Advertisement

Phytochemistry Reviews

, Volume 7, Issue 3, pp 479–497 | Cite as

Plant metabolomics: analytical platforms and integration with functional genomics

  • Jillian M. Hagel
  • Peter J. Facchini
Article

Abstract

As the final downstream product of the genome, the plant metabolome is a highly complex, dynamic assortment of primary and secondary compounds. Although technological platforms to study genomes, transcriptomes and even proteomes are presently available, methods to pursue genuine metabolomics have not yet been developed due to the extensive chemical diversity of plant primary and secondary metabolites. No single analytical method can accurately survey the entire metabolome. However, recent technical, chemometric and bioinformatic advances promise to enhance our global understanding of plant metabolism. Separation-based mass spectrometry (MS) approaches, such as gas (GC) or liquid chromatography (LC)-MS, are relatively inexpensive, highly sensitive and provide excellent identifying capacity. However, Fourier transform-ion cyclotron resonance (FT-ICR)-MS is better suited for rapid, high-throughput applications and is currently the most sensitive method available. Unlike MS-based analyses, nuclear magnetic resonance (NMR) spectroscopy provides a large amount of information regarding molecular structure, and novel software innovations have facilitated the unequivocal identification and absolute quantification of compounds within composite samples. Due to the size and complexity of metabolomics datasets, numerous chemometric methods are used to extract and display systematic variation. Coupled with pattern recognition techniques and plant-specific metabolite databases, broad-scope metabolite analyses have emerged as functional genomics tools for novel gene discovery and functional characterization. In this review, key metabolomics technologies are compared and the applications of FT-ICR-MS and NMR to the study of benzylisoquinoline alkaloid metabolism in opium poppy are discussed.

Keywords

Chemometrics Mass spectrometry Metabolite analysis Nuclear magnetic resonance Opium poppy 

Abbreviations

APCI

Atmospheric pressure chemical ionization

BL

Batch-learning

CE

Capillary electrophoresis

CAS

Chemical Abstract Service

CID

Collision induced dissociation

DIMS

Direct injection mass spectrometry

ESI

Electrospray ionization

EST

Expressed sequence tag

FID

Free induction decay

FT-ICR

Fourier transform-ion cyclotron resonance

GC

Gas chromatography

HCA

Hierarchical cluster analysis

HPLC

High performance liquid chromatography

IMC

Internal mass calibrant

LC

Liquid chromatography

MS

Mass spectrometry

MSn

Tandem mass spectrometry

MALDI

Matrix-assisted laser desorption/ionization

NMR

Nuclear magnetic resonance

OPLS-DA

Orthogonal partial least squares discriminatory analysis

PLS-DA

Partial least squares discriminatory analysis

PDA

Photodiode array detection

PCA

Principle component analysis

SOM

Self-organized mapping

SPE

Solid phase extraction

TOF

Time-of-flight

Notes

Acknowledgements

Program research support is provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to PJF.

