Regulation of metabolic networks: Understanding metabolic complexity in the systems biology era

New Phytologist

Volumn 168, Issue 1, 2005, Pages 9-24

  Sweetlove, Lee J ^a   Fernie, Alisdair R ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

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

Author keywords

Flux; Integrative genomics; Metabolism; Metabolon; Network; Scale free; System

Indexed keywords

BIOLOGICAL CHARACTERISTICS; DEVELOPMENT STRATEGY; LANDSCAPE STRUCTURE; METABOLISM; MOLECULAR ECOLOGY; PLANT ARCHITECTURE; THEORETICAL STUDY;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; PLANT; REVIEW; SIGNAL TRANSDUCTION;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; PLANTS; SIGNAL TRANSDUCTION;

EID: 32944461132     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2005.01513.x     Document Type: Review

References (130)

1. Achnine L Blancaflor EB Rasmussen S Dixon RA. 2004. Co-localisation of 1-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channelling in phenylpropanoid biosynthesis. Plant Cell 16 : 3098 3109.
2. Aebersold R Mann M. 2003. Mass spectrometry-based proteomics. Nature 422 : 198 207.
3. Agius F Gonzalez-Lamothe R Caballero JL Munoz-Blanci J Botella MA Valpuesta V. 2003. Engineering increased vitamin C levels in plants by overexpression of a d-galacturnonic acid reductase. Nature Biotechnology 21 : 177 181.
4. Albert R Jeong H Barabasi AL. 2000. Error and attack tolerance of complex networks. Nature 406 : 378 382.
5. Arita M. 2004. The metabolic world of Escherichia coli is not small. Proceedings of the National Academy of Sciences, USA 101 : 1543 1547.
6. Arkin A Shen PD Ross J. 1997. A test case of correlation metric construction of a reaction pathway from measurements. Science 277 : 1275 1279.
7. Askenazi M Driggers EM Holtzman DA Norman TC Iverson S Zimmer DP Boers ME Blomquist PR Martinez EJ Monreal AW Feibelman TP Mayorga ME Maxon ME Sykes K Tobin JV Cordero E Salama SR Trueheart J Royer JC Madden KT. 2003. Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nature Biotechnology 21 : 150 156.
8. Babitzke P Gollnick P. 2001. Posttranslational initation control of tryptophan metabolism in. Bacillus subtilis by the trp RNA-binding attenuation protein (TRAP), antiTRAP, and RNA structure. Journal of Bacteriology 183 : 5795 5802.
9. Balmer Y Koller A Del Val G Manieri W Schurmann P Buchanan BB. 2003. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proceedings of the National Academy of Sciences, USA 100 : 370 375.
10. Balmer Y Vensel WH Tanaka CK Hurkman WJ Gelhaye E Rouhier N Jacquot JP Manieri W Schurmann P Droux M Buchanan BB. 2004. Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proceedings of the National Academy of Sciences, USA 101 : 2642 2647.
11. Barabasi AL. 2003. Linked. How everything is connected to everything else and what it means for business, science and everyday life. London, UK : Plume, Penguin Books Ltd.
12. Barabasi AL Albert R. 1999. Emergence of scaling in random networks. Science 286 : 509 512.
13. Baxter C Sabar M Quick P Sweetlove LJ. 2005. Comparison of changes in fruit gene expression in tomato introgression lines provides evidence of genome-wide transcriptional changes and reveals links to mapped QTLs and described traits. Journal of Experimental Botany 56 : 1591 1604.
14. Beevers H. 1961. Respiratory metabolism in plants. Evanston, USA : Row Peterson.
15. Berg J Lassig M. 2004. Local graph alignment and motif search in biological networks. Proceedings of the National Academy of Sciences, USA 101 : 14689 14694.
16. Blagoev B Ong SE Kratchmarova I Mann M. 2004. Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nature Biotechnology 22 : 1139 1145.
