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
Arnon D.I. Whatley F.R. and Allen M.B. (1958) Assimilatory power in photosynthesis. Science 127: 1026–1034
Ashton A.R. (1982) A role for ribulose-I. 5 bisphosphate carboxylase as a metabolic buffer. FEBS Lett 145: 1–6
Baker N.R. (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81: 563–570
Bendall D.S. (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim Biophys Acta 683: 119–157
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
Cseke C. and Buchanan B.B. (1986) Regulation of the formation and utilisation of photosynthate in leaves. Biochim Biophys Acta 853: 43–63
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
Demmig-Adams B. (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Horton P. (1983) Control of electron transport by the thylakoid protein kinase. FEBS Lett 152: 47–52
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
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
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
Kitajima M. and Butler W.L. (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376: 105–115
Krause G.H. and Weis E. (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349
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
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
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
Le Gouallec J.L. and Comic G. (1988) Photoinhibition of photosynthesis in Elatostema repens. Plant Physiol Biochem 26: 705–712
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
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
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
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
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
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
Neubauer C. and Schreiber U. (1989) Photochemical and non-photochemical quenching of chlorophyll fluorescence induced by hydrogen peroxide. Z. Naturforsch 44c: 262–270
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
Osterhout W.I.V. and Hass A.R.C. (1919) On the dynamics of photosynthesis. J Gen Physioll: 1–16
Pearcy R.W. (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41: 421–453
Pfündel E. and Strasser R.J. (1988) Violaxanthin de-epoxidase in etiolated leaves. Photosynth Res 15: 67–73
Portis A.R. Jr. (1990) Rubisco activase. Biochim Biophys Acta 1015: 15–28
Powles S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44
Prinsley R.T. and Leegood R.C. (1986) Factors affecting photosynthetic induction in spinach leaves. Biochim Biophys Acta 849: 244–253
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
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
Satoh K. (1981) Fluorescence induction and activity offerredoxin-NADP reductase in Bryopsis chloroplasts. Biochirn Biophys Acta 638: 327–333
Scheibe R. (1987) NADP+ malate dehydrogenase in C3 plants. Regulation and role of a light-activated enzyme. Physiol Plant 71: 393–400
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
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
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
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
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
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
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
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
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
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
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
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
Yamamoto H.Y. (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure and Appl Chem 51: 639–648
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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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