Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana

Abstract

Summary To identify candidate genes involved in Arabidopsis flavonoid biosynthesis, we applied transcriptome coexpression analysis and independent component analyses with 1388 microarray data from publicly available databases. Two glycosyltransferases, UGT79B1 and UGT84A2 were found to cluster with anthocyanin biosynthetic genes. Anthocyanin was drastically reduced in ugt79b1 knockout mutants. Recombinant UGT79B1 protein converted cyanidin 3‐ O ‐glucoside to cyanidin 3‐ O ‐xylosyl(1→2)glucoside. UGT79B1 recognized 3‐ O ‐glucosylated anthocyanidins/flavonols and uridine diphosphate (UDP)‐xylose, but not 3,5‐ O ‐diglucosylated anthocyanidins, indicating that UGT79B1 encodes anthocyanin 3‐ O ‐glucoside: 2′′‐ O ‐xylosyltransferase. UGT84A2 is known to encode sinapic acid: UDP‐glucosyltransferase. In ugt84a2 knockout mutants, a major sinapoylated anthocyanin was drastically reduced. A comparison of anthocyanin profiles in ugt84a knockout mutants indicated that UGT84A2 plays a major role in sinapoylation of anthocyanin, and that other UGT84As contribute the production of 1‐ O ‐sinapoylglucose to a lesser extent. These data suggest major routes from cyanidin 3‐ O ‐glucoside to the most highly modified cyanidin in the potential intricate anthocyanin modification pathways in Arabidopsis.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 73

1. 1.

   Anderson ØM, Markham KR. Flavonoids: Chemistry, Biochemistry, and Applications. 2006.

   Not in our library

2. 2.

   Bar-Peled M, Lewinsohn E, Fluhr R, Gressel J. UDP-rhamnose:flavanone-7-O-glucoside-2′′-O-rhamnosyltransferase. Purification and characterization of an enzyme catalyzing the production of bitter compounds in citrus. J. Biol. Chem. 1991;266:20953-20959.

   Not in our library

3. 3.

   Bloor SJ, Abrahams S. The structure of the major anthocyanin in Arabidopsis thaliana. Phytochemistry. 2002;59:343-346.

   Not in our library10.1016/s0031-9422(01)00460-5

4. 4.

   Bowles D, Lim EK, Poppenberger B, Vaistij FE. Glycosyltransferases of lipophilic small molecules. Annu. Rev. Plant Biol. 2006;57:567-597.

   Not in our library10.1146/annurev.arplant.57.032905.105429

5. 5.

   Brugliera F, Holton TA, Stevenson TW, Farcy E, Lu CY, Cornish EC. Isolation and characterization of a cDNA clone corresponding to the Rt locus of Petunia hybrida. Plant J. 1994;5:81-92.

   Not in our library10.1046/j.1365-313x.1994.5010081.x

6. 6.

   Chiappetta P, Roubaud MC, Torresani B. Blind source separation and the analysis of microarray data. J. Comput. Biol. 2004;11:1090-1109.

   Not in our library10.1089/cmb.2004.11.1090

7. 7.

   Coutinho PM, Deleury E, Davies GJ, Henrissat B. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 2003;328:307-317.

   Not in our library10.1016/s0022-2836(03)00307-3

8. 8.

   D’Auria JC, Gershenzon J. The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr. Opin. Plant Biol. 2005;8:308-316.

   Not in our library10.1016/j.pbi.2005.03.012

9. 9.

   Davies KM, Schwinn KE, Anderson ØM, Markham KR. Molecular biology and biotechnology of flavonoid biosynthesis. Flavonoids: Chemistry, Biochemistry and Applications. 2006;143-218.

   Not in our library

10. 10.

    Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7:1085-1097.

    Not in our library10.1105/tpc.7.7.1085

11. 11.

    Dooner HK, Robbins TP, Jorgensen RA. Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 1991;25:173-199.

    Not in our library10.1146/annurev.ge.25.120191.001133

12. 12.

    Fedoroff NV, Smith DL. A versatile system for detecting transposition in Arabidopsis. Plant J. 1993;3:273-289.

    Not in our library10.1111/j.1365-313x.1993.tb00178.x

13. 13.

    Feinbaum RL, Ausubel FM. Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol. Cell. Biol. 1988;8:1985-1992.

    Not in our library10.1128/mcb.8.5.1985-1992.1988

14. 14.

    Fraser CM, Thompson MG, Shirley AM, Ralph J, Schoenherr JA, Sinlapadech T, Hall MC, Chapple C. Related Arabidopsis serine carboxypeptidase-like sinapoylglucose acyltransferases display distinct but overlapping substrate specificities. Plant Physiol. 2007;144:1986-1999.

    Not in our library10.1104/pp.107.098970

15. 15.

