Inference and prediction of metabolic network fluxes

Plant Physiology

Volumn 169, Issue 3, 2015, Pages 1443-1455

  Nikoloski, Zoran ^a   Perez Storey, Richard ^b   Sweetlove, Lee J ^b  

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

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT PROTEIN;

ENERGY METABOLISM; GENETICS; ISOTOPE LABELING; METABOLIC FLUX ANALYSIS; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; PROCEDURES; SIGNAL TRANSDUCTION;

ENERGY METABOLISM; ISOTOPE LABELING; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; PHOTOSYNTHESIS; PLANT PROTEINS; PLANTS; SIGNAL TRANSDUCTION;

EID: 84946199497     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01082     Document Type: Article

References (97)

1. Agren R, Bordel S, Mardinoglu A, Pornputtapong N, Nookaew I, Nielsen J (2012) Reconstruction of genome-scale active metabolic networks for 69 human cell types and 16 cancer types using INIT. PLoS Comput Biol 8: e1002518
2. Agren R, Mardinoglu A, Asplund A, Kampf C, Uhlen M, Nielsen J (2014) Identification of anticancer drugs for hepatocellular carcinoma through personalized genome-scale metabolic modeling. Mol Syst Biol 10: 721
3. Allen DK, Libourel IGL, Shachar-Hill Y (2009a) Metabolic flux analysis in plants: coping with complexity. Plant Cell Environ 32: 1241–1257
4. Allen DK, Ohlrogge JB, Shachar-Hill Y (2009b) The role of light in soybean seed filling metabolism. Plant J 58: 220–234
5. Allen DK, Young JD (2013) Carbon and nitrogen provisions alter the metabolic flux in developing soybean embryos. Plant Physiol 161: 1458–1475
6. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8: 15–19
7. Alonso AP, Goffman FD, Ohlrogge JB, Shachar-Hill Y (2007) Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos. Plant J 52: 296–308
8. Alonso AP, Val DL, Shachar-Hill Y (2011) Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering. Metab Eng 13: 96–107
9. Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann Bot (Lond) 86: 1–20
10. Arnold A, Nikoloski Z (2014) Bottom-up metabolic reconstruction of Arabidopsis and its application to determining the metabolic costs of enzyme production. Plant Physiol 165: 1380–1391
11. Baghalian K, Hajirezaei MR, Schreiber F (2014) Plant metabolic modeling: achieving new insight into metabolism and metabolic engineering. Plant Cell 26: 3847–3866
12. Baldazzi V, Bertin N, de Jong H, Génard M (2012) Towards multiscale plant models: integrating cellular networks. Trends Plant Sci 17: 728–736
13. Becker SA, Palsson BO (2008) Context-specific metabolic networks are consistent with experiments. PLoS Comput Biol 4: e1000082
14. Bordbar A, Feist AM, Usaite-Black R, Woodcock J, Palsson BO, Famili I (2011) A multi-tissue type genome-scale metabolic network for analysis of whole-body systems physiology. BMC Syst Biol 5: 180
15. Borisjuk L, Neuberger T, Schwender J, Heinzel N, Sunderhaus S, Fuchs J, Hay JO, Tschiersch H, Braun HP, Denolf P, et al (2013) Seed architecture shapes embryo metabolism in oilseed rape. Plant Cell 25: 1625–1640
16. Boyle NR, Morgan JA (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 3: 4
17. Chang RL, Ghamsari L, Manichaikul A, Hom EF, Balaji S, Fu W, Shen Y, Hao T, Palsson BO, Salehi-Ashtiani K, et al (2011) Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol Syst Biol 7: 518
18. Chen X, Shachar-Hill Y (2012) Insights into metabolic efficiency from flux analysis. J Exp Bot 63: 2343–2351
19. Cheung CYM, Poolman MG, Fell DA, Ratcliffe RG, Sweetlove LJ (2014) A diel flux balance model captures interactions between light and dark metabolism during day-night cycles in C3 and Crassulacean acid metabolism leaves. Plant Physiol 165: 917–929
20. Cheung CYM, Ratcliffe RG, Sweetlove LJ (2015) A method of accounting for enzyme costs in flux balance analysis reveals alternative pathways and metabolite stores in an illuminated Arabidopsis leaf. Plant Physiol 169: 1671–1682
21. Cheung CYM, Williams TCR, Poolman MG, Fell DA, Ratcliffe RG, Sweetlove LJ (2013) A method for accounting for maintenance costs in flux balance analysis improves the prediction of plant cell metabolic phenotypes under stress conditions. Plant J 75: 1050–1061
