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Modelling C3 photosynthesis: A sensitivity analysis of the photosynthetic carbon-reduction cycle

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Abstract

A model of the C 3 photosynthetic system is developed which describes the sensitivity of the steadystate rate of carbon dioxide assimilation to changes in the activity of several enzymes of the system. The model requires measurements of the steady-state rate of carbon dioxide assimilation, the concentrations of several intermediates in the photosynthetic system, and the concentration of the active site of ribulose 1,5-bisphosphate carboxyalse/oxygenase (Rubisco). It is shown that in sunflowers (Helianthus annuus L.) at photon flux densities that are largely saturating for the rate of photosynthesis, the steady-stete rate of carbon dioxide assimilation is most sensitive to Rubisco activity and, to a lesser degree, to the activities of the stromal fructose, 6-bisphosphatase and the enzymes catalysing sucrose synthesis. The activities of sedoheptulose 1,7-bisphosphatase, ribulose 5-phosphate kinase, ATP synthase and the ADP-glucose pyrophosphorylase are calculated to have a negligible effect on the flux under the high-light conditions. The utility of this analysis in developing simpler models of photosynthesis is also discussed.

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Abbreviations

c i :

intercellular CO2 concentration

C supJinfP :

control coefficient for enzyme P with respect to flux J

DHAP:

dihydroxyacetonephosphate

E4P:

erythrose 4-phosphate

F6P:

fructose 6-phosphate

FBP:

fructose 1,6-bisphosphate

FBPase:

fructose 1,6-bisphosphatase

G3P:

glyceraldehyde 3-phosphate

G1P:

glucose 1-phosphate

G6P:

glucose 6-phosphate

Pi:

inorganic phosphate

PCR:

photosynthetic carbon reduction

PGA:

3-phosphoglyceric acid

PPFD:

photosynthetically active photon flux density

R Jn :

response coefficient for effector n with respect to flux J

R5P:

ribose 5-phosphate

Rubisco:

ribulose 1,5-bisphosphate carboxylase/oxygenase

Ru5P:

ribulose 5-phosphate

RuBP:

ribulose 1,5-bisphosphate

S7P:

sedoheptulose 7-phosphate

SBP:

sedoheptulose 1,7-bisphosphate

SBPase:

sedoheptulose 1,7-bisphosphatase

SPS:

sucrose-phosphate synthase

Xu5P:

xylulose 5-phosphate

ɛ P n :

elasticity coefficient for effector n with respect to the catalytic velocity of enzyme P

References

  • Andrews, T.J., Lorimer, G.H. (1987) Rubisco: structure, mechanisms, and prospects for improvement. In: The biochemistry of plants, vol. 10, pp. 131–218, Hatch, M.D., ed. Academic Press, New York

    Google Scholar 

  • Ashton, A.R. (1982) A role for ribulose 1,5-bisphosphate carboxylase as a metabolite buffer. FEBS Lett. 145, 1–7

    Google Scholar 

  • Badger, M.R., Sharkey, T.D., von Caemmerer, S. (1984) The relationship between steady-state gas exchange of bean leaves and the levels of carbon reduction cycle intermediates. Planta 160, 305–313

    Google Scholar 

  • Bassham, J.A., Krause, G.H. (1969) Free energy changes and metabolic regulation in steady-state photosynthetic carbon reduction. Biochim. Biophys. Acta 189, 207–221

    Google Scholar 

  • Cardon, Z.G., Mott, K.A. (1989) Evidence that ribulose 1,5-bisphosphate binds to inactive sites of RuBP carboxylase in vivo and an estimate for the rate constant for dissociation. Plant Physiol. 89, 1253–1257

    Google Scholar 

  • Charles, S.A., Halliwell, B. (1980) Properties of freshly purified and thiol treated chloroplast fructose bisphosphatase. Biochem. J. 185, 689–693

    Google Scholar 

  • Copeland, L., Preiss, J. (1981) Purification of the spinach leaf ADP-glucose pyrophosphorylase. Plant Physiol. 68, 996–1001

