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Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light

Estimates from gas-exchange measurements on spinach

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Abstract

Responses of the rate of net CO2 assimilation (A) to the intercellular partial pressure of CO2 (p i ) were measured on intact spinach (Spinacia oleracea L.) leaves at different irradiances. These responses were analysed to find the value of p i at which the rate of photosynthetic CO2 uptake equalled that of photorespiratory CO2 evolution. At this CO2 partial pressure (denoted Г), net rate of CO2 assimilation was negative, indicating that there was non-photorespiratory CO2 evolution in the light. Hence Г was lower than the CO2 compensation point, Γ. Estimates of Г were obtained at leaf temperatures from 15 to 30°C, and the CO2/O2 specificity of ribulose 1,5-bisphosphate (RuBP) carboxylase/oxygenase (E.C. 4.1.1.39) was calculated from these data, taking into account changes in CO2 and O2 solubilities with temperature. The CO2/O2 specificity decreased with increasing temperature. Therefore we concluded that temperature effects on the ratio of photorespiration to photosynthesis were not solely the consequence of differential effects of temperature on the solubilities of CO2 and O2. Our estimates of the CO2/O2 specificity of RuBP carboxylase/oxygenase are compared with in-vitro measurements by other authors. The rate of nonphotorespiratory CO2 evolution in the light (R d ) was obtained from the value of A at Г. At this low CO2 partial pressure, R d was always less than the rate of CO2 evolution in darkness and appeared to decrease with increasing irradiance. The decline was most marked up to about 100 μmol quanta m-2 s-1 and less marked at higher irradiances. At one particular irradiance, however, R d as a proportion of the rate of CO2 evolution in darkness was similar in different leaves and this proportion was unaffected by leaf temperature or by [O2] (ambient and greater). After conditions of high [CO2] and high irradiance for several hours, the rate of CO2 evolution in darkness increased and R d also increased.

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Abbreviations

A:

rate of net CO2-assimilation

Γ:

CO2 compensation point

Г:

CO2 compensation point in the absence of R d

p i :

intercellular partial pressure of CO2

R d (“day respiration”):

rate of non-photorespiratory CO2 evolution in the light

R n (“night respiration”):

rate of CO2 evolution in darkness

RuBP:

ribulose-1,5-bisphosphate

Rubisco:

RuBP carboxylase/oxygenase

References

  • Azcón-Bieto, J., Osmond, C.B. (1983) Relationship between photosynthesis and respiration. The effect of carbohydrate status on the rate of CO2 production by respiration in darkened and illuminated wheat leaves. Plant Physiol. 71, 574–581

    Google Scholar 

  • Azcón-Bieto, J., Farquhar, G.D., Caballero, A. (1981) Effects of temperature, oxygen concentration, leaf age and seasonal variations on the CO2 compensation point of Lolium perenne L. Comparison with a mathematical model including nonphotorespiratory CO2 production in the light. Planta 152, 497–504

    Google Scholar 

  • Badger, M.R., Andrews, T.J. (1974) Effects of CO2, O2 and temperature on a high-affinity form of ribulose diphosphate carboxylase/oxygenase from spinach. Biochim. Biophys. Res. Commun. 60, 204–210

    Google Scholar 

  • Badger, M.R., Lorimer, G.H. (1981) Interaction of sugar phosphates with the catalytic site of ribulose-1,5-bisphosphate carboxylase. Biochemistry 20, 2219–2225

    Google Scholar 

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

    Google Scholar 

  • Björkman, O., Nobs, M.A., Hiesey, W.M. (1970a) Growth, photosynthetic and biochemical responses of contrasting Mimulus clones to light intensity and temperature. Carnegie Inst. Washington Yearb. 68, 614–619

    Google Scholar 

  • Björkman, O., Gauhl, E., Nobs, M.A. (1970b) Comparative studies of Atriplex species with and without β-carboxylation photosynthesis and their first-generation hybrid. Carnegie Inst. Washington Yearb. 68, 620–633

    Google Scholar 

  • Collatz, G.J. (1977) Influence of certain environmental factors on photosynthesis and photorespiration in Simmondsia chinensis. Planta 134, 127–132

