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Dynamics of Photosynthetic CO2 Fixation: Control, Regulation and Productivity

  • Chapter
Regulation of Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 11))

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Summary

Biotechnology is providing the tools to dissect complex interacting pathways in plants and also the means to alter plant traits based on understanding these interactions. There has been a concerted and systematic effort to apply these techniques to alter the levels of enzymes involved in the photosynthetic carbon reduction cycle. This has been informative in locating those reactions of the cycle that exert significant control over the flux of carbon through the cycle and the subsequent effects on partitioning of the photoassimilate in downstream processes. Biotechnology has also provided some understanding of the complexities in communication between the various compartments of an actively photosynthesizing plant cell in both C3 and C4 variants. This account attempts to provide some insight into the nature of this regulation in terms of the structural features of the enzymes involved and, based on this understanding, reveal where there may be opportunities to influence the productivity of photosynthesis.

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References

  • Andralojc PJ, Keys AJ, Martindale W, Dawson GW and Parry MAJ (1996) Conversion of D-hamamelose into 2-carboxy-D-arabinitol and 2-carboxy-D-arabinitol 1-phosphate in leaves of Phaseolus vulgaris L. J Biol Chem 271: 26803–26809

    CAS  PubMed  Google Scholar 

  • Andrews TJ (1988) Catalysis by cyanobacterial ribulose bisphosphate carboxylase large subunit in the complete absence of small subunit. J Biol Chem 263: 12213–12219

    CAS  PubMed  Google Scholar 

  • Andrews TJ (1997) The bait in the rubisco mousetrap. Nat Struct Biol 3: 3–7

    Google Scholar 

  • Andrews TJ and Lorimer GH (1987) Rubisco: Structure, mechanisms, and prospects for improvement. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, Vol 10, pp 131–218. Academic Press, San Diego

    Google Scholar 

  • Andrews TJ, von Caemmerer S, He Z, Hudson GS and Whitney S (1998) Rubisco catalysis in vitro and in vivo. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol V, pp 3307–3313. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Ashton AR, Burnell JN and Hatch MD (1984) Regulation of C4 photosynthesis: Inactivation of pyruvate Pi dikinase by ADP dependent phosphorylation and activation by phosphorylase. Arch Biochem Biophys 230: 492–503

    Article  CAS  PubMed  Google Scholar 

  • Banks FM, Driscoll SP, Parry MA, 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: 1125–1136

    Article  CAS  PubMed  Google Scholar 

  • Benson AA and Calvin M (1950) Carbon dioxide fixation by green plants. Ann Rev Plant Physiol 1: 25–40

    Google Scholar 

  • Berry JA, Lorimer GH, Pierce J, Seemann JR, Meeks J and Freas S (1987) Isolation, identification, and synthesis of 2-carboxyarabinitol 1-phosphate, a diurnal regulator of ribulose bisphosphate carboxylase. Proc Natl Acad Sci USA 84: 734–738

    CAS  Google Scholar 

  • Brandes HK, Larimer FW and Hartman FC (1996) The molecular pathway for the regulation of phosphoribulokinase by thioredoxin f. J Biol Chem 271: 3333–3335

    CAS  PubMed  Google Scholar 

  • Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Ann Rev Plant Physiol 31: 341–374

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Carr PD, Verger D, Ashton AR and Ollis DL (1999) Chloroplast NADP-malate dehydrogenase: Structural basis of light-dependent regulation of activity by thiol oxidation and reduction. Structure 7: 461–475

    Article  CAS  PubMed  Google Scholar 

  • Cleland WW, Andrews TJ, Gutteridge S, Hartman F and Lorimer GH (1998) Mechanism of Rubisco: The carbamate as general base. Chem Rev 98: 549–561

    Article  CAS  PubMed  Google Scholar 

  • Dever L, Bailey KJ, Leegood RC and Lea PJ (1997) Control of photosynthesis in Amaranthus edulis mutants with reduced amounts of PEP carboxylase. Aust J Plant Physiol 24: 469–476

