Cited by 131Microbial Metabolic Engineering and BioproductionBioinformatics and Genomic NetworksGene Regulatory Network Analysis

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Bottom-up Metabolic Reconstruction of Arabidopsis and Its Application to Determining the Metabolic Costs of Enzyme Production

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Arnold, Anne, Nikoloski, Zoran·2014·Plant Physiology

DOI 10.1104/pp.114.235358PMC PMC4081344

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Abstract

Large-scale modeling of plant metabolism provides the possibility to compare and contrast different cellular and environmental scenarios with the ultimate aim of identifying the components underlying the respective plant behavior. The existing models of Arabidopsis (Arabidopsis thaliana) are top-down assembled, whereby the starting point is the annotated genome, in particular, the metabolic genes. Hence, dead-end metabolites and blocked reactions can arise that are subsequently addressed by using gap-filling algorithms in combination with species-unspecific genes. Here, we present a bottom-up-assembled, large-scale model that relies solely on Arabidopsis-specific annotations and results in the inclusion of only manually curated reactions. While the existing models are largely condition unspecific by employing a single biomass reaction, we provide three biomass compositions that pertain to realistic and frequently examined scenarios: carbon-limiting, nitrogen-limiting, and optimal growth conditions. The comparative analysis indicates that the proposed Arabidopsis core model exhibits comparable efficiency in carbon utilization and flexibility to the existing network alternatives. Moreover, the model is utilized to quantify the energy demand of amino acid and enzyme de novo synthesis in photoautotrophic growth conditions. Illustrated by the case of the most abundant protein in the world, Rubisco, we determine its synthesis cost in terms of ATP requirements. This, in turn, allows us to explore the tradeoff between protein synthesis and growth in Arabidopsis. Altogether, the model provides a solid basis for completely species-specific integration of high-throughput data, such as gene expression levels, and for condition-specific investigations of in silico metabolic engineering strategies.

