Can Increase in Rubisco Specificity Increase Carbon Gain by Whole Canopy? A Modeling Analysis

  • Xin-Guang Zhu
  • Stephen P. Long
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 29)

Genetic modification of Ribulose bis-phosphate carboxylase-oxygenase (Rubisco) to increase the specificity for CO2 relative to O2(τ) would decrease photorespiration and in principle should increase crop productivity. When the kinetic properties of Rubisco from different photosynthetic organisms are compared, it appears that Rubiscos with higher τ generally have lower maximum catalytic rates of car-boxylation per active site (k C). Given this inverse relationship, we explored whether increasing τ results in increased leaf and canopy photosynthesis. A steady-state biochemical model of leaf photosynthesis was coupled to a canopy biophysical microclimate model and used in this chapter. C3 photosynthetic CO2uptake rate (A) is either limited by Rubisco or by the rate of regeneration of ribulose-1,5-bisphosphate (RuBP). The latter is mainly determined by the rate of whole chain electron transport (J). Thus, if J is limiting, an increase in τ will increase net CO2 uptake because more products of the electron transport chain will be partitioned away from photorespiration into photosynthetic CO2 fixation. The effect of an increase in τ on Rubisco-limited photosynthesis depends on k C, but differently dependent on the concentration of CO2. Assuming a strict inverse relationship between k C and τ, theoretical simulations showed that a decrease, not an increase, in τ increases Rubisco-limited (light-saturated) photosynthesis at the current atmospheric CO2 concentration. Crop canopies have both sunlit and shaded leaves. In addition, during a diurnal period light levels are high at midday and low at dawn and dusk. As a result, both light-limited and light-saturated photosynthesis contribute to total crop carbon gain. For canopies, the present average τ found in C3 terrestrial plants is supra-optimal for the present ambient atmospheric CO2 concentration of 370 μ mol mol−1, but would be optimal for a CO2 concentration of around 200 μ mol mol−1, a value close to the average of the last 400,000 years. Replacing the Rubisco of terrestrial C3 plants with one with a lower, but optimal τ would increase canopy carbon gain by 3%. Because there are Rubiscos with significant deviations from the average inverse relationship between k Cand τ, we also used the canopy model to compare the rates of canopy photosynthesis for several such Rubiscos. These simulations suggested that very substantial increases (>25%) in crop carbon gain could result if specific Rubiscos deviating either towards a higher τ or higher k C can be expressed in C3 plants.


Leaf Area Index Plant Cell Environ Crop Canopy Canopy Photosynthesis Canopy Carbon Gain 
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 and Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol 165: 351–371PubMedCrossRefGoogle Scholar
  2. Ainsworth EA, Rogers A and Leakey ADB (2008) Targets for crop biotechnology in a future high CO2 and high O3 World. Plant Physiol 147: 13–19PubMedCrossRefGoogle Scholar
  3. Bainbridge G, Madgwick PJ, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ and Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Expt Bot 46: 1269–1276Google Scholar
  4. Barnola JM, Raynaud D, Lorius C and Barkov NI (1999) Historical CO2 record from the Vostok ice core. In: Trends: A Compendium of Data on Global Change. Carbon dioxide Information Analysis Center. Oak Ridge National laboratory, Department of Energy, Oak Ridge, TNGoogle Scholar
  5. Bernacchi CJ, Singsaas EL, Pimentel C, Portis JAR and Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24: 253–259CrossRefGoogle Scholar
  6. Bernacchi CJ, Pimentel C and Long SP (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant Cell Environ 26: 1419–1430CrossRefGoogle Scholar
  7. Bunce JA (2000) Contrasting effects of carbon dioxide and irradiance on the acclimation of photosynthesis in developing soybean leaves. Photosynthetica 38: 83–89CrossRefGoogle Scholar
