Metabolic flux analysis as a tool in metabolic engineering of plants.

Methods of metabolic flux analysis (MFA) provide insights into the theoretical capabilities of metabolic networks and allow probing the in vivo performance of cellular metabolism. In recent years, an increasing awareness has developed that network analysis methods within the systems biology toolbox are serving to improve our understanding and ability to manipulate metabolism. In this minireview the potential of MFA to increase the chances of success in metabolic engineering of plants is presented, recent progress related to engineering and flux analysis in central metabolism of plants is discussed, and some recent advances in flux analysis methodology are highlighted.

[1]  A. Stepansky,et al.  Lysine catabolism, an effective versatile regulator of lysine level in plants , 2006, Amino Acids.

[2]  P. Christou,et al.  Progress in plant metabolic engineering. , 2004, Current opinion in biotechnology.

[3]  G. Stephanopoulos,et al.  Flux amplification in complex metabolic networks , 1997 .

[4]  James E. Bailey,et al.  Lessons from metabolic engineering for functional genomics and drug discovery , 1999, Nature Biotechnology.

[5]  Ganesh Sriram,et al.  Quantification of Compartmented Metabolic Fluxes in Developing Soybean Embryos by Employing Biosynthetically Directed Fractional 13C Labeling, Two-Dimensional [13C, 1H] Nuclear Magnetic Resonance, and Comprehensive Isotopomer Balancing1[w] , 2004, Plant Physiology.

[6]  J. Morgan,et al.  A transient isotopic labeling methodology for 13C metabolic flux analysis of photoautotrophic microorganisms. , 2007, Phytochemistry.

[7]  R. Steuer Computational approaches to the topology, stability and dynamics of metabolic networks. , 2007, Phytochemistry.

[8]  Melvin Calvin,et al.  The Path of Carbon in Photosynthesis: The carbon cycle is a tool for exploring chemical biodynamics and the mechanism of quantum conversion , 1962 .

[9]  Alisdair R Fernie,et al.  The complex network of non-cellulosic carbohydrate metabolism. , 2007, Current opinion in plant biology.

[10]  Nicola Zamboni,et al.  Model-independent fluxome profiling from 2H and 13C experiments for metabolic variant discrimination , 2004, Genome Biology.

[11]  Dominique Rolin,et al.  A New Substrate Cycle in Plants. Evidence for a High Glucose-Phosphate-to-Glucose Turnover from in Vivo Steady-State and Pulse-Labeling Experiments with [13C]Glucose and [14C]Glucose1 , 2005, Plant Physiology.

[12]  D. Fell Understanding the Control of Metabolism , 1996 .

[13]  J. Shanks,et al.  Flux quantification in central carbon metabolism of Catharanthus roseus hairy roots by 13C labeling and comprehensive bondomer balancing. , 2007, Phytochemistry.

[14]  J. Schwender,et al.  Mitochondrial Metabolism in Developing Embryos of Brassica napus*♦ , 2006, Journal of Biological Chemistry.

[15]  H. Rolletschek,et al.  Seed-specific expression of a bacterial phosphoenolpyruvate carboxylase in Vicia narbonensis increases protein content and improves carbon economy. , 2004, Plant biotechnology journal.

[16]  Alisdair R Fernie,et al.  Predictive Metabolic Engineering: A Goal for Systems Biology1 , 2003, Plant Physiology.

[17]  W. Wiechert 13C metabolic flux analysis. , 2001, Metabolic engineering.

[18]  N. Kruger,et al.  Strategies for metabolic flux analysis in plants using isotope labelling. , 2000, Journal of biotechnology.

[19]  J. Ohlrogge,et al.  Compartment-specific labeling information in 13C metabolic flux analysis of plants. , 2007, Phytochemistry.

[20]  Björn H. Junker,et al.  Parallel determination of enzyme activities and in vivo fluxes in Brassica napus embryos grown on organic or inorganic nitrogen source. , 2007, Phytochemistry.

[21]  T. Voelker,et al.  Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. , 1992, Science.

[22]  Steffen Klamt,et al.  Structural and functional analysis of cellular networks with CellNetAnalyzer , 2007, BMC Systems Biology.

[23]  B. M. Lange,et al.  Experimental and mathematical approaches to modeling plant metabolic networks. , 2007, Phytochemistry.