References

  1. Abdel-Farid IB, Kim HK, Choi YH et al (2007) Metabolic characterization of Brassica rapa leaves by NMR spectroscopy. J Agric Food Chem (in press).  doi:10.1021/jf071294b
  2. Aharoni A, De Vos RCH, Verhoeven HA et al (2002) Non-targeted metabolome analysis by use of Fourier transform ion cyclotron mass spectrometry. OMICS 6:217–243PubMedGoogle Scholar
  3. Aharoni A, Giri AP, Deuerlein S et al (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884PubMedGoogle Scholar
  4. Aubert S, Pallett KE (2000) Combined use of 13C and 19F NMR to analyze the mode of action and the mechanism of the herbicide isoxaflutole. Plant Physiol Biochem 38:517–523Google Scholar
  5. Bailey NJC, Cooper P, Hadfield ST et al (2000) Application of directly coupled HPLC-NMR-MS/MS to the identification of metabolites of 5-trifluoromethylpyridone (2-hydroxy-5-trifluoromethylpyridine) in hydroponically grown plants. J Agric Food Chem 48:42–46PubMedGoogle Scholar
  6. Baxter CJ, Redestig H, Schauer N et al (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325PubMedGoogle Scholar
  7. Belov ME, Nikolaev EN, Anderson GA et al (2001) Design and performance of an ESI interface for selective external ion accumulation coupled to a Fourier transform ion cyclotron mass spectrometer. Anal Chem 73:253–261PubMedGoogle Scholar
  8. Bishop CM (1996) Neural networks for pattern recognition. Oxford University Press, Oxford UKGoogle Scholar
  9. Broeckling CD, Reddy IR, Duran AL et al (2006) MET-IDEA: data extraction tool for mass spectrometry-based metabolomics. Anal Chem 78:4334–4341PubMedGoogle Scholar
  10. Brown SC, Kruppa G, Dasseux J-L (2005) Metabolomics applications of FT-ICR mass spectrometry. Mass Spectrom Rev 24:223–231PubMedGoogle Scholar
  11. Budruss J, Herzog H (1980) Coupling of chromatography and NMR. 3-Study of flowing gas chromatographic fractions by proton magnetic resonance. Org Magn Reson 15:211–213Google Scholar
  12. Carrari F, Baxter C, Usadel B et al (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol 142:1380–1396PubMedGoogle Scholar
  13. Catchpole GS, Beckmann M, Enot DP et al (2005) Hierarchical metabolomics demonstrates substantial compositional similarity between genetically modified and conventional potato crops. Proc Natl Acad Sci USA 102:14458–14462PubMedGoogle Scholar
  14. Cech NB, Enke CG (2001) Practical implications of some recent studies in electrospray ionization fundamentals. Mass Spectrom Rev 20:362–387PubMedGoogle Scholar
  15. Chen F, Tholl D, D’Auria JC et al (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494PubMedGoogle Scholar
  16. Choi HK, Choi YH, Verberne M et al (2004a) Metabolic fingerprinting of wild type and transgenic tobacco plants by 1H NMR and multivariate analysis technique. Phytochemistry 65:857–864PubMedGoogle Scholar
  17. Choi YH, Kim HK, Hazekamp A et al (2004b) Metabolic differentiation of Cannabis sativa cultivars using 1H NMR spectroscopy and principle component analysis. J Nat Prod 67:953–957PubMedGoogle Scholar
  18. Choi YH, Tapias EC, Kim HK et al (2004c) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol 135:2398–2410PubMedGoogle Scholar
  19. Choi YH, Sertic S, Kim HK et al (2005) Classification of Ilex species based on metabolomic fingerprinting using nuclear magnetic resonance and multivariate data analysis. J Agric Food Chem 53:1237–1245PubMedGoogle Scholar
  20. Choi YH, Kim HK, Linthorst HJM et al (2006) NMR metabolomics to revisit the Tobacco Mosaic Virus infection in Nicotiana tabacum leaves. J Nat Prod 69:742–748PubMedGoogle Scholar
  21. Chrisophoridou S, Dais P, Tseng L-H et al (2005) Separation and identification of phenolic compounds in olive oil by coupling high-performance liquid chromatography with post-column solid-phase extraction to nuclear magnetic resonance spectroscopy (LC-SPE-NMR). J Agric Food Chem 53:4667–4679Google Scholar
  22. Comisarow MB, Marshall AG (1974) Fourier transform ion cyclotron resonance mass spectroscopy. Chem Phys Lett 25:282–283Google Scholar
