Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis

Plant Cell

Volumn 20, Issue 8, 2008, Pages 2160-2176

  Yonekura Sakakibara, Keiko ^a   Tohge, Takayuki ^a,c   Matsuda, Fumio ^a   Nakabayashi, Ryo ^b   Takayama, Hiromitsu ^b   Niida, Rie ^a   Watanabe Takahashi, Akiko ^a   Inoue, Eri ^a   Saito, Kazuki ^a,b  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b CHIBA UNIVERSITY   (Japan)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 57749089675     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.058040     Document Type: Article

References (47)

1. Akiyama, K., Chikayama, E., Yuasa, H., Shimada, Y., Tohge, T., Shinozaki, K., Hirai, M.Y., Sakurai, T., Kikuchi, J., and Saito, K. (2008). PRIMe: A Web site that assembles tools for metabolomics and transcriptomics. In Silico Biol. 8: 0027.
2. Andersen, Ø.M., and Markham, K.R. (2006). Flavonoids: Chemistry, Biochemistry, and Applications. (Boca Raton, FL: CRC Taylor & Francis).
3. Aoki, K., Ogata, Y., and Shibata, D. (2007). Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol. 48: 381-390.
4. Blanc, G., Hokamp, K., and Wolfe, K.H. (2003). A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137-144.
5. Bloor, S.J., and Abrahams, S. (2002). The structure of the major anthocyanin in Arabidopsis thaliana. Phytochemistry 59: 343-346.
6. Brown, B.A., Cloix, C., Jiang, G.H.,Kaiserli, E., Herzyk, P., Kliebenstein, D.J., and Jenkins, G.I. (2005). A UV-B-specific signaling component orchestrates plantUVprotection. Proc. Natl. Acad. Sci.USA102: 18225-18230.
7. D'Auria, J.C., and Gershenzon, J. (2005). The secondary metabolism of Arabidopsis thaliana: Growing like a weed. Curr. Opin. Plant Biol. 8: 308-316.
8. Diet, A., Link, B., Seifert, G.J., Schellenberg, B., Wagner, U., Pauly, M., Reiter, W.D., and Ringli, C. (2006). The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell 18: 1630-1641.
9. Dixon, R.A., and Paiva, N.L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085-1097.
10. Dixon, R.A., and Strack, D. (2003). Phytochemistry meets genome analysis, and beyond. Phytochemistry 62: 815-816.
11. Dooner, H.K., Robbins, T.P., and Jorgensen, R.A. (1991). Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25: 173-199.
12. Fraser, C.M., Thompson, M.G., Shirley, A.M., Ralph, J., Schoenherr, J.A., Sinlapadech, T., Hall, M.C., and Chapple, C. (2007). Related Arabidopsis serine carboxypeptidase-like sinapoylglucose acyltransferases display distinct but overlapping substrate specificities. Plant Physiol. 144: 1986-1999.
13. Graham, T.L. (1998). Flavonoid and flavonol glycoside metabolism in Arabidopsis. Plant Physiol. Biochem. 36: 135-144.
14. Harborne, J.B., Baxter, H., and Moss, G.P. (1999). Phytochemical Dictionary: A Handbook of Bioactive Compounds from Plants, 2nd ed. (Londong: Taylor & Francis).
15. Hirai, M.Y., et al. (2005). Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem. 280: 25590-25595.
16. Hirai, M.Y., et al. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. USA 104: 6478-6483.
17. Jones, P., Messner, B., Nakajima, J., Schaffner, A.R., and Saito, K. (2003). UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 278: 43910-43918.
18. Kerhoas, L., Aouak, D., Cingoz, A., Routaboul, J.M., Lepiniec, L., Einhorn, J., and Birlirakis, N. (2006). Structural characterization of the major flavonoid glycosides from Arabidopsis thaliana seeds. J. Agric. Food Chem. 54: 6603-6612.
19. Kleine, T., Kindgren, P., Benedict, C., Hendrickson, L., and Strand, A. (2007). Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol. 144: 1391-1406.
20. Kubo, A., Arai, Y., Nagashima, S., and Yoshikawa, T. (2004). Alteration of sugar donor specificities of plant glycosyltransferases by a single point mutation. Arch. Biochem. Biophys. 429: 198-203.
21. Kusano, M., Fukushima, A., Arita, M., Jonsson, P., Moritz, T., Kobayashi, M., Hayashi, N., Tohge, T., and Saito, K. (2007). Unbiased characterization of genotype-depedent metabolic regulations by metabolomic approach in Arabidopsis thaliana. BMC Syst Biol. 1: 53.
22. Lepiniec, L., Debeaujon, I., Routaboul, J.M., Baudry, A., Pourcel, L., Nesi, N., and Caboche, M. (2006). Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57: 405-430.
23. Lim, E.K., Li, Y., Parr, A., Jackson, R., Ashford, D.A., and Bowles, D. J. (2001). Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J. Biol. Chem. 276: 4344-4349.
24. Luo, J., et al. (2007). Convergent evolution in the BAHD family of acyl transferases: Identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J. 50: 678-695.
