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Approaches to the Analysis of Plant-Derived Natural Products

  • Lionel Hill
  • Trevor L. Wang
Chapter

Abstract

The term “plant-derived natural product” is extremely broad and the scope of this chapter is determined by the nature of lower-abundance secondary metabolites rather than storage proteins, starch, cell walls, and lipids. In some instances, however, similar techniques can used to measure both groups of compounds. The bioactivity of secondary metabolites underlines their importance in human nutrition, health, pharmacy and plant defence mechanisms, and is the basis for their commercial value. Consequently, these two features are the driving force behind the continuing development of techniques for their analysis. The most important recent advance has been the advent of metabolomics. The metabolome, by analogy to the genome, proteome and transcriptome, is the entire small-molecule complement of the plant. The study of the metabolome, metabolomics, cannot be achieved by any single method and is largely a consequence of recent improvements to technology permitting high throughput analyses and data-handling. Interest in understanding details of natural product biosynthetic pathways as well as a desire to measure the bioactive end-product means, however, that it is necessary to cover methods of sufficient sensitivity to detect low-abundance intermediates as well as those methods that can investigate metabolite structure. Hence this chapter represents an introduction and overview of the fundamentals that underlie the wide range of methods used in the quantification of plant-derived natural products and a brief introduction to metabolomics. It is hoped that a strong understanding of the fundamentals will allow the reader to judge from the plethora of manufacturers’ brochures, primary literature, and on-line resources, which technologies and approaches best fit their situation. The process of analysis will be followed through its stages, from extraction of material to detection of analytes. Methods have been chosen not only with the chemistry of the analyte in mind, but also with a firm idea of the biological question that is to be answered. There will be an unashamed bias towards chromatography and mass spectroscopy since plants are complex systems containing many interesting chemicals, often in low amounts. Chromatography can simplify the process of addressing a complex mixture, and mass spectroscopy yields rich information from low-abundance analytes. For a brief list of methods for the main secondary metabolites, consult Table 1.

Keywords

High Performance Liquid Chromatography High Performance Liquid Chromatography Electron Ionisation Accurate Mass Select Reaction Monitoring 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alali FQ, Tahboub YR, Ibrahim ES, Qandil AM, Tawaha K, Burgess JP, Sy A, Nakanishi Y, Kroll DJ, and Oberlies NH (2008) Pyrrolizidine alkaloids from Echium glomeratum (Boraginaceae). Phytochemistry 69:2341–2346PubMedCrossRefGoogle Scholar
  2. Allwood JW, Ellis DI, and Goodacre R (2008) Metabolomic technologies and their application to the study of plants and plant-host- interactions. Physiol. Plant. 132:117–135PubMedGoogle Scholar
  3. Antonio C, Larson T, Gilday A, Graham I, Bergström E, and Thomas-Oates J (2007) Quantification of sugars and sugar phosphates in Arabidopsis thaliana tissues using porous graphitic carbon liquid chromatography-electrospray ionization mass spectrometry. J. Chromatogr. A 1172:170–178PubMedCrossRefGoogle Scholar
