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Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate

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Abstract

The effect of phosphate feeding on the influence of low (2%) oxygen on photosynthetic carbon assimilation has been investigated in leaf discs of spinach (Spinacia oleracea L.) at 12°C. The following observations were made. First, after the transition from 20% O2 to 2% O2, the rate of CO2 uptake was inhibited at CO2 concentrations between about 250 and about 800 μl CO2·l-1. Second, phosphate feeding stimulated the rate of CO2 uptake in 20% O2 at higher concentrations of CO2 (500–900 μl·l-1). Third, phosphate feeding stimulated the rate of CO2 uptake in 2% O2 at all but the highest (900 μl·l-1) and lowest 74 (μl·l-1) concentrations of CO2 employed. Phosphate thereby restored the stimulation of photosynthesis by 2% O2 and it did so over a wide range of lower temperatures. Fourth, oscillatory behaviour, however generated, was dampened by phosphate feeding, even at very low concentrations of CO2. Contents of leaf metabolites were measured during the transition to 2% O2 in control and phosphate-fed leaf discs. During this period the ratio glycerate-3-phosphate/triose phosphate rose steeply, but fell again only in the phosphate-treated leaf discs. These data, taken together with measured ATP/ADP ratios, showed that assimilatory power, the ratio [ATP]·[NAD(P)H]/[ADP]·[Pi]·[NAD(P)], decreased when leaves were exposed to 2% O2, but that this decrease was minimised by previous feeding of phosphate. The mechanism of phosphate limitation is discussed in the light of the results.

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Abbreviations

Ci :

intercellular concentration of CO2

RuBP:

ribulose-1,5-bisphosphate

References

  • Arrabaca, M.C., Keys, A.J., Whittingham, C.P. (1981) Effect of temperature on photosynthetic and photorespiratory metabolism. In: Photosynthesis IV, pp. 463–470, Akoyunoglou, G., ed. Balaban Int. Sci. Services, Philadelphia, USA

    Google Scholar 

  • Badger, M.R., Sharkey, T.D., von Caemmerer, S. (1984) The relationship between steady-state gas exchange of leaves and the levels of carbon reduction cycle intermediates. Planta 160, 305–313

    Google Scholar 

  • Brooks, A. (in press) Phosphorus nutrition and photosynthesis of spinach leaves: effects on ribulose-1,5-bisphosphate carboxylase activation, quantum yield and contents of some Calvin cycle intermediates. Aust. J. Plant Physiol.

  • Canvin, D.T. (1978) Photorespiration and the effect of oxygen on photosynthesis. In: Photosynthetic carbon assimilation, pp. 61–76, Siegelman, H., Hind, G. eds. Plenum Press, New York London

    Google Scholar 

  • Carver, K.A., Hope, A.B., Walker, D.A. (1983) Adenine nucleotide status, phosphoglycerate reduction and photosynthetic phosphorylation in a reconstituted chloroplast sustem. Biochem. J. 210, 273–276

    Google Scholar 

  • Chen-She, S.-H., Lewis, D.H., Walker, D.A. (1975) Stimulation of photosynthetic starch formation by sequestration of cytoplasmic orthophosphate. New Phytol. 74, 383–392

    Google Scholar 

  • Cornic, G., Louason, G. (1980) The effects of O2 on net photosynthesis at low temperature (5°C). Plant Cell Environ. 3, 149–157

    Google Scholar 

  • Dietz, K.-J. (1985) A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis of leaves. Biochim. Biophys. Acta 839, 240–248

    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. (1986) Light and CO2 limitation of photosynthesis and states of the reactions regenerating ribulose-1,5-bisphosphate or reducing 3-phosphoglycerate. Biochim. Biophys. Acta 848, 392–401

    Google Scholar 

  • Dietz, K.-J., Foyer, C.H. (1986) The relationship between phosphate status and photosynthesis in leaves. Reversibility of the effects of phosphate deficiency on photosynthesis. Planta 167, 376–381

    Google Scholar 

  • Doehlert, D.C., Huber, S.C. (1983) Spinach leaf sucrose phosphate synthase. Activation by glucose-6-phosphate and interaction with inorganic phosphate. FEBS Lett. 153, 293–297

    Google Scholar 

  • Farquhar, G.D., von Caemmerer, S., Berry, J.A. (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90

    Google Scholar 

  • Furbank, R.T., Foyer, C.H. (in press) Oscillations in levels of metabolites from the photosynthetic carbon reduction cycle in spinach leaf discs generated by the transition from air to 5% CO2. Arch. Biochem. Biophys. 246

  • Harris, G.C., Cheesbrough, J.K., Walker, D.A. (1983) Effects of mannose on photosynthetic gas exchange in spinach leaf discs. Plant Physiol. 71, 108–111

    Google Scholar 

  • Heber, U., Takahama, U., Neimanis, S., Shimizu-Takahama, M. (1982) Transport as the basis of the Kok effect. Levels of some photosynthetic intermediates and activation of light-regulated enzymes during photosynthesis of chloroplasts and green leaf protoplasts. Biochim. Biophys. Acta 679,287–299

