Assessing the metabolic impact of nitrogen availability using a compartmentalized maize leaf genome-scale model

Plant Physiology

Volumn 166, Issue 3, 2014, Pages 1659-1674

  Simons, Margaret ^a   Saha, Rajib ^a   Amiour, Nardjis ^c   Kumar, Akhil ^b   Guillard, Lenaïg ^c   Clément, Gilles ^c   Miquel, Martine ^c   Li, Zhenni ^c   Mouille, Gregory ^c   Lea, Peter J ^d   Hirel, Bertrand ^c   Maranas, Costas D ^a  

^a The Center for Nanotechnology Education and Utilization   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c AGROPARISTECH   (France)

^d LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; PROTEOME;

BIOAVAILABILITY; BIOLOGICAL MODEL; BIOMASS; GENE EXPRESSION PROFILING; GENETICS; MAIZE; METABOLISM; METABOLOME; MUTATION; PLANT GENOME; PLANT LEAF;

BIOLOGICAL AVAILABILITY; BIOMASS; GENE EXPRESSION PROFILING; GENOME, PLANT; METABOLOME; MODELS, BIOLOGICAL; MUTATION; NITROGEN; PLANT LEAVES; PROTEOME; ZEA MAYS;

EID: 84908565339     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.245787     Document Type: Article

References (138)