    CAS  Google Scholar 

  • Edwards G and Walker D (1983) C3, C4: Mechanisms and cellular and environmental regulation of photosynthesis. Blackwell Scientific Publications. University of California Press, Los Angeles

    Google Scholar 

  • Farquhar GD, von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 fixation in leaves of C3 species. Planta 149: 78–90

    Article  CAS  Google Scholar 

  • Furbank RT and Taylor WC (1995) Regulation of photosynthesis in C3 and C4 plants: A molecular approach. Plant Cell 7: 797–807

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S and Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477–485

    CAS  Google Scholar 

  • Furbak RT, Hatch MD and Jenkins C (2000) C4 photosynthesis: Mechanism and regulation. In: Leegood R, Sharkey T and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 435–457. Kluwer Academic Publishers, Dordrectht

    Google Scholar 

  • Gatenby AA (1990) Chaperone function: The assembly of ribulose bisphosphate carboxylase-oxygenase. Annu Rev Cell Biol 6: 125–149

    Article  CAS  PubMed  Google Scholar 

  • Gutteridge S (1991) The relative catalytic specificities of the large subunit core of Synechococcus ribulose bisphosphate carboxylase-oxygenase. J Biol Chem 266: 7359–7362

    CAS  PubMed  Google Scholar 

  • Gutteridge S and Gatenby AA (1995) Rubisco synthesis, assembly, mechanism and regulation. Plant Cell 7: 809–819

    Article  CAS  PubMed  Google Scholar 

  • Gutteridge S and Julien B (1989) A phosphatase from chloroplast stroma of Nicotiana tabacum hydrolyses 2′-carboxyarabinitol 1-phosphate, the natural inhibitor of Rubisco to 2′-carboxyarabinitol. FEBS Lett 254: 225–230

    Article  CAS  Google Scholar 

  • Gutteridge S, Parry MAJ and Schmidt CNG (1982) The reactions between active and inactive forms of wheat ribulose bisphosphate carboxylase and effectors. Eur J Biochem 126: 597–602

    Article  CAS  PubMed  Google Scholar 

  • Gutteridge S, Parry MA, Schmidt CNG and Feeney J (1984) An investigation of ribulose bisphosphate carboxylase activity by high-resolution proton NMR. FEBS Lett 170: 355–359

    Article  CAS  Google Scholar 

  • Gutteridge S, Parry MA, Keys AJ, Mudd A and Pierce J (1986) A nocturnal inhibitor of carboxylation in leaves. Nature 324: 274–276

    Article  CAS  Google Scholar 

  • 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 the growth of potato plants. Plant J 14: 147–157

    Article  CAS  PubMed  Google Scholar 

  • Harrison DHT, Runquist JA, Holub A, and Miziorko HM (1998a) Crystal structure of phosphoribulokinase from Rhodobacter sphaeroides reveals a fold similar to that of adenylate kinase. Biochemistry 37: 5074–5085

    Article  CAS  PubMed  Google Scholar 

  • Harrison EP, Willingham NM, Loyd JC and Raines CA (1998b) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204: 27–36

    CAS  Google Scholar 

  • Heo J and Holbrook GP (1999) Regulation of 2′-carboxyarabinitol 1 phosphate phosphatase: Activation by glutathione and interaction with thiol reagents. Biochem J 338: 409–416

    Article  CAS  PubMed  Google Scholar 

  • Hirasawa M, Brandes HK, Hartman FC and Knaff DB (1998) Oxidation-reduction properties of the regulatory site of spinach phosphoribulokinase. Arch Biochem Biophys 350: 127–131

    Article  CAS  PubMed  Google Scholar 

  • Hudson GS, Evans JR, von Caemmerer S, Arvidsson YBC and Andrews TJ (1992) Reduction of ribulose bisphosphate carboxylase/oxygenase content by anitsense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol 98: 294–302