17. Bouche N Bouchez D. 2001. Arabidopsis gene knockout: phenotypes wanted. Current Opinion in Plant Biology 4 : 111 117.
18. Buchanan B Gruissem W Jones RL. 2001. Biochemistry and Molecular Biology of Plants. Rockville, MD, USA : American Society of Plant Physiologist.
19. Buckhout TJ Thimm O. 2003. Insights into metabolism obtained from microarray analysis. Current Opinions in Plant Biology 6 : 288 296.
20. Budziszewski GJ Lewis SP Glover LW Reineke J Jones G Ziemnik LS Lonowski J Nyfeler B Aux G Zhou Q McElver J Patton DA Martienssen R Grossniklaus U Ma H Law M Levin JZ. 2001. Arabidopsis genes essential for seedling viability. Isolation of insertional mutants and molecular cloning. Genetics 159 : 1765 1778.
21. Bykova NV Egsgaard H Moller IM. 2003. Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Letters 540 : 141 146.
22. Calvin M. 1962. Path of carbon in photosynthesis. Science 135 : 879 882.
23. Camacho D de la Fuente A Mendes P. 2005. The origin of correlations in metabolomics data. Metabolomics 1 : 53 63.
24. Chew O Whelan J Millar AH. 2003. Molecular definition of the ascorbate-glutathione cycle in. Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. Journal of Biological Chemistry 278 : 46869 46877.
25. Conant GC Wagner A. 2003. Convergent evolution of gene circuits. Nature Genetics 34 : 264 266.
26. Cornell M Paton NW Oliver SG. 2004. A critical and integrated view of the yeast interactome. Comparative and Functional Genomics 5 : 382 402.
27. De Luca V St Pierre B. 2000. The cell and developmental biology of alkaloid biosynthesis. Trends in Plant Science 5 : 168 173.
28. Douce R Neuberger M. 1989. The uniqueness of plant mitchondria. Annual Review of Plant Physiological Plant Molecular Biology 40 : 371 414.
29. Eubel H Heinemeyer J Sunderhaus S Braun HP. 2004. Respiratory chain supercomplexes in plant mitochondria. Plant Physiological Biochemistry 42 : 937 942.
30. Even S Lindley ND Cocaign-Bousquet M. 2003. Transcriptional, translational and metabolic regulation of glycolysis in Lactococcus lactis subsp. Cremoris MG 1363 grown in continuous acidic cultures. Microbiology-SGM 149 : 1935 1944.
31. Fafournoux P Bruhat A Jousse C. 2000. Amino acid regulation of gene expression. Biochemistry and Journal 351 : 1 12.
32. Fernie AR Carrari F Sweetlove LJ. 2004a. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinions in Plant Biology 7 : 254 261.
33. Fernie AR Geigenberger P Stitt M. 2005. Flux: an important, but neglected component of functional genomics. Current Opinion in Plant Biology 8 : 174 182.
34. Fernie AR Trethewey RN Krotzky AJ Willmitzer L. 2004b. Metabolite profiling: from diagnostics to systems biology. Nature Review of Molecular Cell Biology 5 : 763 769.
35. Fridman E Pichersky E. 2005. Metabolomics, genomics, proteomics and the identification of enzymes and their substrates and products. Current Opinions in Plant Biology 8 : 242 248.
36. Galili G. 2002. New insights into the regulation and functional significance of lysine metabolism in plants. Annual Review of Plant Biology 53 : 27 43.
37. Galili G Tang GL Zhu XH Gakiere B. 2001. Lysine catabolism: a stress and development super-regulated metabolic pathway. Current Opinions in Plant Biology 4 : 261 266.
38. Geigenberger P Stitt M Fernie AR. 2004. Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers. Plant, Cell & Environment 27 : 655 673.
39. Gibon Y Blaesing OE Hannemann J Carillo P Hohne M Hendriks JH Palacios N Cross J Selbig J Stitt M. 2004. A Robot-Based Platform to Measure Multiple Enzyme Activities in Arabidopsis Using a Set of Cycling Assays. Comparison of Changes of Enzyme Activities and Transcript Levels during Diurnal Cycles and in Prolonged Darkness. Plant Cell 16 : 3304 3325.