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KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232
mapman : a user‐driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes
Thimm, O., Bläsing, O. E., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L. A., Rhee, S. Y., & Stitt, M. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02016.x · Cited by 3,356
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools
Lamesch, P., Berardini, T., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Müller, R., Dreher, K. A., Alexander, D. L., Garcia-Hernandez, M., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1090 · Cited by 2,378
In Vivo Half-Life of a Protein Is a Function of Its Amino-Terminal Residue
Bachmair, A., Finley, D. J., & Varshavsky, A. J. (1986) · Science · doi:10.1126/science.3018930 · Cited by 1,976
A protocol for generating a high-quality genome-scale metabolic reconstruction
Thiele, I., & Palsson, B. Ø. (2010) · Nature Protocols · doi:10.1038/nprot.2009.203 · Cited by 1,789
Activities at the Universal Protein Resource (UniProt)
The UniProt Consortium (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1140 · Cited by 1,736
The use of metabolomics to dissect plant responses to abiotic stresses
Obata, T., & Fernie, A. R. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1091-5 · Cited by 912
Constraining the metabolic genotype–phenotype relationship using a phylogeny of in silico methods
Lewis, N. E., Nagarajan, H., & Palsson, B. O. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2737 · Cited by 779
Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized
Tcherkez, G. G. B., Farquhar, G. D., & Andrews, T. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600605103 · Cited by 777
Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis
Akashi, H. D., & Gojobori, T. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062526999 · Cited by 687
Update on activities at the Universal Protein Resource (UniProt) in 2013
The UniProt Consortium (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1068 · Cited by 674
The most abundant protein in the world
Ellis, R. J. (1979) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(79)90212-3 · Cited by 672
Genomic Analysis of a Nutrient Response in Arabidopsis Reveals Diverse Expression Patterns and Novel Metabolic and Potential Regulatory Genes Induced by Nitrate
Wang, R., Guegler, K. J., LaBrie, S. T., & Crawford, N. M. (2000) · The Plant Cell · doi:10.1105/tpc.12.8.1491 · Cited by 585
Universality and Structure of the N-end Rule
Gonda, D. K., Bachmair, A., Wünning, I., Tobias, J. W., Lane, W. S., & Varshavsky, A. J. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84762-2 · Cited by 476
The N-end rule
Varshavsky, A. J. (1992) · Cell · doi:10.1016/0092-8674(92)90285-k · Cited by 467
Proton-powered turbine of a plant motor
Seelert, H., Poetsch, A., Dencher, N. A., Engel, A. H., Stahlberg, H., & Müller, D. J. (2000) · Nature · doi:10.1038/35013148 · Cited by 465
AraCyc: A Biochemical Pathway Database for Arabidopsis
Mueller, L. A., Zhang, P., & Rhee, S. Y. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.102.017236 · Cited by 432
Sugar transporters in higher plants – a diversity of roles and complex regulation
Williams, L. E., Lemoine, R., & Sauer, N. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01681-2 · Cited by 424
Energy Constraints on the Evolution of Gene Expression
Wagner, A. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi126 · Cited by 419
BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA
Schomburg, I., Chang, A., Placzek, S., Söhngen, C., Rother, M., Lang, M., Munaretto, C., Ulas, S., Stelzer, M., Grote, A., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1049 · Cited by 418
Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post‐translational activation of ADP‐glucose pyrophosphorylase in the following light period
Gibon, Y., Bläsing, O. E., Palacios‐Rojas, N., Panković, D. M., Hendriks, J. H. M., Fisahn, J., Höhne, M., Guenther, M., & Stitt, M. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02173.x · Cited by 413
PPDB, the Plant Proteomics Database at Cornell
Sun, Q., Zybailov, B., Majeran, W., Friso, G., Olinares, P. D. B., & van Wijk, K. J. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn654 · Cited by 400
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de Oliveira Dal'Molin, C. G., Quek, L.-E., Palfreyman, R. W., Brumbley, S. M., & Nielsen, L. K. (2010) · Plant Physiology · doi:10.1104/pp.109.148817 · Cited by 353
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Gibon, Y., Pyl, E., Ronan Sulpice, A., Lunn, J. E., Höhne, M., Guenther, M., & Stitt, M. (2009) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2009.01965.x · Cited by 331
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McCloskey, D., Palsson, B. Ø., & Feist, A. M. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.18 · Cited by 327
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Kumar, V. S., Dasika, M. S., & Maranas, C. D. (2007) · BMC Bioinformatics · doi:10.1186/1471-2105-8-212 · Cited by 315
The principle of flux minimization and its application to estimate stationary fluxes in metabolic networks
Holzhütter, H. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04213.x · Cited by 302
Isolation and Characterization of an Arabidopsis Mutant Deficient in the Thylakoid Lipid Digalactosyl Diacylglycerol
Dörmann, P., Hoffmann-Benning, S., Balbo, I., & Christoph Benning, A. (1995) · The Plant Cell · doi:10.1105/tpc.7.11.1801 · Cited by 299
A Genome-Scale Metabolic Model of Arabidopsis and Some of Its Properties
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Patterns of Expression and Normalized Levels of the Five Arabidopsis Phytochromes
Sharrock, R., & Clack, T. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.005389 · Cited by 295
High‐density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions
Caldana, C., Degenkolbe, T., Inostroza, A. C., Klie, S., Sulpice, R., Leisse, A., Steinhauser, D., Fernie, A. R., Willmitzer, L., & Hannah, M. A. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04640.x · Cited by 292
Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis
Piques, M., Schulze, W. X., Höhne, M., Usadel, B., Gibon, Y., Rohwer, J. M., & Stitt, M. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.68 · Cited by 287
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Mintz-Oron, S., Meir, S., Malitsky, S., Ruppin, E., Aharoni, A., & Shlomi, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100358109 · Cited by 244
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Tschoep, H., Gibon, Y., Carillo, P., Armengaud, P., Szecówka, M., Nunes‐Nesi, A., Fernie, A. R., Koehl, K., & Stitt, M. (2008) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2008.01921.x · Cited by 218
Peak exercise cardiac power output; a direct indicator of cardiac function strongly predictive of prognosis in chronic heart failure
Williams, S. (2001) · European Heart Journal · doi:10.1053/euhj.2000.2547 · Cited by 215
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Pick, T. R., Bräutigam, A., Schulz, M. A., Obata, T., Fernie, A. R., & Weber, A. P. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215142110 · Cited by 160
H+/ATP ratio of proton transport‐coupled ATP synthesis and hydrolysis catalysed by CF0F1—liposomes
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Cost-Minimization of Amino Acid Usage
Seligmann, H. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-002-2388-z · Cited by 147
Mutations in UDP-Glucose:Sterol Glucosyltransferase in Arabidopsis Cause Transparent Testa Phenotype and Suberization Defect in Seeds
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Cheung, C. Y. M., Williams, T. C. R., Poolman, M. G., Fell, D. A., Ratcliffe, R. G., & Sweetlove, L. J. (2013) · The Plant Journal · doi:10.1111/tpj.12252 · Cited by 134
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Williams, T. C. R., Miguet, L., Masakapalli, S. K., Kruger, N. J., Sweetlove, L. J., & Ratcliffe, R. G. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.125195 · Cited by 120
Early Salt Stress Effects on the Differential Expression of Vacuolar H+-ATPase Genes in Roots and Leaves of Mesembryanthemum crystallinum
Low, R., Rockel, B., Kirsch, M., Ratajczak, R., Hörtensteiner, S., Martinoia, E., Lüttge, U. E., & Rausch, T. (1996) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.1.259 · Cited by 118
Identification of protein stability determinants in chloroplasts
Apel, W., Schulze, W. X., & Bock, R. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2010.04268.x · Cited by 113
Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment
Stitt, M., Gibon, Y., Lunn, J. E., & Piques, M. (2007) · Functional Plant Biology · doi:10.1071/fp06249 · Cited by 103
Impact of the Carbon and Nitrogen Supply on Relationships and Connectivity between Metabolism and Biomass in a Broad Panel of Arabidopsis Accessions
Ronan Sulpice, A., Nikoloski, Z., Tschoep, H., António, C., Kleeßen, S., Larhlimi, A., Selbig, J., Ishihara, H., Gibon, Y., Fernie, A. R., et al. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.210104 · Cited by 101
Self-citation
Photosynthate costs associated with the utilization of different nitrogen–forms: influence on the carbon balance of plants and shoot–root biomass partitioning
Zerihun, A., McKenzie, B. A., & Morton, J. D. (1998) · New Phytologist · doi:10.1046/j.1469-8137.1998.00893.x · Cited by 91
Plant Sucrose Transporters from a Biophysical Point of View
Geiger, D. (2011) · Molecular Plant · doi:10.1093/mp/ssr029 · Cited by 81
Combined Transcript and Metabolite Profiling of Arabidopsis Grown under Widely Variant Growth Conditions Facilitates the Identification of Novel Metabolite-Mediated Regulation of Gene Expression
Hannah, M. A., Caldana, C., Steinhauser, D., Balbo, I., Fernie, A. R., & Willmitzer, L. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.147306 · Cited by 78
Structure and evolutionary conservation of the plant N-end rule pathway
Graciet, E., Mesiti, F., & Wellmer, F. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04099.x · Cited by 72
Selection costs of amino acid substitutions in ColE1 and ColIa gene clusters harbored by Escherichia coli
Craig, C. L., & Weber, R. S. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025981 · Cited by 71
Evolutionary Systems Biology of Amino Acid Biosynthetic Cost in Yeast
Barton, M. D., Delneri, D., Oliver, S. G., Rattray, M., & Bergman, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011935 · Cited by 69
Using quantitative proteomics of Arabidopsis roots and leaves to predict metabolic activity
Mooney, B., Miernyk, J. A., Greenlief, C. M., & Thelen, J. J. (2006) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2006.00746.x · Cited by 55
Costs of protein turnover and carbohydrate export in leaves of sun and shade species
Noguchi, K., Go, C.-S. U., Miyazawa, S., Terashima, I., Ueda, S., & Yoshinari, T. (2001) · Australian Journal of Plant Physiology · doi:10.1071/pp00057 · Cited by 54
Rubisco Oligomers Composed of Linked Small and Large Subunits Assemble in Tobacco Plastids and Have Higher Affinities for CO2 and O2
Whitney, S. M., Kane, H. J., Houtz, R. L., & Sharwood, R. E. (2009) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.135210 · Cited by 43
A novel approach for determining environment-specific protein costs: the case of Arabidopsis thaliana
Sajitz-Hermstein, M., & Nikoloski, Z. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq390 · Cited by 22
Self-citation
Structure of the brain.
Calderwood, H. (2011) · Macmillan eBooks · doi:10.1037/12415-002 · Cited by 6

