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Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle

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Abstract

Oscillations in the rate of photosynthesis of sunflower (Helianthus annuus L.) leaves were induced by subjecting leaves, whose photosynthetic apparatus had been activated, to a sudden transition from darkness or low light to high-intensity illumination, or by transfering them in the light from air to an atmosphere containing saturating CO2. It was found that at the first maximum, light-and CO2-saturated photosynthesis can be much faster than steady-state photosynthesis. Both QA in the reaction center of PS II and P700 in the reaction center of PS I of the chloroplast electron-transport chain were more oxidized during the maxima of photosynthesis than during the minima. Maxima of P700 oxidation slightly preceded maxima in photosynthesis. During a transition from low to high irradiance, the assimilatory force FA, which was calculated from ratios of dihydroxyacetone phosphate to phosphoglycerate under the assumption that the reactions catalyzed by NADP-dependent glyceraldehydephosphate dehydrogenase, phosphoglycerate kinase and triosephosphate isomerase are close to equilibrium, oscillated in parallel with photosynthesis. However, only one of its components, the calculated phosphorylation potential (ATP)/(ADP)(Pi), paralleled photosynthesis, whereas calculated NADPH/NADP ratios exhibited antiparallel behaviour. When photosynthetic oscillations were initiated by a transition from low to high CO2, the assimilatory force FA declined, was very low at the first minimum of photosynthesis and increased as photosynthesis rose to its second maximum. The observations indicate that the minima in photosynthesis are caused by lack of ATP. This leads to overreduction of the electron-transport chain which is indicated by the reduction of P700. During photosynthetic oscillations the chloroplast thylakoid system is unable to adjust the supply of ATP and NADPH rapidly to demand at the stoichiometric relationship required by the carbonreduction cycle.

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Abbreviations

PGA:

3-phosphoglycerate

DHAP:

dihydroxyacetone phosphate

P700 :

electron-donor pigment in the reaction enter of PS I

QA :

quinone acceptor in the reaction center of PS II

References

  • Arnon, D.I., Chain, R.K. (1975) Regulation of ferredoxin-catalyzed photosynthetic phosphorylations. Proc. Natl. Acad. Sci. USA 72, 4961–4965

    Google Scholar 

  • Arnon, D.I., Chain, R.K. (1979) Regulatory electron transport pathways in cyclic photophosphorylation. FEBS Lett. 102, 133–138

    Google Scholar 

  • Bradbury, M., Baker, N.R. (1981) Analysis of the slow phases of the chlorophyll fluorescence induction curve. Changes in the redox state of Photosystem II electron acceptors and fluorescence emission from photosystem I and II. Biophys. Acta 635, 542–551

    Google Scholar 

  • Dietz, K.-J., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim. Biophys. Acta 767, 432–443

    Google Scholar 

  • Dietz, K.-J., Heber, U. (1989) Assimilatory force and regulation of photosynthetic carbon reduction in leaves. In: Techniques and new developments in photosynthesis research, vol. 163, pp. 341–363, Barber, J., Malkin, R., eds. NATO ASJ Series A, Plenum Press, New York

    Google Scholar 

  • Furbank, C.H., Foyer, F.T. (1986) Oscillations in levels of metabolites from the photosynthetic carbon reduction cycle in spinach leaf disks generated by the transition from air to 5% CO2. Arch. Biochem. Biophys. 245, 240–244

    Google Scholar 

  • Harris, G.C., Cheesbrough, J.K., Walker, D.A. (1983) Effects of mannose on photosynthetic gas exchange in spinach leaf discs. Plant Physiol. 77, 108–111

    Google Scholar 

  • Heber, U., Santarius, K.A. (1965) Compartmentation and reduction of pyridine nucleotides in relation to photosynthesis. Biochim. Biophys. Acta 100, 390–408

    Google Scholar 

  • Heber, U., Santarius, K.A. (1970) Direct and indirect transport of ATP and ADP across the chloroplast envelop. Z. Naturforsch. 25 b, 718–728

    Google Scholar 

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

    Google Scholar 

  • Heineke, D., Stitt, M., Heldt, H. (1989) Effects of inorganic phosphate on the light dependent thylakoid energization of intact spinach chloroplasts. Plant Physiol. 91, 221–226