40. Giegé P Heazelwood JL Roessner-Tunali U Millar AH Fernie AR Leaver CJ Sweetlove LJ. 2003. Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15 : 2140 2151.
41. Givan CV. 1999. Evolving concepts in plant glycolysis: two centuries of progress. Biology Review 74 : 277 309.
42. Goossens A Hakkinen ST Laakso I Seppanen-Laakso T Biondi S De Sutter V Lammertyn F Nuutila AM Soderlund H Zabeau M Inze D Oksman-Caldentey KM. 2003. A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proceedings of the National Academy of Sciences, USA 100 : 8595 8600.
43. Green MA Fry SC. 2005. Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433 : 83 87.
44. Hardie DG. 2003. Mini-review: The AMP-activated protein kinase cascade. The key sensor of cellular energy status. Endocrinology 144 : 5179 5183.
45. Hartwell LH Hopfield JJ Leibler S Murray AW. 1999. From molecular to modular cell biology. Nature 402 : C47 C52.
46. Hellerstein MK. 2003. In vivo measurement of fluxes through metabolic pathways: The missing link in functional genomics and pharmaceutical research. Annual Review of Nutrition 23 : 379 402.
47. Hellerstein MK Nesse RA. 1999. Mass isotopomer distribution analysis at eight years: theoretical, analytic, and experimental considerations. American Journal of Physiology 276 : E1146 E1170.
48. Hirai MY Yano M Goodenowe DB Kanaya S Kimura T Awazuhara M Arita M Fujiwara T Saito K. 2004. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 101 : 10205 10210.
49. Hofmeyer J. 1996. Co-response analysis: a new experimental strategy for metabolic control analysis. Journal of Theoretical Biology 182 : 371 380.
50. Hyde CC Ahmed SA Padlan EA Miles EW Davies DR. 1988. Three-dimensional structure of the tryptophan synthase alpha 2 beta 2 multienzyme complex from Salmonella typhimurium. Journal of Biological Chemistry 263 : 17857 17871.
51. Jeong H Mason SP Barabasi AL Oltvai ZN. 2001. Lethality and centrality in protein networks. Nature 411 : 41 42.
52. Jeong H Tombor B Albert R Oltvai ZN Barabasi AL. 2000. The large-scale organization of metabolic networks. Nature 407 : 651 654.
53. Jorgensen K Rasmussen AV Morant M Nielsen AH Bjarnholt N Zagrobelny M Bak S Moller BL. 2005. Metabolon formation and metabolic chaneling in the biosynthesis of plant natural products. Current Opinions in Plant Biology 8 : 280 291.
54. Kacser H Burns JA. 1973. The control of flux. Symposium for the Society of Experimental Biology 27 : 65 104.
55. Koffas M Roberge C Lee K Stephanopoulos G. 1999. Metabolic engineering. Annual Review of Biomedical Engineering 1 : 535 557.
56. Krebs HA Johnson WA. 1937. The role of the citric acid cycle in intermediary metabolism in animal tissues. Enzymologia 4 : 148 156.
57. Lee TI Rinaldi NJ Robert F Odom DT Bar-Joseph Z Gerber GK Hannett NM Harbison CT Thompson CM Simon I Zeitlinger J Jennings EG Murray HL Gordon DB Ren B Wyrick JJ Tagne JB Volkert TL Fraenkel E Gifford DK Young RA. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298 : 799 804.
58. Lonosky PM Zhang X Honavar VG Dobbs DL Fu A Rodermel SR. 2004. A proteomic analysis of maize chloroplast biogenesis. Plant Physiology 134 : 560 574.
59. Luscombe NM Babu MM Yu H Snyder M Teichmann SA Gerstein M. 2004. Genomic analysis of regulatory network dynamics reveals large topological changes. Nature 431 : 308 312.
60. Mann M Jensen ON. 2003. Proteomic analysis of post-translational modifications. Nature Biotechnology 21 : 255 261.
61. Marchand C Le Marechal P Meyer Y Miginiac-Maslow M Issakidis-Bourguet E Decottignies P. 2004. New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4 : 2696 2706.
