Abstract
At bicarbonate concentrations equivalent to air levels of CO2, activation of ribulosebisphosphate carboxylase/oxygenase (rubisco) was inhibited by micromolar concentrations of glyoxylate in intact, lysed, and reconstituted chloroplasts and in stromal extracts. The concentration of glyoxylate required for 50% inhibition of light activation in intact chloroplasts was estimated to be 35 micromolar. No direct inhibition by glyoxylate was observed with purified rubisco or rubisco activase at micromolar concentrations. Levels of ribulose 1,5-bisphosphate and ATP increased in intact chloroplasts following glyoxylate treatment. Results from experiments with well-buffered lysed and reconstituted chloroplast systems ruled out lowering of pH as the cause of inhibition. With intact chloroplasts, micromolar glyoxylate did not prevent activation of rubisco at high (10 mM) concentrations of bicarbonate, indicating that rubisco could be spontaneously activated in the presence of glyoxylate. These results suggest the existence of a component of the in vivo rubisco activation system that is not yet identified and which is inhibited by glyoxylate.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- PEP:
-
phosphoenolpyruvate
- PGA:
-
3-phosphoglycerate
- rubisco:
-
ribulosebisphosphate carboxylase/oxygenase
- RuBP:
-
ribulose 1,5-bisphosphate
References
Arnon DI (1949) Copper enzymes in intact chloroplasts. Polyphenoxidase in Beta vulgaris. Plant Physiol 24: 1–15
Bahr JT and Jensen RG (1978) Activation of ribulose bisphosphate carboxylase in intact chloroplasts by CO2 and light. Arch Biochem Biophys 185: 39–48
Brooks A, PortisJr AR and Sharkey TD (1988) Effects of irradiance and methyl viologen treatments on ATP, ADP, and activation of ribulose bisphosphate carboxylase in spinach leaves. Plant Physiol 88: 850–853
Chastain CJ and Ogren WL (1985) Photorespiration-induced reduction of ribulose bisphophate carboxylase activation level. Plant Physiol 77: 851–856
Chastain CJ and Ogren WL (1989) Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation state in vivo. Plant Cell Physiol (in press)
Cook CM, Mulligan RM and Tolbert NE (1985) Inhibition and stimulation ribulose-1,5-bisphosphate carboxylase/oxygenase by glyoxylate. Arch Biochem Biophys 240: 392–401
Enser U and Heber U (1980) Metabolic regulation by pH gradients. Inhibition of photosynthesis by indirect proton transfer across the chloroplast envelope. Biochim Biophys Acta 592: 577–591
Flügge UI, Freisl M and Heldt HW (1980) The mechanism of the control of carbon fixation by the pH in the chloroplast stroma. Planta 149: 48–51
Jordan DB and Ogren WL (1981) A sensitive assay procedure for simultaneous determination of ribulose 1,5-bisphosphate carboxylase and oxygenase activities. Plant Physiol 67: 237–245
Kleczkowski LA, Randall DD and Blevins DG (1986) Purification and characterization of a novel NADPH(NADH)-dependent glyoxylate reductase from spinach leaves. Comparison of immunological properties of leaf glyoxylate reductase and hydroxypyruvate reductase. Biochem J 239: 653–659
Lawyer AL, Cornwell KL, Gee SL and Bassham JA (1983) Glyoxylate and glutamate effects on photosynthetic carbon metabolism in isolated chloroplasts and mesophyll cells of spinach. Plant Physiol 72: 420–425
Lilley RMcC, Fitzgerald MP, Rients KG and Walker DA (1975) Criteria of intactness and the photosynthetic activity of spinach chloroplast preparations. New Phytol 75: 1–10
Lorimer GH, Badger MR and Andrews TJ (1976) The activation of ribulose 1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria kinetics, a suggested mechanism and physiological implications. Biochemistry 15: 529–536
Mächler F and Nösberger J (1980) Regulation of ribulose bisphosphate carboxylase activity in intact wheat leaves by light, CO2, and temperature. J Exp Bot 31: 1485–1491
Mulligan RM, Wilson B and Tolbert NE (1983) Effects of glyoxylate on photosynthesis by intact chloroplasts. Plant Physiol 72: 415–419
Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Ann Rev Plant Physiol 35: 415–442
Oliver DJ (1980) The effect of glyoxylate on photosynthesis and photorespiration by isolated soybean mesophyll cells. Plant Physiol 65: 888–892
Oliver DJ and Zelitch I (1977) Increasing photosynthesis by inhibiting photorespiration with glyoxylate. Science 196: 1450–1451
Perchorowicz JT, Raynes DA and Jensen RG (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc Natl Acad Sci USA 78: 2985–2989
Portis ARJr, Salvucci ME and Ogren WL (1986) Activation of ribulosebisphosphate carboxylase/oxygenase at physiological CO2 and ribulosebisphosphate concentration by rubisco activase. Plant Physiol 82: 967–971
Purczeld P, Chon CJ, PortisJr AR, Heldt HW and Heber U (1978) The mechanism of the control of carbon fixation by the pH in the chloroplast stroma. Biochim Biophys Acta 501: 488–498
Robinson SP and PortisJr AR (1988) Involvement of stromal ATP in the light activation of ribulose-1,5-bisphosphatecar-boxylase/oxygenase in intact chloroplasts. Plant Physiol 86: 293–298
Robinson SP and PortisJr AR (1989) Adenosine triphosphate hydrolysis by purified rubisco activase. Arch Biochem Biophys 268: 93–99
Robinson SP, Streusand VJ, Chatfield JM and PortisJr AR (1988) Purification and assay of rubisco activase from leaves. Plant Physiol 88: 1008–1014
Salvucci ME, PortisJr AR and Ogren WL (1985) A soluble chloroplast protein catalyzes activation of ribulosebisphosphate carboxylase/oxygenase in vivo. Photosynth Res 7: 193–201
Salvucci ME, PortisJr AR and Ogren WL (1986a) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol 80: 655–659
Salvucci ME, PortisJr AR and Ogren WL (1986b) Purification of ribulose-1,5-bisphosphate carboxylase/oxygenase with high specific activity by fast protein liquid chromatography. Anal Biochem 153: 97–101
Somerville CR and Ogren WL (1981) Photorespiration-deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiol 67: 666–671
Streusand VJ and PortisJr AR (1987) Rubisco activase mediates ATP-dependent activation of ribulose bisphosphate carboxylase. Plant Physiol 85: 152–154
Winkler RG, Blevins DG, Polacco JC and Randall DD (1987) Ureide catabolism of soybeans. II. Pathway of catabolism in intact leaf tissue. Plant Physiol 83: 585–591
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Campbell, W.J., Ogren, W.L. Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynth Res 23, 257–268 (1990). https://doi.org/10.1007/BF00034856
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00034856