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Interactions between Electron Transport and Carbon Assimilation in Leaves: Coordination of Activities and Control

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Photosynthesis: Photoreactions to Plant Productivity

Abstract

Concepts of control within photosynthetic syste~ have generally been discussed in tenns of the independent regulation of two discrete, spatially separated reaction sequences. These are the electron transport processes and the carbon reduction cycle, occurring in the thylakoid membrane and the stroma, respectively. The fonner comprise two photosystems operating sequentially to achieve Iight-driven reduction of NADP+ with concomitant production of a proton gradient. This is used to generate ATP. NADPH and ATP thus produced are consumed during the assimilation and reduction of CO2 to the level of sugar phosphate. The producer-consumer relationship between electron transport and CO2 assimilation ensures their tight coupling by virtue of the cycling of intennediates. However, in vivo regulation is complicated by the necessity to reconcile the conflicting requirements of the thylakoid reactions and the stromal enzymes.

Several regulatory mechanisms are involved in the modulation of the activity state of key enzymes of the carbon reduction cycle so as to match their activity to the availability of the products of electron flow. High levels of ATP and NADPH are needed to drive high rates CO2 reduction but high rates of electron transport are difficult to maintain when the electron acceptor NADP and the substrate for photophosphorylation ADP are not freely available. Measurements of (NADPH)/(NADP) ratios and phosphorylation potentials (ATP)/(ADP) + (Pi) in vivo give much lower values than would be predicted from in vitro measurements with isolated thylakoids. In addition, these parameters are surprisingly stable in vivo over a wide range of conditions. The molecular mechanisms whereby electron transport is restrained when ADP and NADP are in short supply are not fully understood. Under these conditions the quantum efficiency of photosystem II is down-regulated and thennodynamic constraints exert a restraining control on the rate of electron flow. The mechanisms that serve to decrease the quantum efficiency of photosystem II also facilitate the coordinate and harmless conversion of light energy directly to heat.

Photoinhibition is a further mechanism that causes a restriction of electron transport. It is exerted under conditions of excessive irradiation and results in a stable down-regulation of photosystem II function.

Much progress has been made in recent years in understanding the relative contributions made by each regulatory process but our insights are far from complete. The most important question to address, however, is why such tight regulation exists. The answeres to this question are complex but undoubtedly such precise regulation confers a physiological advantage. In short, co-regulation serves to prevent deleterious effects that would otherwise occur. Precise coordination of reaction rates prevents continuous oscillations in metabolite flux, allows optimization of resources, and yet confers a degree of flexibility that is essential for the avoidance of the detrimental effects of light in a hazardous and constantly changing environment. The most destructive of these are the mechanisms that produce toxic derivatives of oxygen which are an inevitable consequence of the operation of the electron transport chain in an aerobic environment.

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References

  • Anderson I.W. Foyer C.H. and Walker D.A. (1983) Light-dependent reduction of hydrogen peroxide by intact spinach chloroplasts. Biochim Biophys Acta 724: 69–74

    Article  CAS  Google Scholar 

  • Arnon D.I. Whatley F.R. and Allen M.B. (1958) Assimilatory power in photosynthesis. Science 127: 1026–1034

    Article  CAS  PubMed  Google Scholar 

  • Ashton A.R. (1982) A role for ribulose-I. 5 bisphosphate carboxylase as a metabolic buffer. FEBS Lett 145: 1–6

    Article  CAS  Google Scholar 

  • Baker N.R. (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81: 563–570

    Article  CAS  Google Scholar 

  • Bendall D.S. (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim Biophys Acta 683: 119–157

    Article  CAS  Google Scholar 

  • Berry I.A. Lorimer O.H. Pierce J. Seemann J. Meek J. and Freas S. (1987) Isolation, identification and synthesis of 2-carboxyarabinitol-I-phosphate, a diurnal regulator of ribulose bisphosphate carboxylase activity. Proc Natl Acad Sci USA 84: 734–738

    Article  CAS  PubMed  Google Scholar 

  • Cseke C. and Buchanan B.B. (1986) Regulation of the formation and utilisation of photosynthate in leaves. Biochim Biophys Acta 853: 43–63

    Article  CAS  Google Scholar 

  • Crawford N.A., Droux M., Kosower N.S. and Buchanan B.B. (1989) Evidence for function of the ferredoxinlthioredoxin system in the reductive activation of target enzymes of isolated intact chloroplasts. Arch Biochem Biophys 271: 223–239

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B. (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24