    Google Scholar 

  • Evans, J.R., Sharkey, T.D., Berry, J.A., Farquhar, G.D. (1986) Carbon isotope discrimination measured concurrently with gasexchange to investigate CO2 diffusion in leaves of higher plants. Aust. J. Plant Physiol. 13, 281–292

    Google Scholar 

  • Farquhar, G.D. (1979) Models describing the kinetics of ribulose bisphosphate carboxylase/oxygenase. Arch. Biochem. Biophys. 193, 456–468

    Google Scholar 

  • Farquhar, G.D., von Caemmerer, S., Berry, J.A. (1980) A biochemical model of photosynthetic CO2 fixation in leaves of C3 species. Planta 149, 78–90

    CAS  Google Scholar 

  • Furbank, R.T., Foyer, C.H., Walker, D.A. (1987) Interactions between ribulose 1,5-bisphosphate carboxylase and stromal metabolites. Biochim. Biophys. Acta 894, 165–173

    Google Scholar 

  • Gardemann, A., Stitt, M., Heldt, H.W. (1983) Control of CO2 fixation. Regulation of spinach ribulose 5-phosphate kinase by stromal metabolites. Biochim. Biophys. Acta 722, 51–60

    Google Scholar 

  • Heber, U., Neimanis, S., Deitz, K.J., Viil, J. (1986) Assimilatory power as a driving force in photosynthesis. Biochim. Biophys. Acta 852, 144–155

    Google Scholar 

  • Jordan, D.B., Ogren, W.L. (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Plant 161, 308–313

    Google Scholar 

  • Kacser, H., Burns, J.A. (1973) The control of flux. Symp. Soc. Exp. Biol. 27, 65–104

    Google Scholar 

  • Laing, W.A., Stitt, M., Heldt, H.W. (1981) Changes in the activity of ribulose-phosphate kinase and fructose and sedoheptulosebisphosphatase in chloroplasts. Biochim. Biophys. Acta 637, 348–359

    Google Scholar 

  • Leegood, R.C., Walker, D.A. (1982) Regulation of fructose 1,6-bisphosphatase activity in leaves. Planta 156, 449–456

    Google Scholar 

  • Leegood, R.C., Foyer, C.H., Walker, D.A. (1985) Regulation of the Bensen-Calvin Cycle. In: Photosynthetic mechanisms and the environment, pp. 191–258, Barber, J., Baker, N., eds. Elsevier, New York

    Google Scholar 

  • Lowry, O.H., Passoneau, J.U. (1972) A flexible system of enzymic analysis. Academic Press, New York London

    Google Scholar 

  • Mills, J.D., Mitchell, P. (1982) Thiol modulation of CF0-CF1 stimulates acid-base dependent phosphorylation of ADP by broken pea chloroplasts. FEBS Lett. 144, 63–67

    Google Scholar 

  • Mott, K.A. (1989) Do stomata respond to CO2 concentrations other than intercellular? Plant Physiol. 86, 200–203

    Google Scholar 

  • Neuhaus, H.E., Kruckeberg, A.L., Feil, R., Stitt, M. (1989) Decreased-activity mutants of phosphoglucoisomerase in the chloroplast and cytosol of Clarkia xantiana. Planta 178, 110–122

    Google Scholar 

  • Perchorovicz, J.T., Raynes, D.A., Jensen, R.G. (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc. Natl. Acad. Sci. USA 78, 2985–2989

    Google Scholar 

  • Preiss, J. (1982) Regulation of the biosynthesis and degradation of starch. Annu. Rev. Plant Physiol. 33, 431–454

    Google Scholar 

  • Quick, W.P., Schurr, U., Scheibe, R., Schulze, E.-D., Rodermel, S.R., Bogorad, L., Stitt, M. (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in tobacco transformed with ‘antisense’ rbcS. Impact on photosynthesis in ambient growth conditions. Planta 183, 542–544

    Google Scholar 

  • Soulie, J.M., Buc, J., Meunier, J.-C., Pradel, J., Ricard, J. (1981) Molecular properties of chloroplastic thioredoxin-f and the regulation of fructose 1,6-bisphosphatase. Eur. J. Biochem. 119, 497–502