  4. Antonio C, Pinheiro C, Chaves MM, Ricardo CP, Ortuño MF, and Thomas-Oates J (2008) Analysis of carbohydrates in Lupinus albus stems on imposition of water deficit, using porous graphitic carbon liquid chromatography-electrospray ionization mass spectrometry. J. Chromatogr. A 1187:111–118PubMedCrossRefGoogle Scholar
  5. ap Rees T (1980) Integration of pathways of synthesis and degradation of hexose phosphates. In: Preiss J (ed) The biochemistry of plants: a comprehensive treatise, Vol 3. Academic, New YorkGoogle Scholar
  6. Barkawi LS, Tam Y-Y, Tillman JA, Pederson B, Calio J, Al-Amier H, Emerick M, Normanly J, and Cohen JD (2008) A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue. Anal. Biochem. 372:177–188PubMedCrossRefGoogle Scholar
  7. Bigler L, Schnider CF, Hu W, and Hesse M (1996) Electrospray-ionization mass spectrometry.3. Acid-catalysed isomerisation of N,N’-bis[(E)-3-(4-hydroxyphenyl)prop-2-enoyl]spermidines by the zip reaction. Helv. Chim. Acta 79:2152–2163CrossRefGoogle Scholar
  8. Borisjuk LS, Walenta H, Rolletschek W, et al (2002) Spatial analysis of plant development: sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. Plant J. 29:521–530PubMedCrossRefGoogle Scholar
  9. Burrell MM, Earnshaw CJ, and Clench MR (2007) Imaging matrix assisted laser desorption ionization mass spectrometry: a technique to map plant metabolites within tissues at high spatial resolution. J. Exp. Bot. 58:757–763PubMedCrossRefGoogle Scholar
  10. Cartea ME, Rodriguez VM, de Haro A, et al (2008) Variation of glucosinolates and nutritional value in nabicol (Brassica napus pabularia group). Euphytica 159:111–122CrossRefGoogle Scholar
  11. Cha S, Zhang H, Ilarslan HI, Wurtele ES, Brachova L, Nikolau BJ, and Yeung ES (2008) Direct profiling and imaging of plant metabolites in intact tissues by using colloidal graphite-assisted laser desorption ionization mass spectrometry. Plant J. 55:348–360PubMedCrossRefGoogle Scholar
  12. Chien S-C, Chen C-C, Chiu H-L, Chang C-I, Tseng M-H, and Kuo Y-H (2008) 18-nor-Podocarpanes and podocarpanes from the bark of Taiwania cryptomerioides. Phytochemistry 69:2336–2340PubMedCrossRefGoogle Scholar
  13. Davidovich-Rikanati R, Lewinsohn E, Bar E, Iijima Y, Pichersky E, and Sitrit Y (2008) Overexpression of the lemon basil -zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. Plant J. 56:228–238PubMedCrossRefGoogle Scholar
  14. De Hoffmann E and Stroobant V (2002) Mass spectrometry principles and applications. Wiley, ChichesterGoogle Scholar
  15. De Person M, Chaimbault P, and Elfakir C (2008) Analysis of native amino acids by liquid chromatography/electrospray ionization mass spectrometry: comparative study between two sources and interfaces. J. Mass Spectrom. 43:204–215PubMedCrossRefGoogle Scholar
  16. Deichmann U (2007) “Molecular” versus “Colloidal”: controversies in biology and biochemistry, 1900–1940. Bull. Hist. Chem. 32:105–118Google Scholar
  17. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, and Kämper J (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56:181–195PubMedCrossRefGoogle Scholar
  18. Dunn WB, Overy S, and Quick WP (2005) Evaluation of automated electrospray-TOF mass spectrometry for metabolic fingerprinting of the plant metabolome. Metabolomics 1:137–148CrossRefGoogle Scholar
  19. Edwards WR, Hall JA, Rowlan AR, Schneider-Barfield T, Sun TJ, Patil MA, Pierce ML, Fulcher RG Bell AA, and Essenberg M (2008) Light filtering by epidermal flavonoids during the resistant response of cotton Xanthomonas protects leaf tissue from light-dependent phytoalexin toxicity. Phytochemistry 69:2320–2328PubMedCrossRefGoogle Scholar