  8. Chene P, Day AG and Fersht AR (1992) Mutation of asparagine 111 of Rubisco from Rhodospirillum rubrum alters the carboxylase/oxygenase specificity. J Mol Biol 225: 891–896PubMedCrossRefGoogle Scholar
  9. Dengler NG and Nelson T (1999) Leaf structure and development in C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 133–172, Academic Press, San Diago, CACrossRefGoogle Scholar
  10. Douce R and Heldt HW (2000) Photorespiration. In: Lee-good RC, Sharkey TD and Von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 115–136. Kluwer (now Springer), DordrechtGoogle Scholar
  11. Evans JH and Farquhar GD (1991) Modelling canopy photosynthesis from the biochemistry of C3 chloroplast. In: Boote KJ and Loomis RS (eds) Modelling Crop Photosynthesis — From Biochemistry to Canopy, pp 1–15. Crop Science Society of America, Madison, WIGoogle Scholar
  12. Evans LT (1993) Crop Evolution, Adaptation and Yield. Cambridge University Press, CambridgeGoogle Scholar
  13. Farage PK, McKee IF and Long SP (1998) Does a low nitrogen supply necessarily lead to acclimation of photosynthesis to elevated CO2? Plant Physiol 118: 573–580PubMedCrossRefGoogle Scholar
  14. Farquhar GD, Von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90CrossRefGoogle Scholar
  15. Farquhar GD, Von Caemmerer S and Berry JA (2001) Models of photosynthesis. Plant Physiol 125: 42–45PubMedCrossRefGoogle Scholar
  16. Forseth IN and Norman JM (1991) Modeling of solar irra-diance, leaf energy budget, and canopy photosynthesis. In: Hall DO, Scurlock JMO, Bolhar-Nordenkampf RC, Leegood RC and Long SP (eds) Photosynthesis and Productivity Research in a Changing Environment, pp 207– 219. Chapman & Hall, LondonGoogle Scholar
  17. Forseth IN and Norman JM (1993) Modelling of solar irradi-ance, leaf energy budget, and canopy photosynthesis. In: Hall DO, Scurlock JMO, Bolhar-Nordenkampf RC, Lee-good RC and Long SP (eds) Techniques in Photosynthesis and Productivity Research for a Changing Environment, pp 129–167. Chapman & Hall, LondonGoogle Scholar
  18. Frak E, Le Roux X, Millard P, Dreyer E, Jaouen G, Saint-Joanis B and Wendler R (2001) Changes in total leaf nitrogen and partitioning, of leaf nitrogen drive photosynthetic acclimation to light in fully developed walnut leaves. Plant Cell Environ 24: 1279–1288CrossRefGoogle Scholar
  19. Gatenby AA (1984) The properties of the large subunit of maize ribulose bisphosphate carboxylase-oxygenase synthesized in Escherichia Coli. Eur J Biochem 144: 361–366PubMedCrossRefGoogle Scholar
  20. Gilbert IR, Jarvis PG and Smith H (2001) Proximity signal and shade avoidance differences between early and late successional trees. Nature 411: 792–795PubMedCrossRefGoogle Scholar
  21. Gomes FP, Mielke MS and de Almeida AAF (2002) Leaf gas exchange of green dwarf coconut (Cocos nucifera L. var. nana) in two contrasting environments of the Brazilian north-east region. J Hortic Sci Biotech 77: 766–772Google Scholar
  22. Harley PC (1992) Modeling photosynthesis of cotton in elevated CO2. Plant Cell Environ. 15: 271–282.CrossRefGoogle Scholar
  23. Harrison EP, Olcer H, Lloyd JC, Long SP and Raines CA (2001) Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. J Exp Bot 52: 1779–1784PubMedCrossRefGoogle Scholar
  24. Horken KM and Tabita FR (1999) Closely related form I ribulose bisphosphate carboxylase/oxygenase molecules that possess different CO2/O2 substrate specificities. Arch Biochem Biophys 361: 183–194PubMedCrossRefGoogle Scholar
  25. Houtz RL, Portis AR (2003) The life of ribulose 1,5-bisphosphate carboxylase/oxygenase — Posttranslational facts and mysteries. Arch Biochem Biophys 414: 150–158PubMedGoogle Scholar
  26. Humphries SW and Long SP (1995) WIMOVAC: A software package for modelling the dynamics of plant leaf and canopy photosynthesis. Comput Appl Biosci 11: 361–371PubMedGoogle Scholar
  27. Jordan DB and Chollet R (1985) Subunit dissociation and reconstituation of ribulose-1,5-bisphosphate carboxylase from Chromatium vinosum. Arch Biochem Biophys 236: 487–496PubMedCrossRefGoogle Scholar
  28. Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulose biphosphate carboxylase/ oxygenase. Nature 291: 513–515CrossRefGoogle Scholar
