocyanidin reductases fromMedicago truncatula andArabidopsis thaliana. Arch Biochem Biophys422: 91–102

    Article  PubMed  CAS  Google Scholar 

  • Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science299: 396–399

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki M, Yamagishi E, Gong Z, Fukuchi-Mizutani M, Fukui Y, Tanaka Y, Kusumi T, Yamaguchi M, Saito K (2002) Two flavonoid glucosyltransferases fromPetunia hybrida: Molecular cloning, biochemical properties and developmentally regulated expression. Plant Mol Biol48: 401–411

    Article  PubMed  CAS  Google Scholar 

  • Zufall RA, Rausher MD (2003) The genetic basis of a flower color polymorphism in the common morning glory(Ipomoea purpurea). J Hered94: 442–448

    Article  PubMed  CAS  Google Scholar 

  • Zufall RA, Rausher MD (2004) Genetic changes associated with floral adaptation restrict future evolutionary potential. Nature428: 847–850

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, KAIST, 305-701, Daejeon, Korea

    Yeon Lee, Won-il Chung & Giltsu Choi

  2. Department of Chemistry, Kyung Hee University, 449-701, Suwon, Korea

    Hye Ryon Yoon & Yong Sook Paik

  3. Korea Research Institute of Bioscience and Biotechnology, 305-333, Daejeon, Korea

    Jang Ryul Liu

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  1. Yeon Lee
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  2. Hye Ryon Yoon
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  3. Yong Sook Paik
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  5. Won-il Chung
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Correspondence to Giltsu Choi.

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Lee, Y., Yoon, H.R., Paik, Y.S. et al. Reciprocal regulation ofArabidopsis UGT78D2 and BANYULS is critical for regulation of the metabolic flux of anthocyanidins to condensed tannins in developing seed coats. J. Plant Biol. 48, 356–370 (2005). https://doi.org/10.1007/BF03030577

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