  20. Fiehn O (2002) Metabolomics – the link between genotypes and phenotypes. Plant Mol. Biol. 48:155–171PubMedCrossRefGoogle Scholar
  21. Fiehn O et al (2007) The metabolomics standards initiative. Metabolomics 3:175–178CrossRefGoogle Scholar
  22. Giannoccaro E, Wang Y-J, and Chen P (2008) Comparison of two HPLC systems and an enzymatic method for quantification of soybean sugars. Food Chem. 106:324–330CrossRefGoogle Scholar
  23. Gibon Y, Vigeolas H, Tiessen A, Geigenberger P, and Stitt M (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. Plant J. 30:221–235PubMedCrossRefGoogle Scholar
  24. Glauser G, Grata E, Dubugnon L, Rudaz S, Farmer EE, and Wolfender J-L (2008) Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J. Biol. Chem. 283:16400–16407PubMedCrossRefGoogle Scholar
  25. Goodacre R (2005) Making sense of the metabolome using evolutionary computation: seeing the wood with the trees. J. Exp. Bot. 56:245–254PubMedCrossRefGoogle Scholar
  26. Goossens A, Häkkinen ST, Laakso I, Seppänen-Laakso T, Biondi S, De Sutter V, Lammertyn F, Nuutila AM, Söderlund H, Zabeau M, Inzé D, and Oksman-Caldentey K-M (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc. Natl. Acad. Sci. USA 100:8595–8600PubMedCrossRefGoogle Scholar
  27. Gross ML and Caprioli RM (eds) (2005) In: Nibbering NMM (vol. ed) The encyclopedia of mass spectrometry, Vol 4. Fundamentals of and applications to organic (and organometallic) compounds. Elsevier, AmsterdamGoogle Scholar
  28. Guy C, Kopka J, and Moritz T (2008) Plant metabolomics coming of age. Physiol. Plant. 132:113–116PubMedCrossRefGoogle Scholar
  29. Halket JM, Waterman D, Przyborowska AM, Patel RKP, Fraser PD, and Bramley PM (2005) Chemical derivatization and mass spectral libraries in metabolic profiling by GC/MS and LC/MS/MS. J. Exp. Bot. 56:219–243PubMedCrossRefGoogle Scholar
  30. Hall R, Beale M, Fiehn O, et al (2002) Plant metabolomics: the missing link in functional genomic strategies. Plant Cell 14:1437–1440PubMedCrossRefGoogle Scholar
  31. Issaq HJ (1999) Capillary electrophoresis of natural products - II. Electrophoresis 20:3190–3202PubMedCrossRefGoogle Scholar
  32. Jellito T, Sonnewald U, Willmitzer L, Hajirezaei MR, and Stitt M (1992) Inorganic pyrophosphate content and metabolites in leaves and tubers of potato and tobacco plants expressing E. coli pyrophosphatase in their cytosol. Planta 188:238–244CrossRefGoogle Scholar
  33. Jenkins H, Hardy N, Beckmann M, Draper J, Smith AR, Taylor J, Fiehn O, Goodacre R, Bino R, Hall R, Kopka J, Lane GA, Lange BM, Liu JR, Mendes P, Nikolau BJ, Oliver SJ, Paton NW, Roessner-Tunali U, Saito K, Smedsgaard J, Sumner LW, Wang T, Walsh S, Wurtele ES, and Kell DB (2004) A proposed framework for the description of plant metabolomics experiments and their results. Nat. Biotechnol. 22:1601–1606PubMedCrossRefGoogle Scholar
  34. Jiang H, Somogyi A, Timmermann BN, and Gang DR (2006) Instrument dependence of electrospray ionization and tandem mass spectrometric fragmentation of the gingerols. Rapid Commun. Mass Spectrom. 20:3089–3100PubMedCrossRefGoogle Scholar
  35. Jones WP and Klinghorn AD (2005) Extraction of plant secondary metabolites. In: Sarker SD, Latif Z, and Gray AI (eds) Natural products isolation, methods in biotechnology, Vol 20. Humana Press: Totowa, NJGoogle Scholar
  36. Kai K, Mizutani M, Kawamura N, Yamamoto R, Tamai M, Yamaguchi H, Sakata K, and Shimizu B-I (2008) Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J. 55:989–999PubMedCrossRefGoogle Scholar
  37. Kishimoto K, Matsui K, Ozawa R, and Takabayashi J (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry 69:2127–2132PubMedCrossRefGoogle Scholar