    CAS  Google Scholar 

  • Issakidis E, Saarinen M, Decottignies P, Jacquot J-P, Cretin C, Gadal P and Miginiac-Maslow M (1994) Identification and characterization of the second regulatory disulfide bridge of recombinant sorghum leaf NADP-malate dehydrogenase. J Biol Chem 269: 3511–3517

    CAS  PubMed  Google Scholar 

  • Jacquot JP, Lopez-Jaramilto J, Chueca A, Cherfils J, Lemaire S, Chedozeau B, Miginiac-Maslow M, Decottignies P, Wolosiuk RA 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: 675–681

    Article  CAS  PubMed  Google Scholar 

  • Jacquot JP, Lopez-Jaramilto J, Miginiac-Maslow M, Lemaire S, Cherfils J, Chueca A and Lopez-Gorge J (1997) Cysteine-153 is required for redox regulation of pea chloroplast fructose-1,6-bisphosphatase. FEBS Lett 401: 143–147

    Article  CAS  PubMed  Google Scholar 

  • Jordan DB and Chollet R (1983) Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. J Biol Chem 258: 13752–13758

    CAS  PubMed  Google Scholar 

  • Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291: 513–515

    Article  CAS  Google Scholar 

  • Kanevski I, Maliga P, Rhoades DF and Gutteridge S (1998) Engineering Rubisco in higher plants. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol V, pp 3351–3354. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Kanevski I, Maliga P, Rhoades DF and Gutteridge S (1999) Plastome engineering of ribulose bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119: 133–141

    Article  CAS  PubMed  Google Scholar 

  • Kossmann J, Sonnewald U and Wilmitzer L (1994) Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J 6: 637–650

    Article  CAS  Google Scholar 

  • Ku SB and Edwards GE (1977) Oxygen inhibition of Photosystem I. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol 59: 986–990

    CAS  Google Scholar 

  • Lorimer GH, Gutteridge S and Reddy GS (1989) The orientation of substrate and reaction intermediates in the active site of ribulose-1,5-bisphosphate carboxylase. J Biol Chem 264: 9873–9879

    CAS  PubMed  Google Scholar 

  • Lundqvist T and Schneider G (1989) Crystal Structure of the complex of ribulose-1,5-bisphosphate carboxylase and a transition state analogue, 2-carboxy-D-arabinitol 1,5-bisphosphate. J Biol Chem 264: 7078–7083

    CAS  PubMed  Google Scholar 

  • Mann CM (1999) Crop scientists seek a new revolution. Science 283: 310–314

    CAS  Google Scholar 

  • Mate CJ, Hudson GS, von Caemmerer S, Evans JR and Andrews TJ (1993) Reduction of ribulose bisphosphate carboxylase activase levels in tobacco by antisense RNA reduces ribulose bisphosphate carboxylase activation and impairs photosynthesis. Plant Physiol 102: 1119–1128

    Article  CAS  PubMed  Google Scholar 

  • Newman JM and Gutteridge S (1993) The X-ray structure of Synechococcus ribulose-bisphosphate carboxylase/oxygenase-activated quaternary complex at 2.2 Å resolution. J Biol Chem 268: 25876–25886

    CAS  PubMed  Google Scholar 

  • Newman JM and Gutteridge S (1994) Structure of an effector-induced inactivated state of ribulose 1,5-bisphosphate carboxylase/oxygenase: The binary complex between enzyme. Structure 2: 495–502

    CAS  PubMed  Google Scholar 

  • Pierce J, Lorimer GH and Reddy GS (1986) Kinetic mechanism of ribulose bisphosphate carboxylase: Evidence for an ordered, sequential reaction. Biochemistry 25: 1636–1644

    Article  CAS  Google Scholar 

  • Portis A (1990) Rubisco activase. Biochim Biophys Acta 1015: 15–28

    CAS  PubMed  Google Scholar 

  • Portis A (1995) Regulation of rubisco by rubisco activase. J Exp Bot 46: 1285–1291

    CAS  Google Scholar 

  • Price GD, von Caemmerer S, Evans JR, Yu JW, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A and Badger MR (1994) Specific reduction of the chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193: 331–340

