A novel glycosyltransferase catalyses the transfer of glucose to glucosylated anthocyanins in purple sweet potato

Journal of Experimental Botany

Volumn 69, Issue 22, 2018, Pages 5445-5459

  Wang, Hongxia ^a   Wang, Chengyuan ^b   Fan, Weijuan ^a   Yang, Jun ^a   Appelhagen, Ingo ^c   Wu, Yinliang ^a,d   Zhang, Peng ^a,d  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NORWICH RESEARCH PARK   (United Kingdom)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Anthocyanins; Glucosyltransferase; Glycosyl extension; Ipomoea batatas; Regioselectivity; Stability; UDP glucose

Indexed keywords

ANTHOCYANIN; GLUCOSE; GLYCOSYLTRANSFERASE; PLANT PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; CATALYSIS; CHEMISTRY; GENETICS; METABOLISM; PHYLOGENY; SEQUENCE ALIGNMENT; SWEET POTATO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANTHOCYANINS; ARABIDOPSIS; CATALYSIS; GLUCOSE; GLYCOSYLTRANSFERASES; IPOMOEA BATATAS; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ALIGNMENT;

EID: 85057152049     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ery305     Document Type: Article

References (72)

1. Andersen ØM, Jordheim M. 2010. Anthocyanins. In: Encyclopedia of Life Sciences. Chichester: John Wiley and Sons Ltd. doi:10.1002/9780470015902.a0001909.pub2.
2. Biasini M, Bienert S, Waterhouse A, et al. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42, W252-W258.
3. Brazier-Hicks M, Offen WA, Gershater MC, Revett TJ, Lim EK, Bowles DJ, Davies GJ, Edwards R. 2007. Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proceedings of the National Academy of Sciences, USA 104, 20238-20243.
4. Breton C, Snajdrová L, Jeanneau C, Koca J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16, 29R-37R.
5. Caputi L, Malnoy M, Goremykin V, Nikiforova S, Martens S. 2012. A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. The Plant Journal 69, 1030-1042.
6. Cheng J, Wei G, Zhou H, Gu C, Vimolmangkang S, Liao L, Han Y. 2014. Unraveling the mechanism underlying the glycosylation and methylation of anthocyanins in peach. Plant Physiology 166, 1044-1058.
7. Claudia C, Philippe R, Edith F, Vincent B, Yumei Z, Sharyn EP, Juan JR, Martin Y, Christophe D. 2017. The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation. New Phytologist 213, 250-263.
8. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
9. Davies KM, Albert NW, Schwinn KE. 2012. From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Functional Plant Biology 39, 619-638.
10. de Pascual-Teresa S, Sanchez-Ballesta MT. 2008. Anthocyanins: from plant to health. Phytochemistry Reviews 7, 281-299.
11. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica. Section D, Biological Crystallography 66, 486-501.
12. Fedoroff NV, Furtek DB, Nelson OE. 1984. Cloning of the bronze locus in maize by a simple and generalizable procedure using the transposable controlling element Activator (Ac). Proceedings of the National Academy of Sciences, USA 81, 3825-3829.
13. Gachon CM, Langlois-Meurinne M, Saindrenan P. 2005. Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends in Plant Science 10, 542-549.
14. George Thompson AM, Iancu CV, Neet KE, Dean JV, Choe JY. 2017. Differences in salicylic acid glucose conjugations by UGT74F1 and UGT74F2 from Arabidopsis thaliana. Scientific Reports 7, 46629.
15. Glover BJ, Martin C. 2012. Anthocyanins. Current Biology 22, R147-R150.
16. Griesser M, Hoffmann T, Bellido ML, Rosati C, Fink B, Kurtzer R, Aharoni A, Muñoz-Blanco J, Schwab W. 2008a. Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiology 146, 1528-1539.
17. Griesser M, Vitzthum F, Fink B, Bellido ML, Raasch C, Munoz-Blanco J, Schwab W. 2008b. Multi-substrate flavonol O-glucosyltransferases from strawberry (Fragaria × ananassa) achene and receptacle. Journal of Experimental Botany 59, 2611-2625.
18. He J, Giusti MM. 2010. Anthocyanins: natural colorants with health-promoting properties. Annual Review of Food Science and Technology 1, 163-187.
19. He ZH, Cheeseman I, He D, Kohorn BD. 1999. A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Molecular Biology 39, 1189-1196.
20. Hiromoto T, Honjo E, Noda N, Tamada T, Kazuma K, Suzuki M, Blaber M, Kuroki R. 2015. Structural basis for acceptor-substrate recognition of UDP-glucose: anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. Protein Science 24, 395-407.
21. Hiromoto T, Honjo E, Tamada T, Noda N, Kazuma K, Suzuki M, Kuroki R. 2013. Crystal structure of UDP-glucose:anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. Journal of Synchrotron Radiation 20, 894-898.