    Google Scholar 

  • Stitt, M. (1989) Control analysis of photosynthetic sucrose synthesis: assignment of elasticity coefficients and flux control coefficients to the cytosolic fructose 1,6-bisphosphatase and sucrose phosphate synthase. Philos. Trans. R. Soc. London, Ser. B323, 327–338

    Google Scholar 

  • Stitt, M. (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ. 14, 741–762

    Google Scholar 

  • Stitt, M., Quick, W.P., Schurr, U., Rodermel, S.R., Bogorad, L. (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenause in tobacco transformed with ‘antisense’ rbcS. II. Fluxcontrol coefficients for photosynthesis in varying light, CO2 and air humidity. Planta 183, 555–566

    Google Scholar 

  • Stitt, M., Wirtz, W., Heldt, H.W. (1980) Metabolite levels during induction in the chloroplast and extrachloroplast compartments of spinach protoplasts. Biochim. Biophys. Acta 593, 85–102

    Google Scholar 

  • von Caemmerer, S., Farquhar, G.D. (1985) Kinetics and activation of Rubisco and some preliminary modelling of RuP2 pool sizes. In: Kinetics of photosynthesis and photorespiration in C3 plants, vol. 1, pp. 46–48, Viil, J., ed., Tallinn, Valgus

    Google Scholar 

  • von Caemmerer, S., Edmondson, D.L. (1986) Relationship between steady-state gas exchange, in vivo ribulose bisphosphate carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Aust. J. Plant Physiol. 13, 669–688

    Google Scholar 

  • Woodrow, I.E. (1986) Control of the rate of photosynthetic carbon dioxide fixation. Biochim. Biophys. Acta 851, 181–192

    Google Scholar 

  • Woodrow, I.E., Berry, J.A. (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 533–94

    Google Scholar 

  • Woodrow, I.E., Mott, K.A. (1988) A quantitative assessment of the degree to which RuBP carboxylase/oxygenase limits the steady-state rate of photosynthesis during sun-shade acclimation in Helianthus annuus. Aust. J. Plant Physiol. 15, 253–262

    Google Scholar 

  • Woodrow, I.E., Walker, D.A. (1980) Light-mediated activation of stromal sedoheptulose bisphosphatase. Biochem. J. 191, 845–849

    Google Scholar 

  • Woodrow, I.E., Walker, D.A. (1983) Regulation of stromal sedoheptulose 1,7-bisphosphatase activity and its role in controlling the reductive pentose phosphate pathway. Biochim. Biophys. Acta 722, 508–516

    Google Scholar 

  • Woodrow, I.E., Murphy, D.J., Walker, D.A. (1983) Regulation of photosynthetic carbon metabolism. The effect of inorganic phosphate on stromal sedoheptulose 1,7-bisphosphatase. Eur. J. Biochem. 132, 121–123

    Google Scholar 

  • Woodrow, I.E., Ball, J.T., Berry, J.A. (1986) A general expression for the control of the rate of photosynthetic CO2 fixation by stomata, the boundary layer and radiation exchange. Progr. Photosynth. Res. 4, 225–228

    Google Scholar 

  • Woodrow, I.E., Ball, J.T., Berry, J.A. (1990) Control of photosynthetic carbon dioxide fixation by the boundary layer, stomata and ribulose 1,5-bisphosphate carboxylase/oxygenase. Plant Cell Environ. 13, 339–347

    Google Scholar 

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Authors and Affiliations

  1. Department of Botany and Tropical Agriculture, James Cook University of North Queensland, QLD 4811, Townsville, Australia

    Ian E. Woodrow

  2. Department of Biology, Utah State University, 84322, Logan, UT, USA

    Keith A. Mott

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  1. Ian E. Woodrow
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  2. Keith A. Mott
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Additional information

This research was funded by an Australian Research Council grant to I.E.W. and was undertaken during a visity by K.A.M. to the James Cook University of North Queensland. The expert help of Glenys Hanley and Mick Kelly is greatly appreciated.

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Woodrow, I.E., Mott, K.A. Modelling C3 photosynthesis: A sensitivity analysis of the photosynthetic carbon-reduction cycle. Planta 191, 421–432 (1993). https://doi.org/10.1007/BF00195743

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  • DOI: https://doi.org/10.1007/BF00195743

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