    Article  CAS  Google Scholar 

  • Price GD, Evans JR, von Caemmerer S, Yu JW and Badger MR (1995) Specific reduction of glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in RUBP regeneration in transgenic tobacco plants. Planta 195: 369–378

    Article  CAS  PubMed  Google Scholar 

  • Quick WP, Schurr U, Scheibe R, Schultze E-D, Rodermel SR, Bogorad L and Stitt M (1991) Decreased ribulose bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. I. Impact on photosynthesis in ambient growth conditions. Planta 183: 542–554

    Article  CAS  Google Scholar 

  • 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: 210–218

    Article  CAS  PubMed  Google Scholar 

  • Reismeier JW, Flugge UI, Schutz B, Heineke D, Heldt HW, Willmitzer L and Frommer WB (1993) Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 90: 6160–6164

    Google Scholar 

  • Robinson SP and Portis AR (1989) Adenosine triphosphate hydrolysis by purified rubisco activase. Arch Biochem Biophys 268: 93–99

    Article  CAS  PubMed  Google Scholar 

  • Rodermel SR, Abbott MS and Bogorad L (1988) Nuclear organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55: 673–684

    Article  CAS  PubMed  Google Scholar 

  • Roy H and Andrews J (2000) Rubisco: Assembly and mechanism. In: Leegood R, Sharkey T and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 53–83. Kluwer Academic Publishers

    Google Scholar 

  • Salvucci ME and Holbrook GP (1989) Purification and properties of 2-carboxy-D-arabinitol 1-phosphatase. Plant Physiol 90: 679–685

    CAS  Google Scholar 

  • Sugawara H, Yamamoto H, Inoue T, Miyake C, Yokata A and Kai Y (1998) Crystal structure of rubisco from a thermophilic red alga, Galdiera partita. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol V, pp 3339–3342. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • 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: 95–101

    Article  CAS  PubMed  Google Scholar 

  • Tolbert NE (1971) Microbodies-peroxisomes and glyoxysomes. Annu Rev Plant Physiol 22: 45–74

    Article  CAS  Google Scholar 

  • Trevanion SJ, Furbank RT and Ashton AR (1997) NADP-malate dehydrogenase in the C4 plant Flaveria bidentis. Plant Physiol 113: 1153–1165

    CAS  PubMed  Google Scholar 

  • Wang ZY, Snyder GW, Esau BD, Portis AR and Ogren WL (1992) Species-dependent variation in the interaction of substrate bound ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) and rubisco activase. Plant Physiol 100: 1858–1862

    CAS  Google Scholar 

  • Whitney SM, von Caemmerer S, Hudson GS and Andrews TJ (1999) Directed mutation of the Rubisco large subunit of tobacco influences photorespiration and growth. Plant Physiol 121: 579–588

    CAS  PubMed  Google Scholar 

  • Zhu G and Jensen RG (1991) Xylulose 1,5-bisphosphate synthesized by ribulose bisphosphate carboxylase/oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiol 97: 1348–1353

    CAS  Google Scholar 

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Authors and Affiliations

  1. DuPont Agricultural Products, Stine Haskell Research Center, PO Box 30, Newark, DE, 19714, USA

    Steven Gutteridge & Douglas B. Jordan

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  1. Steven Gutteridge
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  2. Douglas B. Jordan
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Editors and Affiliations

  1. University of Turku, Finland

    Eva-Mari Aro

  2. University of Stockholm/Linköping, Sweden

    Bertil Andersson

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© 2001 Kluwer Academic Publishers

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Gutteridge, S., Jordan, D.B. (2001). Dynamics of Photosynthetic CO2 Fixation: Control, Regulation and Productivity. In: Aro, EM., Andersson, B. (eds) Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, vol 11. Springer, Dordrecht. https://doi.org/10.1007/0-306-48148-0_17

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  • DOI: https://doi.org/10.1007/0-306-48148-0_17

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6332-3

  • Online ISBN: 978-0-306-48148-2

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