Methylation mediated by an anthocyanin, O-methyltransferase, is involved in purple flower coloration in Paeonia

Journal of Experimental Botany

Volumn 66, Issue 21, 2015, Pages 6563-6577

  Du, Hui ^a   Wu, Jie ^a,b   Ji, Kui Xian ^a   Zeng, Qing Yin ^a   Bhuiya, Mohammad Wadud ^c   Su, Shang ^a,b   Shu, Qing Yan ^a   Ren, Hong Xu ^a   Liu, Zheng An ^a   Wang, Liang Sheng ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c MOgene Green Chemicals LC   (United States)

Author keywords

Anthocyanin O methyltransferase; Catalytic activity; Flavonoids; Flower coloration; Paeonia; Single amino acid substitution

Indexed keywords

ANTHOCYANIN; METHYLTRANSFERASE; PLANT PROTEIN;

AMINO ACID SEQUENCE; CHEMISTRY; COLOR; FLOWER; GENETICS; METABOLISM; METHYLATION; MOLECULAR GENETICS; PAEONIA; PHYLOGENY; PIGMENTATION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; TOBACCO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANTHOCYANINS; COLOR; FLOWERS; METHYLATION; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PAEONIA; PHYLOGENY; PIGMENTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ALIGNMENT; TOBACCO;

EID: 84948429864     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv365     Document Type: Article

References (65)