    Fridman E, Pichersky E. Metabolomics, genomics, proteomics, and the identification of enzymes and their substrates and products. Curr. Opin. Plant Biol. 2005;8:242-248.

    Not in our library10.1016/j.pbi.2005.03.004

16. 16.

    Frigyesi A, Veerla S, Lindgren D, Hoglund M. Independent component analysis reveals new and biologically significant structures in microarray data. BMC Bioinformatics. 2006;7:290.

    Not in our library10.1186/1471-2105-7-290

17. 17.

    Fukuchi-Mizutani M, Okuhara H, Fukui Y, Nakao M, Katsumoto Y, Yonekura-Sakakibara K, Kusumi T, Hase T, Tanaka Y. Biochemical and molecular characterization of a novel UDP-glucose:anthocyanin 3′-O-glucosyltransferase, a key enzyme for blue anthocyanin biosynthesis, from gentian. Plant Physiol. 2003;132:1652-1663.

    Not in our library10.1104/pp.102.018242

18. 18.

    Fukushima A, Wada M, Kanaya S, Arita M. SVD-based anatomy of gene expressions for correlation analysis in Arabidopsis thaliana. DNA Res. 2008;15:367-374.

    Not in our library10.1093/dnares/dsn025

19. 19.

    Harborne JB, Baxter H. Handbook of Natural Flavonoids. 1999.

    Not in our library

20. 20.

    de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics. 2004;20:1453-1454.

    Not in our library10.1093/bioinformatics/bth078

21. 21.

    Hori G, Inoue M, Nishimura SI, Nakahara H. Blind gene classification—an application of a signal separation method. Genome Inform. 2001;12:255-256.

    Not in our library

22. 22.

    Hyvärinen A, Oja E. A fast fixed-point algorithm for independent component analysis. Neural Comput. 1997;9:1483-1492.

    Not in our library

23. 23.

    Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-264.

    Not in our library10.1093/biostatistics/4.2.249

24. 24.

    Ito T, Motohashi R, Kuromori T, Noutoshi Y, Seki M, Kamiya A, Mizukado S, Sakurai T, Shinozaki K. A resource of 5,814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant Cell Physiol. 2005;46:1149-1153.

    Not in our library10.1093/pcp/pci112

25. 25.

    Jones P, Messner B, Nakajima J, Schaffner AR, Saito K. UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 2003;278:43910-43918.

    Not in our library10.1074/jbc.m303523200

26. 26.

    Kinoshita K, Obayashi T. Multi-dimensional correlations for gene coexpression and application to the large-scale data of Arabidopsis. Bioinformatics. 2009;25:2677-2684.

    Not in our library10.1093/bioinformatics/btp442

27. 27.

    Kitamura S, Shikazono N, Tanaka A. TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J. 2004;37:104-114.

    Not in our library10.1046/j.1365-313x.2003.01943.x

28. 28.

    Kong W, Vanderburg CR, Gunshin H, Rogers JT, Huang X. A review of independent component analysis application to microarray gene expression data. BioTechniques. 2008;45:501-520.

    Not in our library10.2144/000112950

29. 29.
    Independent component analysis of Alzheimer's DNA microarray gene expression data · 2009

    Not checked
30. 30.

    Kroon J, Souer E, de Graaff A, Xue Y, Mol J, Koes R. Cloning and structural analysis of the anthocyanin pigmentation locus Rt of Petunia hybrida: characterization of insertion sequences in two mutant alleles. Plant J. 1994;5:69-80.

    Not in our library10.1046/j.1365-313x.1994.5010069.x

31. 31.

    Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T, Akiyama K, Kamiya A, Ito T, Shinozaki K. A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 2004;37:897-905.

    Not in our library10.1111/j.1365.313x.2004.02009.x

32. 32.

    Kusano M, Tohge T, Fukushima A, et al. Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. Plant J. 2011;67:354-369.

    Not in our library10.1111/j.1365-313x.2011.04599.x

33. 33.

    Lehfeldt C, Shirley AM, Meyer K, Ruegger MO, Cusumano JC, Viitanen PV, Strack D, Chapple C. Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell. 2000;12:1295-1306.

    Not in our library10.1105/tpc.12.8.1295

34. 34.

    Li L, Modolo LV, Escamilla-Trevino LL, Achnine L, Dixon RA, Wang X. Crystal structure of Medicago truncatula UGT85H2—insights into the structural basis of a multifunctional (iso)flavonoid glycosyltransferase. J. Mol. Biol. 2007;370:951-963.

    Not in our library10.1016/j.jmb.2007.05.036

35. 35.

    Liebermeister W. Linear modes of gene expression determined by independent component analysis. Bioinformatics. 2002;18:51-60.

    Not in our library10.1093/bioinformatics/18.1.51

36. 36.