1. Alberte RS, Thornber JP (1977) Water stress effects on the content and organization of chlorophyll in mesophyll and bundle sheath chloroplasts of maize. Plant Physiol 59: 351–353
2. Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quilleré I, Cañas R, et al (2012) The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 63: 5017–5033
3. Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Balliau B, Quilleré I, Tercé-Laforgue T, Dargel-Graffin C, et al (2014) An integrated “omics” approach to the characterization of maize (Zea mays L.) mutants deficient in the expression of two genes encoding cytosolic glutamine synthetase. BMC Genomics (in press)
4. Andrews M, Lea PJ (2013) Our nitrogen ‘footprint’: the need for increased crop nitrogen use efficiency. Ann Appl Biol 163: 165–169
5. Andrews M, Raven JA, Lea PJ (2013) Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann Appl Biol 163: 174–199
6. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815
7. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1–15
8. Bachlava E, Dewey R, Burton J, Cardinal AJ (2009) Mapping candidate genes for oleate biosynthesis and their association with unsaturated fatty acid seed content in soybean. Mol Breed 23: 337–347
9. Becker SA, Palsson BO (2008) Context-specific metabolic networks are consistent with experiments. PLoS Comput Biol 4: e1000082
10. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57: 289–300
11. Boamfa EI, Veres AH, Ram PC, Jackson MB, Reuss J, Harren FJ (2005) Kinetics of ethanol and acetaldehyde release suggest a role for acetaldehyde production in tolerance of rice seedlings to micro-aerobic conditions. Ann Bot (Lond) 96: 727–736
12. Bonawitz ND, Kim JI, Tobimatsu Y, Ciesielski PN, Anderson NA, Ximenes E, Maeda J, Ralph J, Donohoe BS, Ladisch M, et al (2014) Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 509: 376–380
13. 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
14. Burgener M, Suter M, Jones S, Brunold C (1998) Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves. Plant Physiol 116: 1315–1322
15. Cañas RA, Quilleré I, Gallais A, Hirel B (2012) Can genetic variability for nitrogen metabolism in the developing ear of maize be exploited to improve yield? New Phytol 194: 440–452
16. Cañas RA, Quilleré I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 8: 966–978
17. Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant-tissue by nitration of salicylicacid. Commun Soil Sci Plant Anal 6: 71–80
18. Chandrasekaran S, Price ND (2010) Probabilistic integrative modeling of genome-scale metabolic and regulatory networks in Escherichia coli and Mycobacterium tuberculosis. Proc Natl Acad Sci USA 107: 17845–17850
19. Chang YM, Liu WY, Shih ACC, Shen MN, Lu CH, Lu MYJ, Yang HW, Wang TY, Chen SCC, Chen SM, et al (2012) Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol 160: 165–177
20. Christin PA, Osborne CP (2013) The recurrent assembly of C4 photosynthesis, an evolutionary tale. Photosynth Res 117: 163–175
21. Chung BK, Lee DY (2009) Flux-sum analysis: a metabolite-centric approach for understanding the metabolic network. BMC Syst Biol 3: 117
22. Coïc Y, Lesaint C (1971) Comment assurer une bonne nutrition en eau et en ions minéraux en horticulture. Hortic Francaise 8: 11–14
23. Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, Farhat MR, Cheng TY, Moody DB, Murray M, Galagan JE (2009) Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comput Biol 5: e1000489
24. de Oliveira Dal’Molin CG, Quek LE, Palfreyman RW, Brumbley SM, Nielsen LK (2010a) AraGEM, a genome-scale reconstruction of the primary metabolic network in Arabidopsis. Plant Physiol 152: 579–589
25. de Oliveira Dal’Molin CG, Quek LE, Palfreyman RW, Brumbley SM, Nielsen LK (2010b) C4GEM, a genome-scale metabolic model to study C4 plant metabolism. Plant Physiol 154: 1871–1885
26. Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114: 1031–1037
27. Driever SM, Kromdijk J (2013) Will C3 crops enhanced with the C4, CO2- concentrating mechanism live up to their full potential (yield)? J Exp Bot 64: 3925–3935
28. Duarte NC, Becker SA, Jamshidi N, Thiele I, Mo ML, Vo TD, Srivas R, Palsson BO (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc Natl Acad Sci USA 104: 1777–1782
29. Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285–299
30. Feil B, Thiraporn R, Geisler G, Stamp P (1990) Genotype variation in grain nutrient concentration in tropical maize grown during a rainy and a dry season. Agronomie 10: 717–725
31. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BO (2007) A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol Syst Biol 3: 121
32. Ferrario-Mery S, Valadier MH, Foyer CH (1998) Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. Plant Physiol 117: 293–302
33. Fiehn O (2006) Metabolite profiling in Arabidopsis. Methods Mol Biol 323: 439–447
34. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58: 2339–2358
35. Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152: 1219–1250
36. Fukushima RS, Hatfield RD (2001) Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J Agric Food Chem 49: 3133–3139
37. Furbank RT, Jenkins CLD, Hatch MD (1989) CO2 concentrating mechanism of C4 photosynthesis: permeability of isolated bundle sheath-cells to inorganic carbon. Plant Physiol 91: 1364–1371
38. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92–100
39. Good AG, Beatty PH (2011) Biotechnological approaches to improving nitrogen use efficiency in plants: alanine aminotransferase as a case study. In MJ Hawkesford, P Barraclough, eds, The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops. Wiley-Blackwell, Sussex, UK, pp 165–191
40. Grafahrend-Belau E, Schreiber F, Koschützki D, Junker BH (2009) Flux balance analysis of barley seeds: a computational approach to study systemic properties of central metabolism. Plant Physiol 149: 585–598
41. Gupta P, Jain M, Sarangthem J, Gadre R (2013) Inhibition of 5-aminolevulinic acid dehydratase by mercury in excised greening maize leaf segments. Plant Physiol Biochem 62: 63–69
42. Harholt J, Jensen JK, Sørensen SO, Orfila C, Pauly M, Scheller HV (2006) ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol 140: 49–58
43. Heavner BD, Smallbone K, Barker B, Mendes P, Walker LP (2012) Yeast 5: an expanded reconstruction of the Saccharomyces cerevisiae metabolic network. BMC Syst Biol 6: 55
44. Henry CS, DeJongh M, Best AA, Frybarger PM, Linsay B, Stevens RL (2010) High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol 28: 977–982
45. Hirel B, Gallais A (2011) Nitrogen use efficiency: physiological, molecular and genetic investigations towards crop improvement. In JL Prioul, C Thévenot, T Molnar, eds, Advances in Maize, Vol 3. Society for Experimental Biology, London, pp 285–310
46. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58: 2369–2387
47. Hirel B, Martin A, Terce-Laforgue T, Gonzalez-Moro MB, Estavillo JM (2005) Physiology of maize: I. A comprehensive and integrated view of nitrogen metabolism in a C4 plant. Physiol Plant 124: 167–177
48. Ho CL, Saito K (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20: 243–259
49. Howard TP, Lloyd JC, Raines CA (2011) Inter-species variation in the oligomeric states of the higher plant Calvin cycle enzymes glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. J Exp Bot 62: 3799–3805
50. Howles PA, Birch RJ, Collings DA, Gebbie LK, Hurley UA, Hocart CH, Arioli T, Williamson RE (2006) A mutation in an Arabidopsis ribose 5- phosphate isomerase reduces cellulose synthesis and is rescued by exogenous uridine. Plant J 48: 606–618
51. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43: 476–481
52. International Grains Council (2013) Report for fiscal year 2011/12. International Grains Council, London
53. Ishii N, Nakahigashi K, Baba T, Robert M, Soga T, Kanai A, Hirasawa T, Naba M, Hirai K, Hoque A, et al (2007) Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316: 593–597
54. Jensen PA, Papin JA (2011) Functional integration of a metabolic network model and expression data without arbitrary thresholding. Bioinformatics 27: 541–547
55. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42: D199–D205
56. Kim J, Rudella A, Ramirez Rodriguez V, Zybailov B, Olinares PDB, van Wijk KJ (2009) Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21: 1669–1692
57. Kim S, Schlicke H, Van Ree K, Karvonen K, Subramaniam A, Richter A, Grimm B, Braam J (2013) Arabidopsis chlorophyll biosynthesis: an essential balance between the methylerythritol phosphate and tetrapyrrole pathways. Plant Cell 25: 4984–4993
58. Korn EL, McShane LM, Troendle JF, Rosenwald A, Simon R (2002) Identifying pre-post chemotherapy differences in gene expression in breast tumours: a statistical method appropriate for this aim. Br J Cancer 86: 1093–1096
59. Krumholz EW, Yang H, Weisenhorn P, Henry CS, Libourel IG (2012) Genome-wide metabolic network reconstruction of the picoalga Ostreococcus. J Exp Bot 63: 2353–2362
60. Kumar A, Suthers PF, Maranas CD (2012) MetRxn: a knowledgebase of metabolites and reactions spanning metabolic models and databases. BMC Bioinformatics 13: 6
61. Kumar VS, Dasika MS, Maranas CD (2007) Optimization based automated curation of metabolic reconstructions. BMC Bioinformatics 8: 212
62. Lakshmanan M, Zhang Z, Mohanty B, Kwon JY, Choi HY, Nam HJ, Kim DI, Lee DY (2013) Elucidating rice cell metabolism under flooding and drought stresses using flux-based modeling and analysis. Plant Physiol 162: 2140–2150
63. Lange BM, Ghassemian M (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol Biol 51: 925–948
64. 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
65. Leegood RC (1985) The intercellular compartmentation of metabolites in leaves of Zea mays L. Planta 164: 163–171
66. Lepage M (1967) Identification and composition of turnip root lipids. Lipids 2: 244–250