  38. Klejdus B, Vacek J, Lojková L, Benešová L, and Kubáň V (2008) Ultrahigh-pressure liquid chromatography of isoflavones and phenolic acids on different stationary phases. J. Chromatogr. A 1195:52–59PubMedCrossRefGoogle Scholar
  39. Kobayashi N and DellaPenna D (2008) Tocopherol metabolism, oxidation and recycling under high light stress in Arabidopsis. Plant J. 55:607–618PubMedCrossRefGoogle Scholar
  40. Krishnan P, Kruger NJ, and Ratcliffe RG (2005) Metabolite fingerprinting and profiling in plants using NMR. J. Exp. Bot. 56:255–265PubMedCrossRefGoogle Scholar
  41. Kwon H-J, Jeong J-S, Lee Y-M, and Hong S-P (2008) A reversed-phase high-performance liquid chromatography method with pulsed amperometric detection for the determination of glycosides. J. Chromatogr. A 1185:251–257PubMedCrossRefGoogle Scholar
  42. Larkov O, Zaks A, Bar E, Lewinsohn E, Dudai N, Mayer AM, and Ravid U (2008) Enantioselective monoterpene alcohol acetylation in Origanum, Mentha and Salvia species. Phytochemistry 69:2565–2571PubMedCrossRefGoogle Scholar
  43. Lätti AK, Rihinen KR, and Kainulainen PS (2008) Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland. J. Agric. Food Chem. 56:190–196PubMedCrossRefGoogle Scholar
  44. Laurens JB, Bekker LC, Steenkamp V, and Stewart MJ (2001) Gas chromatographic-mass spectrometric confirmation of atractyloside in a patient poisoned with Callilepsis laureola. J. Chro­matogr. B, 765:127–133CrossRefGoogle Scholar
  45. Lee S-S, Lin H-C, and Chen C-K (2008) Acylated ­flavonol monorhamnosides, α-glucosidase inhibitors, from Machilus philippinensis. Phytochemistry 69:2347–2353PubMedCrossRefGoogle Scholar
  46. Lesney MS (2004) An apple a day. Today’s Chemist at Work, Feb 2004, pp. 32–36Google Scholar
  47. Li B, Abliz Z, Tang M, Fu G, and Yu S (2006) Rapid structural characterization of triterpenoid saponins in crude extract from Symplocos chinensis using liquid chromatography combined with electrospray ioniszation tandem mass spectrometry. J. Chromatogr. A, 1101:53–62PubMedCrossRefGoogle Scholar
  48. Lin CY, Wu HF, Tieerdema RS, and Viant MR (2007) Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics 3:55–67CrossRefGoogle Scholar
  49. Linhardt RJ (1994) Capillary electrophoresis of oligosaccharides. Methods Enzymol. 230:265–280PubMedCrossRefGoogle Scholar
  50. Lísa M and Holčapek M (2008) Triacylglycerols profiling in plant oils important in food industry, dietetics and cosmetics using high-performance liquid chromatography–atmospheric pressure chemical ionization mass spectrometry. J. Chromatogr. A 1198-1199:115–130PubMedCrossRefGoogle Scholar
  51. Lísa M, Lynen F, Holčapek M, and Sandra P (2007) Quantitation of triacylglycerols from plant oils using charged aerosol detection with gradient compensation. J. Chromatogr. A 1176:135–142PubMedCrossRefGoogle Scholar
  52. Liu S, Tian N, Liu Z, Huang J, Li J, and Ferreira JFS (2008) Affordable and sensitive determination of artemisinin in Artemisia annua L. by gas chromatography with electron-capture detection. J. Chromatogr. A 1190:302–306PubMedCrossRefGoogle Scholar
  53. Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L, Tanaka Y, Kitayama M, Yamazaki M, Bailey P, Parr A, Michael AJ, Saito K, and Martin C (2007) Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J. 50:678–695PubMedCrossRefGoogle Scholar
  54. Ma C, Wang H, Lu X, Xu G, and Liu B (2008) Metabolic fingerprinting investigation of Artemisia annua L. in different stages of development by gas chromatography and gas chromatography–mass spectrometry. J. Chromatogr. A 1186:412–419PubMedCrossRefGoogle Scholar