  29. Jordan DB and Ogren WL (1984) The carbon dioxide/oxygen specificity of ribulose-1,5-bisphosphate car-boxylase/oxygenase. Planta 161: 308–313CrossRefGoogle Scholar
  30. Kanevski I, Maliga P, Rhoades DF and Gutteridge S (1999) Plastome engineering of ribulose-1,5-bisphosphate car-boxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119: 133–141PubMedCrossRefGoogle Scholar
  31. Kettleborough CA, Parry MAJ, Keys AJ and Phillips AL (1990) Chimeras of the Rubisco large subunit from wheat and anacystis do not assemble into active enzyme in Escherichia coli. J Exp Bot 41: 1287–1292CrossRefGoogle Scholar
  32. Kimball BA (1983) Carbon dioxide and agricultural yield — An assemblage and analysis of 430 prior observations. Agronomy J 75: 779–788CrossRefGoogle Scholar
  33. Leegood RC (1999) The regulation of C4 pathway. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 89–131. Academic Press, San Diago, CACrossRefGoogle Scholar
  34. Long SP (1985) Leaf gas exchange. In: Barber J and Baker NR (eds) Photosynthetic Mechanistic Mechanisms and the Environment, pp 453–500. Elsevier, LondonGoogle Scholar
  35. Long SP (1991) Modification of the response of photosyn-thetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? Plant Cell Environ 14: 729–739CrossRefGoogle Scholar
  36. Long SP (1998) Rubisco, the key to improved crop production for a world population of more than eight billion people? In: Waterlow JC and Riley R (eds) Feeding the World Population-Rank Prize Symposium, pp 124–136. Oxford University Press, Cary, NCGoogle Scholar
  37. Long SP and Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54: 2393–2401PubMedCrossRefGoogle Scholar
  38. Long SP, Ainsworth EA, Rogers A and Ort DR (2004) Rising atmospheric carbon dioxide: Plants FACE their future. Annu Rev Plant Biol 55: 591–628PubMedCrossRefGoogle Scholar
  39. Long SP, Zhu XG, Naidu SL and Ort DR (2006a) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29: 315–330CrossRefGoogle Scholar
  40. Long SP, Ainsworth EA, Leakey ADB, Nosberger J and Ort DR (2006b) Food for thought: Lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312: 1918–1921CrossRefGoogle Scholar
  41. Madgwick PJ, Parmar S and Parry MAJ (1998) Effect of mutations of residue 340 in the large subunit polypeptide of rubisco from Anacystic nidulans. Eur J Biochem 253: 476–479PubMedCrossRefGoogle Scholar
  42. Norman JM (1980) Interfacing leaf and canopy light interception models. In: Hesketh JD and Jones JW (eds) Predicting Photosynthesis for Ecosystem Models, Vol. 2, pp 49–67. CRC Press, Boca Raton, FLGoogle Scholar
  43. Ogren WL (1984) Photorespiration, pathway, regulation & modification. Annu Rev Plant Physiol 35: 415–442CrossRefGoogle Scholar
  44. Oguchi R, Hikosaka K and Hirose T (2003) Does the photo-synthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26: 505–512CrossRefGoogle Scholar
  45. Parry MAJ, Keys AJ and Gutteridge S (1989) Variation in the specificity factor of C3 higher plant Rubiscos determined by the total consumption of RuBP. J Exp Bot 40: 317–320CrossRefGoogle Scholar
  46. Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ and Keys AJ (2003) Manipulation of Rubisco: The amount, activity, function and regulation. J Exp Bot 54: 1321–1333PubMedCrossRefGoogle Scholar
  47. Pyke KA and Leech RM (1987) The control of chloroplast number in wheat mesophyll cells. Planta 170: 416–420CrossRefGoogle Scholar
  48. Raines CA (2006) Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. Plant Cell Environ 29: 331–339PubMedCrossRefGoogle Scholar
  49. Ramage RT, Read BA and Tabita FR (1998) Alteration of the alpha helix region of cyanobacterial ribu-lose 1,5-bisphosphate carboxylase/oxygenase to reflect sequences found in high substrate specificity enzymes. Arch Biochem Biophys 349: 81–88PubMedCrossRefGoogle Scholar
  50. Read BA and Tabita FR (1994) High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial rubisco containing “algal” residue modifications. Arch Biochem Biophys 312: 210–218PubMedCrossRefGoogle Scholar
  51. Romanova AK, Cheng ZQ and McFadden BA (1997) Activity and carboxylation specificity factor of mutant ribulose 1,5-bisphosphate carboxylase/oxygenase from Anacystis nidulans. Biochem Mol Biol Int 42: 299–307PubMedGoogle Scholar