67. Leveau V, Lorgeou J, Prioul JL (2011) Maize in the world economy: a challenge for scientific research–how to produce more cheaper! In JL Prioul, C Thévenot, C Molnar, eds, Advances in Maize, Vol 3. Society for Experimental Biology, London, pp 509–534
68. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42: 1060–1067
69. Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54: 569–581
70. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, et al (2010) Acyl-lipid metabolism. The Arabidopsis Book 8: e0133, doi/10.1199/tab.0133
71. Majeran W, Cai Y, Sun Q, van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17: 3111–3140
72. Martin A, Belastegui-Macadam X, Quilleré I, Floriot M, Valadier MH, Pommel B, Andrieu B, Donnison I, Hirel B (2005) Nitrogen management and senescence in two maize hybrids differing in the persistence of leaf greenness: agronomic, physiological and molecular aspects. New Phytol 167: 483–492
73. Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, et al (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18: 3252–3274
74. McAllister CH, Facette M, Holt A, Good AG (2013) Analysis of the enzymatic properties of a broad family of alanine aminotransferases. PLoS ONE 8: e55032
75. McCourt JA, Duggleby RG (2006) Acetohydroxyacid synthase and its role in the biosynthetic pathway for branched-chain amino acids. Amino Acids 31: 173–210
76. McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD (2001) Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Natl Acad Sci USA 98: 10001–10005
77. Méchin V, Thévenot C, Le Guilloux M, Prioul JL, Damerval C (2007) Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 143: 1203–1219
78. Mekhedov S, de Ilárduya OM, Ohlrogge J (2000) Toward a functional catalog of the plant genome: a survey of genes for lipid biosynthesis. Plant Physiol 122: 389–402
79. Mérigout P, Lelandais M, Bitton F, Renou JP, Briand X, Meyer C, Daniel- Vedele F (2008) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiol 147: 1225–1238
80. 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
81. Miquel M, Browse J (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis: biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. J Biol Chem 267: 1502–1509
82. Monaco MK, Sen TZ, Dharmawardhana PD, Ren L, Schaeffer M, Naithani S, Amarasinghe V, Thomason J, Harper L, Gardiner J, et al (2013) Maize metabolic network construction and transcriptome analysis. Plant Genome 6: 1–12
83. Moore TS (1982) Phospholipid biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 33: 235–259
84. Murata N (1983) Molecular-species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 24: 81–86
85. Murata N, Tasaka Y (1997) Glycerol-3-phosphate acyltransferase in plants. Biochim Biophys Acta 1348: 10–16
86. Nakamoto H, Edwards GE (1987) Effect of adenine-nucleotides on the reaction catalyzed by pyruvate, ortho-phosphate dikinase in maize. Biochim Biophys Acta 924: 360–368
87. Nelson DL, Cox MM (2009) Oxidative phosphorylation and photophosphorylation. In K Ahr, ed, Lehninger Principles of Biochemistry, Ed 5. WH Freeman, New York, pp 707–772
88. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35: 454–484
89. Ohnishi J, Yamada M (1980) Glycerolipid synthesis in Avena leaves during greening of etiolated seedlings. II. Alpha-linolenic acid synthesis. Plant Cell Physiol 21: 1607–1618
90. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551–556
91. Penna S, Sági L, Swennen R (2002) Positive selectable marker genes for routine plant transformation. In Vitro Cell Dev Biol Plant 38: 125–128
92. Peterhansel C, Krause K, Braun HP, Espie GS, Fernie AR, Hanson DT, Keech O, Maurino VG, Mielewczik M, Sage RF (2013) Engineering photorespiration: current state and future possibilities. Plant Biol (Stuttg) 15: 754–758
93. Pilalis E, Chatziioannou A, Thomasset B, Kolisis F (2011) An in silico compartmentalized metabolic model of Brassica napus enables the systemic study of regulatory aspects of plant central metabolism. Biotechnol Bioeng 108: 1673–1682
94. 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
95. Poolman MG, Miguet L, Sweetlove LJ, Fell DA (2009) A genome-scale metabolic model of Arabidopsis and some of its properties. Plant Physiol 151: 1570–1581
96. Rahantaniaina MS, Tuzet A, Mhamdi A, Noctor G (2013) Missing links in understanding redox signaling via thiol/disulfide modulation: how is glutathione oxidized in plants? Front Plant Sci 4: 477
97. Ramazzina I, Folli C, Secchi A, Berni R, Percudani R (2006) Completing the uric acid degradation pathway through phylogenetic comparison of whole genomes. Nat Chem Biol 2: 144–148
98. Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91: 357–363
99. 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
100. Rolland N, Curien G, Finazzi G, Kuntz M, Maréchal E, Matringe M, Ravanel S, Seigneurin-Berny D (2012) The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annu Rev Genet 46: 233–264
101. Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67: 10–15