22. Holm L, Laakso LM. 2016. Dali server update. Nucleic Acids Research 44, W351-W355.
23. Hsu TM, Welner DH, Russ ZN, Cervantes B, Prathuri RL, Adams PD, Dueber JE. 2018. Employing a biochemical protecting group for a sustainable indigo dyeing strategy. Nature Chemical Biology 14, 256-261.
24. Ito T, Motohashi R, Kuromori T, Noutoshi Y, Seki M, Kamiya A, Mizukado S, Sakurai T, Shinozaki K. 2005. A resource of 5814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant & Cell Physiology 46, 1149-1153.
25. Jones P, Vogt T. 2001. Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213, 164-174.
26. Kim HS, Kim BG, Sung S, Kim M, Mok H, Chong Y, Ahn JH. 2013. Engineering flavonoid glycosyltransferases for enhanced catalytic efficiency and extended sugar-donor selectivity. Planta 238, 683-693.
27. Kovinich N, Kayanja G, Chanoca A, Riedl K, Otegui MS, Grotewold E. 2014. Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis. Planta 240, 931-940.
28. Kroon J, Souer E, de Graaff A, Xue Y, Mol J, Koes R. 1994. Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. The Plant Journal 5, 69-80.
29. Kubo A, Arai Y, Nagashima S, Yoshikawa T. 2004. Alteration of sugar donor specificities of plant glycosyltransferases by a single point mutation. Archives of Biochemistry and Biophysics 429, 198-203.
30. Kubo H, Nawa N, Lupsea SA. 2007. Anthocyaninless1 gene of Arabidopsis thaliana encodes a UDP-glucose:flavonoid-3-O-glucosyltransferase. Journal of Plant Research 120, 445-449.
31. Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T, Akiyama K, Kamiya A, Ito T, Shinozaki K. 2004. A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. The Plant Journal 37, 897-905.
32. Lairson LL, Henrissat B, Davies GJ, Withers SG. 2008. Glycosyltransferases: structures, functions, and mechanisms. Annual Review of Biochemistry 77, 521-555.
33. Leuzinger K, Dent M, Hurtado J, Stahnke J, Lai H, Zhou X, Chen Q. 2013. Efficient agroinfiltration of plants for high-level transient expression of recombinant proteins. Journal of Visualized Experiments 77, 50521.
34. Lee MJ, Park JS, Choi DS, Jung MY. 2013. Characterization and quantitation of anthocyanins in purple-fleshed sweet potatoes cultivated in Korea by HPLC-DAD and HPLC-ESI-QTOF-MS/MS. Journal of Agricultural and Food Chemistry 61, 3148-3158.
35. Mano H, Ogasawara F, Sato K, Higo H, Minobe Y. 2007. Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiology 143, 1252-1268.
36. Matsuba Y, Sasaki N, Tera M, et al. 2010. A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. The Plant Cell 22, 3374-3389.
37. Modolo LV, Li L, Pan H, Blount JW, Dixon RA, Wang X. 2009. Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso)flavonoids. Journal of Molecular Biology 392, 1292-1302.
38. Moglia A, Lanteri S, Comino C, Hill L, Knevitt D, Cagliero C, Rubiolo P, Bornemann S, Martin C. 2014. Dual catalytic activity of hydroxycinnamoyl-coenzyme A quinate transferase from tomato allows it to moonlight in the synthesis of both mono- and dicaffeoylquinic acids. Plant Physiology 166, 1777-1787.
39. Montefiori M, Espley RV, Stevenson D, Cooney J, Datson PM, Saiz A, Atkinson RG, Hellens RP, Allan AC. 2011. Identification and characterisation of F3GT1 and F3GGT1, two glycosyltransferases responsible for anthocyanin biosynthesis in red-fleshed kiwifruit (Actinidia chinensis). The Plant Journal 65, 106-118.
40. 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.
41. Nelson BK, Cai X, Nebenführ A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant Journal 51, 1126-1136.
42. Noguchi A, Horikawa M, Fukui Y, Fukuchi-Mizutani M, Iuchi-Okada A, Ishiguro M, Kiso Y, Nakayama T, Ono E. 2009. Local differentiation of sugar donor specificity of flavonoid glycosyltransferase in Lamiales. The Plant Cell 21, 1556-1572.
43. Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis BG, Tarling CA, Ford CM, Bowles DJ, Davies GJ. 2006. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. The EMBO Journal 25, 1396-1405.
44. Ono E, Fukuchi-Mizutani M, Nakamura N, Fukui Y, Yonekura-Sakakibara K, Yamaguchi M, Nakayama T, Tanaka T, Kusumi T, Tanaka Y. 2006. Yellow flowers generated by expression of the aurone biosynthetic pathway. Proceedings of the National Academy of Sciences, USA 103, 11075-11080.
45. Ono E, Homma Y, Horikawa M, Kunikane-Doi S, Imai H, Takahashi S, Kawai Y, Ishiguro M, Fukui Y, Nakayama T. 2010. Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera). The Plant Cell 22, 2856-2871.
46. Osmani SA, Bak S, Møller BL. 2009. Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 70, 325-347.
47. Pireyre M, Burow M. 2015. Regulation of MYB and bHLH transcription factors: a glance at the protein level. Molecular Plant 8, 378-388.
