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

Volumn 188, Issue 4, 2010, Pages 985-1000

  Stracke, Ralf ^a   Jahns, Oliver ^a   Keck, Matthias ^a   Tohge, Takayuki ^b,c   Niehaus, Karsten ^a   Fernie, Alisdair R ^c   Weisshaar, Bernd ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b RIKEN Center for Sustainable Resource Science   (Japan)

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

Author keywords

Arabidopsis thaliana; Flavonoid biosynthesis; Flavonol glycosides; Flavonols; Gene regulation; R2R3 MYB

Indexed keywords

ARABIDOPSIS PROTEIN; FLAVONOL DERIVATIVE; GLUCURONOSYLTRANSFERASE; GLYCOSIDE; MYB11 PROTEIN, ARABIDOPSIS; MYB12 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

BIOACCUMULATION; DICOTYLEDON; GENETIC ANALYSIS; LIQUID CHROMATOGRAPHY; METABOLISM; METABOLITE; PHOTOCHEMISTRY; POLLEN;

ANTIBODY SPECIFICITY; ARABIDOPSIS; ARTICLE; CYTOLOGY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; MUTATION; PLANT GENE; POLLEN; STAINING; THIN LAYER CHROMATOGRAPHY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATOGRAPHY, THIN LAYER; FLAVONOLS; GENES, PLANT; GLUCURONOSYLTRANSFERASE; GLYCOSIDES; MUTATION; ORGAN SPECIFICITY; POLLEN; STAINING AND LABELING; TRANSCRIPTION FACTORS; TRANSFECTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 78149380797     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03421.x     Document Type: Article

References (76)

1. Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Dominguez E, Wang Z, De Vos RC, Jetter R et al. 2009. Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genetics 5: e1000777.
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. 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 Journal 39: 366-380.
4. Bischoff SC. 2008. Quercetin: potentials in the prevention and therapy of disease. Current Opinion in Clinical Nutrition and Metabolic Care 11: 733-740.
5. Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C. 2000. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2393.
6. Bowman J. 1994. Arabidopsis: an atlas of morphology and development. New York, NY, USA: Springer.
7. Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK. 2001. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126: 524-535.
8. Buer CS, Muday GK. 2004. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16: 1191-1205.
9. Buer CS, Muday GK, Djordjevic MA. 2007. Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiology 145: 478-490.
10. Buer CS, Sukumar P, Muday GK. 2006. Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiology 140: 1384-1396.
11. Cazarolli LH, Zanatta L, Alberton EH, Figueiredo MS, Folador P, Damazio RG, Pizzolatti MG, Silva FR. 2008. Flavonoids: prospective drug candidates. Mini Reviews in Medicinal Chemistry 8: 1429-1440.
12. Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J. 2009. The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiology 151: 1513-1530.
13. Davies KM, Schwinn KE. 2003. Transcriptional regulation of secondary metabolism. Functional Plant Biology 30: 913-925.
14. Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. The Plant Cell 7: 1085-1097.
15. Van Eldik GJ, Reijnen WH, Ruiter RI, Van Herpen MMA, Schrauwen JAM, Wullems GJ. 1997. Regulation of flavonol biosynthesis during anther and pistil development, and during pollen tube growth in Solanum tuberosum. Plant Journal 11: 105-113.
16. Gonzalez A, Mendenhall J, Huo Y, Lloyd A. 2009. TTG1 complex MYBs, MYB5 and TT2, control outer seed coat differentiation. Developmental Biology 325: 412-421.
17. 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 Journal 53: 814-827.
18. Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57: 761-780.
19. Grotewold E, Drummond BJ, Bowen B, Peterson T. 1994. The MYB-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543-553.
20. Harborne JB, Williams CA. 2000. Advances in flavonoid research since 1992. Phytochemistry 55: 481-504.
21. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B. 2005. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Molecular Biology 57: 155-171.
22. Hernandez JM, Heine GF, Irani NG, Feller A, Kim MG, Matulnik T, Chandler VL, Grotewold E. 2004. Different mechanisms participate in the R-dependent activity of the R2R3 MYB transcription factor C1. Journal of Biological Chemistry 279: 48205-48213.
23. Hughes M, Donnelly C, Crozier A, Wheeler CT. 1999. Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Canadian Journal of Botany 77: 1311-1315.
24. Jacobs M, Rubery PH. 1988. Naturally occurring auxin transport regulators. Science 241: 346-349.
25. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C. 2000. Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. The EMBO Journal 19: 6150-6161.
26. Johnson-Brousseau SA, McCormick S. 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant Journal 39: 761-775.
27. Jones P, Messner B, Nakajima J, Schaffner AR, Saito K. 2003. UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. Journal of Biological Chemistry 278: 43910-43918.
28. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M. 2006. Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 57: 405-430.
29. Marles MA, Ray H, Gruber MY. 2003. New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry 64: 367-383.
30. Van Der Meer IM, Stam ME, Van Tunen AJ, Mol JNM, Stuitje AR. 1992. Antisense inhibition of flavonoid biosynthesis in Petunia anthers results in male sterility. Plant Cell 4: 253-262.
31. Mehrtens F, Kranz H, Bednarek P, Weisshaar B. 2005. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology 138: 1083-1096.
32. Mo Y, Nagel C, Taylor LP. 1992. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proceedings of the National Academy of Sciences, USA 89: 7213-7217.
33. Mol J, Jenkins GI, Schäfer E, Weiss D. 1996. Signal perception, transduction, and gene expression involved in anthocyanin biosynthesis. Critical Reviews in Plant Sciences 15: 525-557.
34. Murphy A, Peer WA, Taiz L. 2000. Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211: 315-324.
35. Nakabayashi R, Kusano M, Kobayashi M, Tohge T, Yonekura-Sakakibara K, Kogure N, Yamazaki M, Kitajima M, Saito K, Takayama H. 2009. Metabolomics-oriented isolation and structure elucidation of 37 compounds including two anthocyanins from Arabidopsis thaliana. Phytochemistry 70: 1017-1029.
36. Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L. 2000. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12: 1863-1878.
37. Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L. 2001. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 13: 2099-2114.
38. Neu R. 1957. Chelate von Diarylborsäuren mit aliphatischen Oxyal-kylaminen als Reagenzien für den Nachweis von Oxyphenyl-benzo-γ-pyronen. Die Naturwissenschaften 44: 181-182.
39. Olsson LC, Veit M, Weissenböck G, Bornman JF. 1998. Differential flavonoid response to enhanced UV-B radiation in Brassica napus. Phytochemistry 49: 1021-1028.
40. Ormrod DP, Landry LG, Conklin PL. 1995. Short-term UV-B radiation and ozone exposure effects on aromatic secondary metabolite accumulation and shoot growth of flavonoid-deficient Arabidopsis mutants. Physiologia Plantarum 93: 602-610.
