Modeling the Kinetics of Activation and Reaction of Rubisco from Gas Exchange

  • Hadi Farazdaghi
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 29)

Oxygenic life begins with photosynthesis. This process controls natural CO2 sequestration and is responsible for terrestrial and marine life on the planet. An increase in the global CO2/O2 concentration ratio creates positive feedback cycles, which in the atmosphere, lead to increases in temperature and water holding capacity. In the oceans, the holding capacities of CO2 and other gases are decreased, leading to their release into the atmosphere and accelerated climate change.

Rubisco kinetic models are used as core modules for simulations of agricultural and natural productivity, environmental and ecological management, and climate change. Thus, a scientific theory that can be used reliably as the core module of such interactive processes is essential for maintaining the vitality of the planet. This chapter provides a comparison of the kinetic theories for Rubisco activation and reaction and their mathematical models. The two dominant schools of thought in the theory of Rubisco reaction are (1) the single-process or co-limitation theory and (2) the two-process theory. In the single-process theory, Rubisco is the gatekeeper and thus the paramount controller of CO2 fixation under any condition. The most widely used two-process theory assumes that carboxylation is limited by one of the two independent processes: (a) fully-activated RuBP-saturated capacity of Rubisco at low CO2, and (b) RuBP regeneration capacity at high CO2. The single-process model is consistent with a biochemically correct understanding of Rubisco reaction.


Plant Cell Environ Rubisco Activase Biochemical Model Menten Curve RuBP Regeneration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ainsworth EA, Rogers A, Blum H, Nösberger J and Long SP (2003) Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to Free Air CO2 Enrichment (FACE). J Exp Bot 54: 2769–2774PubMedCrossRefGoogle Scholar
  2. Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59(7): 1555–1568PubMedCrossRefGoogle Scholar
  3. Andralojc PJ, Dawson GW, Parry MA and Keys AJ (1994) Incorporation of carbon from photosynthetic products into 2-carboxyarabinitol-1-phosphate and 2-carboxyarabinitol. Biochemistry 304: 781–786Google Scholar
  4. Andrews TJ and Lorimer GH (1978) Photorespiration still unavoidable? FEBS Lett 90: 1–9CrossRefGoogle Scholar
  5. Arulanantham A, Raviraj L, Madhusudana R and Terry N (1990) Limiting factors in photosynthesis VI: Regeneration of ribulose 1,5-bisphosphate limits photosynthesis at low photochemical capacity. Plant Physiol 93: 1466–1475PubMedCrossRefGoogle Scholar
  6. Ashida H, Danchin A and Yokota A (2005) Was photosyn-thetic RuBisCO recruited by acquisitive evolution from RuBisCO-like proteins involved in sulfur metabolism? Research in Microbiology 156: 611–618PubMedCrossRefGoogle Scholar
  7. Ashida H, Saito Y, Nakano T, Tandeau de Marsac N, Sekowska A, Danchin A and Yokota A (2008) RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO. J Exp Bot 59: 1543–1554PubMedCrossRefGoogle Scholar
  8. Baldocchi DD and Wilson KB (2001) Modeling CO2 and water vapor exchange of a temperate broadleaved forest across hourly to decadal time scales. Ecol Modell 142: 155–184CrossRefGoogle Scholar
  9. Bernacchi CJ, Portis AR, Nakano H, Von Caemmerer S and Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130: 1992–1998PubMedCrossRefGoogle Scholar
  10. Blackman FF (1905) Optima and limiting factors. Ann Bot 19: 281–295Google Scholar
  11. Bowes G, Ogren WL and Hageman R (1971) Phosphogly-colate production catalysed by ribulose diphsophate car-boxylase. Biochem Biophys Res Commun 45: 716–722PubMedCrossRefGoogle Scholar
  12. Brooks A and Portis AR Jr (1988) Protein-bound Ribu-lose bisphosphate correlates with deactivation of ribu-lose bisphosphate carboxylase in leaves. Plant Physiol 87: 244–249PubMedCrossRefGoogle Scholar
  13. Buckley TN and Farquhar GD (2004) A new analytical model for whole-leaf potential electron transport rate. Plant Cell Environ 27: 1487–1502CrossRefGoogle Scholar
  14. Campbell WJ and Ogren WL (1990) Glyoxylate inhibition of ribulose bisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynth Res 23: 257–268CrossRefGoogle Scholar