1. Aida R, Yoshida K, Kondo T, Kishimoto S, Shibata M. 2000. Copigmentation gives bluer flowers on transgenic torenia plants with the antisense dihydroflavonol-4-reductase gene. Plant Science 160, 49-56.
2. Akita Y, Kitamura S, Hase Y, et al. 2011. Isolation and characterization of the fragrant cyclamen O-methyltransferase involved in flower coloration. Planta 234, 1127-1136.
3. Asen S, Stewart RN, Norris KH. 1971. Co-pigmentation effect of quercetin glycosides on absorption characteristics of cyanidin glycosides and color of Red Wing azalea. Phytochemistry 10, 171-175.
4. Berim A, Gang DR. 2013. Characterization of two candidate flavone 8-O-methyltransferases suggests the existence of two potential routes to nevadensin in sweet basil. Phytochemistry 92, 33-41.
5. Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C. 2000. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. The Plant Cell 12, 2383-2393.
6. Brugliera F, Demelis L, Koes R, Tanaka Y. 2003. Genetic sequences having methyltransferase activity and uses therefor. WO Patent 2,003,062,428.
7. Cheng XD, Roberts RJ. 2001. AdoMet-dependent methylation, DNA methyltransferases and base flipping. Nucleic Acids Research 29, 3784-3795.
8. da Silva FL, Escribano-Bailon MT, Alonso JJP, Rivas-Gonzalo JC, Santos-Buelga C. 2007. Anthocyanin pigments in strawberry. LWT-Food Science and Technology 40, 374-382.
9. Ferrer JL, Zubieta C, Dixon RA, Noel JP. 2005. Crystal structures of alfalfa caffeoyl coenzyme A 3-O-methyltransferase. Plant Physiology 137, 1009-1017.
10. Ford CM, Boss PK, Hoj PB. 1998. Cloning and characterization of Vitis vinifera UDP-glucose: flavonoid 3-O-glucosyltransferase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidins in vivo. Journal of Biological Chemistry 273, 9224-9233.
11. Freeman AM, Mole BM, Silversmith RE, Bourret RB. 2011. Action at a distance: amino acid substitutions that affect binding of the phosphorylated CheY response regulator and catalysis of dephosphorylation can be far from the CheZ phosphatase active site. Journal of Bacteriology 193, 4709-4718.
12. Gonnet JF. 1998. Colour effects of co-pigmentation of anthocyanins revisited-1. A colorimetric definition using the CIELAB scale. Food Chemistry 63, 409-415.
13. Grosdidier A, Zoete V, Michielin O. 2011. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Research 39, W270-W277.
14. Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57, 761-780.
15. Heredia FJ, Francia-Aricha EM, Rivas-Gonzalo JC, Vicario IM, Santos-Buelga C. 1998. Chromatic characterization of anthocyanins from red grapes-I. pH effect. Food Chemistry 63, 491-498.
16. Hoffmann T, Kalinowski G, Schwab W. 2006. RNAi-induced silencing of gene expression in strawberry fruit (Fragaria×ananassa) by agroinfiltration: a rapid assay for gene function analysis. The Plant Journal 48, 818-826.
17. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT. 1985. A simple and general method for transferring genes into plants. Science 227, 1229-1231.
18. Hugueney P, Provenzano S, Verries C, Ferrandino A, Meudec E, Batelli G, Merdinoglu D, Cheynier V, Schubert A, Ageorges A. 2009. A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine. Plant Physiology 150, 2057-2070.
19. 2+-dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. Journal of Biological Chemistry 278, 43961-43972.
20. Ibrahim RK, Bruneau A, Bantignies B. 1998. Plant O-methyltransferases: molecular analysis, common signature and classification. Plant Molecular Biology 36, 1-10.
21. Ji LJ, Wang Q, da Silva JAT, Yu XN. 2012. The genetic diversity of Paeonia L. Scientia Horticulturae 143, 62-74.
22. Jia N, Shu QY, Wang LS, Du H, Xu YJ, Liu ZA. 2008. Analysis of petal anthocyanins to investigate coloration mechanism in herbaceous peony cultivars. Scientia Horticulturae 117, 167-173.
23. Jonsson LMV, Devlaming P, Wiering H, Aarsman MEG, Schram AW. 1983. Genetic control of anthocyanin-O-methyltransferase activity in flowers of Petunia hybrida. Theoretical and Applied Genetics 66, 349-355.
24. Joshi CP, Chiang VL. 1998. Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Molecular Biology 37, 663-674.
25. Ketterman AJ, Prommeenate P, Boonchauy C, Chanama U, Leetachewa S, Promtet N, Prapanthadara L. 2001. Single amino acid changes outside the active site significantly affect activity of glutathione S-transferases. Insect Biochemistry and Molecular Biology 31, 65-74.
26. Klimasauskas S, Weinhold E. 2007. A new tool for biotechnology: AdoMet-dependent methyltransferases. Trends in Biotechnology 25, 99-104.
27. Kondo E, Nakayama M, Kameari N, Tanikawa N, Morita Y, Akita Y, Hase Y, Tanaka A, Ishizaka H. 2009. Red-purple flower due to delphinidin 3,5-diglucoside, a novel pigment for Cyclamen spp., generated by ion-beam irradiation. Plant Biotechnology 26, 565-569.
28. 2+-dependent O-methyltransferases. Journal of Molecular Biology 378, 154-164.
29. Kovinich N, Saleem A, Arnason JT, Miki B. 2011. Combined analysis of transcriptome and metabolite data reveals extensive differences between black and brown nearly-isogenic soybean (Glycine max) seed coats enabling the identification of pigment isogenes. BMC Genomics 12, 381-398.
30. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallographica Section D-Biological Crystallography 60, 2256-2268.
31. Lam KC, Ibrahim RK, Behdad B, Dayanandan S. 2007. Structure, function, and evolution of plant O-methyltransferases. Genome 50, 1001-1013.
32. Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY. 2009. Extensive functional diversification of the Populus glutathione S-transferase supergene family. The Plant Cell 21, 3749-3766.
33. Lee YJ, Kim BG, Chong Y, Lim Y, Ahn JH. 2008. Cation dependent O-methyltransferases from rice. Planta 227, 641-647.