    Google Scholar 

  • Kurkidjian, A., Guern, J. (1989) Intracellular pH: Measurement and importance in cell activity. Annu. Rev. Plant Physiol. 40, 271–303

    Google Scholar 

  • Laisk, A., Walker, D.A. (1986) Control of phosphate turnover as a rate-limiting factor and possible source of oscillations in photosynthesis, a mathematical model. Proc. R. Soc. London B 227 281–302

    Google Scholar 

  • Laisk, A., Eichelmann, H. (1989) Towards understanding oscillations: a mathematical model of the biochemistry of photosynthesis. In: New vistas in measurement of photosynthesis pp 143–157, Walker, D.A. Osmond, C.B., eds. The Royal Society, London

    Google Scholar 

  • Lechtenberg, D., Voss, B., Weis, E. (1990) Regulation of photosynthesis: Photosynthetic control and thioredoxin-dependent enzyme regulation. In: Current research in photosynthesis, vol. 4, pp. 171–174, Baltscheffsky, M., ed. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Michal, G. (1984) d-fructose 1,6-bisphosphate, dihydroxyacetone phospate and d-glyceraldehyde 3-phosphate. In: Methods of enzymatic analysis, vol. 6, pp.342–350, Bergmeyer, H.U., ed. Verlag Chemie, Weinheim, FRG

    Google Scholar 

  • Moss, D.A., Bendall, D.S. (1984) Cyclic electron transport in chloroplasts, the Q-cycle and the site of action of antimycin. Biochim. Biophys. Acta 767, 389–395

    Google Scholar 

  • Oja, V. (1983) A quick-operating gas measuring device for studying the kinetics of leaf photosynthesis. Fiziol. Rastenii (Sov. Plant Physiol) 30, 1045–52

    Google Scholar 

  • Oja, V., Laisk, A., Heber, U. (1986) Light-induced alkalization of chloroplast stroma in vivo as estimated from the CO2 capacity of intact sunflower leaves. Biochim. Biophys. Acta 849, 355–365

    Google Scholar 

  • Ogawa, T. (1982) Simple oscillations in photosynthesis of higher plants. Biochim. Biophys. Acta 681, 103–109

    Google Scholar 

  • Pfanz, H., Heber, U. (1986) Buffer capcities of leaves, leaf cells and leaf cell organelles in relation to fluxes of potentially acidic gases. Plant Physiol 81, 597–602

    Google Scholar 

  • Racker, E. (1984) spl-glyceraldehyde 3-phosphate. In: Methods of enzymic analysis, vol. 4, pp. 561–565, Bergmeyer, H.U., Bergmeyer, J., Graßl, M., eds. Verlag Chemie, Weinheim, FRG

    Google Scholar 

  • Santarius, K.A., Heber, U. (1965) Changes in the intracellular levels of ATP, ADP, AMP and Pi and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim. Biophys. Acta 100, 39–54

    Google Scholar 

  • Scheibe, R., Stitt, M. (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol. Biochem. 26 (4), 473–481

    Google Scholar 

  • Schreiber, U., Neubauer, C. (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth. Res. 25, 279–293

    Google Scholar 

  • Schreiber, U., Bilger, W., Schliwa, U. (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51–62

    Google Scholar 

  • Schreiber, U., Klughammer, C., Neubauer, C. (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z. Naturforsch. 43c, 686–698

    Google Scholar 

  • Siebke, K., Laisk, A., Oja, V., Kiirats, O., Raschke, K., Heber, U. (1990) Control of photosynthesis in leaves as revealed by rapid gas exchange and measurements of the assimilatory force FA. Planta 182, 513–522

    Google Scholar 

  • Sivak, M.N., Walker, D.A. (1987) Oscillations and other symptoms of limitation of photosynthesis by inadequate phosphate supply to the chloroplast. Plant Physiol. Biochem. 25 (5), 635–648

    Google Scholar 

  • Sivak, M.N., Dietz, K.-J., Heber, U., Walker, D.A. (1985) The relationship between light scattering and chlorophyll a fluorescence during oscillations in photosynthetic carbon assimilation. Arch. Biochem. Biophys. 237, 513–519