  23. Defernez M, Colquhoun IJ (2003) Factors affecting the robustness of metabolite fingerprinting using 1H NMR spectra. Phytochemistry 62:1009–1017PubMedGoogle Scholar
  24. De Hoffmann E, Stroobant V (2002) Mass spectrometry. Principles and Applications, 2nd ed. WileyGoogle Scholar
  25. Delatte T, Trevisan M, Parker ML et al (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41:815–830PubMedGoogle Scholar
  26. Dettmer K, Aronov PA, Hammock BD (2007) Mass spectrometry-based metabolomics. Mass Spectrom Rev 26:51–78PubMedGoogle Scholar
  27. Drozd J (1981) Chemical derivatization in gas chromatography. Elsevier, AmsterdamGoogle Scholar
  28. Dunn WB, Ellis DI (2005) Metabolomics: current analytical platforms and methodologies. Trends Anal Chem 24:285–294Google Scholar
  29. Dunn WB, Bailey NJC, Johnson HE (2005) Measuring the metabolome: current analytical technologies. Analyst 130:606–625PubMedGoogle Scholar
  30. El-Deredy W (1997) Pattern recognition approaches in biomedical and clinical magnetic resonance spectroscopy: a review. NMR Biomed 10:99–124PubMedGoogle Scholar
  31. Eriksson L, Antti H, Gottfries J et al (2004) Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabolomics (gpm). Anal Bioanal Chem 380:419–429PubMedGoogle Scholar
  32. Exarchou V, Godejohann M, van Beek TA et al (2003) LC-UV-solid-phase-extraction-NMR-MS combined with a cryogenic flow probe and its application to the identification of compounds present in Greek oregano. Anal Chem 75:6288–6294PubMedGoogle Scholar
  33. Facchini PJ, De Luca V (1995) Phloem-specific expression of tyrosine/dopa decarboxylase genes and the biosynthesis of isoquinoline alkaloids in opium poppy. Plant Cell 7:1811–1821PubMedGoogle Scholar
  34. Facchini PJ, Johnson AG, Poupart J, De Luca V (1996) Uncoupled defense gene expression and antimicrobial alkaloid accumulation in elicited opium poppy cell cultures. Plant Physiol 111:687–697PubMedGoogle Scholar
  35. Fiamegos Y, Nanos CG, Vervoort J et al (2004) Analytical procedure for the in-vial derivatization–extraction of phenolic acids and flavonoids in methanolic and aqueous plant extracts followed by gas chromatography with mass-selective detection. J Chromatogr A 1041:11–18PubMedGoogle Scholar
  36. Fraser PD, Enfissi EMA, Goodfellow M et al (2007) Metabolite profiling of plant carotenoids using the matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Plant J 49:552–564PubMedGoogle Scholar
  37. Frédérich M, Choi YH, Angenot L et al (2004) Metabolomic analysis of Strychnos nux-vomica, Strychnos icaja and Strychnos ignatii extracts by 1H nuclear magnetic resonance spectrometry and multivariate analysis techniques. Phytochemistry 65:1993–2001PubMedGoogle Scholar
  38. Forshed J, Torgrip RJ, Aberg KM et al (2005) A comparison of methods for alignment of NMR peaks in the context of cluster analysis. J Pharm Biomed Anal 38:824–832PubMedGoogle Scholar
  39. Frick S, Kramell R, Schmidt J et al (2005) Comparative qualitative and quantitative determination of alkaloids in narcotic and condiment Papaver somniferum cultivars. J Nat Prod 68:666–673PubMedGoogle Scholar
  40. Glish GL, Vachet RW (2000) The basics of mass spectrometry in the twenty-first century. Nat Rev Drug Discov 2:140–150Google Scholar
  41. Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic Press, LondonGoogle Scholar
  42. Halket JM, Przyborowska A, Stein SE et al (1999) Deconvolution gas chromatography/mass spectrometry of urinary organic acids—potential for pattern recognition and automated identification of metabolic disorders. Rapid Commun Mass Spectrom 13:279–284PubMedGoogle Scholar
  43. Halket JM, Waterman D, Przyborowska AM et al (2005) Chemical derivatisation and mass spectral libraries in metabolic profiling by GC/MS and LC/MS/MS. J Exp Bot 56:219–243PubMedGoogle Scholar
  44. Hall RD (2006) Plant metabolomics: from holistic hope, to hype, to hot topic. New Phytol 169:453–468PubMedGoogle Scholar
