8 Control of Phosphoenolpyruvate Carboxylase in Plants
Annual Plant Reviews book series, Volume 22: Control of Primary Metabolism Plants
Hugh G. Nimmo,
Hugh G. Nimmo
Division of Biochemistry & Molecular Biology, Institute of Biomedical & Life Sciences, University of Glasgow, Glasgow, G12 8QQ UK
Search for more papers by this authorHugh G. Nimmo,
Hugh G. Nimmo
Division of Biochemistry & Molecular Biology, Institute of Biomedical & Life Sciences, University of Glasgow, Glasgow, G12 8QQ UK
Search for more papers by this authorFirst published: 19 April 2018
This article was originally published in 2006 in Control of Primary Metabolism Plants, Volume 22 (ISBN 9781405130967) of the Annual Plant Reviews book series, this volume edited by William C. Plaxton and Michael T. Mcmanus. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
The sections in this article are
- Introduction
- PPCK Genes and Their Roles
- Signalling Pathways that Control PPCK Expression in CAM and C4 Plants
- The ‘Bacterial-Type’ PEPC
- Conclusions
- Acknowledgements
References
- 1 C.S. Andreo, D.H. Gonzales and A.A. Iglesias (1987) Vascular plant phosphoenolpyruvate carboxylase. Structure and regulation. FEBS Letters 213, 1–8.
- 2 R. Chollet, J. Vidal and M.H. O'Leary (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Reviews of Plant Physiology and Plant Molecular Biology 47, 273–296.
- 3 K. Izui, H. Matsumura, T. Furumoto and Y. Kai (2004) Phosphoenolpyruvate carboxylase: a new era of structural biology. Annual Reviews of Plant Biology 55, 69–84.
- 4 Y. Kai, H. Matsumura, T. Inoue et al. (1999) Three-dimensional structure of phosphoenolpyruvate carboxylase: a proposed mechanism for allosteric inhibition. Proceedings of the National Academy of Sciences of the United States of America 96, 823–828.
- 5 H. Matsumura, M. Terada, S. Shirakata et al. (1999) Plausible phosphoenolpyruvate binding site revealed by 2.6 A structure of Mn2+-bound phosphoenolpyruvate carboxylase from Escherichia coli . FEBS Letters 458, 1–4.
- 6 H. Matsumura, Y. Xie, S. Shirakata et al. (2002) Crystal structures of C4 form maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10, 1721–1730.
- 7 R.D. Law and W.C. Plaxton (1995) Purification and characterization of a novel phosphoenolpyruvate carboxylase from banana fruit. Biochemical Journal 307, 807–816.
- 8 S. Golombek, U. Heim, C. Horstmann, U. Wobus and H. Weber (1999) Phosphoenolpyruvate carboxylase in developing seeds of Vicia faba L.: gene expression and metabolic regulation. Planta 208, 66–72.
- 9 T.F. Moraes and W.C. Plaxton (2000) Purification and characterization of phosphoenolpyruvate carboxylase from Brassica napus (rapeseed) suspension cell cultures. Implications for phosphoenolpyruvate carboxylase regulation during phosphate starvation, and the integration of glycolysis with nitrogen assimilation. European Journal of Biochemistry 267, 4465–4476.
- 10 J.D. Blonde and W.C. Plaxton (2003) Structural and kinetic properties of high and low molecular mass phosphoenolpyruvate carboxylase isoforms from the endosperm of developing castor oilseeds. Journal of Biological Chemistry 278, 11867–11873.
- 11 H.G. Nimmo (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Sciences 5, 75–80.
- 12 H.G. Nimmo (2003) Control of the phosphorylation of phosphoenolpyruvate carboxylase in vascular plants. Archives of Biochemistry and Biophysics 414, 189–196.
- 13 N. Bakrim, J.L. Prioul, E. Dellens et al. (1993) Regulatory phosphorylation of C4 phosphoenolpyruvate carboxylase. Plant Physiology 101, 891–897.