    Lim EK, Li Y, Parr A, Jackson R, Ashford DA, Bowles DJ. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J. Biol. Chem. 2001;276:4344-4349.

    Not in our library10.1074/jbc.m007263200

37. 37.

    Luo J, Nishiyama Y, Fuell C, et al. Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J. 2007;50:678-695.

    Not in our library10.1111/j.1365-313x.2007.03079.x

38. 38.

    Mackenzie PI, Owens IS, Burchell B, et al. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics. 1997;7:255-269.

    Not in our library10.1097/00008571-199708000-00001

39. 39.

    Matsuba Y, Sasaki N, Tera M, et al. A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell. 2010;22:3374-3389.

    Not in our library10.1105/tpc.110.077487

40. 40.

    Meissner D, Albert A, Bottcher C, Strack D, Milkowski C. The role of UDP-glucose:hydroxycinnamate glucosyltransferases in phenylpropanoid metabolism and the response to UV-B radiation in Arabidopsis thaliana. Planta. 2008;228:663-674.

    Not in our library10.1007/s00425-008-0768-3

41. 41.

    Mochida K, Shinozaki K. Genomics and bioinformatics resources for crop improvement. Plant Cell Physiol. 2010;51:497-523.

    Not in our library10.1093/pcp/pcq027

42. 42.

    Montefiori M, Espley RV, Stevenson D, Cooney J, Datson PM, Saiz A, Atkinson RG, Hellens RP, Allan AC. Identification and characterisation of F3GT1 and F3GGT1, two glycosyltransferases responsible for anthocyanin biosynthesis in red-fleshed kiwifruit (Actinidia chinensis. Plant J. 2011;65:106-118.

    Not in our library10.1111/j.1365-313x.2010.04409.x

43. 43.

    Moreno-Risueno MA, Busch W, Benfey PN. Omics meet networks – using systems approaches to infer regulatory networks in plants. Curr. Opin. Plant Biol. 2010;13:126-131.

    Not in our library10.1016/j.pbi.2009.11.005

44. 44.

    Morita Y, Hoshino A, Kikuchi Y, et al. 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. Plant J. 2005;42:353-363.

    Not in our library10.1111/j.1365-313x.2005.02383.x

45. 45.

    Noguchi A, Fukui Y, Iuchi-Okada A, Kakutani S, Satake H, Iwashita T, Nakao M, Umezawa T, Ono E. Sequential glucosylation of a furofuran lignan, (+)-sesaminol, by Sesamum indicum UGT71A9 and UGT94D1 glucosyltransferases. Plant J. 2008;54:415-427.

    Not in our library10.1111/j.1365-313x.2008.03428.x

46. 46.

    Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K. ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 2009;37:D987-D991.

    Not in our library10.1093/nar/gkn807

47. 47.

    Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis BG, Tarling CA, Ford CM, Bowles DJ, Davies GJ. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 2006;25:1396-1405.

    Not in our library10.1038/sj.emboj.7600970

48. 48.

    Osmani SA, Bak S, Imberty A, Olsen CE, Moller BL. Catalytic key amino acids and UDP-sugar donor specificity of a plant glucuronosyltransferase, UGT94B1: molecular modeling substantiated by site-specific mutagenesis and biochemical analyses. Plant Physiol. 2008;148:1295-1308.

    Not in our library10.1104/pp.108.128256

49. 49.

    Paquette SM, Jensen K, Bak S. A web-based resource for the Arabidopsis P450, cytochromes b5, NADPH-cytochrome P450 reductases, and family 1 glycosyltransferases (http://www.P450.kvl.dk. Phytochemistry. 2009;70:1940-1947.

    Not in our library10.1016/j.phytochem.2009.08.024

50. 50.

    Pelletier MK, Shirley BW. Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings. Coordinate regulation with chalcone synthase and chalcone isomerase. Plant Physiol. 1996;111:339-345.

    Not in our library10.1104/pp.111.1.339

51. 51.

    Pelletier MK, Murrell JR, Shirley BW. Characterization of flavonol synthase and leukoanthocyanidin dioxygenase genes in Arabidopsis. Further evidence for differential regulation of ‘early’ and ‘late’ genes. Plant Physiol. 1997;113:1437-1445.

    Not in our library10.1104/pp.113.4.1437

52. 52.

    Saidi SA, Holland CM, Kreil DP, MacKay DJ, Charnock-Jones DS, Print CG, Smith SK. Independent component analysis of microarray data in the study of endometrial cancer. Oncogene. 2004;23:6677-6683.

    Not in our library10.1038/sj.onc.1207562

53. 53.

    Saito K, Matsuda F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 2010;61:463-489.

    Not in our library10.1146/annurev.arplant.043008.092035

54. 54.

    Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987;4:406-425.

