Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1996 Jun;111(2):497–505. doi: 10.1104/pp.111.2.497

Phosphoenolpyruvate Carboxylase Kinase in Tobacco Leaves Is Activated by Light in a Similar but Not Identical Way as in Maize.

B Li 1, X Q Zhang 1, R Chollet 1
PMCID: PMC157860  PMID: 12226305

Abstract

We have previously reported the partial purification of a Ca2+- independent phosphoenolpyruvate carboxylase (PEPC) protein-serine/threonine kinase (PEPC-PK) from illuminated leaves of N-sufficient tobacco (Nicotiana tabacum L.) plants (Y.-H. Wang, R. Chollet [1993] FEBS Lett 328: 215-218). We now report that this C3 PEPC-kinase is reversibly light activated in vivo in a time-dependent manner. As the kinase becomes light activated, the activity and L-malate sensitivity of its target protein increases and decreases, respectively. The light activation of tobacco PEPC-PK is prevented by pretreatment of detached leaves with various photosynthesis and cytosolic protein-synthesis inhibitors. Similarly, specific inhibitors of glutamine synthetase block the light activation of tobacco leaf PEPC-kinase under both photorespiratory and nonphotorespiratory conditions. This striking effect is partially and specifically reversed by exogenous glutamine, whereas it has no apparent effect on the light activation of the maize (Zea mays L.) leaf kinase. Using an in situ "activity-gel" phosphorylation assay, we have identified two major Ca2+-independent PEPC-kinase catalytic polypeptides in illuminated tobacco leaves that have the same molecular masses (approximately 30 and 37 kD) as found in illuminated maize leaves. Collectively, these results indicate that the phosphorylation of PEPC in N-sufficient leaves of tobacco (C3) and maize (C4) is regulated through similar but not identical light-signal transduction pathways.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bakrim N., Echevarria C., Cretin C., Arrio-Dupont M., Pierre J. N., Vidal J., Chollet R., Gadal P. Regulatory phosphorylation of Sorghum leaf phosphoenolpyruvate carboxylase. Identification of the protein-serine kinase and some elements of the signal-transduction cascade. Eur J Biochem. 1992 Mar 1;204(2):821–830. doi: 10.1111/j.1432-1033.1992.tb16701.x. [DOI] [PubMed] [Google Scholar]
  2. Bakrim N., Prioul J. L., Deleens E., Rocher J. P., Arrio-Dupont M., Vidal J., Gadal P., Chollet R. Regulatory Phosphorylation of C4 Phosphoenolpyruvate Carboxylase (A Cardinal Event Influencing the Photosynthesis Rate in Sorghum and Maize). Plant Physiol. 1993 Mar;101(3):891–897. doi: 10.1104/pp.101.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  4. Duff SMG., Chollet R. In Vivo Regulation of Wheat-Leaf Phosphoenolpyruvate Carboxylase by Reversible Phosphorylation. Plant Physiol. 1995 Mar;107(3):775–782. doi: 10.1104/pp.107.3.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Echevarria C., Pacquit V., Bakrim N., Osuna L., Delgado B., Arrio-Dupont M., Vidal J. The effect of pH on the covalent and metabolic control of C4 phosphoenolpyruvate carboxylase from Sorghum leaf. Arch Biochem Biophys. 1994 Dec;315(2):425–430. doi: 10.1006/abbi.1994.1520. [DOI] [PubMed] [Google Scholar]
  6. Echevarría C., Vidal J., Jiao J. A., Chollet R. Reversible light activation of the phosphoenolpyruvate carboxylase protein-serine kinase in maize leaves. FEBS Lett. 1990 Nov 26;275(1-2):25–28. doi: 10.1016/0014-5793(90)81430-v. [DOI] [PubMed] [Google Scholar]
  7. Giglioli-Guivarc'h N., Pierre J. N., Brown S., Chollet R., Vidal J., Gadal P. The Light-Dependent Transduction Pathway Controlling the Regulatory Phosphorylation of C4 Phosphoenolpyruvate Carboxylase in Protoplasts from Digitaria sanguinalis. Plant Cell. 1996 Apr;8(4):573–586. doi: 10.1105/tpc.8.4.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jiao J. A., Chollet R. Light activation of maize phosphoenolpyruvate carboxylase protein-serine kinase activity is inhibited by mesophyll and bundle sheath-directed photosynthesis inhibitors. Plant Physiol. 1992 Jan;98(1):152–156. doi: 10.1104/pp.98.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jiao J. A., Chollet R. Light/dark regulation of maize leaf phosphoenolpyruvate carboxylase by in vivo phosphorylation. Arch Biochem Biophys. 1988 Mar;261(2):409–417. doi: 10.1016/0003-9861(88)90357-8. [DOI] [PubMed] [Google Scholar]