62. Masse G Belt ST Rowland SJ Rohmer S. 2004. Isoprenoid biosynthesis in the diatoms. Rhizosolenia setigera (Brightwell) and Haulea ostrearia (Simonsen). Proceedings of the National Academy of Sciences, USA 101 : 4413 4418.
63. Mendes P Kell DB Westerhoff HV. 1992. Channelling can decrease pool size. European Journal of Biochemistry 204 : 257 266.
64. Millar AHM Heazlewood JL Kristensen BK Braun HP Moller IM. 2004. The plant mitochondrial proteome. Trends in Plant Science 10 : 36 43.
65. Milo R Shen-Orr S Itzkovitz S Kashtan N Chklovskii D Alon U. 2002. Network motifs: simple building blocks of complex networks. Science 298 : 824 827.
66. Moller B Conn E. 1980. The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (limm) Moench. Journal of Biological Chemistry 255 : 3049 3056.
67. Motohashi K Kondoh A Stumpp MT Hisabori T. 2001. Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proceedings of the National Academy of Sciences, USA 98 : 11224 11229.
68. Mueller LA Zhang PF Rhee SY. 2003. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiology 122 : 453 460.
69. Nuhse TS Stensballe A Jensen ON Peck SC. 2004. Phosphoproteomics of the Arabidopsis Plasma Membrane and a New Phosphorylation Site Database. Plant Cell 16 : 2394 2405.
70. Oksmann Kaldentey KM Saito K. 2005. Integrating genomics and metabolomics for engineering plant metabolic pathways. Current Opinions in Biotech 16 : 174 179.
71. Oltvai ZN Barabasi AL. 2002. Life's complexity pyramid. Science 298 : 763 764.
72. Ong SE Blagoev B Kratchmarova I Kristensen DB Steen H Pandey A Mann M. 2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular Cell Proteomics 1 : 376 386.
73. Panicot M Minguet EG Ferrando A Alcazar R Blazquez MA Carbonell J Altabella T Koncz. C Tiburcio AF. 2002. A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14 : 2539 2551.
74. Plaxton WC. 1996. The organization and regulation of plant glycolysis. Annual Review of Plant Physiology and Plant Molecular Biology 47 : 185 214.
75. Raamsdoonk LM Teusink B Broadhurst D Zhang NS Hayes A Walsh MC Berden JA Brindle KM Kell DB Rowland JJ Westerhoff HV van Dam K Oliver SG. 2001. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutants. Nature Biotechnology 19 : 45 50.
76. Ratcliffe RG Shachar-Hill Y. 2004. Revealing metabolic phenotypes in plants: inputs from NMR analysis. Biology Reviews 80 : 27 43.
77. Ravasz E Somera AL Mongru DA Oltvai ZN Barabasi AL. 2002. Hierarchical organization of modularity in metabolic networks. Science 297 : 1551 1555.
78. Rey P Cuine S Eymery F Garin J Court M Jacquot JP Rouhier N Broin M. 2005. Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant Journal 41 : 31 42.
79. Robinson JB Inman L Sumegi B Srere PA. 1987. Further characterisation of the Krebs tricarboxylic acid cycle metabolon. Journal of Biological Chemistry 262 : 1786 1790.
80. Roessner U Luedemann A Brust D Fiehn O Linke T Willmitzer L Fernie AR. 2001. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13 : 11 29.
81. Roessner-Tunali U Hegemann B Lytovchenko A Carrari F Bruedigam C Granot D Fernie AR. 2003. Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiology 133 : 84 99.
82. Roessner-Tunali U Liu J Leisse A Balbo I Perez-Melis A Willmitzer L Fernie AR. 2004. Kinetics of labelling of organic and amino acids in potato tubers by gas-chromatography mass spectrometry following incubation in C-13 labelled isotopes. Plant Journal 39 : 668 679.
83. Rohila JS Chen M Cerny R Fromm ME. 2004. Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant Journal 38 : 172 181.
84. Rontein D Dieuaide-Noubhani M Duforc EJ Raymond P Rolin D. 2002. The metabolic architecture of plant cells - stability of central metabolism and flexibility of metabolic pathways during the growth cycle of tomato cells. Journal of Biological Chemistry 277 : 43948 43960.