22. Chew YH, Wenden B, Flis A, Mengin V, Taylor J, Davey CL, Tindal C, Thomas H, Ougham HJ, de Reffye P, et al (2014) Multiscale digital Arabidopsis predicts individual organ and whole-organism growth. Proc Natl Acad Sci USA 111: E4127–E4136
23. Chung BKS, Lee DY (2009) Flux-sum analysis: a metabolite-centric approach for understanding the metabolic network. BMC Syst Biol 3: 117
24. Colombié S, Nazaret C, Bénard C, Biais B, Mengin V, Solé M, Fouillen L, Dieuaide-Noubhani M, Mazat JP, Beauvoit B, et al (2015) Modelling central metabolic fluxes by constraint-based optimization reveals metabolic reprogramming of developing Solanum lycopersicum (tomato) fruit. Plant J 81: 24–39
25. de Oliveira Dal’Molin CG, Quek LE, Palfreyman RW, Brumbley SM, Nielsen LK (2010) C4GEM, a genome-scale metabolic model to study C4 plant metabolism. Plant Physiol 154: 1871–1885
26. de Oliveira Dal’Molin CG, Quek LE, Saa PA, Nielsen LK (2015) A multitissue genome-scale metabolic modeling framework for the analysis of whole plant systems. Front Plant Sci 6: 4
27. Farré G, Blancquaert D, Capell T, Van Der Straeten D, Christou P, Zhu C (2014) Engineering complex metabolic pathways in plants. Annu Rev Plant Biol 65: 187–223
28. Feist AM, Palsson BO (2010) The biomass objective function. Curr Opin Microbiol 13: 344–349
29. Grafahrend-Belau E, Junker A, Eschenröder A, Müller J, Schreiber F, Junker BH (2013) Multiscale metabolic modeling: dynamic flux balance analysis on a whole-plant scale. Plant Physiol 163: 637–647
30. Heise R, Arrivault S, Szecowka M, Tohge T, Nunes-Nesi A, Stitt M, Nikoloski Z, Fernie AR (2014) Flux profiling of photosynthetic carbon metabolism in intact plants. Nat Protoc 9: 1803–1824
31. Heise R, Fernie AR, Stitt M, Nikoloski Z (2015) Pool size measurements facilitate the determination of fluxes at branching points in non-stationary metabolic flux analysis: the case of Arabidopsis thaliana. Front Plant Sci 6: 386
32. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11: 228–231
33. Hoppe A, Hoffmann S, Holzhütter HG (2007) Including metabolite concentrations into flux balance analysis: thermodynamic realizability as a constraint on flux distributions in metabolic networks. BMC Syst Biol 1: 23
34. Hörl M, Schnidder J, Sauer U, Zamboni N (2013) Non-stationary 13C-metabolic flux ratio analysis. Biotechnol Bioeng 110: 3164–3176
35. Ishihara H, Obata T, Sulpice R, Fernie AR, Stitt M (2015) Quantifying protein synthesis and degradation in Arabidopsis by dynamic 13CO2 labeling and analysis of enrichment in individual amino acids in their free pools and in protein. Plant Physiol 168: 74–93
36. Iyer VV, Sriram G, Fulton DB, Zhou R, Westgate ME, Shanks JV (2008) Metabolic flux maps comparing the effect of temperature on protein and oil biosynthesis in developing soybean cotyledons. Plant Cell Environ 31: 506–517
37. Jerby L, Shlomi T, Ruppin E (2010) Computational reconstruction of tissue-specific metabolic models: application to human liver metabolism. Mol Syst Biol 6: 401
38. Junker BH (2014) Flux analysis in plant metabolic networks: increasing throughput and coverage. Curr Opin Biotechnol 26: 183–188
39. Kajihata S, Furusawa C, Matsuda F, Shimizu H (2014) OpenMebius: an open source software for isotopically nonstationary 13C-based metabolic flux analysis. BioMed Res Int 2014: 627014
40. Karr JR, Sanghvi JC, Macklin DN, Gutschow MV, Jacobs JM, Bolival B Jr, Assad-Garcia N, Glass JI, Covert MW (2012) A whole-cell computational model predicts phenotype from genotype. Cell 150: 389–401
41. Kleessen S, Araújo WL, Fernie AR, Nikoloski Z (2012) Model-based confirmation of alternative substrates of mitochondrial electron transport chain. J Biol Chem 287: 11122–11131
42. Kleessen S, Irgang S, Klie S, Giavalisco P, Nikoloski Z (2015) Integration of transcriptomics and metabolomics data specifies the metabolic response of Chlamydomonas to rapamycin treatment. Plant J 81: 822–835
43. Knoop H, Gründel M, Zilliges Y, Lehmann R, Hoffmann S, Lockau W, Steuer R (2013) Flux balance analysis of cyanobacterial metabolism: the metabolic network of Synechocystis sp. PCC 6803. PLoS Comput Biol 9: e1003081
44. Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155: 70–78