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Authors: Arnold, A., & Nikoloski, Z.
Affiliations: Max Planck Institute of Molecular Plant Physiology (DE)
ORCID: Arnold, Anne
Nikoloski, Zoran
Venue: Plant Physiology
Publisher: Oxford University Press (OUP)
Published: 2014-05-07
Volume: 165
Issue: 3
Pages: 1380-1391
ISSN: 0032-0889 (ISSN-L)
1532-2548
DOI: 10.1104/pp.114.235358
PMC: PMC4081344
OpenAlex: W2055280476
Cited by: 131
References: 62
Citations by year: 2026: 5 · 2025: 14 · 2024: 7 · 2023: 18 · 2022: 7 · 2021: 18 · 2020: 11 · 2019: 10 · 2018: 13 · 2017: 5 · 2016: 8 · 2015: 10 · 2014: 5
FWCI: 3.83
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: aspb.org/publications/aspb-journals/open-articles (vor, 420 d)
Locations: PLANT PHYSIOLOGY (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords: Arabidopsis thaliana, biomass composition, carbon limitation, nitrogen limitation, photoautotrophic growth, ATP requirement, metabolic engineering

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Bottom-up Metabolic Reconstruction of Arabidopsis and Its Application to Determining the Metabolic Costs of Enzyme Production

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