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PMID: 15466217 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Quantification of compartmented metabolic fluxes in developing soybean embryos by employing biosynthetically directed fractional (13)C labeling, two-dimensional [(13)C, (1)H] nuclear magnetic resonance, and comprehensive isotopomer balancing.

Plant physiology ·Vol. 136 ·No. 2 ·2004-10-00 ·Pages 3043-57

Sriram G, Fulton DB, Iyer VV, Peterson JM, Zhou R, Westgate ME, Spalding MH, Shanks JV

Abstract

Metabolic flux quantification in plants is instrumental in the detailed understanding of metabolism but is difficult to perform on a systemic level. Toward this aim, we report the development and application of a computer-aided metabolic flux analysis tool that enables the concurrent evaluation of fluxes in several primary metabolic pathways. Labeling experiments were performed by feeding a mixture of U-(13)C Suc, naturally abundant Suc, and Gln to developing soybean (Glycine max) embryos. Two-dimensional [(13)C, (1)H] NMR spectra of seed storage protein and starch hydrolysates were acquired and yielded a labeling data set consisting of 155 (13)C isotopomer abundances. We developed a computer program to automatically calculate fluxes from this data. This program accepts a user-defined metabolic network model and incorporates recent mathematical advances toward accurate and efficient flux evaluation. Fluxes were calculated and statistical analysis was performed to obtain sds. A high flux was found through the oxidative pentose phosphate pathway (19.99 +/- 4.39 micromol d(-1) cotyledon(-1), or 104.2 carbon mol +/- 23.0 carbon mol per 100 carbon mol of Suc uptake). Separate transketolase and transaldolase fluxes could be distinguished in the plastid and the cytosol, and those in the plastid were found to be at least 6-fold higher. The backflux from triose to hexose phosphate was also found to be substantial in the plastid (21.72 +/- 5.00 micromol d(-1) cotyledon(-1), or 113.2 carbon mol +/-26.0 carbon mol per 100 carbon mol of Suc uptake). Forward and backward directions of anaplerotic fluxes could be distinguished. The glyoxylate shunt flux was found to be negligible. Such a generic flux analysis tool can serve as a quantitative tool for metabolic studies and phenotype comparisons and can be extended to other plant systems.

