Abstract
The rate and extent of light activation of PEPC may be used as another criterion to distinguish C3 and C4 plants. Light stimulated phosphoenolypyruvate carboxylase (PEPC) in leaf discs of C4 plants, the activity being three times greater than that in the dark but stimulation of PEPC was limited about 30% over the dark-control in C3 species. The light activation of PEPC in leaves of C3 plants was complete within 10 min, while maximum activation in C4 plants required illumination for more than 20 min, indicating that the relative pace of PEPC activation was slower in C4 plants than in C3 plants. Similarly, the dark-deactivation of the enzyme was also slower in leaves of C4 than in C3 species. The extent of PEPC stimulation in the alkaline pH range indicated that the dark-adapted form of the C4 enzyme is very sensitive to changes in pH. The pH of cytosol-enriched cell sap extracted from illuminated leaves of C4 plants was more alkaline than that of dark-adapted leaves. The extent of such light-dependent alkalization of cell sap was three times higher in C4 leaves than in C3 plants. The course of light-induced alkalization and dark-acidification of cytosol-enriched cell sap was markedly similar to the pattern of light activation and dark-deactivation of PEPC in Alternanthera pungens, a C4 plant. Our report provides preliminary evidence that the photoactivation of PEPC in C4 plants may be mediated at least partially by the modulation of cytosolic pH.
Similar content being viewed by others
Abbreviations
- CAM:
-
Crassulacean acid metabolism
- G-6-P:
-
glucose-6-phosphate
- PMSF:
-
phenylmethylsulfonyl fluoride
- PEPC:
-
phosphoenolpyruvate carboxylase
- PEPC-PK:
-
phosphoenolpyruvate ca carboxylase-protein kinase
References
Adams CA, Leung F and Sun SSM (1986) Molecular properties of phosphoenolpyruvate carboxylase from C3, C3-C4 intermediate, and C4 Flaveria species. Planta 167: 216–225
Andreo CS, Gonzalez DH and Iglesias AA (1987) Higher plant phosphoenolpyruvate carboxylase. Structure and regulation. FEBS Lett 213: 1–8
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1–15
Bauwe H and Chollet R (1986) Kinetic properties of phosphoenolpyruvate carboxylase from C3, C4 and C3-C4 intermediate species of Flaveria (Asteraceae). Plant Physiol 82: 695–699
Carter PJ, Nimmo HG, Fewson CA and Wilkins MB (1990) Bryophyllum fedtschenkoi protein phosphatase type 2A can dephopshorylate phosphoenolpyruvate carboxylase. FEBS Lett 263: 233–236
Chastin CJ and Chollet R (1989) Interspecific variation in assimilation of 14CO2 into C4 acids by leaves of C3, C4 and C3-C4 intermediate Flaveria species near the CO2 compensation concentration. Planta 179: 81–88
Davies DD (1979) The central role of phosphoenolpyruvate in plant metabolism. Annu Rev Plant Physiol 30: 131–158
Devi MT and Raghavendra AS (1992) Light activation of phosphoenolpyruvate carboxylase in maize mesophyll protoplasts. J Plant Physiol 138: 435–439
Devi MT and Raghavendra AS (1993) Partial reduction in activities of photorespiratory enzymes in C3-C4 intermediates of Alternanthera and Parthenium. J. Exp Bot 44: 779–784
Doncaster HD and Leegood RC (1987) Regulation of phosphoenolpyruvate carboxylase activity in maize leaves. Plant Physiol 84: 82–87
Echévarria C, Vidal J, Jiao JA and Chollet R (1990) Reversible light activation of phosphoenolpyruvate carboxylase protein-serine kinase in maize leaves. FEBS Lett 275: 25–28
Huber SC and Sugiyama T (1986) Changes in sensitivity to effectors of maize leaf phosphoenolpyruvate carboxylase during light/dark transitions. Plant Physiol 81: 674–677
Jiao JA and Chollet R (1988) Light/dark regulation of maize leaf phosphoenolpyruvate carboxylase by in vivo phosphorylation. Arch Biochem Biophys 261: 409–417
Jiao JA and Chollet R (1989) Regulatory seryl-phosphorylation of C4 phosphoenolpyruvate carboxylase by a soluble protein kinase from maize leaves. Arch Biochem Biophys 269: 526–535
Jiao JA and Chollet R (1990) Regulatory phosphorylation of serine-15 in maize phosphoenolpyruvate carboxylase by a C4-leaf protein-serine kinase. Arch Biochem Biophys 283: 300–305