  45. Harrigan GG, Goodacre R (2003) Metabolic profiling: its role in biomarker discovery and gene function analysis. Kluwer Academic PublishersGoogle Scholar
  46. Hendrawati O, Yao Q, Kim HK et al (2006) Metabolic differentiation of Arabidopsis treated with methyl jasmonate using nuclear magnetic resonance spectroscopy. Plant Sci 170:1118–1124Google Scholar
  47. Hirai MY, Yano M, Goodenowe DB et al (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10205–10210PubMedGoogle Scholar
  48. Hirai MY, Klein M, Fujikawa Y et al (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. Proc Natl Acad Sci USA 280:25590–25595Google Scholar
  49. Holmes E, Antii H (2002) Chemometric contributions to the evolution of metabolomics: mathematical solutions to characterizing and interpreting complex biological NMR spectra. Analyst 127:1549–1557PubMedGoogle Scholar
  50. Hotelling H (1935) The most predictable criterion. J Educ Psychol 26:139–142Google Scholar
  51. Hu Q, Noll RJ, Li H et al (2005) The Orbitrap: the new mass analyzer. J Mass Spectrom 40: 430–443PubMedGoogle Scholar
  52. Hughey CA, Rodgers RP, Marshall AG (2002) Resolution of 11,000 compositionally distinct components in a single electrospray ionization Fourier transform ion cyclotron resonance mass spectrum of crude oil. Anal Chem 74:3877–3886Google Scholar
  53. Jacobson B, Anderson WA, Arnold JT (1954) Influence of deoxyribonucleic acid on the intermolecular structure of water. Nature 17:772–773Google Scholar
  54. Johnson KL, Mason CJ, Muddiman DC (2004) Analysis of the low molecular weight fraction of serum by LC-dual ESI-FT-ICR mass spectrometry: precision of retention time, mass, and ion abundance. Anal Chem 76:5097PubMedGoogle Scholar
  55. Kaplan F, Kopka J, Sung DY et al (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981PubMedGoogle Scholar
  56. Katajamma M, Orešič M (2007) Data processing for mass spectrometry-based metabolomics. J Chromatogr A 1158:318–328Google Scholar
  57. Kikuchi J, Shinozaki K, Hirayama T (2004) Stable isotope labeling of Arabidopsis thaliana for and NMR-based metabolomics approach. Plant Cell Physiol 45:1099–1104PubMedGoogle Scholar
  58. Kim HK, Choi YH, Erkelens C et al (2005) Metabolic fingerprinting of Ephedra species using 1H-NMR spectroscopy and principle component analysis. Chem Pharm Bull 53:105–109PubMedGoogle Scholar
  59. Krishnan P, Kruger NJ, Ratcliffe RG (2005) Metabolite fingerprinting and profiling in plants using NMR. J Exp Bot 56:255–265PubMedGoogle Scholar
  60. Kruger NJ, Ratcliffe RG, Roscher A (2003) Quantitative approaches for analyzing fluxes through plant metabolic networks using NMR and stable isotope labeling. Phytochem Rev 2:17–30Google Scholar
  61. Last RL, Jones AD, Shachar-Hill Y (2007) Towards the plant metabolome and beyond. Nat Rev Mol Cell Biol 8:167–174PubMedGoogle Scholar
  62. Lavine B, Workman JJ Jr (2004) Chemometrics. Anal Chem 76:3365–3371PubMedGoogle Scholar
  63. Liang Y-S, Choi YH, Kim HK, Linthorst HJM, Verpoorte R (2006a) Metabolomic analysis of methyl jasmonate treated Brassica rapa leaves by 2-dimensional NMR spectroscopy. Phytochemistry 67:2503–2511PubMedGoogle Scholar
  64. Liang Y-S, Kim HK, Lefeber AWM et al (2006b) Identification of phenylpropanoids in methyl jasmonate treated Brassica rapa leaves using two-dimensional nuclear magnetic resonance spectroscopy. J Chromatogr A 1112:148–155PubMedGoogle Scholar
  65. Lindon JC, Holmes E, Nicholson JK (2001) Pattern recognition methods and applications in biological magnetic resonance. Prog Nucl Magn Reson Spectrosc 39:1–40Google Scholar
  66. Liscombe DK, Facchini PJ (2007) Molecular cloning and characterization of tetrahydroprotoberberine cis-N-methyltransferase, an enzyme involved in alkaloid biosynthesis in opium poppy. J Biol Chem 282:14741–14751PubMedGoogle Scholar
  67. Liscombe DK, MacLeod BP, Loukanina N, Nandi OI, Facchini PJ (2005) Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 66:1374–1393PubMedGoogle Scholar
  68. Manetti C, Bianchetti C, Bizzarri M et al (2004) NMR-based metabolomic study of transgenic maize. Phytochemistry 65:3187–3198PubMedGoogle Scholar