  15. Canadell JG, Corinne B, Le Quéré CD, Raupacha MR, Fielde CB, Buitenhuisc ET, Ciaisf P, Conwayg TJ, Gillette NP, Houghton RA and Marland G (2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proc Natl Acad Sci USA 104: 18866–18870PubMedCrossRefGoogle Scholar
  16. Charles-Edwards DA and Ludwig LJ (1974) A model for leaf photosynthesis by C3 plant species. Ann Bot 38: 921–930Google Scholar
  17. Chartier P and Prioul JL (1976) The effects of irradiance, carbon dioxide and oxygen on the net photosynthetic rate of the leaf: a mechanistic model. Photosynthetica 10: 20–24Google Scholar
  18. Collatz GJ, Berry JA, Farquhar GD and Pierce J (1990) The relationship between the Rubisco reaction mechanism and models of photosynthesis. Plant Cell Environ 13: 219–225CrossRefGoogle Scholar
  19. Cox PM, Betts RA, Jones CD, Spall SA and Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408: 184–187PubMedCrossRefGoogle Scholar
  20. Cramer W, Bondeau A, Woodward FI, Prentice IC, Betts RA, Brovkin V, Cox PM, Fisher V, Foley J, Friend AD, Kucharik C, Lomas MR, Ramankutty N, Sitch S, Smith B, White A and Young-Molling C (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change: Results from six dynamic global vegetation models. Global Change Biol 7: 357–373CrossRefGoogle Scholar
  21. Cramer W, Bondeau A, Schaphoff S, Lucht W, Smith B and Sitch S (2004) Tropical forests and the global carbon cycle: Impacts of atmospheric CO2, climate change and rate of deforestation. Phil Trans R Soc Lond B 359: 331–343CrossRefGoogle Scholar
  22. de Wit CT (1965) Photosynthesis of leaf canopies. Ver-slag Landbouwkundig Onderzoek (Agr. Research Rep.) nr. 663, PUDOC, WageningenGoogle Scholar
  23. Eichelman H and Laisk A (1999) Ribulose-1,5-bisphosphate carboxylase/oxygenase content, assimilatory charge, and mesophyll conductance in leaves. Plant Physiol 119: 179–189CrossRefGoogle Scholar
  24. Ellis RJ (1979) The most abundant protein in the world. Trends Biochem Sci 4: 241–244CrossRefGoogle Scholar
  25. Evans JR, Farquhar GD (1991) Canopy photosynthesis from the biochemistry of the C3 chloroplast. In: Boote KJ and Loomis RS (eds) Modeling Crop Photosynthesis — From Biochemistry to Canopy, p 140. ASA, Madison, WIGoogle Scholar
  26. Farazdaghi H (2004) A theory and model for the kinetics of the two-substrate ordered reaction of Rubisco with rate-determining steps, and the effects of RuBP regeneration on the hierarchy of limitations. http://www.
  27. Farazdaghi H (2005) Modeling of C3 photosynthesis. Comments: = 5
  28. Farazdaghi H (2007) Modeling Rubisco reaction with a new two-substrate ordered model with a rate-limiting step. Solar Energy and Artificial Photosynthesis conference, The Royal Society, London, 17–19 July 2007. http://www.
  29. Farazdaghi H and Edwards GE (1988a) A mechanistic model for photosynthesis based on the multisubstrate ordered reaction of ribulose-1,5-bisphosphate carboxylase. Plant Cell Environ 11: 789–798CrossRefGoogle Scholar
  30. Farazdaghi H and Edwards GE (1988b) A model for photosynthesis and photorespiration in C3 plants based on the biochemistry and stoichiometry of the pathways. Plant Cell Environ 11: 799–809CrossRefGoogle Scholar
  31. Farazdaghi H and Edwards GE (1992) The co-limiting and mono-limiting theories of photosynthesis and photorespi-ration in C3 plants. Plant Physiol 99: Special Issue-P 9. Abst. 49Google Scholar
  32. Farquhar GD, Von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 plants. Planta 149: 78–90CrossRefGoogle Scholar
  33. Farquhar GD, Von Caemmerer S and Berry JA (2001) Models of photosynthesis. Plant Physiol 125: 42–45PubMedCrossRefGoogle Scholar
  34. Finn MW and Tabita FR (2004) Modified pathway to synthesize ribulose 1,5-bisphosphate in methanogenic archaea. J Bacteriol 185: 3049–3059CrossRefGoogle Scholar
  35. Haldane JBS (1930) Enzymes. Longmans Green and Co, LondonGoogle Scholar
  36. Hammond ET, Andrews TJ and Woodrow IE (1998) Regulation of ribulose-1,5-bisphosphate Carboxylase/Oxygenase by carbamylation and 2-carboxyarabinitol 1-phosphate in tobacco: insights from studies of antisense plants containing reduced amounts of rubisco activase. Plant Physiol 118: 1463–1471PubMedCrossRefGoogle Scholar
  37. Harley P and Sharkey TD (l99l) An improved model of C3 photosynthesis at high CO2: Reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynth Res 27: l69–l78Google Scholar
