Comprehensive classification and perspective for modelling photorespiratory metabolism.

Biological processes involved in photorespiratory and photosynthetic metabolism operate concurrently and affect the interplay between carbon and nitrogen assimilation reflected in plant growth. Experimental evidence has indicated that photorespiratory metabolism has a wide-ranging influence not only on other principal metabolic pathways but also on a multitude of signalling cascades. Therefore, accurate quantitative models of photorespiration can provide a means for predicting and in silico probing of plant behaviour at various levels of the system. We first present a comprehensive classification of current models of photorespiratory metabolism developed within the existing carbon-centric modelling paradigm. We then offer a perspective for modelling photorespiratory metabolism by considering the coupling of carbon and nitrogen metabolism in the context of compartmentalised, genome-scale metabolic models of C3 plants. In addition, we outline the challenges stemming from the need to consider plant metabolic and signalling pathways in assessing the still controversial role of photorespiration and to confront the devised models with the ever-increasing amounts of high-throughput data.

[1]  Yixin Chen,et al.  Integrating Flux Balance Analysis into Kinetic Models to Decipher the Dynamic Metabolism of Shewanella oneidensis MR-1 , 2012, PLoS Comput. Biol..

[2]  H. Schultz.  Extension of a Farquhar model for limitations of leaf photosynthesis induced by light environment, phenology and leaf age in grapevines (Vitis vinifera L. cvv. White Riesling and Zinfandel). , 2003, Functional plant biology : FPB.

[3]  A. Rogers,et al.  Rising atmospheric carbon dioxide: plants FACE the future. , 2004, Annual review of plant biology.

[4]  Jamey D. Young,et al.  Mapping photoautotrophic metabolism with isotopically nonstationary (13)C flux analysis. , 2011, Metabolic engineering.

[5]  C. Maranas,et al.  Zea mays iRS1563: A Comprehensive Genome-Scale Metabolic Reconstruction of Maize Metabolism , 2011, PloS one.

[6]  A. Igamberdiev,et al.  The role of photorespiration in redox and energy balance of photosynthetic plant cells: A study with a barley mutant deficient in glycine decarboxylase. , 2001, Physiologia plantarum.

[7]  D. Fell,et al.  A Genome-Scale Metabolic Model of Arabidopsis and Some of Its Properties1[C][W] , 2009, Plant Physiology.

[8]  G. Farquhar,et al.  Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase. , 1979, Archives of biochemistry and biophysics.

[9]  E. B. Tregunna,et al.  Effect of Oxygen on the Rate of Photorespiration in Detached Tobacco Leaves , 1966 .

[10]  Xin-Guang Zhu,et al.  Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm1[W][OA] , 2007, Plant Physiology.

[11]  B. Palsson,et al.  Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis , 2012, Proceedings of the National Academy of Sciences.

[12]  C T Verrips,et al.  A structured, minimal parameter model of the central nitrogen metabolism in Saccharomyces cerevisiae: the prediction of the behavior of mutants. , 1998, Journal of theoretical biology.

[13]  A. Fernie,et al.  Photorespiration: players, partners and origin. , 2010, Trends in plant science.

[14]  S. Driscoll,et al.  Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? , 2002, Annals of botany.

[15]  W. Lockau,et al.  The Metabolic Network of Synechocystis sp. PCC 6803: Systemic Properties of Autotrophic Growth1[C][W] , 2010, Plant Physiology.

[16]  W. Ogren,et al.  Ribulose diphosphate carboxylase regulates soybean photorespiration. , 1971, Nature: New biology.

[17]  Robert W. Pearcy,et al.  Observed and modelled stomatal responses to dynamic light environments in the shade plant Alocasia macrorrhiza , 1988 .

[18]  J. Cheeseman.  Hydrogen Peroxide and Plant Stress: A Challenging Relationship , 2007 .

[19]  P. Horton,et al.  Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons , 2004, Photosynthesis Research.

[20]  Nan Xiao,et al.  Integrating metabolic, transcriptional regulatory and signal transduction models in Escherichia coli , 2008, Bioinform..

[21]  Zoran Nikoloski,et al.  A quantitative comparison of Calvin-Benson cycle models. , 2011, Trends in plant science.

[22]  W. Parton,et al.  Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide , 2004 .

[23]  Jim K. Fredrickson,et al.  Genome-Scale Modeling of Light-Driven Reductant Partitioning and Carbon Fluxes in Diazotrophic Unicellular Cyanobacterium Cyanothece sp. ATCC 51142 , 2012, PLoS Comput. Biol..

[24]  R. Häusler,et al.  The regulation and control of photorespiration , 1995 .

[25]  M. Spalding.  Chapter 8 – The CO2-Concentrating Mechanism and Carbon Assimilation , 2009 .