[24]  R. Garcés,et al.  The sources of carbon and reducing power for fatty acid synthesis in the heterotrophic plastids of developing sunflower (Helianthus annuus L.) embryos. , 2005, Journal of experimental botany.

[25]  D. Fell,et al.  Getting to grips with the plant metabolic network. , 2008, The Biochemical journal.

[26]  H. Jenner,et al.  Transgenesis and yield: what are our targets? , 2003, Trends in biotechnology.

[27]  G. Stephanopoulos,et al.  Metabolic flux analysis in a nonstationary system: fed-batch fermentation of a high yielding strain of E. coli producing 1,3-propanediol. , 2007, Metabolic engineering.

[28]  G. Stephanopoulos,et al.  Metabolic Engineering: Principles And Methodologies , 1998 .

[29]  Yves Gibon,et al.  GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after 13CO2 labelling. , 2007, Phytochemistry.

[30]  J. Schwender,et al.  Understanding flux in plant metabolic networks. , 2004, Current opinion in plant biology.

[31]  H. Rolletschek,et al.  Antisense inhibition of the plastidial glucose-6-phosphate/phosphate translocator in Vicia seeds shifts cellular differentiation and promotes protein storage. , 2007, The Plant journal : for cell and molecular biology.

[32]  Y. Shachar-Hill,et al.  Measuring multiple fluxes through plant metabolic networks. , 2006, The Plant journal : for cell and molecular biology.

[33]  H. Rolletschek,et al.  Ectopic Expression of an Amino Acid Transporter (VfAAP1) in Seeds of Vicia narbonensis and Pea Increases Storage Proteins1 , 2005, Plant Physiology.

[34]  W. Römisch,et al.  Robustness of central carbohydrate metabolism in developing maize kernels. , 2006, Phytochemistry.

[35]  Fernando Carrari,et al.  Engineering central metabolism in crop species: learning the system. , 2003, Metabolic engineering.

[36]  J. Gregory,et al.  Folate biofortification of tomato fruit , 2007, Proceedings of the National Academy of Sciences.

[37]  N. Kruger,et al.  Vacuolar compartmentation complicates the steady-state analysis of glucose metabolism and forces reappraisal of sucrose cycling in plants. , 2007, Phytochemistry.

[38]  J. Ohlrogge,et al.  Expression of Lauroyl–Acyl Carrier Protein Thioesterase in Brassica napus Seeds Induces Pathways for Both Fatty Acid Oxidation and Biosynthesis and Implies a Set Point for Triacylglycerol Accumulation , 1998, Plant Cell.

[39]  B. Palsson,et al.  Theory for the systemic definition of metabolic pathways and their use in interpreting metabolic function from a pathway-oriented perspective. , 2000, Journal of theoretical biology.

[40]  A. Glieder,et al.  Engineering primary metabolic pathways of industrial micro-organisms. , 2007, Journal of biotechnology.

[41]  G. Stephanopoulos,et al.  Network rigidity and metabolic engineering in metabolite overproduction , 1991, Science.

[42]  J. Schwender,et al.  Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds , 2004, Nature.

[43]  U. Sauer,et al.  Article number: 62 REVIEW Metabolic networks in motion: 13 C-based flux analysis , 2022 .

[44]  D. Rolin,et al.  The Metabolic Architecture of Plant Cells , 2002, The Journal of Biological Chemistry.

[45]  Xinlu Chen,et al.  Understanding in Vivo Benzenoid Metabolism in Petunia Petal Tissue1 , 2004, Plant Physiology.

[46]  J. Bailey,et al.  Toward a science of metabolic engineering , 1991, Science.

[47]  M. Dieuaide-Noubhani,et al.  Quantification of Compartmented Metabolic Fluxes in Maize Root Tips Using Isotope Distribution from 13C- or 14C-Labeled Glucose (*) , 1995, The Journal of Biological Chemistry.

[48]  W. Eisenreich,et al.  13CO2 as a universal metabolic tracer in isotopologue perturbation experiments. , 2007, Phytochemistry.

[49]  A. Alonso,et al.  Substrate cycles in the central metabolism of maize root tips under hypoxia. , 2007, Phytochemistry.