    Google Scholar 

  • Heldt, H.W., Chon, C.J., Maronde, D., Herold, A., Stankovic, Z.S., Walker, D.A., Kraminer, A., Kirk, R., Heber, U. (1977) Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol. 59, 1146–1155

    Google Scholar 

  • Jolliffe, P.A., Tregunna, E.B. (1968) Effect of temperature, CO2 concentration, and light intensity on oxygen inhibition of photosynthesis in wheat leaves. Plant Physiol. 43, 902–906

    Google Scholar 

  • Jolliffe, P.A., Tregunna, E.B. (1973) Environmental regulation of the oxygen effect on apparent photosynthesis in wheat. Can. J. Bot. 51, 841–853

    Google Scholar 

  • Jensen, R.G., Bahr, J.T. (1977) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu. Rev. Plant Physiol. 28, 379–400

    Google Scholar 

  • Leegood, R.C. (1985) Regulation of photosynthetic CO2-pathway enzymes by light and other factors. Photosynth. Res. 6, 247–259

    Google Scholar 

  • Leegood, R.C., Walker, D.A. (1983) The role of transmembrane solute flux in regulation of CO2 fixation in chloroplasts. Biochem. Soc. Trans. 11, 74–76

    Google Scholar 

  • Lowry, O., Passonneau, J.V. (1972) A flexible system of enzymatic analysis. Academic Press, New York London

    Google Scholar 

  • Mächler, F., Schnyder, H., Nösberger, J. (1984) Influence of inorganic phosphate on photosynthesis of wheat chloroplasts. I. Photosynthesis and assimilate export at 5° C and 25°C. J. Exp. Bot. 153, 481–487

    Google Scholar 

  • McVetty, P.B.E., Canvin, D.T. (1981) Inhibition of photosynthesis by low oxygen concentrations. Can. J. Bot. 59, 721–725

    Google Scholar 

  • Prinsley, R.T., Leegood, R.C. (1986) Factors affecting photosynthetic induction in spinach leaf discs. Biochim. Biophys. Acta (in press)

  • Portis, A.R. (1983) Analysis of the role of the phosphate translocator and external metabolites in steady-state chloroplast photosynthesis. Plant Physiol. 71, 936–943

    Google Scholar 

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

    Google Scholar 

  • Sanwal, G.G., Greenberg, E., Hardie, J., Cameron, E.C., Press, J. (1968) Regulation of starch biosynthesis in plant leaves Activation and inhibition of ADP-glucose pyrophosphorylase. Plant Physiol. 43, 417–427

    Google Scholar 

  • Schnyder, H., Mächler, F., Nösberger, J. (1984) Influence of temperature and O2 concentration on photosynthesis and light activation of ribulosebisphosphate carboxylase oxygenase in intact leaves of white clover (Trifolium repens J. Exp. Bot. 151, 147–156

    Google Scholar 

  • Sestak, Z., Catsky, J., Jarvis, P.G. (1971) In: Plant photosynthetic production: Manual of methods, pp. 316–342, W-Junk, The Hague

    Google Scholar 

  • Sharkey, T.D. (1985) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol. 78, 71–75

    Google Scholar 

  • Stitt, M., Heldt, H.W. (1985) Control of photosynthetic sucrose synthesis by fructose 2,6-bisphosphate. VI. Regulation of the cytosolic fructose 1,6-bisphosphatase in spinach leaves by an interaction between metabolic intermediates and fructose 2,6-bisphosphate. Plant Physiol. 79, 599–608

    Google Scholar 

  • Usuda, H., Edwards, G.E. (1982) Influence of varying CO2 and orthophosphate concentrations on rates of photosynthesis, and synthesis of glycolate and dihydroxyacetone phosphate by wheat chloroplasts. Plant Physiol. 69, 469–473

    Google Scholar 

  • Viil, J., Ivanova, H., Pärnik, T. (1985) Effects of O2 and irradiance on CO2 assimilation in Phaseolus vulgaris. Photosynthetica 19, 88–97

    Google Scholar 

  • Viil, J., Laisk, A., Oja, V., Pärnik, T. (1977) Enhancement of photosynthesis caused by oxygen under saturating inadiance and high CO2 concentrations. Photosynthetica 10 251–259

    Google Scholar 

  • Walker, D.A. (1976) Regulatory mechanisms in photosynthetic carbon metabolism. Curr. Top. Cell. Regul. 11, 203–241

    Google Scholar 

  • Walker D.A., Robinson, S.P. (1978) Chloroplast and cell. A contemporary view of photosynthetic carbon assimilatic. Ber. Deutsch. Bot. Ges. 91, 513–526

    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., Sivak, M.N. (1985) Can phosphate limit photosynthetic carbon assimilation in vivo?. Physiol. Vég. 23, 829–841

    Google Scholar 

  • Woo, K.C., Wong, S.C. (1983) Inhibition of CO2 assimilation by supraoptimal CO2: Effect of light and temperature. A J. Plant Physiol. 10, 75–85

    Google Scholar 

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Leegood, R.C., Furbank, R.T. Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 168, 84–93 (1986). https://doi.org/10.1007/BF00407013

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