45. Kruger NJ, Ratcliffe RG (2015) Fluxes through plant metabolic networks: measurements, predictions, insights and challenges. Biochem J 465: 27–38
46. Lee D, Smallbone K, Dunn WB, Murabito E, Winder CL, Kell DB, Mendes P, Swainston N (2012) Improving metabolic flux predictions using absolute gene expression data. BMC Syst Biol 6: 73
47. Lewis NE, Nagarajan H, Palsson BO (2012) Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat Rev Microbiol 10: 291–305
48. Linster CL, Van Schaftingen E, Hanson AD (2013) Metabolite damage and its repair or pre-emption. Nat Chem Biol 9: 72–80
49. Lobit P, Genard M, Soing P, Habib R (2006) Modelling malic acid accumulation in fruits: relationships with organic acids, potassium, and temperature. J Exp Bot 57: 1471–1483
50. Ma F, Jazmin LJ, Young JD, Allen DK (2014) Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation. Proc Natl Acad Sci USA 111: 16967–16972
51. Machado D, Herrgård M (2014) Systematic evaluation of methods for integration of transcriptomic data into constraint-based models of metabolism. PLoS Comput Biol 10: e1003580
52. Mallmann J, Heckmann D, Bräutigam A, Lercher MJ, Weber APM, Westhoff P, Gowik U (2014) The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife 3: e02478
53. Marashi SA, David L, Bockmayr A (2012) On flux coupling analysis of metabolic subsystems. J Theor Biol 302: 62–69
54. Masakapalli SK, Ritala A, Dong L, van der Krol AR, Oksman-Caldentey KM, Ratcliffe RG, Sweetlove LJ (2014) Metabolic flux phenotype of tobacco hairy roots engineered for increased geraniol production. Phytochemistry 99: 73–85
55. Mintz-Oron S, Meir S, Malitsky S, Ruppin E, Aharoni A, Shlomi T (2012) Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. Proc Natl Acad Sci USA 109: 339–344
56. Miyake C (2010) Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51: 1951–1963
57. Morandini P (2013) Control limits for accumulation of plant metabolites: brute force is no substitute for understanding. Plant Biotechnol J 11: 253–267
58. Nelson CJ, Alexova R, Jacoby RP, Millar AH (2014) Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiol 166: 91–108
59. Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I (2012) Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc Natl Acad Sci USA 109: 2678–2683
60. O’Brien EJ, Lerman JA, Chang RL, Hyduke DR, Palsson BØ (2013) Genome-scale models of metabolism and gene expression extend and refine growth phenotype prediction. Mol Syst Biol 9: 693
61. O’Grady J, Schwender J, Shachar-Hill Y, Morgan JA (2012) Metabolic cartography: experimental quantification of metabolic fluxes from isotopic labelling studies. J Exp Bot 63: 2293–2308
62. Poolman MG, Kundu S, Shaw R, Fell DA (2013) Responses to light intensity in a genome-scale model of rice metabolism. Plant Physiol 162: 1060–1072
63. Ratcliffe RG, Shachar-Hill Y (2005) Revealing metabolic phenotypes in plants: inputs from NMR analysis. Biol Rev Camb Philos Soc 80: 27–43
64. Recht L, Töpfer N, Batushansky A, Sikron N, Gibon Y, Fait A, Nikoloski Z, Boussiba S, Zarka A (2014) Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis. J Biol Chem 289: 30387–30403
65. Reznik E, Mehta P, Segrè D (2013) Flux imbalance analysis and the sensitivity of cellular growth to changes in metabolite pools. PLoS Comput Biol 9: e1003195
66. Robaina Estévez S, Nikoloski Z (2015) Context-specific metabolic model extraction based on regularized least squares optimization. PLoS One 10: e0131875
67. Rohwer JM (2012) Kinetic modelling of plant metabolic pathways. J Exp Bot 63: 2275–2292
68. Saha R, Suthers PF, Maranas CD (2011) Zea mays iRS1563: a comprehensive genome-scale metabolic reconstruction of maize metabolism. PLoS One 6: e21784
69. Schmidt BJ, Ebrahim A, Metz TO, Adkins JN, Palsson BØ, Hyduke DR (2013) GIM3E: condition-specific models of cellular metabolism developed from metabolomics and expression data. Bioinformatics 29: 2900–2908
70. Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y (2004) Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432: 779–782
71. Schwender J, Hay JO (2012) Predictive modeling of biomass component tradeoffs in Brassica napus developing oilseeds based on in silico manipulation of storage metabolism. Plant Physiol 160: 1218–1236