    Not in our library10.1093/oxfordjournals.molbev.a040454

55. 55.

    Sawada S, Suzuki H, Ichimaida F, Yamaguchi MA, Iwashita T, Fukui Y, Hemmi H, Nishino T, Nakayama T. UDP-glucuronic acid:anthocyanin glucuronosyltransferase from red daisy (Bellis perennis) flowers. Enzymology and phylogenetics of a novel glucuronosyltransferase involved in flower pigment biosynthesis. J. Biol. Chem. 2005;280:899-906.

    Not in our library10.1074/jbc.m410537200

56. 56.

    Seki M, Carninci P, Nishiyama Y, Hayashizaki Y, Shinozaki K. High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated CAP trapper. Plant J. 1998;15:707-720.

    Not in our library10.1046/j.1365-313x.1998.00237.x

57. 57.

    Seki M, Narusaka M, Kamiya A, et al. Functional annotation of a full-length Arabidopsis cDNA collection. Science. 2002;296:141-145.

    Not in our library10.1126/science.1071006

58. 58.

    Shao H, He X, Achnine L, Blount JW, Dixon RA, Wang X. Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell. 2005;17:3141-3154.

    Not in our library10.1105/tpc.105.035055

59. 59.

    Shirley BW, Hanley S, Goodman HM. Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. Plant Cell. 1992;4:333-347.

    Not in our library10.1105/tpc.4.3.333

60. 60.

    Shirley AM, McMichael CM, Chapple C. The sng2 mutant of Arabidopsis is defective in the gene encoding the serine carboxypeptidase-like protein sinapoylglucose:choline sinapoyltransferase. Plant J. 2001;28:83-94.

    Not in our library10.1046/j.1365-313x.2001.01123.x

61. 61.

    Sinlapadech T, Stout J, Ruegger MO, Deak M, Chapple C. The hyper-fluorescent trichome phenotype of the brt1 mutant of Arabidopsis is the result of a defect in a sinapic acid: UDPG glucosyltransferase. Plant J. 2007;49:655-668.

    Not in our library10.1111/j.1365-313x.2006.02984.x

62. 62.

    Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 2006;140:637-646.

    Not in our library10.1104/pp.105.072579

63. 63.

    Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007;24:1596-1599.

    Not in our library10.1093/molbev/msm092

64. 64.

    Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008;54:733-749.

    Not in our library10.1111/j.1365-313x.2008.03447.x

65. 65.

    Teusch M. Uridine 5′-diphosphate-xylose: anthocyanidin 3-O-glucose-xylosyltransferase from petals of Matthiola incana R.Br. Planta. 1986;169:559-563.

    Not in our library10.1007/bf00392107

66. 66.

    Tohge T, Nishiyama Y, Hirai MY, et al. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J. 2005;42:218-235.

    Not in our library10.1111/j.1365-313x.2005.02371.x

67. 67.

    Valvekens D, Montagu MV, Lijsebettens MV. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl Acad. Sci. USA. 1988;85:5536-5540.

    Not in our library10.1073/pnas.85.15.5536

68. 68.

    Yamazaki M, Gong Z, Fukuchi-Mizutani M, Fukui Y, Tanaka Y, Kusumi T, Saito K. Molecular cloning and biochemical characterization of a novel anthocyanin 5-O-glucosyltransferase by mRNA differential display for plant forms regarding anthocyanin. J. Biol. Chem. 1999;274:7405-7411.

    Not in our library10.1074/jbc.274.11.7405

69. 69.

    Yonekura-Sakakibara K, Hanada K. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 2011;66:182-193.

    Not in our library10.1111/j.1365-313x.2011.04493.x

70. 70.

    Yonekura-Sakakibara K, Saito K. Functional genomics for plant natural product biosynthesis. Nat. Prod. Rep. 2009;26:1466-1487.

    Not in our library10.1039/b817077k

71. 71.

    Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H. Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol. 2004;134:1654-1661.

    Not in our library10.1104/pp.103.037176

72. 72.

    Yonekura-Sakakibara K, Tohge T, Niida R, Saito K. Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J. Biol. Chem. 2007;282:14932-14941.

    Not in our library10.1074/jbc.m611498200

73. 73.

    Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, Watanabe-Takahashi A, Inoue E, Saito K. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell. 2008;20:2160-2176.

    Not in our library10.1105/tpc.108.058040

Cited by papers we hold 4

• Glycosylation Is a Major Regulator of Phenylpropanoid Availability and Biological Activity in Plants · 2016
  No notice
• Role of a chalcone isomerase-like protein in flavonoid biosynthesis in Arabidopsis thaliana · 2015
  No notice
• Biosynthesis and Metabolic Engineering of Anthocyanins in Arabidopsis thaliana · 2014
  No notice
• Plant cell wall lignification and monolignol metabolism · 2013
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.