    Article  CAS  Google Scholar 

  • Dujardyn M. and Foyer C.H. (1989) Limitation of CO2 assimilatioo and regulation of Benson-Calvin cycle activity in barley leaves in response to changes in irradiance, photoinhibition and recovery. Plant Physiol 91: 1562–1568

    Article  CAS  PubMed  Google Scholar 

  • Edwards G. and Walker D.A. (1983) Induction. In: C3, C4: mechanisms and Cellular and Environmental Regulation of Phatosynthesis, Blackwell Science Publications, Oxford, London, pp 156–200

    Google Scholar 

  • Egneus H., Heber U., Matthiesen U. and Kirk M.R. (1975) Reduction of oxygen by the electron transport chain of chloroplasts during assimilation of carbon dioxide. Biochim Biophys Acta 408: 252–268

    Article  CAS  PubMed  Google Scholar 

  • Evron Y. and Avron M. (1990) Characterization of an alkaline pH-dependent proton “slip”, in the ATP synthase of lettuce thylakoids. Biochim Biophys Acta 109: 115–120

    Google Scholar 

  • Foyer C.H. (1989) The role of orthophosphate in photosynthetic control: Studies using phosphorus-31 nuclear magnetic resonance. Plant Physiol (Life Science Advances) 8: 81–89

    Google Scholar 

  • Foyer C.H., Anderson J. and Walker D.A. (1984) Light dependent reduction of hydrogen peroxide via the ascorbate-glutathione cycle in intact spinach chloroplasts. In: (C Sybesma, ed) Advances in Photosynthesis Research, Vol III Martinus Nijhoff/Dr W Junk Publishers, pp 689–692

    Google Scholar 

  • Foyer C.H., Dujardyn M. and Lemoine Y. (1989) Responses of photosynthesis and the xanthophyll and ascorbate-glutathione cycles to changes in irradiance, photoinhibition and recovery. Plant Physiol Biochem 27: 751–760

    CAS  Google Scholar 

  • Foyer C.H., Furbank R., Harbinson J. and Horton P. (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25: 83–100

    Article  CAS  Google Scholar 

  • Fredeen A.L., Raab T., Rao I.M. and Terry N. (1990) Effects of phosphorus nutrition on photosynthesis in Glycine max (L.) Merr. Planta 181: 399–405

    Article  CAS  Google Scholar 

  • Furbank R.T., Foyer C.H. and Walker D.H. (1987) Interactioos between ribulose-I, 5-bisphosphate carboxylase and stromal metabolites. III Corroboration of the role of this enzyme as a metabolite buffer. Biochim Biophys Acta 894: 165–173

    Article  CAS  Google Scholar 

  • Genty B., Briantais J.M. and Baker N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and photochemical quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92

    Article  CAS  Google Scholar 

  • Genty B., Harbinson J. and Baker N.R. (1990) Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiol Biochem 28: 1–10

    CAS  Google Scholar 

  • Guinon C. and Mache R. (1987) Photophosphorylation in vitro of the large subunit of the ribulose 1,5-bisphosphate carboxylase and of the glyceraldehyde 3-phosphate dehydrogenase. Eur J Biochem 166: 249–254

    Article  Google Scholar 

  • Gutteridge S., Parry M.A.J., Burton S., Keys A.J., Mudd A., Feeny J., Servaites J.C. and Pierce J. (1986) A nocturnal inhibitor of carboxylation in leaves. Nature 324: 274–276

    Article  CAS  Google Scholar 

  • Harbinson J. and Foyer C.H. (1991) Relationships between the efficiencies of photosystems I and II and stromal redox state in CO2-free air: Evidence for cyclic electron flow in vivo. Plant Physiol 91: 41–49

    Article  Google Scholar 

  • Harbinson J., Genty B. and Baker N.R. (1989) Relationship between the quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol 90: 1029–1034

    Article  CAS  PubMed  Google Scholar 

  • Harbinson J., Genty B. and Foyer C.H. (1990) The relationship between photosynthetic electron transport and stromal enzyme activity in pea leaves: Towards an understanding of the nature of photosynthetic control, Plant Physiol 94: 545–553

    Article  CAS  PubMed  Google Scholar 

  • Harbinson J. and Hedley C.L. (1989) The kinetics of p-700+ reduction in leaves: A novel in situ probe of thylakoid functioning. Plant Cell Environ 12: 357–369

    Article  CAS  Google Scholar 

  • Harbinson J. and Woodward F.I. (1987) The use of light induced absorbance changes at 820 nm to monitor the oxidation state of P-700 leaves. Plant Cell Environ 9: 131–140