  69. Mattoo AK, Sobolev AP, Neelam A et al (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen–carbon interactions. Plant Physiol 142:1759–1770PubMedGoogle Scholar
  70. Messerli G, Nia VP, Trevisan M et al (2007) Rapid classification of phenotypic mutants of Arabidopsis via metabolite fingerprinting. Plant Physiol 143:1484–1492PubMedGoogle Scholar
  71. Moco S, Bino RJ, Vorst O et al (2006) A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiol 141:1205–1218PubMedGoogle Scholar
  72. Moing A, Maucourt M, Renaud C et al (2004) Quantitative metabolic profiling by 1-dimensional 1H-NMR analyses: application to plant genetics and functional genomics. Funct Plant Biol 31:889–902Google Scholar
  73. Monton MRN, Soga T (2007) Metabolome analysis by capillary electrophoresis–mass spectrometry. J Chromatogr A (in press).  doi:10.1016/j.chroma.2007.02.065
  74. Munger R, Glass ADM, Goodenow DB (2005) Metabolite fingerprinting in transgenic Nicotiana tabacum altered by the Escherichia coli glutamate dehydrogenase gene. J Biomed Biotechnol 2:198–214Google Scholar
  75. Nakamura Y, Kimura A, Saga H et al (2007) Differential metabolomics unraveling light/dark regulation of metabolic activities in Arabidopsis cell culture. Planta (in press).  doi:10.1007/s00425-007-0594-z
  76. Oikawa A, Nakamura Y, Ogura T et al (2006) Clarification of pathway-specific inhibition by Fourier transform ion cyclotron resonance/mass spectrometry-based metabolomic phenotyping studies. Plant Physiol 142:398–413PubMedGoogle Scholar
  77. Oksman-Caldentey K-M, Inzé D (2004) Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends Plant Sci 9:433–440PubMedGoogle Scholar
  78. Ounaroon A, Decker G, Schmidt J, Lottspeich F, Kutchan TM (2003) (R,S)-Reticuline 7-O-methyltransferase and (R,S)-norcoclaurine 6-O-methyltransferase of Papaver somniferum – cDNA cloning and characterization of methyl transfer enzymes of alkaloid biosynthesis in opium poppy. Plant J 36:808–819PubMedGoogle Scholar
  79. Pan Z, Raftery D (2007) Comparing and combining NMR spectroscopy and mass spectrometry in metabolomics. Anal Bioanal Chem 387:525–527PubMedGoogle Scholar
  80. Pierce KM, Hoggard JC, Mohler RE et al (2007) Recent advancements in comprehensive two-dimensional separations with chemometrics. J Chromatogr A (in press).  doi:10.1080/10826070600574762
  81. Provart NJ, McCourt P (2004) Systems approaches to understanding cell signaling and gene regulation. Curr Opin Plant Biol 7:605–609PubMedGoogle Scholar
  82. Pukalskas A, van Beek TA, de Waard P (2005) Development of a triple hyphenated HPLC-radical scavenging detection-DAD-SPE-NMR system for the rapid identification of antioxidants in complex plant extracts. J Chromatogr A 1074:81–88PubMedGoogle Scholar
  83. Rabiner LR, Juang BH (1986) An Introduction to Hidden Markov Models. IEEE ASSP Mag 3:4–16Google Scholar
  84. Ratcliffe RG (1994) In vivo NMR studies of higher plants and algae. Adv Bot Res 20:43–123CrossRefGoogle Scholar
  85. Ratcliffe RG, Shachar-Hill Y (2001) Probing plant metabolism with NMR. Annu Rev Plant Phys 52:499–526Google Scholar
  86. Ratcliffe RG, Shachar-Hill Y (2005) Revealing metabolic phenotypes in plants: inputs from NMR analysis. Biol Rev 80:27–83PubMedGoogle Scholar
  87. Rhee SY, Dickerson J, Xu D (2006) Bioinformatics and its applications in plant biology. Annu Rev Plant Biol 57:335–360PubMedGoogle Scholar
  88. Ryan D, Robards K (2006) Metabolomics: the greatest omics of them all? Anal Chem 78:7954–7958PubMedGoogle Scholar
  89. Schauer N, Fernie AR (2006) Plant metabolomics: towards biological function and mechanism. Trends Plant Sci 11:508–516PubMedGoogle Scholar
  90. Schmidt J, Boettcher C, Kuhnt C et al (2007) Poppy alkaloid profiling by electrospray tandem mass spectrometry and electrospray FT-ICR mass spectrometry after [ring-13C6]-tyramine feeding. Phytochemistry 68:189–202PubMedGoogle Scholar