  55. Matsubara N and Terabe S (1996) Micellar electrokinetic chromatography. Methods Enzymol. 270:319–341PubMedCrossRefGoogle Scholar
  56. McDonnell LA and Heeren RMA (2007) Imaging mass spectrometry. Mass Spectrom. Rev. 26: 606–643PubMedCrossRefGoogle Scholar
  57. Mellon FA, Bennett RN, Holst B, and Williamson G (2002) Intact glucosinolate analysis in plant extracts by programmed cone voltage electrospray LC/MS: performance and comparison with LC/MS/MS methods. Anal. Biochem. 306:83–91PubMedCrossRefGoogle Scholar
  58. Novák O, Hauserová E, Amakorová P, Doležal K, and Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69:2214–2224PubMedCrossRefGoogle Scholar
  59. Otieno DO and Shah NP (2007) A comparison of changes in the transformation of isoflavones in soymilk using varying concentrations of exogenous and probiotic-derived endogenous β-glucosidases. J. Appl. Microbiol. 103:601–612PubMedCrossRefGoogle Scholar
  60. Ouattara B, Angenot L, Guissou P, Fondu P, Dubois J, Frédérich M, Jansen O, van Heugen J-C, Wauters J-N, and Tits M (2004) LC/MS/NMR analysis of isomeric divanilloylquinic acids from the root bark of Fagara zanthoxyloides Lam. Phytochemistry 65:1145–1151PubMedCrossRefGoogle Scholar
  61. Pan J, Zhang S, Yan L, Tai J, Xiao Q, Zou K, Zhou Y, and Wu J (2008) Separation of flavanone enantiomers and flavanone glucoside diastereomers from Balanophora involucrata Hook by capillary electrophoresis and reversed-phase high-performance liquid chromatography on a C18 column. J. Chromatogr. A 1185:117–129PubMedCrossRefGoogle Scholar
  62. Papadopoulou K, Melton RE, Leggett M, Daniels MJ, and Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. PNAS 96:12923–12928PubMedCrossRefGoogle Scholar
  63. Pauli GF, Jaki BU, and Lankin DC (2005) Quantitative 1H NMR: development and potential of a method for natural products analysis. J Nat. Prod. 68:133–149PubMedCrossRefGoogle Scholar
  64. Reichelt M, Brown PD, Schneider B, Oldham NJ, Stauber E, Tokuhisa J, Kliebenstein DJ, Mitchell-Olds T, and Gershenzon J (2002) Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59:663–671PubMedCrossRefGoogle Scholar
  65. Rellán-álvarez R, Hernández LE, Abadía J, and álvarez-Fernández A (2006) Direct and simultaneous determination of reduced and oxidized glutathione and homoglutathione by liquid chromatography–electrospray/mass spectrometry in plant tissue extracts. Anal. Biochem. 356:254–264PubMedCrossRefGoogle Scholar
  66. Řezanka T, Nedbalová L, and Sigler K (2008) Identification of very-long-chain polyunsaturated fatty acids from Amphidinium carterae by atmospheric pressure chemical ionization liquid chromatography-mass spectroscopy. Phytochemistry 69:2391–2399PubMedCrossRefGoogle Scholar
  67. Rupasinghe HPV, Jackson C-JC, Poysa V, Di Berardo C, Bewley JD, and Jenkinson J (2003) Soyasapogenol A and B distribution in soybean (Glycine max L. Merr.) in relation to seed physiology, genetic variability, and growing location. J. Agric. Food Chem. 51:5888–5894PubMedCrossRefGoogle Scholar
  68. Sadek PC (2002) The HPLC solvent guide, 2nd ed. Wiley, New YorkGoogle Scholar
  69. Sana TR, Waddell K, and Fischer SM (2008) A sample extraction and chromatographic strategy for increasing LC/MS detection coverage of the erythrocyte metabolome. J. Chromatogr. B. 871:314–321CrossRefGoogle Scholar
  70. Schulze B, Lauchli R, Sonwa MM, Schmidt A, and Boland W (2006) Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Anal. Biochem. 348:269–283PubMedCrossRefGoogle Scholar
  71. Shimoda K, Sato N, Kobayashi T, Hamada H, and Hamada H (2008) Glycosylation of daidzein by the Eucalyptus cell cultures. Phytochemistry 69:2303–2306PubMedCrossRefGoogle Scholar