    Google Scholar 

  • Collatz, G.J. (1978) The interaction between photosynthesis and ribulose-P2 concentration—effects of light, CO2, and O2. Carnegie Inst. Washington Yearb. 77, 248–251

    Google Scholar 

  • Cséke, C., Nishizawa, A.N., Buchanan, B.B. (1982) Modulation of chloroplast phosphofructokinase by NADPH. A mechanism for linking light to the regulation of glycolysis. Plant Physiol. 70, 658–661

    Google Scholar 

  • Day, D.A., Neuburger, M., Douce, R. (1985) Interactions between glycine decarboxylase, the tricarboxylic acid cycle and the respiratory chain in pea leaf mitochondria. Aust. J. Plant Physiol. 12, in press.

  • Dennis, D.T., Miernyk, J.A. (1982) Compartmentation of nonphotosynthetic carbohydrate metabolism. Annu. Rev. Plant Physiol. 33, 27–50

    Google Scholar 

  • Farquhar, G.D. (1979) Models describing the kinetics of ribulose bisphosphate carboxylase-oxygenase. Arch. Biochem. Biophys. 193, 456–468

    Google Scholar 

  • Farquhar, G.D., von Caemmerer, S. (1981) Modelling of photosynthetic response to environmental conditions. In: Encyclopedia of plant physiology, N.S., vol. 12: Physiological plant ecology, pt. B: Water relations and photosynthetic productivity, pp. 549–587, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer, Berlin Heidelberg New York

    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 

  • Graham, D. (1980) Effects of light and “dark” respiration. In: The biochemistry of plants. A comprehensive treatise, vol. 2: Metabolism and respiration, pp. 525–579, Davies, D.D., ed. Academic Press, New York London

    Google Scholar 

  • Hall, N.P., Keys, A.J. (1983) Temperature dependence of the enzymic carboxylation and oxygenation of ribulose 1,5-bisphosphate in relation to effects of temperature on photosynthesis. Plant Physiol. 72, 945–948

    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 

  • Hoagland, D.R., Arnon, D.I. (1938) The water-culture method for growing plants without soil. Univ. Cal. Agric. Exp. St. (Berkeley), Circ. No. 347, 1–39

    Google Scholar 

  • Hodgman, C.D., Weast, R.C., Selby, S.M. (1958) Handbook of chemistry and physics, edn. 40, pp. 1606–1607, Chemical Rubber Publishing Co., Cleveland, O., USA

    Google Scholar 

  • Jackson, W.A., Volk, R.J. (1970) Photorespiration. Annu. Rev. Plant Physiol. 21, 385–432

    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 

  • Jordan, D.B., Ogren, W.L. (1981a) A sensitive assay procedure for simultaneous determination of ribulose 1,5-bisphosphate carboxylase and oxygenase activities. Plant Physiol. 67, 237–245

    Google Scholar 

  • Jordan, D.B., Ogren, W.L. (1981b) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291, 513–515

    Google Scholar 

  • Jordan, D.B., Ogren, W.L. (1983) Species variation in kinetic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase. Arch. Biochem. Biophys. 227, 425–433

    Google Scholar 

  • Jordan, D.B., Ogren, W.L. (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161, 308–313

    Google Scholar 

  • Jordan, D.B., Chollet, R., Ogren, W.L. (1983) Binding of phosphorylated effectors by active and inactive forms of ribulose-1,5-bisphosphate carboxylase. Biochemistry 22, 3410–3418

    Google Scholar 

  • Keck, R.W., Ogren, W.L. (1976) Differential oxygen response of photosynthesis in soybean and Panicum milioides. Plant Physiol. 58, 552–555

    Google Scholar 

  • Kirschbaum, M.U.F., Farquhar, G.D. (1984) Temperature dependence of whole leaf photosynthesis in Eucalyptus pauciflora. Aust. J. Plant Physiol. 11, 519–538

    Google Scholar 

  • Ku, S.B., Edwards, G.E. (1977) Oxygen inhibition of photosynthesis. 1. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol. 59, 986–990

    Google Scholar 

  • Laing, W.A., Ogren, W.L., Hageman, R.H. (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose 1,5-diphosphate carboxylase. Plant Physiol. 54, 678–685