34. Li CH. 2010. The flavonoid composition in tree peony petals and their effects on the coloration. PhD thesis, University of Chinese Academy of Sciences, China.
35. Li CH, Du H, Wang LS, Shu QY, Zheng YR, Xu YJ, Zhang JJ, Yang RZ, Ge Y. 2009. Flavonoid composition and antioxidant activity of tree peony (Paeonia section moutan) yellow flowers. Journal of Agricultural and Food Chemistry 57, 8496-8503.
36. Liscombe DK, Louie GV, Noel JP. 2012. Architectures, mechanisms and molecular evolution of natural product methyltransferases. Natural Product Reports 29, 1238-1250.
37. Lucker J, Martens S, Lund ST. 2010. Characterization of a Vitis vinifera cv. Cabernet Sauvignon 3′,5′-O-methyltransferase showing strong preference for anthocyanins and glycosylated flavonols. Phytochemistry 71, 1474-1484.
38. Martin JL, McMillan FM. 2002. SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Current Opinion in Structural Biology 12, 783-793.
39. Morita Y, Hoshino A, Kikuchi Y, et al. 2005. 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. The Plant Journal 42, 353-363.
40. Nagel ZD, Cun SJ, Klinman JP. 2013. Identification of a long-range protein network that modulates active site dynamics in extremophilic alcohol dehydrogenases. Journal of Biological Chemistry 288, 14087-14097.
41. Nakayama M, Tanikawa N, Morita Y, Ban Y. 2012. Comprehensive analyses of anthocyanin and related compounds to understand flower color change in ion-beam mutants of cyclamen (Cyclamen spp.) and carnation (Dianthus caryophyllus). Plant Biotechnology 29, 215-221.
42. Nielsen K, Deroles SC, Markham KR, Bradley MJ, Podivinsky E, Manson D. 2002. Antisense flavonol synthase alters copigmentation and flower color in lisianthus. Molecular Breeding 9, 217-229.
43. Noel JP, Dixon RA, Pichersky E, Zubieta C, Ferrer JL. 2003. Structural, functional, and evolutionary basis for methylation of plant small molecules. Integrative Phytochemistry: From Ethnobotany to Molecular Ecology 37, 37-58.
44. Provenzano S, Spelt C, Hosokawa S, et al. 2014. Genetic control and evolution of anthocyanin methylation. Plant Physiology 165, 962-977.
45. Rausher MD. 2008. Evolutionary transitions in floral color. International Journal of Plant Sciences 169, 7-21.
46. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5, 725-738.
47. Sakata Y, Aoki N, Tsunematsu S, Nishikouri H, Johjima T. 1995. Petal coloration and pigmentation of tree peony bred and selected in Daikon Island (Shimane Prefecture). Journal of the Japanese Society for Horticultural Science 64, 351-357.
48. Shiono M, Matsugaki N, Takeda K. 2005. Structure of the blue cornflower pigment - Packaging red-rose anthocyanin as part of a 'superpigment' in another flower turns it brilliant blue. Nature 436, 791-791.
49. Shu QY, Wischnitzki E, Liu ZA, Ren HX, Han XY, Hao Q, Gao FF, Xu SX, Wang LS. 2009. Functional annotation of expressed sequence tags as a tool to understand the molecular mechanism controlling flower bud development in tree peony. Physiologia Plantarum 135, 436-449.
50. Tahara S. 2007. A journey of twenty-five years through the ecological biochemistry of flavonoids. Bioscience Biotechnology and Biochemistry 71, 1387-1404.
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731-2739.
52. Tanaka Y, Brugliera F, Chandler S. 2009. Recent progress of flower colour modification by biotechnology. International Journal of Molecular Sciences 10, 5350-5369.
53. Tanaka Y, Sasaki N, Ohmiya A. 2008. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal 54, 733-749.
54. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882.
55. Wang LS, Shiraishi A, Hashimoto F, Aoki N, Shimizu K, Sakata Y. 2001. Analysis of petal anthocyanins to investigate flower coloration of Zhongyuan (Chinese) and Daikon Island (Japanese) tree peony cultivars. Journal of Plant Research 114, 33-43.
56. Wang XQ. 2011. Structure, function, and engineering of enzymes in isoflavonoid biosynthesis. Functional & Integrative Genomics 11, 13-22.
57. Wessinger CA, Rausher MD. 2012. Lessons from flower colour evolution on targets of selection. Journal of Experimental Botany 63, 5741-5749.
58. Wiering H, Devlaming P. 1977. Glycosylation and methylation patterns ofanthocyanins in Petunia hybrida. II. Genes Mf 1 and Mf 2. Plant Breeding 78, 113-123.
59. Yang RZ. 2009. Studies on petal pigment composition and coloration mechanism of lotus cultivars. Master thesis, University of Chinese Academy of Sciences.
60. Yang RZ, Wei XL, Gao FF, Wang LS, Zhang HJ, Xu YJ, Li CH, Ge YX, Zhang JJ, Zhang J. 2009. Simultaneous analysis of anthocyanins and flavonols in petals of lotus (Nelumbo) cultivars by high-performance liquid chromatography-photodiode array detection/electrospray ionization mass spectrometry. Journal of Chromatography A 1216, 106-112.
61. Ye ZH, Kneusel RE, Matern U, Varner JE. 1994. An alternative methylation pathway in lignin biosynthesis in Zinnia. The Plant Cell 6, 1427-1439.
62. Yoshida K, Mori M, Kondo T. 2009. Blue flower color development by anthocyanins: from chemical structure to cell physiology. Natural Product Reports 26, 884-915.
63. Zhang JJ, Wang LS, Shu QY, Liu ZA, Li CH, Zhang J, Wei XL, Tian D. 2007. Comparison of anthocyanins in non-blotches and blotches of the petals of Xibei tree peony. Scientia Horticulturae 114, 104-111.
64. Zhao DQ, Tao J, Han CX, Ge JT. 2012. Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.). Molecular Biology Reports 39, 11263-11275.
65. Zhu ML, Zheng XC, Shu QY, Li H, Zhong PX, Zhang HJ, Xu YJ, Wang LJ, Wang LS. 2012. Relationship between the composition of flavonoids and flower colors variation in tropical water lily (Nymphaea) cultivars. PLoS One 7, e 34335.