85. Sauer U. 2004. High-throughput phenomics: experimental methods for mapping fluxomes. Current Opinions in Biotechnology 15 : 58 63.
86. Savageau M. 1976. Biochemical Systems Analysis: a Study of Function and Design in Molecular Biology. Reading, MA, USA : Addison-Wesley.
87. Schuster S Dandekar T Fell DA. 1999. Detection of elementary flux modes in biochemical networks: a promising tool for pathway analysis and metabolic engineering. Trends in Biotechnology 17 : 53 60.
88. Schwender J Goffmann F Ohlrogge JB Schachar-Hill Y. 2004. Rubicso without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432 : 779 782.
89. Schwender J Ohlrogge JB 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.
90. Sessions A Burke E Presting G Aux G McElver J Patton D Dietrich B Ho P Bacwaden J Ko C Clarke JD Cotton D Bullis D Snell J Miguel T Hutchison D Kimmerly B Mitzel T Katagiri F Glazebrook J Law M Goff SA. 2002. A high-throughput Arabidopsis reverse genetics system. Plant Cell 14 : 2985 2994.
91. Sheen J. 1990. Metabolic repression of transcription in higher plants. Plant Cell 2 : 1027 1038.
92. Shen-Orr SS Milo R Mangan S Alon U. 2002. Network motifs in the transcriptional regulation network of Escherichia coli. Nature Genetics 31 : 64 68.
93. Srere PA. 1985. The metabolon. Trends in Biochemistry and Sciences 10 : 109 110.
94. Sriram G Fulton DB Iyer VV Peterson JM Zhou RL Westgate ME Spalding MH Shanks JV. 2004. Quantification of compartmented metabolic fluxes in developing soybean embryos by employing biosynthetically directed fractional C-13 labelling, [C-13, H-1] two-dimensional nuclear magnetic resonance and comprehensive isotopomer balancing. Plant Physiology 136 : 3043 3057.
95. Stepansky A Yao YL Tang GL Galili G. 2005. Regulation of lysine catabolism in Arabidopsis through concertedly regulated synthesis of the two distinct gene products of the composite AtLKR/SDH locus. Journal of Experimental Botany 56 : 525 536.
96. Stephanopoulos G Alper H Moxley J. 2004. Exploiting biological complexity for strain improvement through systems biology. Nature Biotechology 22 : 1261 1267.
97. Steuer R Kurths J Fiehn O Weckwerth W. 2003. Observing and interpreting correlations in metabolomic networks. Bioinformatics 19 : 1019 1026.
98. Stitt M Fernie AR. 2003. From measurement of metabolites to metabolomics an 'on the fly' perspective illustrated by recent studies of carbon-nitrogen interactions. Current Opinions in Biotechnology 14 : 136 144.
99. Stitt M Mueller C Matt P Gibon Y Carillo P Morcuende R Scheible WR Krapp A. 2002. Steps towards an integrated view of nitrogen metabolism. Journal of Experimental Botany 53 : 959 970.
100. Sudarasan N Barrick JE Breaker RR. 2003. Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9 : 644 647.
101. Suss KH Arkona C Manteuffel R Adler K. 1993. Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Proceedings of the National Academy of Sciences, USA 90 : 5514 5518.
102. Suzuki H Achnine L Xu R Matsuda SPT Dixon RA. 2002. A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula. Plant Journal 32 : 1033 1048.
103. Sweetlove LJ Last RL Fernie AR. 2003. Predictive metabolic engineering: a goal for systems biology. Plant Physiology 132 : 420 425.
104. Tang GQ Hardin SC Dewey R Huber SC. 2003. A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds. Plant Journal 34 : 77 93.
105. Templeton GW Moorhead GBG. 2004. A renaissance of metabolite sensing and signalling from modular domains to riboswitches. Plant Cell 16 : 2252 2257.
106. Ter Kuile BH Westerhoff HV. 2001. Transcriptome meets metabolome: hierarchical and metabolic regulation of the glycolytic pathway. FEBS Letters 500 : 169 171.
107. The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 : 796 815.