  52. Sage RF (1999) Why C4 photosynthesis? In Sage RF and Monson RK (eds) C4 Plant Biology, pp 3–14. Academic Press, San Diego, CACrossRefGoogle Scholar
  53. Sage RF (2002) Variation in the k cat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53: 609–620PubMedCrossRefGoogle Scholar
  54. Sage RF (2004) The evolution of C-4 photosynthesis. New Phytol 161: 341–370CrossRefGoogle Scholar
  55. Seeman JR, Badger MR and Berry JA (1984) Variations in the specificity activity of ribulose-1,5-bisphosphate car-boxylase between species utilizing differing photosyn-thetic pathways. Plant Physiol 74: 791–794CrossRefGoogle Scholar
  56. Sims DA and Pearcy RW (1992) Response of leaf anatomy and photosynthetic capacity in Alocasia-Macrorrhiza (Araceae) to a transfer from low to high light. Am J Bot 79: 449–455CrossRefGoogle Scholar
  57. Somerville CR and Ogren WL (1982) Mutants of the cruciferous plant Arabidopsis thaliana lacking glycine decar-boxylase activity. Biochem J 202: 373–380PubMedGoogle Scholar
  58. Somerville SC and Somerville CR (1983) Effects of oxygen and carbon dioxide on photorespiratory flux determined from glycine accumulation in a mutant of Arabidopsis thaliana. J Exp Bot 34: 415–424CrossRefGoogle Scholar
  59. Spreitzer RJ (1999) Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxy-lase/oxygenase. Photosynth Res 60: 29–42CrossRefGoogle Scholar
  60. Spreitzer RJ and Salvucci ME (2002) RUBISCO: Structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449–475PubMedCrossRefGoogle Scholar
  61. Spreitzer RJ, Peddi SR and Satagopan S (2005) Phyloge-netic 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
  62. Tabita FR (1999) Microbial ribulose 1,5-bisphosphate car-boxylase/oxygenase: A different perspective. Photosynth Res 60: 1–28CrossRefGoogle Scholar
  63. 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
  64. Von Caemmerer S (2000) Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Collingwood, AustraliaGoogle Scholar
  65. Von Caemmerer S and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387CrossRefGoogle Scholar
  66. Whitney SM and Andrews TJ (2001a) The gene for the ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) small subunit relocated to the plastid genome of tobacco directs the synthesis of small subunits that assemble into Rubisco. Plant Cell 13: 193–205CrossRefGoogle Scholar
  67. Whitney SM and Andrews TJ (2001b) Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxy-lase/oxygenase (RubisCO) supports photosynthesis and growth in tobacco. Proc Natl Acad Sci USA 98: 14738–14743CrossRefGoogle Scholar
  68. Whitney SM and Sharwood RE (2007) Linked Rubisco subunits can assemble into functional oligomers without impeding catalytic performance. J Biol Chem 282: 3809– 3818PubMedCrossRefGoogle Scholar
  69. Whitney SM, Baldett P, Hudson GS and Andrews TJ (2001) Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26: 535–547PubMedCrossRefGoogle Scholar
  70. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants — A retrospective analysis of the A/C i curves from 109 species. J Exp Bot 44: 907–920CrossRefGoogle Scholar
  71. Yeoh H-H, Badger MR and Watson L (1981) Variations in kinetic properties of ribulose-1,5-bisphosphate carboxy-lases among plants. Plant Physiol 67: 1151–1155PubMedCrossRefGoogle Scholar
  72. Zhu X-G, Portis Jr. AR and Long SP (2004a) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27: 155–165CrossRefGoogle Scholar
  73. Zhu X-G, Ort DR, Whitmarsh J and Long SP (2004b) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies. A theoretical analysis. J Exp Bot 55: 1167– 1175Google Scholar
  74. Zhu X-G, de Sturler E and Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: A numerical simulation using an evolutionary algorithm. Plant Physiol 145: 513–526PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Xin-Guang Zhu
    • 1
  • Stephen P. Long
    • 2
  1. 1.Partner Institute of Computational BiologyChinese Academy of Sciences-Max Planck Society of GermanyShanghaiChina
  2. 2.Department of Plant BiologyUniversity of Illinois at Urbana Champaign, Edgar R. Madigan LaboratoryUrbanaUSA

Personalised recommendations