41. Owens DK, Crosby KC, Runac J, Howard BA, Winkel BS. 2008. Biochemical and genetic characterization of Arabidopsis flavanone 3beta-hydroxylase. Plant Physiology and Biochemistry 46: 833-843.
42. Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS. 2001. Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiology 126: 536-548.
43. Petroni K, Falasca G, Calvenzani V, Allegra D, Stolfi C, Fabrizi L, Altamura MM, Tonelli C. 2008. The AtMYB11 gene from Arabidopsis is expressed in meristematic cells and modulates growth in planta and organogenesis in vitro. Journal of Experimental Botany 59: 1201-1213.
44. Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW. 2004. AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant Journal 40: 979-995.
45. Quattrocchio F, Baudry A, Lepiniec L, Grotewold E. 2006. The regulation of flavonoid biosynthesis. In: Grotewold E, ed. The science of flavonoids. Columbus, OH, USA: The Ohio State University, 97-122.
46. Ross J, Li Y, Lim E, Bowles DJ. 2001. Genome Biology 2: reviews3004.3001-reviews3004.3006.
47. Ross JA, Kasum CM. 2002. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annual Review of Nutrition 22: 19-34.
48. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B. 2003. An Arabidopsis thaliana T-DNA mutagenised population (GABI-Kat) for flanking sequence tag based reverse genetics. Plant Molecular Biology 53: 247-259.
49. Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L. 2006. Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224: 96-107.
50. Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M et al. 2008. Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. Journal of Biological Chemistry 283: 31218-31226.
51. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU. 2005. A gene expression map of Arabidopsis thaliana development. Nature Genetics 37: 501-506.
52. Sheahan JJ, Rechnitz GA. 1992. Flavonoid-specific staining of Arabidopsis thaliana. BioTechniques 13: 880-883.
53. Shikazono N, Yokota Y, Kitamura S, Suzuki C, Watanabe H, Tano S, Tanaka A. 2003. Mutation rate and novel tt mutants of Arabidopsis thaliana induced by carbon ions. Genetics 163: 1449-1455.
54. Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM. 1995. Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant Journal 8: 659-671.
55. Solovchenko A, Schmitz-Eiberger M. 2003. Significance of skin flavonoids for UV-B-protection in apple fruits. Journal of Experimental Botany 54: 1977-1984.
56. Sprenger-Haussels M, Weisshaar B. 2000. Transactivation properties of parsley proline rich bZIP transcription factors. Plant Journal 22: 1-8.
57. Stracke R, De Vos RCH, Bartelniewoehner L, Ishihara H, Sagasser M, Martens S, Weisshaar B. 2009. Metabolomic and genetic analyses of flavonol synthesis in Arabidopsis thaliana support the in vivo involvement of leucoanthocyanidin dioxygenase. Planta 229: 427-445.
58. Stracke R, Favory J-J, Gubler H, Bartelniewöhner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R. 2010. The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell & Environment 33: 88-103.
59. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant Journal 50: 660-677.
60. Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology 4: 447-456.
61. Subramanian S, Stacey G, Yu O. 2007. Distinct, crucial roles of flavonoids during legume nodulation. Trends in Plant Science 12: 282-285.
62. Taylor LP, Grotewold E. 2005. Flavonoids as developmental regulators. Current Opinion in Plant Biology 8: 317-323.
63. Tohge T, Matsui K, Ohme-Takagi M, Yamazaki M, Saito K. 2005a. Enhanced radical scavenging activity of genetically modified Arabidopsis seeds. Biotechnology Letters 27: 297-303.
64. Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M et al. 2005b. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant Journal 42: 218-235.
65. Tohge T, Yonekura-Sakakibara K, Niida R, Watanabe-Takahashi A, Saito K. 2007. Phytochemical genomics in Arabidopsis thaliana: a case study for functional identification of flavonoid biosynthesis genes. Pure and Applied Chemistry 79: 811-823.
66. Trezzini GF, Horrichs A, Somssich IE. 1993. Isolation of putative defense-related genes from Arabidopsis thaliana and expression in fungal elicitor-treated cells. Plant Molecular Biology 21: 385-389.
67. Veit M, Pauli G. 1999. Major flavonoids from Arabidopsis thaliana leaves. Journal of Natural Products 62: 1301-1303.
68. Vogt T, Taylor LP. 1995. Flavonol 3-O-glycosyltransferases associated with Petunia pollen produce gametophyte-specific flavonol diglycosides. Plant Physiology 108: 903-911.
69. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC. 1999. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11: 1337-1350.
70. Weisshaar B, Jenkins GI. 1998. Phenylpropanoid biosynthesis and its regulation. Current Opinion in Plant Biology 1: 251-257.
71. Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126: 485-493.
72. Ylstra B, Busscher J, Franken J, Hollman PCH, Mol JNM, Van Tunen AJ. 1994. Flavonols and fertilization in Petunia hybrida: localization and mode of action during pollen tube growth. Plant Journal 6: 201-212.
73. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, Watanabe-Takahashi A, Inoue E, Saito K. 2008. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20: 2160-2176.
74. Yonekura-Sakakibara K, Tohge T, Niida R, Saito K. 2007. Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. Journal of Biological Chemistry 282: 14932-14941.
75. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH. 2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20: 2763-2782.
76. Zhou J, Lee C, Zhong R, Ye Z. 2009. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant Cell 21: 248-266.