48. Poustka F, Irani NG, Feller A, Lu Y, Pourcel L, Frame K, Grotewold E. 2007. A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiology 145, 1323-1335.
49. Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR. 2013. The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiology and Biochemistry 72, 21-34.
50. Sasaki N, Nishizaki Y, Ozeki Y, Miyahara T. 2014. The role of acyl-glucose in anthocyanin modifications. Molecules 19, 18747-18766.
51. Sawada S, Suzuki H, Ichimaida F, Yamaguchi MA, Iwashita T, Fukui Y, Hemmi H, Nishino T, Nakayama T. 2005. UDP-glucuronic acid:anthocyanin glucuronosyltransferase from red daisy (Bellis perennis) flowers. Enzymology and phylogenetics of a novel glucuronosyltransferase involved in flower pigment biosynthesis. The Journal of Biological Chemistry 280, 899-906.
52. Shao H, He X, Achnine L, Blount JW, Dixon RA, Wang X. 2005. Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. The Plant Cell 17, 3141-3154.
53. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.
54. Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie AR, Weisshaar B. 2010. 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 188, 985-1000.
55. Sun W, Liang L, Meng X, Li Y, Gao F, Liu X, Wang S, Gao X, Wang L. 2016. Biochemical and molecular characterization of a flavonoid 3-O-glycosyltransferase responsible for anthocyanins and flavonols biosynthesis in Freesia hybrida. Frontiers in Plant Science 7, 410.
56. Sun Y, Li H, Huang JR. 2012. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Molecular Plant 5, 387-400.
57. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725-2729.
58. Tian Q, Konczak I, Schwartz SJ. 2005. Probing anthocyanin profiles in purple sweet potato cell line (Ipomoea batatas L. Cv. Ayamurasaki) by high-performance liquid chromatography and electrospray ionization tandem mass spectrometry. Journal of Agricultural and Food Chemistry 53, 6503-6509.
59. Tohge T, Nishiyama Y, Hirai MY, et al. 2005. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. The Plant Journal 42, 218-235.
60. Truong VD, Deighton N, Thompson RT, McFeeters RF, Dean LO, Pecota KV, Yencho GC. 2010. Characterization of anthocyanins and anthocyanidins in purple-fleshed sweetpotatoes by HPLC-DAD/ESI-MS/ MS. Journal of Agricultural and Food Chemistry 58, 404-410.
61. Wang H, Fan W, Li H, Yang J, Huang J, Zhang P. 2013. Functional characterization of dihydroflavonol-4-reductase in anthocyanin biosynthesis of purple sweet potato underlies the direct evidence of anthocyanins function against abiotic stresses. PLoS ONE 8, e78484.
62. Wetterhorn KM, Newmister SA, Caniza RK, Busman M, McCormick SP, Berthiller F, Adam G, Rayment I. 2016. Crystal structure of Os79 (Os04g0206600) from Oryza sativa: a UDP-glucosyltransferase involved in the detoxification of deoxynivalenol. Biochemistry 55, 6175-6186.
63. Xu W, Dubos C, Lepiniec L. 2015. Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science 20, 176-185.
64. Yang J, Bi HP, Fan WJ, Zhang M, Wang HX, Zhang P. 2011. Efficient embryogenic suspension culturing and rapid transformation of a range of elite genotypes of sweet potato (Ipomoea batatas [L.] Lam.). Plant Science 181, 701-711.
65. Yang JY, Yan RX, Roy A, Xu D, Poissonl J, Zhang Y. 2015. The I-TASSER Suite: protein structure and function prediction. Nature Methods 12, 7-8.
66. Yonekura-Sakakibara K, Fukushima A, Nakabayashi R, et al. 2012. Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. The Plant Journal 69, 154-167.
67. Yonekura-Sakakibara K, Hanada K. 2011. An evolutionary view of functional diversity in family 1 glycosyltransferases. The Plant Journal 66, 182-193.
68. Yonekura-Sakakibara K, Nakabayashi R, Sugawara S, Tohge T, Ito T, Koyanagi M, Kitajima M, Takayama H, Saito K. 2014. A flavonoid 3-O-glucoside:2″-O-glucosyltransferase responsible for terminal modification of pollen-specific flavonols in Arabidopsis thaliana. The Plant Journal 79, 769-782.
69. Yonekura-Sakakibara K, Nakayama T, Yamazaki M, Saito K. 2008. Modification and stabilization of anthocyanins. In: Winefield C, Davies K, Gould K. eds. Anthocyanins. New York: Springer, 169-190.
70. Zhang Y, Butelli E, Martin C. 2014. Engineering anthocyanin biosynthesis in plants. Current Opinion in Plant Biology 19, 81-90.
71. Zhao J, Huhman D, Shadle G, He XZ, Sumner LW, Tang Y, Dixon RA. 2011. MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. The Plant Cell 23, 1536-1555.
72. Zhao J. 2015. Flavonoid transport mechanisms: how to go, and with whom. Trends in Plant Science 20, 576-585.