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Heldt H.W., Werden K., Milovancev M. and Geller G. (1973) Alkalisation of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta 314: 224–241

    Article  CAS  PubMed  Google Scholar 

  • Horton P. (1983) Control of electron transport by the thylakoid protein kinase. FEBS Lett 152: 47–52

    Article  CAS  Google Scholar 

  • Horton P. (1989) Interactions between electron transport and carbon assimilation: Regulation of lightharvesting and photochemistry. In: (WR Briggs, ed) Photosynthesis, Plant Biology Series Vol 8, Alan R Liss Inc, New York, pp 393–406

    Google Scholar 

  • Kirschbaum M.U.F. and Pearcy R.W. (1988a) Gas exchange analysis of the fast phase of photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 87: 818–821

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum M.U.F. and Pearcy R.W. (1988b) Concurrent measurements of O2 and CO2 exchange during lightflecks in Alocasia macrorrhiza (L.) G. Don. Planta 174: 527–533

    Article  CAS  Google Scholar 

  • Kitajima M. and Butler W.L. (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105–115

    Article  CAS  PubMed  Google Scholar 

  • Krause G.H. and Weis E. (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349

    Article  CAS  Google Scholar 

  • Laing W.A., Stitt M. and Heldt H.W. (1981) Control of CO2 fixation. Changes in the activity of ribulose phosphate kinase and fructose and sedoheptulose bisphosphatase in chloroplasts. Biochim Biophys. Acta 637: 348–359

    Article  CAS  Google Scholar 

  • Leegood R.C. (1990) Enzymes of the Calvin cycle. In: (PI Lea, ed) Methods in Plant Biochemistry, Vol 3, Academic Press, London, pp 15–37

    Google Scholar 

  • Leegood R.C., Walker O.A. and Foyer C.H. (1985) Regulation of the Benson-Calvin cycle. In: (1 Barber and NR Baker, eds) Photosynthetic Mechanisms and the Environment. Elsevier Science Publishers, Amsterdam, New York, pp 191–258

    Google Scholar 

  • Le Gouallec J.L. and Comic G. (1988) Photoinhibition of photosynthesis in Elatostema repens. Plant Physiol Biochem 26: 705–712

    Google Scholar 

  • Macioszek J. and Anderson L.E. (1987) Changing kinetic properties of the two-enzyme phosphoglycerate kinaseINADP-linked glyceraldehyde-3-phosphate dehydrogenase couple from pea chloroplasts during photosynthetic induction. Biochim Biophys Acta 892: 185–190

    Article  CAS  Google Scholar 

  • Macioszek J., Anderson I.B. and Anderson L.E. (1990) Isolation of chloroplastic phosphoglycerate kinase. Kinetics of the two-enzyme phosphoglycerate kinase/glyceraldehyde 3-phosphate dehydrogenase couple. Plant Physiol 94: 291–296

    Article  CAS  PubMed  Google Scholar 

  • Marsho T.V., Behrens P.N. and Radmer K.J. (1979) Photosynthetic oxygen reduction in isolated intact chloroplasts and cells from spinach. Plant Physiol 64: 656–659

    Article  CAS  PubMed  Google Scholar 

  • McTavish H., Picorel R. and Seibert M. (1989) Stabilisation of isolated photosystem II reaction center complex in the dark and in the light using polyethylene glycol and an oxygen-scrubbing system. Plant Physiol 89: 452–456

    Article  CAS  PubMed  Google Scholar 

  • Miginiac-Maslow M., Decottignies P., Jacquot I.P. and Gadal P. (1990) Regulation of com leaf NAOPmalate dehydrogenase light activation by the photosynthetic electron flow. Effect of photoinhibition studied in a reconstituted system. Biochim Biophys Acta 1017 273–279

    Article  CAS  Google Scholar 

  • Nedbal L., Masojidek J., Komenda J, Prasil O. and Setlik I. (1990) Three types of photosystem II photoinactivation 2. Slow processes. Photosynth Res 24: 89–97

    Article  CAS  Google Scholar 

  • Neubauer C. and Schreiber U. (1989) Photochemical and non-photochemical quenching of chlorophyll fluorescence induced by hydrogen peroxide. Z. Naturforsch 44c: 262–270

    Google Scholar 

  • Ohad I., Adir N., Kioke H. and Kyle O. (1990) Mechanism of photoinhibition in vivo. A reversible lightinduced conformational change of reaction center II is related to an irreversible modification of the 01 protein. J Biol Chem 265: 1972–1979

    CAS  PubMed  Google Scholar 

  • Osterhout W.I.V. and Hass A.R.C. (1919) On the dynamics of photosynthesis. J Gen Physioll: 1–16

