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Photosynthesis Research

, Volume 75, Issue 1, pp 1–10 | Cite as

The Calvin cycle revisited

  • Christine A. Raines
Article

Abstract

The sequence of reactions in the Calvin cycle, and the biochemical characteristics of the enzymes involved, have been known for some time. However, the extent to which any individual enzyme controls the rate of carbon fixation has been a long standing question. Over the last 10 years, antisense transgenic plants have been used as tools to address this and have revealed some unexpected findings about the Calvin cycle. It was shown that under a range of environmental conditions, the level of Rubisco protein had little impact on the control of carbon fixation. In addition, three of the four thioredoxin regulated enzymes, FBPase, PRKase and GAPDH, had negligible control of the cycle. Unexpectedly, non-regulated enzymes catalysing reversible reactions, aldolase and transketolase, both exerted significant control over carbon flux. Furthermore, under a range of growth conditions SBPase was shown to have a significant level of control over the Calvin cycle. These data led to the hypothesis that increasing the amounts of these enzymes may lead to an increase in photosynthetic carbon assimilation. Remarkably, photosynthetic capacity and growth were increased in tobacco plants expressing a bifunctional SBPase/FBPase enzyme. Future work is discussed which will further our understanding of this complex and important pathway, particularly in relation to the mechanisms that regulate and co-ordinate enzyme activity.

carbon allocation overexpression photosynthesis primary carbon fixation transgenic plants 

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References

  1. Badger MR, Caemmerer S von, Ruuska S and Nakomo H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and Rubsico oxygenase. Phil Trans R Soc London B 335: 1433–1446Google Scholar
  2. Banks FM, Driscoll SP, Parry MAJ, Lawlor DW, Knight JS, Gray JC and Paul MJ (1999) Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. Relationship between photosynthesis, growth and allocation at different nitrogen levels. Plant Physiol 119: 1125–1136Google Scholar
  3. Björkman O (1981) Response to different quantum flux intensities. In: Lange OL, Nobel PS, Osmond CB and Zeigler H (eds) Encyclopedia of Plant Physiology, Vol 12, pp 57–107. Springer-Verlag, HeidelbergGoogle Scholar
  4. Bryant B (2000) The production and analysis of tobacco plants with reduced levels of the Calvin cycle enzyme sedoheptulose-1,7-bisphosphatase. University of Essex, PhD thesisGoogle Scholar
  5. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31: 341–374Google Scholar
  6. Caemmerer S von (2000) Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Collingwood, AustraliaGoogle Scholar
  7. Caemmerer S von and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387Google Scholar
  8. Caemmerer S von and Farquhar GD (1984) Effects of partial defoliation, changes of irradiance during growth, short-term water stress and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. Planta 160: 320–329Google Scholar
  9. Dunford RP, Durrant MC, Catley MA and Dyer TA (1998) Location of the redox-active cysteines in chloroplast sedoheptulose-1,7-bisphosphatase indicates that it is allosteric regulation is similar but not identical to that of fructose-1,6-bisphosphatase. Photosynth Res 58: 221–230Google Scholar
  10. Evans JR (1986) The relationship between carbon-dioxide-limited photosynthetic rate and ribulose-1,5-bisphosphate-carboxylase content in 2 nuclear-cytoplasm substitution lines of wheat, and the coordination of ribulose-bisphosphate-carboxylation and electron-transport capacities. Planta 167: 351–358Google Scholar
  11. Evans JR (1996) Effects of light and nutrition on photosynthesis. In: Baker NR (ed) Photosynthesis and the Environment, Vol 5, pp 281–304. Kluwer Academic Publishers, Dordecht, The NetherlandsGoogle Scholar
  12. Evans JR and Farquhar GD (1991) Modeling canopy photosynthesis from the biochemistry of the C3 chloroplast. In: Boote KJ and Loomis RS (eds) Modeling Crop Photosynthesis – from Biochemistry to Canopy, pp 1–16. Madison, Wisconsin, Crop Science Society of AmericaGoogle Scholar
  13. Fell D (1997) Understanding the Control of Metabolism. Portland Press, LondonGoogle Scholar
  14. Fichtner K, Quick WP, Schulze E-D, Mooney HA, Rodermel SR, Bogorad L and Stitt M (1993) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. V. Relationship between photosynthetic rate, storage strategy, biomass allocation and vegetative plant growth at three different nitrogen supplies. Planta 190: 1–9Google Scholar
  15. Furbank RT and Taylor WC (1995) Regulation of photosynthesis in C3 and C4 plants: a molecular approach. Plant Cell 7: 797–807Google Scholar
  16. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, Caemmerer S von and Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C-4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477–485Google Scholar
  17. Geiger DR and Servaites JC (1994) Diurnal regulation of photosynthetic carbon metabolism in C3 plants. Annu Rev Plant Phys Plant Mol Biol 45: 235–256Google Scholar
  18. Giersch C (2001) Mathematical modelling of metabolism. Curr Opin Plant Biol 3: 249–253Google Scholar
  19. Haake V, Zrenner R, Sonnewald U and Stitt M (1998) A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch and inhibits growth of potato plants. Plant J 14: 147–157Google Scholar
  20. Haake V, Geiger M, Walch-Liu P, Engels C, Zrenner R and Stitt M (1999) Changes in aldolase activity in wild-type potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. Plant J 17: 479–489Google Scholar
  21. Harrison EP, Willingham NM, Lloyd JC and Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate partitioning. Planta 204: 27–36Google Scholar
  22. 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 Rubsico carboxylation capacity. J Exp Bot 52: 1779–1784Google Scholar
  23. Hartman FC and Harpel MR (1994) Structure, function, regulation and assembly of D-ribulose-1,5-bisphosphate carboxylase oxygenase. Annu Rev Biochem 63: 197–234Google Scholar
  24. Henkes S, Sonnewald U, Badur R, Flachmann R and Stitt M (2001) A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 13: 535–551Google Scholar
  25. Hudson GS, Evans JR, Caemmerer S, von Arvidsson YBC and Andrews TJ. (1992) Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol 98: 294– 302Google Scholar
  26. Jacquot J-P, Lopez-Jaramillo J, Chueca A, Cherfils J, Lemaire S, Chedozeau B, Migniac-Maslow m, Decottignies P, Wolosiuk R and Lopez-Gorge J (1995) High-level expression of recombinant pea chloroplast fructose-1,6-bisphosphatase and mutagenesis of its regulatory site. Eur J Biochem 229: 675–681Google Scholar
  27. Jiang C-Z and Rodermel SR (1995) Regulation of photosynthesis during leaf development in rbcS antisense DNA mutants of tobacco. Plant Physiol 107: 215–22Google Scholar
  28. Kossmann J, Sonnewald U and Willmitzer L (1994) Reduction of the chloroplastic fructose-16-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J 6: 637– 650Google Scholar
  29. Krapp A, Chaves MM, David MM, Rodriguez ML, Pereira JS and Stitt M (1994) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. VII. Impact on photosynthesis and growth in tobacco growing under extreme high irradiance and high temperature. Plant Cell Environ 17: 945–953Google Scholar
  30. Leunig R (1997) Scaling to a common temperature improves the correlation between the photosynthesis parameters J(max) and V-cmax. J Exp Bot 48: 345–347Google Scholar
  31. Lichtentahler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Phys Plant Mol Biol 50: 47–65Google Scholar
  32. Masle J, Hudson GS and Badger MR (1993) Effects of ambient CO2 concentration on growth and nitrogen use in tobacco (Nicotiana tabacum) plants transformed with an antisense gene to the small subunit of ribulose-1,5-bisphosphate carboxylase oxygenase. Plant Physiol 103: 1075–1088Google Scholar