[50]  W. Eisenreich,et al.  Changes in flux pattern of the central carbohydrate metabolism during kernel development in maize. , 2005, Phytochemistry.

[51]  F. Podestá,et al.  The Functional Organization and Control of Plant Respiration , 2006 .

[52]  U. Sauer,et al.  Fluxome Profiling in Microbes , 2005 .

[53]  Lothar Willmitzer,et al.  Sucrose to starch: a transition in molecular plant physiology. , 2002, Trends in plant science.

[54]  Gregory Stephanopoulos,et al.  Evaluation of regression models in metabolic physiology: predicting fluxes from isotopic data without knowledge of the pathway , 2006, Metabolomics.

[55]  H. Rolletschek,et al.  Antisense-inhibition of ADP-glucose pyrophosphorylase in Vicia narbonensis seeds increases soluble sugars and leads to higher water and nitrogen uptake , 2002, Planta.

[56]  Chen Yang,et al.  Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. , 2002, Metabolic engineering.

[57]  Fumio Matsuda,et al.  Estimation of metabolic fluxes, expression levels and metabolite dynamics of a secondary metabolic pathway in potato using label pulse-feeding experiments combined with kinetic network modelling and simulation. , 2007, The Plant journal : for cell and molecular biology.

[58]  H. Weber,et al.  Uptake and allocation of carbon and nitrogen in Vicia narbonensis plants with increased seed sink strength achieved by seed-specific expression of an amino acid permease. , 2007, Journal of experimental botany.

[59]  J J Heijnen,et al.  Metabolic flux control analysis of branch points: an improved approach to obtain flux control coefficients from large perturbation data. , 2004, Metabolic engineering.

[60]  Jörg Schwender,et al.  Probing in Vivo Metabolism by Stable Isotope Labeling of Storage Lipids and Proteins in Developing Brassica napusEmbryos1 , 2002, Plant Physiology.

[61]  J. L. Liu,et al.  Determination of metabolic fluxes in a non-steady-state system. , 2007, Phytochemistry.

[62]  A. D. de Graaf,et al.  A metabolic flux analysis to study the role of sucrose synthase in the regulation of the carbon partitioning in central metabolism in maize root tips. , 2007, Metabolic engineering.

[63]  E. Pichersky,et al.  Reduction of Benzenoid Synthesis in Petunia Flowers Reveals Multiple Pathways to Benzoic Acid and Enhancement in Auxin Transport[W] , 2006, The Plant Cell Online.

[64]  P. Beyer,et al.  Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. , 2000, Science.

[65]  Y. Shachar-Hill,et al.  Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. , 2000, Plant physiology.

[66]  F. Goffman,et al.  Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos. , 2007, The Plant journal : for cell and molecular biology.

[67]  B. Palsson,et al.  Metabolic modelling of microbes: the flux-balance approach. , 2002, Environmental microbiology.

[68]  F. Salamini,et al.  Plant biotechnology and breeding: allied for years to come. , 2003, Trends in plant science.

[69]  D. Fell,et al.  Detection of elementary flux modes in biochemical networks: a promising tool for pathway analysis and metabolic engineering. , 1999, Trends in biotechnology.

[70]  J. Schwender,et al.  A Flux Model of Glycolysis and the Oxidative Pentosephosphate Pathway in Developing Brassica napus Embryos* , 2003, Journal of Biological Chemistry.

[71]  S. Lee,et al.  Metabolic flux analysis and metabolic engineering of microorganisms. , 2008, Molecular bioSystems.

[72]  G. Stephanopoulos,et al.  Elementary metabolite units (EMU): a novel framework for modeling isotopic distributions. , 2007, Metabolic engineering.

[73]  M. Calvin The path of carbon in photosynthesis. , 1948, Harvey lectures.

[74]  D. DellaPenna,et al.  Elevating the vitamin E content of plants through metabolic engineering. , 1998, Science.

[75]  U. Wobus,et al.  Molecular physiology of legume seed development. , 2005, Annual review of plant biology.

[76]  Andreas Richter,et al.  Ectopic expression of phosphoenolpyruvate carboxylase in Vicia narbonensis seeds: effects of improved nutrient status on seed maturation and transcriptional regulatory networks. , 2007, The Plant journal : for cell and molecular biology.