    Google Scholar 

  • Stitt, M., (1986) Limitation of photosynthesis by carbon metabolism. 1. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol. 81, 1115–1122

    Google Scholar 

  • Stitt, M., Grosse, H., Woo, K.-C. (1988) Interactons between sucrose synthesis and CO2` `fixation. II. Alterations of fructose 2,6-bisphosphate during photosynthetic oscillations. J. Plant Physiol. 133, 133–143

    Google Scholar 

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

    Google Scholar 

  • Usuda, H. (1988) Adenine nucleotide levels, the redox state of the NADP system, and assimilatory force in nonaqueously purified mesophyll chloroplasts from maize leaves under different light intensities. Plant Physiol. 88, 1461–1468

    Google Scholar 

  • Wagner, U., Kolbowski, J., Oja, V., Laisk, A., Heber, U. (1990) pH homeostasis of the chloroplast stroma can protect photosynthesis of leaves during the influx of potentially acidic gases. Biochim. Biophys. Acta 1016, 115–120

    Google Scholar 

  • Weis, E., Lechtenberg, D., Krieger, A. (1990) Physiological control of primary energy conversion in higher plants. In: Current research in photosynthesis, vol. 4, pp. 307–312, Baltscheffsky, M., ed. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Walker, D.A., Osmond, C.B. (1986) Measurement of photosynthesis in vivo with a leaf disk electrode; correlations between light dependence of steady state photosynthetic O2 evolution and chlorophyll a fluorescence transients. Proc. R. Soc. London B 227, 281–302

    Google Scholar 

  • Walker, D.A., Sivak, M.N., Prinsley, R.T., Cheesbrough, J.K. (1983) Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol. 73, 542–549

    Google Scholar 

  • Walker, D.A., Plant, N., Sivak, M.N. (1988) The oxidation status of P700 during oscillations in photosynthetic carbon assimilation, pp. 22–24, Annual Report, Research Institute of Photosynthesis, University of Sheffield

  • Wulff, K., Döppen, W., (1985) ATP: Luminometric method. In: Methods of enzymatic analysis, vol. 7, pp.357–364, Bergmeyer, H.U., Bergmeyer, J., Graßl, M., eds. Verlag Chemie, Weinheim, FRG

    Google Scholar 

  • Yin, Z.-H., Neimanis, S., Heber, U. (1990) Light-dependent pH changes in leaves of C3 plants. I. Recording pH changes in various cellular compartments by fluorescent probes. Planta 182, 244–252

    Google Scholar 

  • Yokota, A., Kitaoka, S. (1985) Correct pK values for dissociation constant of carbonic acid lower the reported Km values of ribulose bisphosphate carboxylase to half. Presentation of a homograph and an equation for determinig the pK values. Biochem. Biophys. Res. Comm. 131, 1075–1079

    Google Scholar 

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Authors and Affiliations

  1. Astrofüüsika ja Atmosfäärifüüsika Instituut, Eesti Teaduste Akadeemia, Toravere Observatoorium, 202444, Tartu, Eesti

    Agu Laisk, Ulvi Gerst, Hillar Eichelmann, Vello Oja & Ulrich Heber

  2. Julius-von-Sachs-Institut für Biowissenschaften der Universität Würzburg, Lehrstuhl Botanik I, Mittlerer Dallenbergweg 64, W-8700, Würzburg, Germany

    Katharina Siebke

Authors
  1. Agu Laisk
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  2. Katharina Siebke
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  3. Ulvi Gerst
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  4. Hillar Eichelmann
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  5. Vello Oja
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  6. Ulrich Heber
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Additional information

This work received support from the Estonian Academy of Sciences, the Bavarian Ministry of Science and Art and the Sonderforschungsbereich 251 of the University of Würzburg. We are grateful for criticism by D.A. Walker, Robert Hill Institute, University of Sheffield, U.K. and by Mark Stitt, Institute of Botany, University of Heidelberg, FRG.

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Laisk, A., Siebke, K., Gerst, U. et al. Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. Planta 185, 554–562 (1991). https://doi.org/10.1007/BF00202966

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  • DOI: https://doi.org/10.1007/BF00202966

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