  33. Miyawaga, Y, Tamoi M and Shigeoka S (2001) Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphat ase in tobacco enhances photosynthesis and growth. Nature Biotech 19: 965–969Google Scholar
  34. Olcer H, Lloyd JC and Raines CA (2001) Photosynthetic capacity is differentially affected by reductions in sedoheptulose-1,7-bisphosphatase activity during leaf development in transgenic tobacco plants. Plant Physiol 125: 982–989Google Scholar
  35. Paul MJ, Knight JS, Habash D, Parry MAJ, Lawlor DW, Barnes SA, Loynes A, and Gray JC (1995) Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco: effect on CO2assimilation and growth at low irradiance. Plant J 7: 535–542Google Scholar
  36. Paul MJ and Lawlor D (1999) Genetic manipulation of photosynthesis. J Exp Bot 51 (special issue)Google Scholar
  37. Paul MJ, Driscoll SP, Andralojc PJ, Knight JS, Gray JC and Lawlor DW (2000) Decrease of phosphoribulokinase activity by antisense RNA in transgenic tobacco: definition of the light environment under which phosphoribulokinase is not in large excess. Planta 211: 112–119Google Scholar
  38. Poolman MG, Fell DA and Thomas S (2000) Modelling photosynthesis and its control. J Exp Bot 51: 319–328Google Scholar
  39. Poolman MG, Olcer H, Lloyd JC, Raines CA and Fell DA (2001) Computer modelling and experimental evidence for two steady states in the photosynthetic in Calvin cycle. Eur J Biochem 268: 2810–2816Google Scholar
  40. Portis AR, Chon CJA, Mosbac A and Heldt HW (1977) Fructoseand sedoheptulose-bisphosphatase. The sites of a possible control of CO2 fixation by light dependent changes of the stromal Mg2+ concentration. Biochim Biophys Acta 461: 313– 325.Google Scholar
  41. Price GD, Evans JR, Caemmerer S von, Yu J-W and Badger MR (1995) Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic plants. Planta 195: 369–378Google Scholar
  42. Quick WP and Neuhaus HE (1997) The regulation and control of photosynthetic carbon assimilation. In: Foyer CH and Quick WP (eds) A Molecular Approach to Primary Metabolism in Higher Plants, pp 41–62. Taylor and Francis, LondonGoogle Scholar
  43. Quick WP, Schurr U, Fichtner K, Schulze E-D, Rodermel SR, Bogorad L and Stitt M (1991a) The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant J 1: 51–58Google Scholar
  44. Quick WP, Schurr U, Scheibe R, Schulze E-D, Rodermel SR, Bogorad L and Stitt M (1991b) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. I Impact on photosynthesis in ambient growth conditions. Planta 183: 542–554Google Scholar
  45. Quick WP, Schurr U, Fichtner K, Schultze E-D, Wendler R, Leegood RC, Mooney H, Rodermel SR, Bogorad L and Stitt M (1992) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. IV. Impact on photosynthesis in conditions of altered nitrogen supply. Planta 188: 522–531Google Scholar
  46. Raines CA, Harrison EP, Olcer H and Lloyd JC (2000) Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis. Physiol Plant 110: 303–308Google Scholar
  47. Rodermel SR, Abbott MS and Bogorad L (1988) Nuclearorganelle interactions: nuclear antisense gene inhibits ribulose-1,5-bisphophate carboxylase enzymes levels in transformed tobacco plants. Cell 55: 673–681Google Scholar
  48. Ruuska S, Andrews TJ, Badger MR, Hudson GS, Laisk A, Price GD and Caemmerer S von (1998) The interplay between limiting processes in C-3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis. Aust J Plant Physiol 25: 859–870Google Scholar
  49. Ruuska S, Andrews TJ, Badger MR, Price GD and Caemmerer S von (2000a) The role of chloroplast electron transport and metabolites in modulating Rubisoc activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/f complex or glyceraldehydes 3-phosphate dehydrogenase. Plant Physiol 122: 491–504Google Scholar
  50. Ruuska S, Badger MR, Andrews TJ and Caemmerer von S (2000b) Photosynthetic electron sinks in transgenic tobacco with reduced amonts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51: 357–368Google Scholar
  51. Ruuska S, Caemmerer S von, Badger MR, Andrews TJ and Robinson SA (2000c) Xanthophyll cycle, light energy dissipation and electron transport in transgenic tobacco with reduced carbon assimilation capacity. Aust J Plant Physiol 27: 289–300Google Scholar
  52. Spreitzer R (1993) Genetic dissection of Rubisco structure and function. Annu Rev Plant Phys Plant Mol Biol 44: 411–434Google Scholar
  53. Stitt M and Schulze E-D (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ 17: 465–487Google Scholar
  54. Stitt M and Sonnewald U (1995) Regulation of metabolism in transgenic plants. Annu Rev Plant Physiol Plant Mol Biol 46: 341–368Google Scholar
  55. Stitt M, Quick WP, Schurr U, Schulze ED, Rodermel SR and Bogorad L (1991) Decreased ribulose-1,5-bisphosphate carboxylase/oxygenase in transgenic tobacco transformed with antisense rbcS II. Flux control coefficients for photosynthesis in varying light, CO2 and air humidity. Planta 183: 555–566Google Scholar
  56. Tsai C-H, Miller A, Spalding M and Rodermel S (1997) Source strength regulates an early phase transition of tobacco shoot morphogenesis. Plant Physiol 115: 907–914Google Scholar
  57. Wedel N and Soll J (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/glyceraldehyde-3-p hosphate dehydrogenase complex dissociation. Proc Natl Acad Sci USA 95, 9699–9704Google Scholar
  58. Wedel N, Soll J and Paap BK (1997) CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc Natl Acad Sci USA 94: 10479–10484Google Scholar
  59. Woodrow IE and Berry JA. (1988) Enzymic regulation of photosynthetic CO2 fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol 39: 533–594Google Scholar
  60. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants-A retrospective analysis of the A/ci curves of 109 species. J Exp Bot 44: 907–920Google Scholar
  61. Zhang N, Kallis R, Ewy RG and Portis AR (2002) Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 99: 3330–3334Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Christine A. Raines
    • 1
  1. 1.Department of Biological SciencesUniversity of EssexColchesterUK

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