  72. Skorupinska-Tudek K, Poznanski J, Wojcik J, Bienkowski T, Szostkiewicz I, Zelman-Femiak M, Bajda A, Chojnacki T, Olszowska O, Grunler J, Meyer O, Rohmer M, Danikiewicz W, and Swiezewska E (2008) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of dolichols in plants. J. Biol. Chem. 283:21024–21035PubMedCrossRefGoogle Scholar
  73. Snyder LR, Kirkland JJ, and Glajch JL (1997) Practical HPLC method development, 2nd ed. Wiley, New YorkGoogle Scholar
  74. Sumner LW, Amberg A, Barrett D, et al (2007) Proposed minimum reporting standards for chemical analysis. Metabolomics 3:211–221CrossRefGoogle Scholar
  75. van der Klift EJC, Vivó-Truyols G, Claassen FW, van Holthoon FL, and van Beek TA (2008) Comprehensive two-dimensional liquid chromatography with ultraviolet, evaporative light scattering and mass spectrometric detection of triacylglycerols in corn oil. J. Chromatogr. A 1178:43–55PubMedCrossRefGoogle Scholar
  76. Vogler B and Setzer WN (2006) Characterisation of natural products. In: Cseke LJ, Kirakosyan A, Kaufman PB, Warber S, Duke JA, and Brielmann HL (eds) Natural products from plants. CRC Press, Boca Raton, FL, pp. 319–389CrossRefGoogle Scholar
  77. Vollhardt KPC (1987) Organic chemistry. WH Freeman, New YorkGoogle Scholar
  78. Wade KL, Garrard IJ, and Fahey JW (2007) Improved hydrophilic interaction chromatography method for the identification and quantification of glucosinolates. J. Chromatogr. A 1154:469–472PubMedCrossRefGoogle Scholar
  79. Wang XK, He YZ, and Qian LL (2007) Determination of polyphenol components in herbal medicine by micellar electrokinetic capillary chromatography with Tween 20. Talanta 74:1–6PubMedCrossRefGoogle Scholar
  80. Ward JL, Harris C, Lewis J, Beale MH (2003) Assessment of 1H NMR spectroscopy and multi­variate analysis as a technique for metabolite fingerprinting of Arabidopsis. Phytochemistry 62:949–957PubMedCrossRefGoogle Scholar
  81. Ward JL, Baker JM, and Beale MH (2007) Recent applications of NMR spectroscopy in plant metabolomics. FEBS J. 274:1126–1131PubMedCrossRefGoogle Scholar
  82. Weckwerth W (2007) Metabolomics: methods and protocols. Humana press, Totowa, NJGoogle Scholar
  83. Weckwerth W (2008) Integration of metabolomics and proteomics in molecular plant physiology - coping with the complexity by data-dimensionality reduction. Physiol. Plant. 132:176–189PubMedCrossRefGoogle Scholar
  84. Weckwerth W, Wenzel K, and Fiehn O (2004) Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4:78–83PubMedCrossRefGoogle Scholar
  85. Wouters FS, Verveer PJ, and Bastiaens PIH (2001) Imaging biochemistry inside cells. Trends Cell Biol. 11:203–211PubMedCrossRefGoogle Scholar
  86. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, Watanabe-Takahashi A, Inoue E, and Saito K (2008) Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20:2160–2176PubMedCrossRefGoogle Scholar
  87. Zhang Q, Wang G, Du Y, Zhu L, and Jiye A (2007) GC/MS analysis of the rat urine for metabonomic research. J. Chromatogr. B 854:20–25CrossRefGoogle Scholar
  88. Zhang H, Xie X, Kim M-S, Kornyeyev DA, Holaday S, and Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J. 56:264–273PubMedCrossRefGoogle Scholar
  89. Zhou Y, Han Q-B, Song J-Z, Qiao C-F, and Xu H-X (2008) Characterization of polyprenylated xanthones in Garcinia xipshuanbannaensis using liquid chromatography coupled with electrospray ionization quadrupole time-of-flight tandem mass spectrometry. J. Chromatogr. A 1206:131–139PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Metabolic BiologyJohn Innes CentreNorwichUK

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