108. Thimm O Blasing O Gibon Y Nagel A Meyer S Kruger P Selbig J Muller LA Rhee SY Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal 37 : 914 939.
109. Tohge T Nishiyama Y Hirai MY Yano M Nakajima J Awazuhara M Inoue E Takahashi H Goodenowe DB Kitayama M Noji M Yamazaki M Saito K. 2005. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidoposis plants overexpressing a MYB transcription factor. Plant Journal 42 : 218 235
110. Tyers M Mann M. 2003. From genomics to proteomics. Nature 422 : 193 197.
111. Urbanczyk-Wochniak E Leisse A Roessner-Tunali U Lytovchenko A Reismeier J Willmitzer. L Fernie AR. 2003b. Expression of a bacterial xylose isomerase in potato tubers results in an altered hexose composition and a consequent induction of metabolism. Plant Cell Physiology 44 : 1359 1367.
112. Urbanczyk-Wochniak E Luedemann A Kopka J Selbig J Roessner-Tunali U Willmitzer L Fernie AR. 2003a. Parallel analysis of transcript and metabolite profiles: a new approach in systems biology. EMBO Reports 4 : 989 993.
113. Wagner A Fell DA. 2001. The small world inside large metabolic networks. Proceedings of the Royal Society of London, B 268 : 1803 1810.
114. Wang RC Okamoto M Xing XJ Crawford NM. 2003. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiology 132 : 556 567.
115. Wasaki J Yonetani R Kuroda S Shinano T Yazaki J Fujii F Shimbo K Yamamoto K Sakata. K Sasaki T Kishimoto N Kikuchi S Yamagishi M Osaki M. 2003. Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant, Cell & Environment 26 : 1515 1523.
116. Watts DJ Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature 393 : 440 442.
117. Weckwerth W. 2004. Metabolomics in systems biology. Annual Review of Plant Biology 54 : 669 689.
118. Weckwerth W Fiehn O. 2002. Can we discover novel pathways using metabolomic analysis? Current Opinion in Biotechnology 13 : 156 160.
119. Wheeler GL Jones MA Smirnoff N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393 : 365 369.
120. van Wijk KJ. 2004. Plastid proteomics. Plant Physiological Biochemistry 42 : 963 977.
121. Winkel BSJ. 2004. Metabolic channeling in plants. Annual Review of Plant Biology 55 : 85 107.
122. Winkel-Shirley B. 1999. Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiological Plant 107 : 142 149.
123. Wolferetz M Sharkey TD Boland W Kühnemann F. 2004. Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis. Plant Physiology 135 : 1939 1945.
124. Wong JH Cai N Balmer Y Tanaka CK Vensel WH Hurkman WJ Buchanan BB. 2004. Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches. Phytochemistry 65 : 1629 1640.
125. Yano H Wong JH Lee YM Cho MJ Buchanan BB. 2001. A strategy for the identification of proteins targeted by thioredoxin. Proceedings of the National Academy of Sciences, USA 98 : 4794 4799.
126. Yanofsky C Rachmeier M. 1958. The exclusion of free indole as an intermediate in the biosynthesis of tryptophan in Neurosporra crassa. Biochimica et Biophysica Acta 28 : 640 641.
127. Zalokar M. 1960. Cytochemistry of centrifuged hyphae of Neurosporra. Experimental Cell Research 19 : 114 132.
128. Zaslaver A Mayo AE Rosenberg R Bashkin P Sberro H Tsalyuk M Surette MG Alon U. 2004. Just-in-time transcription program in metabolic pathways. Nature Genetics 36 : 486 491.
129. Zhu XH Galili G. 2003. Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulated the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15 : 845 853.
130. Zhu XH Tang GL Galili G. 2002. The activity of the Arabidopsis bifunctional lysine-ketoglutarate reductase/saccharopine dehydrogenase enzyme of lysine catabolism is regulated by functional interaction between its two enzyme domains. Journal of Biological Chemistry 277 : 49655 49661.