72. Schwender J, König C, Klapperstück M, Heinzel N, Munz E, Hebbelmann I, Hay JO, Denolf P, De Bodt S, Redestig H, et al (2014) Transcript abundance on its own cannot be used to infer fluxes in central metabolism. Front Plant Sci 5: 668
73. Schwender J, Shachar-Hill Y, Ohlrogge JB (2006) Mitochondrial metabolism in developing embryos of Brassica napus. J Biol Chem 281: 34040–34047
74. Seaver SM, Bradbury LM, Frelin O, Zarecki R, Ruppin E, Hanson AD, Henry CS (2015) Improved evidence-based genome-scale metabolic models for maize leaf, embryo, and endosperm. Front Plant Sci 6: 142
75. Simons M, Saha R, Amiour N, Kumar A, Guillard L, Clément G, Miquel M, Li Z, Mouille G, Lea PJ, et al (2014) Assessing the metabolic impact of nitrogen availability using a compartmentalized maize leaf genomescale model. Plant Physiol 166: 1659–1674
76. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126–1149
77. Spielbauer G, Margl L, Hannah LC, Römisch W, Ettenhuber C, Bacher A, Gierl A, Eisenreich W, Genschel U (2006) Robustness of central carbohydrate metabolism in developing maize kernels. Phytochemistry 67: 1460–1475
78. Stitt M (2013) Progress in understanding and engineering primary plant metabolism. Curr Opin Biotechnol 24: 229–238
79. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15: 462–470
80. Sweetlove LJ, Obata T, Fernie AR (2014) Systems analysis of metabolic phenotypes: what have we learnt? Trends Plant Sci 19: 222–230
81. Sweetlove LJ, Ratcliffe RG (2011) Flux-balance modeling of plant metabolism. Front Plant Sci 2: 38
82. Sweetlove LJ, Williams TC, Cheung CY, Ratcliffe RG (2013) Modelling metabolic CO₂ evolution: a fresh perspective on respiration. Plant Cell Environ 36: 1631–1640
83. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, et al (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694–714
84. Taniguchi M, Miyake H (2012) Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr Opin Plant Biol 15: 252–260
85. Tepper N, Noor E, Amador-Noguez D, Haraldsdóttir HS, Milo R, Rabinowitz J, Liebermeister W, Shlomi T (2013) Steady-state metabolite concentrations reflect a balance between maximizing enzyme efficiency and minimizing total metabolite load. PLoS One 8: e75370
86. Töpfer N, Caldana C, Grimbs S, Willmitzer L, Fernie AR, Nikoloski Z (2013) Integration of genome-scale modeling and transcript profiling reveals metabolic pathways underlying light and temperature acclimation in Arabidopsis. Plant Cell 25: 1197–1211
87. Töpfer N, Kleessen S, Nikoloski Z (2015) Integration of metabolomics data into metabolic networks. Front Plant Sci 6: 49
88. Vanhercke T, El Tahchy A, Liu Q, Zhou XR, Shrestha P, Divi UK, Ral JP, Mansour MP, Nichols PD, James CN, et al (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J 12: 231–239
89. Vlassis N, Pacheco MP, Sauter T (2014) Fast reconstruction of compact context-specific metabolic network models. PLoS Comput Biol 10: e1003424
90. Wang Y, Eddy JA, Price ND (2012) Reconstruction of genome-scale metabolic models for 126 human tissues using mCADRE. BMC Syst Biol 6: 153
91. Wiechert W, Nöh K (2013) Isotopically non-stationary metabolic flux analysis: complex yet highly informative. Curr Opin Biotechnol 24: 979–986
92. Williams TCR, Miguet L, Masakapalli SK, Kruger NJ, Sweetlove LJ, Ratcliffe RG (2008) Metabolic network fluxes in heterotrophic Arabidopsis cells: stability of the flux distribution under different oxygenation conditions. Plant Physiol 148: 704–718
93. Yizhak K, Benyamini T, Liebermeister W, Ruppin E, Shlomi T (2010) Integrating quantitative proteomics and metabolomics with a genomescale metabolic network model. Bioinformatics 26: i255–i260
94. Young JD (2014) INCA: a computational platform for isotopically nonstationary metabolic flux analysis. Bioinformatics 30: 1333–1335
95. Yuan J, Bennett BD, Rabinowitz JD (2008) Kinetic flux profiling for quantitation of cellular metabolic fluxes. Nat Protoc 3: 1328–1340
96. Yuan J, Fowler WU, Kimball E, Lu W, Rabinowitz JD (2006) Kinetic flux profiling of nitrogen assimilation in Escherichia coli. Nat Chem Biol 2: 529–530
97. Zur H, Ruppin E, Shlomi T (2010) iMAT: an integrative metabolic analysis tool. Bioinformatics 26: 3140–3142