Abstract
The relationship between the gas-exchange characteristics of attached leaves of Amaranthus edulis L. and the contents of photosynthetic intermediates was examined in response to changing irradiance and intercellular partial pressure of CO2. After determination of the rate of CO2 assimilation at known intercellular CO2 pressure and irradiance, the leaf was freeze-clamped and the contents of ribulose-1,5-bisphosphate, glycerate-3-phosphate, fructose-1,6-bisphosphate, glucose-6-phosphate, fructose-6-phosphate, triose phosphates, phosphoenolpyruvate, pyruvate, oxaloacetate, aspartate, alanine, malate and glutamate were measured. A comparison between the sizes of metabolite pools and theoretical calculations of metabolite gradients required for transport between the mesophyll and the bundle-sheath cells showed that aspartate, alanine, glycerate-3-phosphate and triose phosphates were present in sufficient quantities to support transport by diffusion, whereas pyruvate and oxaloacetate were not likely to contribute appreciably to the flux of carbon between the two cell types. The amounts of ribulose-1,5-bisphosphate were high at low intercellular partial pressures of CO2, and fell rapidly as the CO2-assimilation rate increased with increasing intercellular partial pressures of CO2, indicating that bundle-sheath CO2 concentrations fell at low intercellular partial pressures of CO2. In contrast, the amount of phosphoenolpyruvate and of C4-cycle intermediates declined at low intercellular partial pressures of CO2. This behaviour is discussed in relation to the co-ordination of carbon assimilation between the Calvin and C4 cycles.
Similar content being viewed by others
Abbreviations
- PEP:
-
phosphoenolpyruvate
- PGA:
-
glycerate-3-phosphate
- p i :
-
intercellular CO2 pressure
- RuBP:
-
ribulose-1,5-bisphosphate
- triose-P:
-
triose phosphates
References
Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24, 1–15
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
Berry, J.A., Farquhar, G.D. (1978) The CO2 concentrating function of C4 photosynthesis. A biochemical model. In: Proceedings 4th International Congress on Photosynthesis, pp. 119–131, Hall, D.O., Coombs, J., Goodwin, T.W., eds. Biochemical Society, London
Burnell, J.N., Hatch, M.D. (1985) Light-dark regulation of leaf pyruvate, Pi dikinase. Trends. Biochem. Sci. 10, 288–291
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
Doncaster, H.D., Leegood, R.C. (1987) Regulation of phosphoenolpyruvate carboxylase activity in maize leaves. Plant Physiol. 84, 82–87
Furbank, R.T., Leegood, R.C. (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Interaction between the C3 and C4 pathways during photosynthetic induction. Planta 162, 457–462
Furbank, R.T., Hatch, M.D. (1987) Mechanism of C4 photosynthesis. The size and composition of the inorganic carbon pool in bundle-sheath cells. Plant Physiol. 85, 958–964
Hanson, C.P., Cleland, W.W. (1964) Kinetic studies of glutamic oxaloacetic transaminase isozymes. Biochemistry 3, 338–345
Hatch, M.D., Mau, S. (1973) Activity, location and role of aspartate aminotransferase and alanine aminotransferase isoenzymes in leaves with C4 pathway photosynthesis. Arch. Biochem. Biophys. 156, 195–206
Hatch, M.D., Osmond, C.B. (1976) Compartmentation and transport in C4 photosynthesis. In: Encyclopedia of Plant Physiology, N.S. vol. 3: pp. 114–184, Stocking, C.R., Heber, U. eds. Springer, Berlin, Heidelberg, New York
Hatch, M.D. (1979) Mechanism of C4 photosynthesis in Chloris gayana: Pool sizes and kinetics of 14CO2 incorporation into 4-carbon and 3-carbon intermediates. Arch. Biochem. Biophys. 194, 117–127
Hewitt, E.J., Smith, T.A. (1975) Plant mineral nutrition. English University Press, London
Kagawa, T., Hatch, M.D. (1975) Mitochondria as a site of C4 acid decarboxylation in C4 pathway photosynthesis. Arch. Biochem. Biophys. 167, 687–696
Leegood, R.C. (1985) The intercellular compartmentation of metabolites in leaves of Zea mays. Planta 164, 163–171
Leegood, R.C., Furbank, R.T. (1984) Carbon metabolism and gas exchange in leaves of Zea mays L. Changes in CO2 fixation, chlorophyll a fluorescence and metabolite levels during photosynthetic induction. Planta 162, 450–456
Lowe, J., Slack, C.R. (1971) Inhibition of maize leaf phosphopyruvate carboxylase by oxaloacetate. Biochim. Biophys. Acta 235, 207–209
Lowry, O.H., Passonneau, J.V. (1972) A flexible system of enzymatic analysis. Academic Press, New York
Ohnishi, J., Kanai, R. (1987) Pyruvate uptake by mesophyll and bundle sheath chloroplasts of a C4 plant, Panicum miliaceum L. Plant Cell Physiol. 28, 1–10
O'Leary, M. (1982) Phosphoenolpyruvate carboxylase: An enzymologist's view. Annu. Rev. Plant Physiol. 33, 297–315
Raven, J.A. (1977) Ribulose bisphosphate carboxylase activity in terrestrial plants: Significance of O2 and CO2 diffusion. Curr. Adv. Plant Sci. 9, 579–590
Seeman, J.R., Badger, M.R., Berry, J.A. (1984) Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiol. 74, 791–794
Servaites, J.C., Parry, M.A.J., Gutteridge, S., Keys, A.J. (1986) Species variation in the predawn inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol. 82, 1161–1163
Slack, C.R., Hatch, M.D., Goodchild, D.J. (1969) Distribution of enzymes in mesophyll and parenchyma-sheath chloroplasts of maize leaves in relation to the C4-dicarboxylic acid pathway of photosynthesis. Biochem. J. 114, 489–498
Smith, F.A., Raven, J.A. (1979) Intracellular pH and its regulation. Annu. Rev. Plant Physiol. 30, 289–311
Stitt, M., Heldt, H.W. (1985a) Control of photosynthetic sucrose synthesis by fructose-2,6-bisphosphate. Intercellular metabolite distribution and properties of the cytosolic fructose bisphosphatase in leaves of Zea mays L. Planta 164, 179–188
Stitt, M., Heldt, H.W. (1985b) Generation and maintenance of concentration gradients between the mesophyll and bundle-sheath in maize leaves. Biochim. Biophys. Acta 808, 400–414
Usuda, H. (1985) The activation state of ribulose-1,5-bisphosphate carboxylase in maize leaves in dark and light. Plant Cell Physiol. 26, 1455–1463
Usuda, H. (1987) Photosynthetic carbon assimilation in C4 maize leaves. Adv. Photosynth. Res. 3, 507–514
von Caemmerer, S., Edmonson, D.L. (1986) The relation between steady-state gas exchange, in vivo ribulose bisphosphate carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Aust. J. Plant Physiol. 13, 669–688
Vu, J.C.V., Allen, L.H., Bowes, G. (1984) Dark/light modulation and ribulose bisphosphate carboxylase activity in plants from different photosynthetic categories. Plant Physiol. 76, 843–845
Williamson, D.H., Lund, P., Krebs, H.A. (1967) The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 103, 514–527
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Leegood, R.C., von Caemmerer, S. The relationship between contents of photosynthetic metabolites and the rate of photosynthetic carbon assimilation in leaves of Amaranthus edulis L.. Planta 174, 253–262 (1988). https://doi.org/10.1007/BF00394779
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00394779