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.

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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

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• Biosynthesis and Metabolic Engineering of Anthocyanins in Arabidopsis thaliana · 2014
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• Plant cell wall lignification and monolignol metabolism · 2013
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