  91. Seger C, Sturm S (2007) Analytical aspects of plant metabolite profiling platforms: current standings and future aims. J Proteome Res 6:480–497PubMedGoogle Scholar
  92. Shellie RA (2005) Comprehensive two-dimensional gas chromatography-mass spectrometry and its use in high-resolution metabolomics. Aust J Chem 58:619–619Google Scholar
  93. Shinbo Y, Nakamura Y, Altaf-Ul-Amin M et al (2006) KNApSAcK: a comprehensive species-metabolite relationship database. Biotechnol Agr For 57:166–181Google Scholar
  94. Shulaev V (2006) Metabolomics technology and bioinformatics. Brief Bioinform 7:128–139PubMedGoogle Scholar
  95. Sivia DS (1996) Data analysis: a Bayesian tutorial. Oxford University Press, OxfordGoogle Scholar
  96. Smith CA, Want EJ, O’Maille G et al (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching and identification. Anal Chem 78:779–787PubMedGoogle Scholar
  97. Stoyanova R, Nicholls AW, Nicholson JK et al (2004) Automatic alignment of individual peaks in large high-resolution spectral data sets. J Magn Reson 170:329–335PubMedGoogle Scholar
  98. Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62:817–836PubMedGoogle Scholar
  99. Thureson-Klein A (1970) Observations on the development and fine structure of the articulated laticifers of Papaver somniferum. Ann Bot 34:751–759Google Scholar
  100. Tian C, Chikayama E, Tsuboi Y et al (2007) Top-down phenomics of Arabidopsis thaliana—metabolic profiling by one- and two-dimensional nuclear magnetic resonance spectroscopy and transcriptome analysis of albino mutants. J Biol Chem 282:18532–18541PubMedGoogle Scholar
  101. Tikunov Y, Lommen A, de Vos CH et al (2005) A novel approach for nontargeted data analysis for metabolomics. Large-scale profiling of tomato fruit volatiles. Plant Physiol 139:1125–1137PubMedGoogle Scholar
  102. 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. Plant J 42:218–235PubMedGoogle Scholar
  103. Trygg J, Holmes E, Lundstedt T (2007) Chemometrics in metabolomics. J Proteome Res 6:469–479PubMedGoogle Scholar
  104. Verpoorte R, Choi YH, Kim HK (2007) NMR-based metabolomics at work in phytochemistry. Phytochem Rev 6:3–14Google Scholar
  105. Viant MR (2003) Impoved methods for the acquisition and interpretation of NMR metabolomic data. Biochem Bioph Res Commun 310:943–948Google Scholar
  106. Wang YS, Shi SD-H, Hendrickson CL et al (2000) Mass-selective ion accumulation and fragmentation in a linear octopole ion trap external to a Fourier transform ion cyclotron resonance mass spectrometer. Int J Mass Spectrom 198:113–120Google Scholar
  107. Ward JL, Beale MH (2006) NMR spectroscopy in plant metabolomics. Biotechnol Agr For 57:81–91Google Scholar
  108. Weckwerth W (2003) Metabolomics in systems biology. Ann Rev Plant Biol 54:669–689Google Scholar
  109. Weljie AM, Newton J, Mercier P et al (2006) Targeted profiling: quantitative analysis of 1H NMR metabolomics data. Anal Chem 78:4430–4442PubMedGoogle Scholar
  110. Widarto HR, Van Der Meijden E, Lefeber AWM et al (2006) Metabolomic differentiation of Brassica rapa following herbivory by different insect instars using two-dimensional nuclear magnetic resonance spectroscopy. J Chem Ecol 32:2417–2428PubMedGoogle Scholar
  111. Wu Z, Rodgers RP, Marshall AG (2004) Characterization of vegetable oils: detailed compositional fingerprints derived from electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. J Agr Food Chem 52:5322–5328Google Scholar
  112. Ziegler J, Voigtländer S, Schmidt J et al (2006) Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis. Plant J 48:177–192PubMedGoogle Scholar
  113. Zulak KG, Cornish A, Daskalchuk TE et al (2007) Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta 225:1085–1106PubMedGoogle Scholar
  114. Zulak KG, Weljie A, Vogel HJ, Facchini PJ (2008) Quantitative 1H-NMR metabolomics reveals extensive metabolic reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures. BMC Plant Biol (in press)Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of CalgaryCalgaryCanada

Personalised recommendations