Skip to main content
Log in

Patterns of phosphoenolpyruvate carboxylase activity and cytosolic pH during light activation and dark deactivation in C3 and C4 plants

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

    Google Scholar 

  • Andreo CS, Gonzalez DH and Iglesias AA (1987) Higher plant phosphoenolpyruvate carboxylase. Structure and regulation. FEBS Lett 213: 1–8

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Davies DD (1979) The central role of phosphoenolpyruvate in plant metabolism. Annu Rev Plant Physiol 30: 131–158

    Google Scholar 

  • Devi MT and Raghavendra AS (1992) Light activation of phosphoenolpyruvate carboxylase in maize mesophyll protoplasts. J Plant Physiol 138: 435–439

    Google Scholar 

  • 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

    Google Scholar 

  • Doncaster HD and Leegood RC (1987) Regulation of phosphoenolpyruvate carboxylase activity in maize leaves. Plant Physiol 84: 82–87

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Jiao JA and Chollet R (1988) Light/dark regulation of maize leaf phosphoenolpyruvate carboxylase by in vivo phosphorylation. Arch Biochem Biophys 261: 409–417

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Jiao JA and Chollet R (1991) Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and crassulacean acid metabolism plants. Plant Physiol 95: 981–985

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Karabourniotis G, Manetas Y and Gavalas NA (1983) Photoregulation of phosphoenolpyruvate carboxylase in Salsola soda and other C4 plants. Plant Physiol 73: 735–739

    Google Scholar 

  • 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

    Google Scholar 

  • Latzko E and Kelly GJ (1983) The many faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiol Veg 21: 805–815

    Google Scholar 

  • Maheswari V and Bharadwaj R (1991) Photoactivation and regulation of maize leaf phosphoenolpyruvate carboxylase. Indian J Exp Biol 29: 1058–1061

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • O'Leary MH (1982) Phosphoenolpyruvate carboxylase: An enzymologist's view. Annu Rev Plant Physiol 33: 297–315

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Schnabl H, Denecke M and Schulz M (1992) In vivo phosphorylation of stomatal phosphoenolpyruvate carboxylase from Vicia faba L. Bot Acta 105: 367–369

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00015061

Key words

Navigation