    Google Scholar 

  • Laisk, A.K. (1977) Kinetics of photosynthesis and photorespiration in C3-plants. [In Russ.] Nauka, Moscow

    Google Scholar 

  • Mächler, F., Nösberger, J. (1980) Regulation of ribulose bisphosphate carboxylase activity in intact wheat leaves by light, CO2, and temperature. J. Exp. Bot. 31, 1485–1491

    Google Scholar 

  • McCurry, S.D., Pierce, J., Tolbert, M.E., Orme-Johnson, W.H. (1981) On the mechanism of effector-mediated activation of ribulose bisphosphate carboxylase/oxygenase. J. Biol. Chem. 256, 6623–6628

    Google Scholar 

  • Miflin, B.J., Lea, P.J. (1977) Amino acid metabolism. Annu. Rev. Plant Physiol. 28, 299–329

    Google Scholar 

  • Mott, K.A., Jensen, R.G., O'Leary, J.W., Berry, J.A. (1984) Photosynthesis and ribulose 1,5-bisphosphate concentrations in intact leaves of Xanthium strumarium. Plant Physiol. 76, 968–971

    Google Scholar 

  • Peisker, M., Apel, P. (1980) Dark respiration and the effect of oxygen on CO2 compensation concentration in wheat leaves. Z. Planzenphysiol. 100, 389–395

    Google Scholar 

  • Peisker, M., Apel, P. (1981) Influence of oxygen on photosynthesis and photorespiration in leaves of Triticum aestivum L. 4. Oxygen dependence of apparent quantum yield of CO2 uptake. Photosynthetica 15, 435–441

    Google Scholar 

  • Peisker, M., Tichá, I., Čatský, J. (1981) Ontogenetic changes in the internal limitations to bean-leaf photosynthesis. 7. Interpretation of the linear correlation between CO2 compensation concentration and CO2 evolution in darkness. Photosynthetica 15, 161–168

    Google Scholar 

  • Perchorowicz, J.T., Jensen, R.G. (1983) Photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Regulation by CO2 and O2. Plant Physiol. 71, 955–960

    Google Scholar 

  • Perchorowicz, J.T., Raynes, D.A., Jensen, R.G. (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc. Nat. Acad. Sci. USA 78, 2985–2989

    Google Scholar 

  • Rasulov, B.K., Laisk, A.K., Asrorov, K.A. (1984) Photosynthesis and photorespiration during ontogenesis of severa species of cotton. Sov. Plant Physiol. 30, 486–493

    Google Scholar 

  • Sharp, R.E., Matthews, M.A., Boyer, J.S. (1984) Kok effect and the quantum yield of photosynthesis: light partially inhibits dark respiration. Plant Physiol. 75, 95–101

    Google Scholar 

  • Sicher, R.C., Jensen, R.G. (1979) Photosynthesis and ribulose 1,5-bisphosphate levels in intact chloroplasts. Plant Physiol. 64, 880–883

    Google Scholar 

  • Solomos, T. (1977) Cyanide-resistant respiration in higher plants. Annu. Rev. Plant Physiol. 28, 279–297

    Google Scholar 

  • Stumpf, P.K. (1980) Biosynthesis of saturated and unsaturated fatty acids. In: The biochemistry of plants. A comprehensive treatise. vol. 4: Lipids: structure and function, pp. 177–204, Stumpf, P.K., ed. Academic Press, New York

    Google Scholar 

  • Taylor, S.E., Terry, N. (1984) Limiting factors in photosynthesis. V. Photochemical energy supply colimits photosynthesis at low values of intercellular CO2 concentration. Plant Physiol. 75, 82–86

    Google Scholar 

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

    Google Scholar 

  • Wong, S.C. (1979) Elevated atmospheric partial pressure of CO2 and plant growth. I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 44, 68–74

    Google Scholar 

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

    Google Scholar 

  • Woodrow, I.E., Furbank, R.T., Brooks, A., Murphy, D.J. (1985) The requirements for a steady state in the reductive pentose phosphate pathway of photosynthesis. Biochim. Biophys. Acta, in press.

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Brooks, A., Farquhar, G.D. Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406 (1985). https://doi.org/10.1007/BF00392238

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