102. Sage RF (2014) Stopping the leaks: new insights into C4 photosynthesis at low light. Plant Cell Environ 37: 1037–1041
103. Saha R, Suthers PF, Maranas CD (2011) Zea mays iRS1563: a comprehensive genome-scale metabolic reconstruction of maize metabolism. PLoS ONE 6: e21784
104. Sangwan RS, Bourgeois Y, Brown S, Vasseur G, Sangwan-Norreel B (1992) Characterization of competent cells and early events of Agrobacterium- mediated genetic transformation in Arabidopsis thaliana. Planta 188: 439–456
105. Schaeffer ML, Harper LC, Gardiner JM, Andorf CM, Campbell DA, Cannon EK, Sen TZ, Lawrence CJ (2011) MaizeGDB: curation and outreach go hand-in-hand. Database (Oxford) 2011: bar022
106. Schellenberger J, Lewis NE, Palsson BO (2011) Elimination of thermodynamically infeasible loops in steady-state metabolic models (vol 100, pg 544, 2010). Biophys J 100: 1381
107. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178–183
108. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115
109. Schnarrenberger C, Martin W (2002) Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants: a case study of endosymbiotic gene transfer. Eur J Biochem 269: 868–883
110. Schreiber F, Colmsee C, Czauderna T, Grafahrend-Belau E, Hartmann A, Junker A, Junker BH, Klapperstück M, Scholz U, Weise S (2012) MetaCrop 2.0: managing and exploring information about crop plant metabolism. Nucleic Acids Res 40: D1173–D1177
111. Shlomi T, Cabili MN, Herrgård MJ, Palsson BO, Ruppin E (2008) Network-based prediction of human tissue-specific metabolism. Nat Biotechnol 26: 1003–1010
112. Simons M, Saha R, Guillard L, Clément G, Armengaud P, Cañas R, Maranas CD, Lea PJ, Hirel B (2014) Nitrogen-use efficiency in maize (Zea mays L.): from ‘omics’ studies to metabolic modelling. J Exp Bot 65: 5657–5671
113. Sowiński P, Szczepanik J, Minchin PEH (2008) On the mechanism of C4 photosynthesis intermediate exchange between Kranz mesophyll and bundle sheath cells in grasses. J Exp Bot 59: 1137–1147
114. Stitt M, Heldt HW (1985) Generation and maintenance of concentration gradients between the mesophyll and bundle sheath in maize leaves. Biochim Biophys Acta 808: 400–414
115. Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeström P (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23: 759–770
116. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PDB, van Wijk KJ (2009) PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res 37: D969–D974
117. Taiz L (2010) Plant Physiology, Ed 5. Sinauer Associates, Sunderland, MA
118. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321–346
119. Taniguchi Y, Nagasaki J, Kawasaki M, Miyake H, Sugiyama T, Taniguchi M (2004) Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. Plant Cell Physiol 45: 187–200
120. Tercé-Laforgue T, Mack G, Hirel B (2004) New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum) plants grown under different nitrogen regimes. Physiol Plant 120: 220–228
121. Thiele I, Swainston N, Fleming RM, Hoppe A, Sahoo S, Aurich MK, Haraldsdottir H, Mo ML, Rolfsson O, Stobbe MD, et al (2013) A community-driven global reconstruction of human metabolism. Nat Biotechnol 31: 419–425
122. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116–5121
123. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596–1604
124. Tzin V, Galili G (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book 8: e0132, doi/10.1199/tab.0132
125. Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32: 420–424
126. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11: 278–285
127. Verwoerd TC, Dekker BMM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17: 2362
128. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7: 737–750
129. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3: 2–20
130. Wang Y, Suzek T, Zhang J, Wang J, He S, Cheng T, Shoemaker BA, Gindulyte A, Bryant SH (2014) PubChem BioAssay: 2014 update. Nucleic Acids Res 42: D1075–D1082
131. Weiner H, Heldt HW (1992) Inter- and intracellular distribution of amino acids and other metabolites in maize (Zea mays L.) leaves. Planta 187: 242–246
132. Xiong Y, DeFraia C, Williams D, Zhang X, Mou Z (2009) Deficiency in a cytosolic ribose-5-phosphate isomerase causes chloroplast dysfunction, late flowering and premature cell death in Arabidopsis. Physiol Plant 137: 249–263
133. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79–92
134. Zhao Q, Chen S, Dai S (2013) C4 photosynthetic machinery: insights from maize chloroplast proteomics. Front Plant Sci 4: 85
135. Zomorrodi AR, Islam MM, Maranas CD (2014) d-OptCom: dynamic multilevel and multi-objective metabolic modeling of microbial communities. ACS Synth Biol 3: 247–257
136. Zomorrodi AR, Maranas CD (2012) OptCom: a multi-level optimization framework for the metabolic modeling and analysis of microbial communities. PLoS Comput Biol 8: e1002363
137. Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57: 805–836
138. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3: e1994