  38. Jamin M, Adam M, Damblon C, Christiaens L and Frere J (1991) Accumulation of acyl-enzyme in DD-peptidase-catalyzed reactions with analogues of peptide substrates. Biochem J 280: 499–506PubMedGoogle Scholar
  39. Jensen RG (2000) From the cover: Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proc Natl Acad Sci USA 97: 12937–12938PubMedCrossRefGoogle Scholar
  40. Johnson, KA (1992) Transient state kinetic analysis of enzyme reaction pathways. In: Sigman DS (ed) The Enzymes, 3rd ed, vol 20, pp 1–61. Academic Press, New YorkGoogle Scholar
  41. Jordan DB and Ogren WL (l984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161: 308–313CrossRefGoogle Scholar
  42. Karl TR and Trenberth KE (2003) Modern global climate change. Science 302: 1719–1723PubMedCrossRefGoogle Scholar
  43. Khan S, Andralojc PJ, Lea PJ and Parry MA (1999) 2′-carboxy-D-arabitinol 1-phosphate protects ribulose 1, 5-bisphosphate carboxylase/oxygenase against proteolytic breakdown. Eur J Biochem 266: 840–847PubMedCrossRefGoogle Scholar
  44. Ku SG and Edwards GE (1978) Photosynthetic efficiency of Panicum hiatts and Panicum milioides in relation to C3 and C4 plants. Plant Cell Physiol 19: 665–675Google Scholar
  45. Laing WA and Christeller JT (1976) A model for the kinetics of activation and catalysis of ribulose 1,5-bisphosphate carboxylase. Biochem J 159: 563–570PubMedGoogle Scholar
  46. Laing WA, Ogren WL and Hageman RH (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2, and ribulose-1,5-diphosphate-carboxylase. Plant Physiol 54: 678–685PubMedCrossRefGoogle Scholar
  47. Laisk A (1985) Kinetics of photosynthetic CO2 uptake in C3 plants. In: Viil J, Grishina G and Laisk A (eds) Kinetics of Photosynthetic Carbon Metabolism in C3 Plants, pp 21–34. Valgus Publishing, Tallinn, EstoniaGoogle Scholar
  48. Laisk A and Oja V (1998) Dynamics of leaf photosynthesis: Rapid response measurements and their interpretations. CSIRO Publishing, Collingwood, AustraliaGoogle Scholar
  49. Leuning R (1997) Scaling to a common temperature improves the correlation between photosynthesis parameters Jmax and Vcmax. J Exp Bot 48: 345–347CrossRefGoogle Scholar
  50. Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A, Wang K and Loustau D (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant Cell Environ 25: 1167–1179CrossRefGoogle Scholar
  51. Michaelis L and Menten M (1913) Die Kinetik der Invertinwirkung. Biochem Z 49: 333–369Google Scholar
  52. Miziorko HM and Lorimer GH (1983) Ribulose-1,5-bisphosphate carboxylase oxygenase. Annu Rev Biochem 52: 507–553PubMedCrossRefGoogle Scholar
  53. Monteith JL (1965) Light distribution and photosynthesis in field crops. Ann Bot 29: 17–37Google Scholar
  54. Mott KA and Woodrow IE (1993) Effects of O2 and CO2 on non-steady-state photosynthesis. Further evidence for ribulose-1,5-bisphosphate carboxylase/oxygenase limitation. Plant Physiol 102: 859–866PubMedGoogle Scholar
  55. Mott KA and Woodrow IE (2000) Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. J Exp Bot 51: 399–406PubMedCrossRefGoogle Scholar
  56. Mullis J, Holmquist B and Vallee BL (1991) Hydrophobic anion activation of human liver xx alcohol dehydrogenase. Biochemistry 30: 5743–5749CrossRefGoogle Scholar
  57. Ogren WL and Bowes G (1971) Ribulose diphosphate carboxylase regulates soybean photorespiration. Nature New Biol 230: 159–160PubMedGoogle Scholar
  58. ögren E (1993) Convexity of the photosynthetic light response curve in relation to intensity and direction of light during growth. Plant Physiol 101: 1013–1019PubMedGoogle Scholar
  59. Ögren E and Evans JR (1993) Photosynthetic light-response curves. I. The influence of CO2 partial pressure and leaf inversion. Planta 189: 182–190CrossRefGoogle Scholar
  60. Parry MAJ, Loveland JE and Andralojc PJ (1999) Regulation of Rubisco. In: Bryant JA, Burrell MM and Kruger NJ (eds) Plant Carbohdrate Biochemistry, pp 127–145. Bios Scientific Publishers, OxfordGoogle Scholar
  61. Portis AR Jr, Lilley RM and Andrews TJ (1995) Subsaturating ribulose-1,5-bisphosphate concentration promotes inactivation of ribulose-1,5-bisphosphate carb-oxylase/oxygenase (Rubisco). Studies using continuous substrate addition in the presence and absence of Rubisco Activase. Plant Physiol 109: 1441–1451PubMedGoogle Scholar
  62. Price GD, Evans JR, Von Caemmerer S, Yu JW and Badger MR (1995) Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195: 369–378PubMedCrossRefGoogle Scholar