  10. Jiao J. A., Chollet R. Posttranslational regulation of phosphoenolpyruvate carboxylase in c(4) and crassulacean Acid metabolism plants. Plant Physiol. 1991 Apr;95(4):981–985. doi: 10.1104/pp.95.4.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jiao J. A., Vidal J., Echevarría C., Chollet R. In vivo regulatory phosphorylation site in c(4)-leaf phosphoenolpyruvate carboxylase from maize and sorghum. Plant Physiol. 1991 May;96(1):297–301. doi: 10.1104/pp.96.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jiao J., Echevarría C., Vidal J., Chollet R. Protein turnover as a component in the light/dark regulation of phosphoenolpyruvate carboxylase protein-serine kinase activity in C4 plants. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2712–2715. doi: 10.1073/pnas.88.7.2712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Le Van Quy, Foyer C., Champigny M. L. Effect of Light and NO(3) on Wheat Leaf Phosphoenolpyruvate Carboxylase Activity: Evidence for Covalent Modulation of the C(3) Enzyme. Plant Physiol. 1991 Dec;97(4):1476–1482. doi: 10.1104/pp.97.4.1476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Li B., Chollet R. Resolution and identification of C4 phosphoenolpyruvate-carboxylase protein-kinase polypeptides and their reversible light activation in maize leaves. Arch Biochem Biophys. 1993 Dec;307(2):416–419. doi: 10.1006/abbi.1993.1609. [DOI] [PubMed] [Google Scholar]
  16. Li B., Chollet R. Salt induction and the partial purification/characterization of phosphoenolpyruvate carboxylase protein-serine kinase from an inducible crassulacean-acid-metabolism (CAM) plant, Mesembryanthemum crystallinum L. Arch Biochem Biophys. 1994 Oct;314(1):247–254. doi: 10.1006/abbi.1994.1437. [DOI] [PubMed] [Google Scholar]
  17. Martin F., Winspear M. J., Macfarlane J. D., Oaks A. Effect of Methionine Sulfoximine on the Accumulation of Ammonia in C(3) and C(4) Leaves : The Relationship between NH(3) Accumulation and Photorespiratory Activity. Plant Physiol. 1983 Jan;71(1):177–181. doi: 10.1104/pp.71.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pierre J. N., Pacquit V., Vidal J., Gadal P. 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. 1992 Dec 1;210(2):531–537. doi: 10.1111/j.1432-1033.1992.tb17451.x. [DOI] [PubMed] [Google Scholar]
  19. Sugiharto B., Suzuki I., Burnell J. N., Sugiyama T. Glutamine Induces the N-Dependent Accumulation of mRNAs Encoding Phosphoenolpyruvate Carboxylase and Carbonic Anhydrase in Detached Maize Leaf Tissue. Plant Physiol. 1992 Dec;100(4):2066–2070. doi: 10.1104/pp.100.4.2066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Vincentz M., Moureaux T., Leydecker M. T., Vaucheret H., Caboche M. Regulation of nitrate and nitrite reductase expression in Nicotiana plumbaginifolia leaves by nitrogen and carbon metabolites. Plant J. 1993 Feb;3(2):315–324. doi: 10.1111/j.1365-313x.1993.tb00183.x. [DOI] [PubMed] [Google Scholar]
  21. Wang Y. H., Chollet R. In vitro phosphorylation of purified tobacco-leaf phosphoenolpyruvate carboxylase. FEBS Lett. 1993 Aug 9;328(1-2):215–218. doi: 10.1016/0014-5793(93)80995-7. [DOI] [PubMed] [Google Scholar]
  22. Weiner H., McMichael R. W., Huber S. C. Identification of factors regulating the phosphorylation status of sucrose-phosphate synthase in vivo. Plant Physiol. 1992 Aug;99(4):1435–1442. doi: 10.1104/pp.99.4.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zhang X. Q., Li B., Chollet R. In Vivo Regulatory Phosphorylation of Soybean Nodule Phosphoenolpyruvate Carboxylase. Plant Physiol. 1995 Aug;108(4):1561–1568. doi: 10.1104/pp.108.4.1561. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES