Revealing metabolic phenotypes in plants: Inputs from NMR analysis

Biological Reviews of the Cambridge Philosophical Society

Volumn 80, Issue 1, 2005, Pages 27-43

  Ratcliffe, R G ^a   Shachar Hill, Y ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Metabolic flux analysis; Metabolic networks; Metabolite profiling; Metabolomics; Nuclear magnetic resonance spectroscopy; Plant metabolism; Stable isotope labelling

Indexed keywords

ALANINE; AMINO ACID; ASPARTIC ACID; CARBOHYDRATE; CARBON 13; DEUTERIUM; GLUTAMIC ACID; ISOTOPE; LEUCINE; LONG CHAIN FATTY ACID; NITROGEN 15; PHOSPHORUS 31; PROLINE; PROTON; SHORT CHAIN FATTY ACID; STARCH; SUCROSE; VALINE;

CARBON NUCLEAR MAGNETIC RESONANCE; COMPUTER; GENOME; ISOTOPE LABELING; MAGNETIC FIELD; MEASUREMENT; METABOLITE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHENOTYPE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PLANT; PLANT METABOLISM; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SIGNAL NOISE RATIO; STEADY STATE;

BIOTECHNOLOGY; ISOTOPE LABELING; MAGNETIC RESONANCE SPECTROSCOPY; PHENOTYPE; PLANT PHYSIOLOGY; PLANTS;

EID: 13244254993     PISSN: 14647931     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1464793104006530     Document Type: Review

References (103)

1. ALLEN, J., DAVEY, H. M., BROADHURST, D., HEALD, J. K., ROWLAND, J. J., OLIVER, S. G. & KELL, D. B. (2003). High-throughput classification of yeast mutants for functional genomics using metabolic, footprinting. Nature Biotechnology 21, 692-696.
2. AP REES, T. (1987). Compartmentation of plant metabolism. In The Biochemistry of Plants, Vol. 12 (ed. D. D. Davies), pp. 87-115. Academic Press, New York.
3. ARKIN, A., SHEN, P. & Ross, J. (1997). A test case of correlation metric construction of a reaction pathway from measurements. Science 277, 1275-1279.
4. AUBERT, S., CURIEN, G., BLIGNY, R., GOUT, E. & DOUCE, R. (1998). Transport, compartmentation and metabolism of homoserine in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. Plant Physiology 116, 547-557.
5. ALBERT, S., GOUT, E., BLIGNY, R. & DOUCE, R. (1994). Multiple effects of glycerol on plant cell metabolism. Phosphorus-31 nuclear magnetic resonance studies. Journal of Biological Chemistry 269, 21420-21427.
6. BACHER, A., RIEDER, C., EICHINGER, D., ARIGONI, D., FUCHS, G. & EISENREICH, W. (1999). Elucidation of novel biosynthetic pathways and metabolite flux patterns by retrobiosynthetic NMR analysis. FEMS Microbiology Reviews 22, 567-598.
7. BAILEY, N. J. C., COOPER, P., HADFIELD, S. T., LENZ, E. M., LINDON, J. C., NICHOLSON, J. K., STANLEY, P. D., WILSON, I. D., WRIGHT, B. & TAYLOR, S. D. (2000 a). Application of directly coupled HPLC-NMR-MS/MS to the identification of metabolites of 5-trifluoromethylpyridone (2-hydroxy-5- trifluoromethyl-pyridine) in hydroponically grown plants. Journal of Agricultural and Food Chemistry 48, 42-46.
8. 1H NMR spectroscopy and chemometrics. Phytochemistry 62, 851-858.
9. BAILEY, N. J. C., STANLEY, P. D., HADFIELD, S. T., LINDON, J. C. & NICHOLSON, J. K. (2000 b). Mass spectrometrically detected directly coupled high performance liquid chromatography/nuclear magnetic resonance spectroscopy/mass spectrometry for the identification of xenobiotic metabolites in maize plants. Rapid Communications in Mass Spectrometry 14, 679-684.
10. BRINDLE, K. M. (1988). NMR methods for measuring enzyme kinetics in vivo. Progress in Nuclear Magnetic Resonance Spectroscopy 20, 257-293.
11. BUCKHOUT, T. J. & THIMM, O. (2003). Insights into metabolism obtained from microarray analysis. Current Opinion in Plant Biology 6, 288-296.
12. CARROLL, A. D., Fox, G. G., LAURIE, S., PHILLIPS, R., RATCLIFFE, R. G. & STEWART, G. R. (1994). Ammonium assimilation and the role of γ-aminobutyric acid in pH homeostasis in carrot cell suspensions. Plant Physiology 106, 513-520.
13. 1H NMR spectra. Phytochemistry 62, 1009-1017.
14. 31P-NMR spectroscopy. Archives of Microbiology 171, 371-385.
15. 14C-labeled glucose. Journal of Biological Chemistry 270, 13147-13159.
16. EDWARDS, S., NGUYEN, B.-T., DO, B. & ROBERTS, J. K. M. (1998). Contribution of malic enzyme, pyruvate kinase, phosphenolpyruvate carboxylase, and the Krebs cycle to respiration and biosynthesis and to intracellular pH regulation in maize root tips observed by nuclear magnetic resonance and gas-chromatography-mass spectrometry. Plant Physiology 116, 1073-1081.
17. 13C NMR analysis. Biosynthesis of anthraquinones in Rubia tinctorum. Journal of the American Chemical Society 121, 7469-7475.
18. EISEN, M. B. & BROWN, P.O. (1999). DNA arrays for analysis of gene expression. Methods in Enzymology 303, 179-205.
19. FAN, T. W.-M. (1996). Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Progress in Nuclear Magnetic Resonance Spectroscopy 28, 161-219.
20. FAN, T. W.-M., LANE, A. N., SHENKER, M., HARTLEY, J. P., CROWLEY, D. & HIGASHI, R. M. (2001). Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57, 209-221.
21. FELL, D. (1997). Understanding the Control of Metabolism. Portland Press, London.
22. FELL, D. A. & WAGNER, A. (2000). The small world of metabolism. Nature Biotechnology 18, 1121-1122.
23. FERNIE, A. R., ROSCHER, A., RATCLIFFE, R. G. & KRUGER, N. J. (2001). Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212, 250-263.
24. FIEHN, O. (2002). Metabolomics - the link between genotypes and phenotypes. Plant Molecular Biology 48, 155-171.
25. FIEHN, O., KOPKA, J., DÖRMANN, P., ALTMANN, T., TRETHEWEY, R. N. & WILLMITZER, L. (2000). Metabolite profiling for plant functional genomics. Nature Biotechnology 18, 1157-1161.
26. 15N NMR studies of secondary metabolism in transformed root cultures of Datura stramonium and Nicotiana tabacum. Phytochemistry 36, 333-339.
27. FORD, Y. Y., RATCLIFFE, R. G. & ROBINS, R. J. (1998). In vivo nuclear magnetic resonance analysis of polyamine and alkaloid metabolism in transformed root cultures of Datura stramonium L.: evidence for the involvement of putrescine in phytohormone-induced de-differentiation. Planta 205, 205-213.
28. FÖRSTER, J., FAMILI, I., FU, P., PALSSON, B. Ø. & NIELSEN, J. (2003). Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Research 13, 244-253.
29. GLAWISCHNIG, E., GIERL, A., TOMAS, A., BACHER, A. & EISENREICH, W. (2001). Retrobiosynthetic nuclear magnetic resonance analysis of amino acid biosynthesis and intermediary metabolism. Metabolic flux in developing maize kernels. Plant Physiology 125, 1178-1186.
30. GLAWISCHNIG, E., GIERL, A., TOMAS, A., BACHER, A. & EISENREICH, W. (2002). Starch biosynthesis and intermediary metabolism in maize kernels. Quantitative analysis of metabolite flux by nuclear magnetic resonance. Plant Physiology 130, 1717-1727.
31. GOUT, E., AUBERT, S., BLIGNY, R., RÉBEILLÉ, F., NONOMURA, A. R., BENSON, A. A. & DOUCE, R. (2000). Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. Plant Physiology 123, 287-296.
32. 1H NMR spectroscopy using a 1 mm microlitre probe. Analyst 127, 582-584.
33. HANSON, A. D., GAGE, D. A. & SHACHAR-HILL, Y. (2000). Plant one-carbon metabolism and its engineering. Trends in Plant Science 5, 206-213.
34. HARTUNG, W. & RATCLIFFE, R. G. (2002). Utilization of glycine and serine as nitrogen sources in the roots of Zea mays and Chamaegigas intrepidus. Journal of Experimental Botany 53, 2305-2314.
35. HELLERSTEIN, M. K. & NEESE, R. A. (1999). Mass isotopomer distribution analysis at eight years: theoretical, analytic, and experimental considerations. American Journal of Physiology 276, A1146-A1170.
36. HINSE, C., RICHTER, C., PROVENZANI, A. & STÖCKIGT, J. (2003). In vivo monitoring of alkaloid metabolism in hybrid plant cell cultures by 2D cryo-NMR without labelling. Bioorganic and Medicinal Chemistry 11, 3913-3919.
37. JEONG, H., TOMBOR, B., ALBERT, R., OLTVAL, Z. N. & BARABÁSI, A.-L. (2000). The large-scale organization of metabolic networks. Nature 407, 651-654.
38. 13C NMR measurements of hepatocellular tricarboxylic acid cycle flux. Journal of Biological Chemistry 273, 12187-12194.
39. KEELING, P. L., WOOD, J. R., TYSON, R. H. & BRIDGES, I. G. (1988). Starch biosynthesis in developing wheat grain. Evidence against the direct involvement of triose phosphates in the metabolic pathway. Plant Physiology 87, 311-319.
40. KNAPPE, S., FLÜGGE, U. I. & FISCHER, K. (2003). Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiology 131, 1178-1190.
41. KRUGER, N. J. & RATCLIFFE, R. G. (2004). Metabolic organization in plants: a challenge for the metabolic engineer. In Advances in Plant Biochemistry and Molecular Biology, Vol. 1, Bioengineering and Molecular Biology of Plant Pathways (eds. H. J. Bohnert and H. T. Nguyen), in press.
42. KRUGER, N. J., RATCLIFFE, R. G. & ROSCHER, A. (2003). Quantitative approaches for analysing fluxes through plant metabolic networks using NMR and stable isotope labelling. Phytochemistry Reviews 2, 17-30.
43. KRUGER, N. J. & VON SCHAEWEN, A. (2003). The oxidative pentose phosphate pathway : structure and organisation. Current Opinion in Plant Biology 6, 236-246.
44. LACEY, M. E., SUBRAMANIAN, R., OLSON, D. L., WEBB, A. G. & SWEEDLER, J. V. (1999). High resolution NMR spectroscopy from sample volumes from 1 nl to 10 μl. Chemical Reviews 99, 3133-3152.
45. 1H NMR spectroscopy as a tool to detect potential unintended effects following a genetic modification. Journal of Agricultural and Food Chemistry 51, 2447-2456.
46. 1H NMR. Biodegradation 9, 513-525.
47. MARTIN, G. J., MARTIN, M. L. & ZHANG, B.-L. (1992). Site-specific natural isotope fractionation of hydrogen in plant natural products studied by nuclear magnetic resonance. Plant, Cell and Environment 15, 1037-1050.
48. MARX, A., EIKMANNS, B. J., SAHM, H., DE GRAAF, A. A. & EGGELING, L. (1999). Response of the central metabolism in Corynebacterium glutamicum to the use of an NADH-dependent glutamate dehydrogenase. Metabolic Engineering 1, 35-48.
49. 13C isotopic turnover to determine rates of brain metabolism in vivo. Metabolic Engineering 6, 75-84.
50. MCNEIL, S. D., RHODES, D., RUSSELL, B. L., NUCCIO, M. L., SHACHAR-HILL, Y. & HANSON, A. D. (2000). Metabolic modelling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiology 124, 153-162.
51. 15N reverse gradient two-dimensional nuclear magnetic resonance spectroscopy to follow metabolic activity in Nicotiana plumbaginifolia cell suspension cultures. Planta 210, 446-453.
52. MORANDINI, P. & SALAMINI. F. (2003). Plant biotechnology and breeding: allied for years to come. Trends in Plant Science 8, 70-75.
53. MORGAN, D. A. & RHODES, D. (2002). Mathematical modelling of plant metabolic pathways. Metabolic Engineering 4, 80-89.
54. MOUILLON, J.-M., AUBERT, S., BOURGUIGNON, J., GOUT, E., DOUCE, R. & RÉBEILLÉ, F. (1999). Glycine and serine catabolism in non-photosynthetic higher plant cells: their role in C1 metabolism. The Plant Journal 20, 197-205.
55. NEUHAUS, H. E. & EMES, M. J. (2000). Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 51, 111-140.
56. NEWMAN, M. E. J. (2003). The structure and function of complex networks. SIAM Review 45, 167-256.
57. NICHOLSON, J. K., LINDON, J. C. & HOLMES, E. (1999). 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 11, 1181-1189.
58. NOTEBORN, H. P. J. M., LOMMEN, A., VAN DER JAGT, R. C. & WESEMAN, J. M. (2000). Chemical fingerprinting for the evaluation of unintended secondary metabolic changes in transgenic food crops. Journal of Biotechnology 77, 103-114.
59. PALSSON, B. (2000). The challenges of in silico biology. Nature Biotechnology 18, 1147-1150.
60. PALSSON, B. (2002). In silica biology through 'omics'. Nature Biotechnology 20, 649-650.
61. 13C nuclear magnetic resonance detection of interactions of serine hydroxymethyltransferase with C1-tetrahydrofolate synthase and glycine decarboxylase complex activities in Arabidopsis. Plant Physiology 112, 207-216.
62. PRICE, N. D., PAPIN, J. A., SCHILLING, C. H. & PALSSON, B. O. (2003). Genome-scale microbial in silico models: the constraints-based approach. Trends in Biotechnology 21, 162-169.
63. RAAMSDONK, L. M., TEUSINK, B., BROADHURST, D., ZHANG, N. S., HAYES, A., WALSH, M. C., BERDEN, J. A., BRINDLE, K. M., KELL, D. B., ROWLAND, J. J., WESTERHOFF, H. V., VAN DAM, K. & OLIVER, S. G. (2001). A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nature Biotechnology 19, 45-50.
64. RATCLIFFE, R. G. (1994). In vivo NMR studies of higher plants and algae. Advances in Botanical Research 20, 43-123.
65. RATCLIFFE, R. G., ROSCHER, A. & SHACHAR-HILL, Y. (2001). Plant NMR spectroscopy. Progress in Nuclear Magnetic Resonance Spectroscopy 39, 267-300.
66. RATCLIFFE, R. G. & SHACHAR-HILL, Y. (2001). Probing plant metabolism with NMR. Annual Review of Plant Phsiology and Plant Molecular Biology 52, 499-526.
67. REED, J. L. & PALSSON, B. Ø. (2003). Thirteen years of building constraints-based in silico models of Escherichia coli. Journal of Bacteriology 185, 2692-2699.
68. REED, J. L., VO, T. D., SCHILLING, C. H. & PALSSON, B. O. (2003). An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biology 4, R54.
69. ROBERTS, J. K. M. (2000). NMR adventures in the metabolic labyrinth within plants. Trends in Plant Science 5, 30-34.
70. ROBERTS, J. K. M., HOOKS, M. A., MIAULLIS, A. P., EDWARDS, S. & WEBSTER, C. (1992). Contribution of malate and amino acid metabolism to cytoplasmic pH regulation in hypoxic maize root tips studied using nuclear magnetic resonance spectroscopy. Plant Physiology 98, 480-487.
71. ROBINSON, S. A., SLADE, A. P., FOX, G. G., PHILLIPS, R., RATCLIFFE, R. G. & STEVVART, G. R. (1991). The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiology 95, 509-516.
72. ROESSNER, U., LUEDEMANN, A., BRUST, D., FIEHN, O., LINKE, T., WILLMITZER, L. & FERNIE, A. R. (2001 a). Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13, 11-29.
73. ROESSNER, U., WAGNER, C., KOPKA, J., TRETHEWEY, R. N. & WILLMITZER, L. (2000). Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. The Plant Journal 23, 131-142.
74. ROESSNER, U., WILLMITZER, L. & FERNIE, A. R. (2001 b). High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiology 127, 749-764.
75. ROESSNER, U., WILLMITZER, L. & FERNIE, A. R. (2002). Metabolic profiling and biochemical phenotyping of plant systems. Plant Cell Reports 21, 189-196.
76. RONTEIN, D., DIEUAIDE-NOUBHANI, M., DUFOURC, E. J., RAYMOND, P. & ROLIN, D. (2002). The metabolic architecture of plant cells. Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells. Journal of Biological Chemistry 277, 43948-43960.
77. ROSCHER, A., EMSLEY, L., RAYMOND, P. & ROBY, C. (1998). Uni-directional steady state rates of central metabolism enzymes measured simultaneously in a living plant tissue. Journal of Biological Chemistry 273, 25053-25061.
78. ROSCHER, A., KRUGER, N. J. & RATCLIFFE, R. G. (2000). Strategies for metabolic flux analysis in plants using isotope labelling. Journal of Biotechnology 77, 81-102.
79. RUUSKA, S. A., GIRKE, T., BENNING, C. & OHLROGGE, J. B. (2002). Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14, 1191-1206.
80. SAMOILOV, M., ARKIN, A. & Ross, J. (2001). On the deduction of chemical reaction pathways from measurements of time series of concentrations. Chaos 11, 108-114.
81. SAUER, U., LASKO, D. R., FIAUX, J., HOCHULI, M., GLASER, R., SZYPERSKI, T., WÜTHRICH, K. & BAILEY, J. E. (1999). Metabolic flux ratio analysis of genetic and environmental modulations of Escherichia coli central metabolism. Journal of Bacteriology 181, 6679-6688.
82. 15N nuclear magnetic resonance spectroscopy and liquid chromatography-mass spectrometry. Plant Physiology 131, 367-378.
83. SCHLEUCHER, J., VANDERVEER, P. J. & SHARKEY, T. D. (1998). Export of carbon from chloroplasts at night. Plant Physiology 118, 1439-1445.
84. SCHWENDER, J., OHLROGGE, J. B. & SHACHAR-HILL, Y. (2003). A flux model of glycolysis and the oxidative pentose phosphate pathway in developing Brassica napus embryos. Journal of Biological Chemistry 278, 29442-29453.
85. SHACHAR-HILL, Y., PFEFFER, P. E. & GERMANN, M. W. (1996). Following plant metabolism in vivo and in extracts with heteronuclear two-dimensional nuclear magnetic resonance spectroscopy. Analytical Biochemistry 243, 110-118.
86. STELLING, J., KLAMT, S., BETTENBROCK, K., SCHUSTER, S. & GILLES, E. D. (2002). Metabolic network structure determines key aspects of functionality and regulation. Nature 420, 190-193.
87. STYLES, P., SOFFE, N. F., SCOTT, C. A., CRAGG, D. A., Row, F., WHITE, D. J. & WHITE, P. C. J. (1984). A high-resolution NMR probe in which the coil and preamplifier are cooled with liquid-helium. Journal of Magnetic Resonance 60, 397-404.
88. SUMNER, L. W., MENDES, P. & DIXON, R. A. (2003). Plant metabolomics: large-scale phytochemistry in the functional genomics era. Photochemistry 62, 817-836.
89. SWEETLOVE, L. J., LAST, R. L. & FERNIE, A. R. (2003). Predictive metabolic engineering: a goal for systems biology. Plant Physiology 132, 420-425.
90. 13C-labeling of proteinogenic amino acids. An efficient analytical tool to investigate intermediary metabolism. European Journal of Biochemistry 232 433-448.
91. 13C-NMR, MS and metabolite flux balancing in biotechnology research. Quarterly Review of Biophysics 31, 41-106.
92. TER KUILE, B. H. & WESTERHOFF, H. V. (2001). Transcriptome meets metabolome: hierachical and metabolic regulation of the glycolytic pathway. FEBS Letters 500, 169-171.
93. 10N nuclear magnetic resonance. Applied and Environmental Microbiology 65, 1099-1109.
94. URBANCZYK-WOCHNIAK, E., LUEDEMANN, A., KOPKA, J., SELBIG, J., ROESSNER-TUNALI, U., WILLMITZER, L. & FERNIE, A. R. (2003). Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Reports 4, 989-993.
95. 13C-labeling. Metabolic Engineering 3, 151-162.
96. 1H NMR spectroscopy and multivariate analysis as a technique for metabolite fingerprinting of Arabidopsis thaliana. Phytochemistry 62, 949-957.
97. WECKWERTH, W. (2003). Metabolomics in systems biology. Annual Review of Plant Biology 54, 669-689.
98. WECKWERTH, W. & FIEHN, O. (2002). Can we discover novel pathways using metabolomic analysis? Current Opinion in Biotechnology 13, 156-160.
99. WEISE, S. E., WEBER, A. P. M. & SHARKEY, T. D. (2003). Maltose is the major form of carbon exported from the chloroplast at night. Planta 218, 474-482.
100. WIBACK, S. J. & PALSSON, B. O. (2002). Extreme pathway analysis of human red blood cell metabolism. Biophysical Journal 83, 808-818.
101. 13C metabolic flux analysis. Metabolic Engineering 3, 195-206.
102. 13C metabolic flux analysis. Metabolic Engineering 3, 265-283.
103. ZHU, H., BILGIN, M. & SNYDER, M. (2003). Proteomics. Annual Review of Biochemistry 72, 783-812.