  63. Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR, Bogorad L and Stitt M (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with antisense rbcs. 1. Impact on photosynthesis in ambient growth-conditions. Planta 183: 542–554CrossRefGoogle Scholar
  64. Rabinowitch E (1951) Photosynthesis and Related Processes. Interscience Publishers, New YorkGoogle Scholar
  65. Ruuska SA, Andrews TJ, Badger MR, Hudson GS, Laisk A, Price GD and Von Caemmerer S (1998) The interplay between limiting processes in C3 photosynthesis studied by rapid response gas exchange using transgenic tobacco impaired in photosynthesis. Funct Plant Biol 25: 859–870CrossRefGoogle Scholar
  66. Sage RF and Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field-grown plants. Plant Physiol 84: 658–664PubMedCrossRefGoogle Scholar
  67. Salvucci ME and Crafts-Brandner SJ (2004) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plantarum 122: 513–519CrossRefGoogle Scholar
  68. Scheffer M, Brovkin V and Cox P (2006) Positive feedback between global warming and atmospheric 2 concentration inferred from past climate change. Geophys Res Lett 33: L10702CrossRefGoogle Scholar
  69. Sharkey TD (1985) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol 78: 71–75PubMedCrossRefGoogle Scholar
  70. Sharkey TD (1989) Evaluating the role of Rubisco regulation in photosynthesis of C3 plants. Phil Trans R Soc Lond B 323(121) 435–448CrossRefGoogle Scholar
  71. Sharkey TD, Bernacchi CJ, Farquhar GD and Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30: 1035– 1040PubMedCrossRefGoogle Scholar
  72. Spreitzer RJ and Salvucci ME (2002) RUBISCO: Structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449–475PubMedCrossRefGoogle Scholar
  73. Spreitzer RJ, Peddi SR and Satagopan S (2005) Phylogenetic engineering at an interface between large and small subunits imparts land-plant kinetic properties to algal Rubisco. Proc Natl Acad Sci USA 102: 17225–17230PubMedCrossRefGoogle Scholar
  74. Taylor TC and Andersson I (1996) Structural transitions during activation and ligand binding in hexadecameric Rubisco inferred from the crystal structure of the activated unliganded spinach enzyme. Nat Struct Biol 3: 95–101PubMedCrossRefGoogle Scholar
  75. Taylor SE and Terry N (1984) Limiting factors in photosynthesis. V: Photochemical energy supply co-limits photosynthesis at low values of intercellular CO2 concentration. Plant Physiol 75: 82–86.PubMedCrossRefGoogle Scholar
  76. Taylor TC, Backlund A, Bjorhall K, Spreitzer RJ and Andersson I (2001) First crystal structure of Rubisco from a green alga, Chlamydomonas reinhardtii. J Biol Chem 276: 48159–48164PubMedGoogle Scholar
  77. Tcherkez GGB, Farquhar GD and Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103: 7246–7251PubMedCrossRefGoogle Scholar
  78. Terry N (1980) Limiting factors in photosynthesis. I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol 65: 114–120PubMedCrossRefGoogle Scholar
  79. Terry N (1983) Limiting factors in photosynthesis. IV. Iron stress mediated changes on light-harvesting and electron transport capacity and its effects on photosynthesis in vivo. Plant Physiol 71: 855–860PubMedCrossRefGoogle Scholar
  80. Thornley JHM (1976) Mathematical Models in Plant Physiology. Academic Press, LondonGoogle Scholar
  81. Torn MS and Harte J (2006) Missing feedbacks, asymmetric uncertainties, and the underestimation of future warming. Geophys Res Lett 33: 1–56CrossRefGoogle Scholar
  82. Van Bavel CHM (1975) A behavioral equation for leaf carbon dioxide assimilation and a test of its validity. Photosynthetica 9: 165–76Google Scholar
  83. Von Caemmerer S (2000) Biochemical Models of Photosynthesis. Techniques in Plant Sciences, No.2. CSIRO Publishing, Collingwood, AustraliaGoogle Scholar
  84. Von Caemmerer S and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 53: 376–387CrossRefGoogle Scholar
  85. Von Caemmerer S, Evans JR, Hudson GS and Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferredfrom measurements of photosynthesis in leaves of transgenic tobacco. Planta 195: 88–97CrossRefGoogle Scholar
  86. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants — a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44: 907–920CrossRefGoogle Scholar
  87. Zhang N and Portis AR (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96: 9438–944PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Hadi Farazdaghi

There are no affiliations available

Personalised recommendations