Jiao JA and Chollet R (1991) Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and crassulacean acid metabolism plants. Plant Physiol 95: 981–985
Jiao JA and Chollet R (1992) Light activation of maize phosphoenolpyruvate carboxylase protein-serine kinase activity is inhibited by mesophyll and bundle sheathdirected photosynthesis inhibitors. Plant Physiol 98: 152–156
Jiao JA, Echèvarria C, Vidal J and Chollet R (1991) Protein turnover as a component in the light/dark regulation of phosphoenolpyruvate carboxylase protein-serine kinase activity in C4 plants. Proc Natl Acad Sci USA 88: 2712–2715
Karabourniotis G, Manetas Y and Gavalas NA (1983) Photoregulation of phosphoenolpyruvate carboxylase in Salsola soda and other C4 plants. Plant Physiol 73: 735–739
Karabourniotis G, Manetas Y and Gavalas NA (1985) Detecting photoactivation of phosphoenolpyruvate carboxylase in C4 plants. An effect of pH. Plant Physiol 77: 300–302
Latzko E and Kelly GJ (1983) The many faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiol Veg 21: 805–815
Maheswari V and Bharadwaj R (1991) Photoactivation and regulation of maize leaf phosphoenolpyruvate carboxylase. Indian J Exp Biol 29: 1058–1061
Nakamoto H, Ku MSB and Edwards GE (1983) Photosynthetic characteristics of C3-C4 intermediate Flaveria species. II. Kinetic properties of phosphoenolpyruvate carboxylase from C3, C4, and C3-C4 intermediate species. Plant Cell Physiol 24: 1387–1393
Nimmo GA, McNaughton GAL, Fewson CA, Wilkins MB and Nimmo HG (1987) Changes in the kinetic properties and phosphorylation state of phosphoenolpyruvate carboxylase in Zea mays leaves in response to light and dark. FEBS Lett 213: 18–22
O'Leary MH (1982) Phosphoenolpyruvate carboxylase: An enzymologist's view. Annu Rev Plant Physiol 33: 297–315
Pierre JN, Pacquit V, Vidal J and Gadal P (1992) Regulatory phosphorylation of phosphoenolpyruvate carboxylase in protoplasts from sorghum mesophyll cells and the role of pH and Ca2+ as possible components of the light-transduction pathway. Eur J Biochem 210: 531–538
Raghavendra AS, Yin Z-H and Heber U (1993) Light-dependent pH changes in leaves of C4 plants. II. pH response to CO2 and oxygen in comparison to the responses of C3 plants. Planta 189: 278–287
Ranjeva R and Boudet AM (1987) Phosphorylation of proteins in plants: Regulatory effects and potential involvement in stimulus/response coupling. Annu Rev Plant Physiol 38: 73–93
Schnabl H, Denecke M and Schulz M (1992) In vivo phosphorylation of stomatal phosphoenolpyruvate carboxylase from Vicia faba L. Bot Acta 105: 367–369
Van Quy L and Champigny ML (1992) NO3 − enhances the kinase activity for phosphorylation of phosphoenolpyruvate carboxylase and sucrose phosphate synthase proteins in wheat leaves. Plant physiol 99: 344–347
Van Quy L, Lamaze T and Champigny ML (1991) Effect of light and NO3 − on wheat leaf phosphoenolpyruvate carboxylase activity. Evidence for covalent modulation of the C3 enzyme. Plant Physiol 97: 1476–1482
Willmer CM, Petropoulou Y and Manetas Y (1990) No light activation and high malate sensitivity of phosphoenolpyruvate carboxylase in guard cell protoplasts of Commelina communis L. J Exp Bot 41: 1103–1107
Wu M-X, Meyer CR, Willeford KO and Wedding RT (1990) Regulation of the aggregation state of maize phosphoenolpyruvate carboxylase: Evidence from dynamic light-scattering measurements. Arch Biochem Biphys 281: 324–329
Yin Z-H, Neimanis S, Wagner U and 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
Yin Z-H, Heber U and Raghavendra AS (1993) Light-dependent pH changes in leaves of C4 plants. I. Cytosolic alkalization and vacuolar acidification in comparison to C3 plants. Planta 189: 267–277
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rajagopalan, A.V., Devi, M.T. & Raghavendra, A.S. Patterns of phosphoenolpyruvate carboxylase activity and cytosolic pH during light activation and dark deactivation in C3 and C4 plants. Photosynth Res 38, 51–60 (1993). https://doi.org/10.1007/BF00015061
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00015061