MeSH Terms
Carbon/metabolism Carbon Isotopes Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Isotope Labeling Magnetic Resonance Spectroscopy Plant Leaves/embryology,metabolism Plant Proteins/metabolism Seeds/metabolism Soybeans/embryology,metabolism
Chemicals
Carbon Isotopes Plant Proteins Carbon
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Sriram Ganesh
Department of Chemical Engineering , Iowa State University, Ames, Iowa 50011, USA.
Fulton D Bruce
Iyer Vidya V
Peterson Joan Marie
Zhou Ruilian
Westgate Mark E
Spalding Martin H
Shanks Jacqueline V
References (50)
50 references, click to expand
  1. THE SHIKIMATE PATHWAY.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:473-503 PMID: 15012217
  2. Towards a modeling infrastructure for studying plant cells.
    Plant Physiol. 2003 Jun;132(2):410-4 PMID: 12805570
  3. Metabolic isotopomer labeling systems. Part I: global dynamic behavior.
    Math Biosci. 2001 Feb;169(2):173-205 PMID: 11166321
  4. Predictive metabolic engineering: a goal for systems biology.
    Plant Physiol. 2003 Jun;132(2):420-5 PMID: 12805573
  5. Manipulating PEPC levels in plants.
    J Exp Bot. 2002 Sep;53(376):1837-45 PMID: 12177121
  6. Quantification of compartmented metabolic fluxes in maize root tips using isotope distribution from 13C- or 14C-labeled glucose.
    J Biol Chem. 1995 Jun 2;270(22):13147-59 PMID: 7768910
  7. Nuclear magnetic resonance and plant metabolic engineering.
    Metab Eng. 2002 Jan;4(1):90-7 PMID: 11800578
  8. Subcellular localization of sugar nucleotide synthetases.
    J Biol Chem. 1980 Oct 10;255(19):9225-9 PMID: 6251080
  9. Bidirectional reaction steps in metabolic networks: III. Explicit solution and analysis of isotopomer labeling systems.
    Biotechnol Bioeng. 1999;66(2):69-85 PMID: 10567066
  10. Auxin biosynthesis in maize kernels.
    Plant Physiol. 2000 Jul;123(3):1109-19 PMID: 10889260
  11. 13C metabolic flux analysis.
    Metab Eng. 2001 Jul;3(3):195-206 PMID: 11461141
  12. Probing in vivo metabolism by stable isotope labeling of storage lipids and proteins in developing Brassica napus embryos.
    Plant Physiol. 2002 Sep;130(1):347-61 PMID: 12226514
  13. THE MOLECULAR-GENETICS OF NITROGEN ASSIMILATION INTO AMINO ACIDS IN HIGHER PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:569-593 PMID: 15012301
  14. Identification and characterization of GONST1, a golgi-localized GDP-mannose transporter in Arabidopsis.
    Plant Cell. 2001 Oct;13(10):2283-95 PMID: 11595802
  15. Innovations in generation and analysis of 2D [(13)C,(1)H] COSY NMR spectra for metabolic flux analysis purposes.
    Metab Eng. 2001 Oct;3(4):322-43 PMID: 11676568
  16. NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways.
    FEBS Lett. 2001 Feb 9;490(1-2):1-6 PMID: 11172800
  17. Metabolic fluxes and metabolic engineering.
    Metab Eng. 1999 Jan;1(1):1-11 PMID: 10935750
  18. High-throughput phenomics: experimental methods for mapping fluxomes.
    Curr Opin Biotechnol. 2004 Feb;15(1):58-63 PMID: 15102468
  19. Biosynthetically directed fractional 13C-labeling of proteinogenic amino acids. An efficient analytical tool to investigate intermediary metabolism.
    Eur J Biochem. 1995 Sep 1;232(2):433-48 PMID: 7556192
  20. Starch biosynthesis and intermediary metabolism in maize kernels. Quantitative analysis of metabolite flux by nuclear magnetic resonance.
    Plant Physiol. 2002 Dec;130(4):1717-27 PMID: 12481054
  21. Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch.
    Biochem J. 1990 Oct 15;271(2):467-72 PMID: 2173563
  22. Ultra-high-resolved HSQC spectra of multiple- 13C-labeled biofluids.
    J Magn Reson. 1997 Mar;125(1):216-9 PMID: 9245385
  23. The isocitrate lyase gene of cucumber: isolation, characterisation and expression in cotyledons following seed germination.
    Plant Mol Biol. 1995 Feb;27(3):487-97 PMID: 7894014
  24. NMR View: A computer program for the visualization and analysis of NMR data.
    J Biomol NMR. 1994 Sep;4(5):603-14 PMID: 22911360
  25. The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression.
    Plant Cell. 1999 Sep;11(9):1609-22 PMID: 10488230
  26. Glutamate synthesis in barley roots: the role of the plastidic glucose-6-phosphate dehydrogenase.
    Planta. 2003 Feb;216(4):639-47 PMID: 12569406
  27. Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato.
    Plant Physiol. 2003 Sep;133(1):47-62 PMID: 12970474
  28. Improvements in metabolic flux analysis using carbon bond labeling experiments: bondomer balancing and Boolean function mapping.
    Metab Eng. 2004 Apr;6(2):116-32 PMID: 15113565
  29. PROBING PLANT METABOLISM WITH NMR.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:499-526 PMID: 11337407
  30. Subcellular Compartmentation of the 4-Aminobutyrate Shunt in Protoplasts from Developing Soybean Cotyledons.
    Plant Physiol. 1995 May;108(1):99-103 PMID: 12228455
  31. Sugar-nucleotide-binding and autoglycosylating polypeptide(s) from nasturtium fruit: biochemical capacities and potential functions.
    Biochem J. 2000 May 1;347 Pt 3:857-64 PMID: 10769192
  32. A flux model of glycolysis and the oxidative pentosephosphate pathway in developing Brassica napus embryos.
    J Biol Chem. 2003 Aug 8;278(32):29442-53 PMID: 12759349
  33. A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter.
    Plant Cell. 1997 Mar;9(3):453-62 PMID: 9090886
  34. The biosynthetic pathway of vitamin C in higher plants.
    Nature. 1998 May 28;393(6683):365-9 PMID: 9620799
  35. Sucrose uptake by developing soybean cotyledons.
    Plant Physiol. 1981 Sep;68(3):693-8 PMID: 16661981
  36. PHOSPHOENOLPYRUVATE CARBOXYLASE: A Ubiquitous, Highly Regulated Enzyme in Plants.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:273-298 PMID: 15012290
  37. Attacking complex problems with the power of systems biology.
    Plant Physiol. 2003 Jun;132(2):417-9 PMID: 12805572
  38. The oxidative pentose phosphate pathway: structure and organisation.
    Curr Opin Plant Biol. 2003 Jun;6(3):236-46 PMID: 12753973
  39. The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris. Structural homologies of genes and proteins.
    J Biol Chem. 1986 Jul 15;261(20):9228-38 PMID: 3013879
  40. Retrobiosynthetic nuclear magnetic resonance analysis of amino acid biosynthesis and intermediary metabolism. Metabolic flux in developing maize kernels.
    Plant Physiol. 2001 Mar;125(3):1178-86 PMID: 11244098
  41. Achieving the in silico plant. Systems biology and the future of plant biological research.
    Plant Physiol. 2003 Jun;132(2):404-9 PMID: 12822566
  42. The metabolic architecture of plant cells. Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells.
    J Biol Chem. 2002 Nov 15;277(46):43948-60 PMID: 12226084
  43. Quantification of intracellular metabolic fluxes from fractional enrichment and 13C-13C coupling constraints on the isotopomer distribution in labeled biomass components.
    Metab Eng. 1999 Apr;1(2):166-79 PMID: 10935929
  44. Isozymes of the glycolytic and pentose-phosphate pathways in storage tissues of different oilseeds.
    Planta. 1980 Oct;149(5):476-9 PMID: 24306476
  45. Strategies for metabolic flux analysis in plants using isotope labelling.
    J Biotechnol. 2000 Jan 28;77(1):81-102 PMID: 10674216
  46. The transketolase gene family of the resurrection plant Craterostigma plantagineum: differential expression during the rehydration phase.
    EMBO J. 1995 Feb 1;14(3):610-8 PMID: 7859749
  47. Metabolic isotopomer labeling systems. Part II: structural flux identifiability analysis.
    Math Biosci. 2003 Jun;183(2):175-214 PMID: 12711410
  48. 13C-NMR, MS and metabolic flux balancing in biotechnology research.
    Q Rev Biophys. 1998 Feb;31(1):41-106 PMID: 9717198
  49. The Impact of Chlorophyll-Retention Mutations, d1d2 and cyt-G1, during Embryogeny in Soybean.
    Plant Physiol. 1995 Jan;107(1):253-262 PMID: 12228359
  50. The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants.
    Plant Physiol. 2002 Feb;128(2):512-22 PMID: 11842155
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2004-10-00
Epub
2004-00-01
Pages
3043-57
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC523366
Subset
IM
Corrections
ErratumIn
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