25. Mulinacci, N., Vincieri, F.F., Baldi, A., Bambagiotti-alberti, M., Sendl, A., and Wagner, H. (1995). Flavonol glycosides from Sedum telephium subspecies maximum leaves. Phytochemistry 38: 531-533.
26. Obayashi, T., Kinoshita, K., Nakai, K., Shibaoka, M., Hayashi, S., Saeki, M., Shibata, D., Saito, K., and Ohta, H. (2007). ATTED-II: A database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res. 35: D863-D869.
27. Offen, W., Martinez-Fleites, C., Yang, M., Kiat-Lim, E., Davis, B.G., Tarling, C.A., Ford, C.M., Bowles, D.J., and Davies, G.J. (2006). Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 25: 1396-1405.
28. Oka, T., Nemoto, T., and Jigami, Y. (2007). Functional analysis of Arabidopsis thaliana RHM2/MUM4, a multidomain protein involved in UDP-D-glucose to UDP-L-rhamnose conversion. J. Biol. Chem. 282: 5389-5403.
29. Ringli, C., Bigler, L., Kuhn, B.M., Leiber, R.M., Diet, A., Santelia, D., Frey, B., Pollmann, S., and Klein, M. (2008). The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation. Plant Cell 20:.
30. Routaboul, J.M., Kerhoas, L., Debeaujon, I., Pourcel, L., Caboche, M., Einhorn, J., and Lepiniec, L. (2006). Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224: 96-107.
31. Ruegger, M., and Chapple, C. (2001). Mutations that reduce sinapoylmalate accumulation in Arabidopsis thaliana define loci with diverse roles in phenylpropanoid metabolism. Genetics 159: 1741-1749.
32. Saito, K., Hirai, M.Y., and Yonekura-Sakakibara, K. (2008). Decoding genes with coexpression networks and metabolomics - 'Majority report by precogs.' Trends Plant Sci. 13: 36-43.
33. Sakar, M.K., Şöhretoǧlu, D., Özalp, M., Ekizoǧlu, M., Piacente, S., and Pizza, C. (2005). Polyphenolic compounds and antimicrobial activity of Quercus aucheri leaves. Turk. J. Chem. 29: 555-559.
34. Shikazono, N., Yokota, Y., Kitamura, S., Suzuki, C., Watanabe, H., Tano, S., and Tanaka, A. (2003). Mutation rate and novel tt mutants of Arabidopsis thaliana induced by carbon ions. Genetics 163: 1449-1455.
35. Shirley, B.W., Kubasek, W.L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F.M., and Goodman, H.M. (1995). Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J. 8: 659-671.
36. Stracke, R., Ishihara, H., Huep, G., Barsch, A., Mehrtens, F., Niehaus, K., and Weisshaar, B. (2007). Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J. 50: 660-677.
37. Stuart, J.M., Segal, E., Koller, D., and Kim, S.K. (2003). A gene-coexpression network for global discovery of conserved genetic modules. Science 302: 249-255.
38. Tanaka, Y., and Filippa, B. (2006). Flower color. In Flowering and Its Manipulation, Vol, 20, C. Ainsworth, ed (London: Blackwell Publishers), pp. 201-239.
39. Tohge, T., et al. (2005). Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J. 42: 218-235.
40. Tohge, T., Yonekura-Sakakibara, K., Niida, R., Watanabe-Takahashi, A., and Saito, K. (2007). Phytochemical genomics in Arabidopsis thaliana: A case study for functional identification of flavonoid biosynthsis genes. Pure Appl. Chem. 79: 811-823.
41. Usadel, B., Kuschinsky, A.M., Rosso, M.G., Eckermann, N., and Pauly, M. (2004). RHM2 is involved in mucilage pectin synthesis and is required for the development of the seed coat in Arabidopsis. Plant Physiol. 134: 286-295.
42. Valvekens, D., Van Montagu, M., and Van Lijsebettens, M. (1988). Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl. Acad. Sci. USA 85: 5536-5540.
43. Veit, M., and Pauli, G.F. (1999). Major flavonoids from Arabidopsis thaliana leaves. J. Nat. Prod. 62: 1301-1303.
44. von Roepenack-Lahaye, E., Degenkolb, T., Zerjeski, M., Franz, M., Roth, U., Wessjohann, L., Schmidt, J., Scheel, D., and Clemens, S. (2004). Profiling of Arabidopsis secondary metabolites by capillary liquid chromatography coupled to electrospray ionization quadrupole time-of-flight mass spectrometry. Plant Physiol. 134: 548-559.
45. Western, T.L., Young, D.S., Dean, G.H., Tan, W.L., Samuels, A.L., and Haughn, G.W. (2004). MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat. Plant Physiol. 134: 296-306.
46. Yonekura-Sakakibara, K., Kojima, M., Yamaya, T., and Sakakibara, H. (2004). Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to ciszeatin. Plant Physiol. 134: 1654-1661.
47. Yonekura-Sakakibara, K., Tohge, T., Niida, R., and Saito, K. (2007). Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J. Biol. Chem. 282: 14932-14941.