[26]  P. Karp,et al.  Creation of a Genome-Wide Metabolic Pathway Database for Populus trichocarpa Using a New Approach for Reconstruction and Curation of Metabolic Pathways for Plants1[W][OA] , 2010, Plant Physiology.

[27]  Bernhard O. Palsson,et al.  Metabolic Reconstruction and Modeling of Nitrogen Fixation in Rhizobium etli , 2007, PLoS Comput. Biol..

[28]  S. Rabouille,et al.  Modeling the Dynamic Regulation of Nitrogen Fixation in the Cyanobacterium Trichodesmium sp , 2006, Applied and Environmental Microbiology.

[29]  Holger Fröhlich,et al.  Modeling ERBB receptor-regulated G1/S transition to find novel targets for de novo trastuzumab resistance , 2009, BMC Systems Biology.

[30]  Jason A. Papin,et al.  Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism , 2011, Molecular systems biology.

[31]  J. Hancock,et al.  Hydrogen peroxide and nitric oxide as signalling molecules in plants. , 2002, Journal of experimental botany.

[32]  Thomas D. Sharkey,et al.  Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations , 2008, The Botanical Review.

[33]  Y. Shachar-Hill,et al.  Plant one-carbon metabolism and its engineering. , 2000, Trends in plant science.

[34]  D. Lawlor,et al.  Compartmental modelling of photorespiration and carbon metabolism of water stressed leaves , 1981 .

[35]  M CALVIN.  Chemical and photochemical reactions of thioctic acid and related disulfides. , 1954, Federation proceedings.

[36]  G. Edwards,et al.  A mechanistic model for photosynthesis based on the multisubstrate ordered reaction of ribulose 1,5 bisphosphate carboxylase , 1988 .

[37]  L. Gross,et al.  A dynamic model of photosynthesis in varying light taking account of stomatal conductance, C3-cycle intermediates, photorespiration and Rubisco activation , 1991 .

[38]  B. D. Hahn.  Photosynthesis and photorespiration: Modelling the essentials , 1991 .

[39]  A. Bloom.  As carbon dioxide rises, food quality will decline without careful nitrogen management , 2009 .

[40]  B. D. Hahn.  A Mathematical Model of the Calvin Cycle: Analysis of the Steady State , 1986 .

[41]  C. Foyer,et al.  Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. , 2009, Annual review of plant biology.

[42]  E. Ruppin,et al.  Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity , 2011, Proceedings of the National Academy of Sciences.

[43]  L. Quek,et al.  AraGEM, a Genome-Scale Reconstruction of the Primary Metabolic Network in Arabidopsis1[W] , 2009, Plant Physiology.

[44]  R. L. Baldwin,et al.  Quantitative and dynamic aspects of nitrogen metabolism in the rumen: a modeling analysis. , 1979, Journal of animal science.

[45]  B. D. Hahn.  A Mathematical Model of Leaf Carbon Metabolism , 1984 .

[46]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[47]  H Sinoquet,et al.  A biochemical model of photosynthesis for mango leaves: evidence for the effect of fruit on photosynthetic capacity of nearby leaves. , 2003, Tree physiology.

[48]  Olaf Wolkenhauer,et al.  Modeling the Calvin-Benson cycle , 2011, BMC Systems Biology.

[49]  John A. Morgan,et al.  BMC Systems Biology BioMed Central Research article , 2009 .

[50]  Hermann Bauwe,et al.  Photorespiration has a dual origin and manifold links to central metabolism. , 2012, Current opinion in plant biology.

[51]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[52]  Lake-Ee Quek,et al.  AlgaGEM – a genome-scale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome , 2011, BMC Genomics.

[53]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[54]  Lee J. Sweetlove,et al.  Flux-Balance Modeling of Plant Metabolism , 2011, Front. Plant Sci..

[55]  W. Laing,et al.  Regulation of Soybean Net Photosynthetic CO(2) Fixation by the Interaction of CO(2), O(2), and Ribulose 1,5-Diphosphate Carboxylase. , 1974, Plant physiology.

[56]  F. Llaneras,et al.  Stoichiometric modelling of cell metabolism. , 2008, Journal of bioscience and bioengineering.

[57]  B. Palsson,et al.  Regulation of gene expression in flux balance models of metabolism. , 2001, Journal of theoretical biology.

[58]  D. Smart,et al.  Nitrogen assimilation and growth of wheat under elevated carbon dioxide , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  W. Weckwerth,et al.  A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis[W] , 2008, The Plant Cell Online.

[60]  Brian D. Hahn,et al.  A Mathematical Model of Photorespiration and Photosynthesis , 1987 .

[61]  L. Quek,et al.  C4GEM, a Genome-Scale Metabolic Model to Study C4 Plant Metabolism1[W][OA] , 2010, Plant Physiology.

[62]  G. Krotkov,et al.  Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. I. Soybean. , 1966, Plant physiology.