    Google Scholar 

  • Pearcy R.W. (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41: 421–453

    Article  CAS  Google Scholar 

  • Pfündel E. and Strasser R.J. (1988) Violaxanthin de-epoxidase in etiolated leaves. Photosynth Res 15: 67–73

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Powles S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44

    Article  CAS  Google Scholar 

  • Prinsley R.T. and Leegood R.C. (1986) Factors affecting photosynthetic induction in spinach leaves. Biochim Biophys Acta 849: 244–253

    Article  CAS  Google Scholar 

  • Richter M., Rühle W. and Wild A. (1990) Studies on the mechanism of photosystem II photoinhibition. A two-step degradation of D1-protein. Photosynth Res 24: 237–243

    Article  CAS  Google Scholar 

  • Robinson S.P. and Walker O.A. (1980) The significance of light activation of enzymes during the induction phase of photosynthesis in isolated chloroplasts. Arch Biochem Biophys 202: 617–623

    Article  CAS  PubMed  Google Scholar 

  • Satoh K. (1981) Fluorescence induction and activity offerredoxin-NADP reductase in Bryopsis chloroplasts. Biochirn Biophys Acta 638: 327–333

    Article  CAS  Google Scholar 

  • Scheibe R. (1987) NADP+ malate dehydrogenase in C3 plants. Regulation and role of a light-activated enzyme. Physiol Plant 71: 393–400

    Article  CAS  Google Scholar 

  • Scheibe R. and Stitt M. (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol Biochern 26: 473–482

    CAS  Google Scholar 

  • Schreiber U. and Neubauer C. (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II Partial control by the photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c: 1255–1264

    Google Scholar 

  • Seemann J.R., Kirschbaum M.U.F., Sharkey T.D. and Pearcy R.W. (1988) Regulation of ribulose 1,5-bisphosphate carboxylase activity in Alocasia macrorrhiza in response to step changes in irradiance. Plant Physiol 88: 148–152

    Article  CAS  PubMed  Google Scholar 

  • Seaton G.G.R. and Walker D.A. (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc R Soc Lond B 242: 29–35

    Article  Google Scholar 

  • Servaites J.C., Shieh W.J. and Geiger D.R. (1991) Regulation of photosynthetic carbon reduction cycle by ribulose bisphosphate and phosphoglyceric acid. Plant Physiol 97: 1115–1121

    Article  CAS  PubMed  Google Scholar 

  • Stitt M. (1986) Limitation of photosynthesis by carbon metabolism. I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol 81: 1115–1122

    Article  CAS  PubMed  Google Scholar 

  • Takahama U., Shimizu-Takahama M. and Heber U. (1981) The redox state of the NADP system in illuminated chloroplasts. Biochirn Biophys Acta 637: 530–539

    Article  CAS  Google Scholar 

  • Telfer A., He W-Z. and Barber J. (1990) Spectral resolution of more than one chlorophyll electron donor in the isolated photosystem II reaction center complex. Biochirn Biophys Acta 101: 143–151

    Article  Google Scholar 

  • Von Caemmerer S. and Farquhar G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387

    Article  Google Scholar 

  • Walker D.A. (1981) Photosynthetic induction. In: (G Akoyunoglou, ed) Proceedings of the 5th International Congress on Photosynthesis, Vol IV, Balaban International Sciences Series, Philadelphia, pp 189–202

    Google Scholar 

  • Weis E., Ball J.R. and Berry J. (1987) Photosynthetic control of electron transport in leaves of Phaseolus vulgaris. Evidence for regulation of photosystem II by the proton gradient. In: (J Biggins, ed) Progress in Photosynthesis Research, Vol 02, Martinus Nijhoff Publ, Dordrecht, pp 553–556

    Chapter  Google Scholar 

  • Woodrow I.E. and Motte K.A. (1989) Rate limitation of non-steady state photosynthesis by ribulose 1,5-bisphosphate carboxylase in spinach. Aust J Plant Physiol 16: 487–500

    Article  CAS  Google Scholar 

  • Yamamoto H.Y. (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure and Appl Chem 51: 639–648

    Article  CAS  Google Scholar 

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Foyer, C.H. (1993). Interactions between Electron Transport and Carbon Assimilation in Leaves: Coordination of Activities and Control. In: Abrol, Y.P., Mohanty, P., Govindjee (eds) Photosynthesis: Photoreactions to Plant Productivity. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-2708-0_8

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  • DOI: https://doi.org/10.1007/978-94-011-2708-0_8

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