- 14 P.J. Carter, H.G. Nimmo, C.A. Fewson and M.B. Wilkins (1990) Bryophyllum fedtschenkoi protein phosphatase type 2A can dephosphorylate phosphoenolpyruvate carboxylase. FEBS Letters 263, 233–236.
- 15 L. Dong, N.V. Ermolova and R. Chollet (2001) Partial purification and biochemical characterization of a heteromeric protein phosphatase 2A holoenzyme from maize (Zea mays L.) leaves that dephosphorylates C4 phosphoenolpyruvate carboxylase. Planta 213, 379–389.
- 16 H. Saze, Y. Ueno, T. Hisabori, H. Hayashi and K. Izui (2001) Thioredoxin-mediated reductive activation of a protein kinase for the regulatory phosphorylation of C4-form phosphoenolpyruvate carboxylase from maize. Plant and Cell Physiology 42, 1295–1302.
- 17 J. Hartwell, A. Gill, G.A. Nimmo, M.B. Wilkins, G.I. Jenkins and H.G. Nimmo (1999) Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant Journal 20, 333–342.
- 18 T. Taybi, S. Patil, R. Chollet and J.C. Cushman (2000) A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in Crassulacean acid metabolism-induced leaves of the common ice plant. Plant Physiology 123, 1471–1481.
- 19 Y. Tsuchida, T. Furumoto, A. Izumida, S. Hata and K. Izui (2001) Phosphoenolpyruvate carboxylase kinase involved in C4 photosynthesis in Flaveria trinervia: cDNA cloning and characterization. FEBS Letters 507, 318–322.
- 20 G.A. Nimmo, M.B. Wilkins and H.G. Nimmo (2001) Partial purification and characterization of a protein inhibitor of phosphoenolpyruvate carboxylase kinase. Planta 213, 250–257.
- 21 Y.H. Wang and R. Chollet (1993) Partial purification and characterization of phosphoenolpyruvate carboxylase protein-serine kinase from illuminated maize leaves. Archives of Biochemistry and Biophysics 304, 496–502.
- 22 V. Fontaine, J. Hartwell, G.I. Jenkins and H.G. Nimmo (2002) Arabidopsis thaliana contains two phosphoenolpyruvate carboxylase kinase genes with different expression patterns. Plant Cell and Environment 25, 115–122.
- 23 S. Sullivan, G.I. Jenkins and H.G. Nimmo (2004) Roots, cycles and leaves. Expression of the phosphoenolpyruvate carboxylase kinase gene family in soybean. Plant Physiology 135, 2078–2087.
- 24 W. Xu, Y. Zhou and R. Chollet (2003) Identification and expression of a soybean nodule-enhanced PEP-carboxylase kinase gene (NE-PpcK) that shows striking up-/down-regulation in vivo . Plant Journal 34, 441–452.
- 25 N.V. Ermolova, M.A. Cushman, T. Taybi, S.A. Condon, J.C. Cushman and R. Chollet (2003) Expression, purification, and initial characterization of a recombinant form of plant PEP-carboxylase kinase from CAM-induced Mesembryanthemum crystallinum with enhanced solubility in Escherichia coli . Protein Expression and Purification 29, 123–131.
- 26 M.B. Wilkins (1992) Circadian rhythms – their origin and control. New Phytologist 121, 347–375.
- 27 G.A. Nimmo, H.G. Nimmo, C.A. Fewson and M.B. Wilkins (1987) Persistent circadian rhythms in the phosphorylation state of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi leaves and in its sensitivity to inhibition by malate. Planta 170, 408–415.
- 28 P.J. Carter, H.G. Nimmo, C.A. Fewson and M.B. Wilkins (1991) Circadian rhythms in the activity of a plant protein kinase. EMBO Journal 10, 2063–2068.
- 29 T.L. Hennessey and C.B. Field (1987) Environmental effects of circadian rhythms in photosynthesis and stomatal opening. Planta 189, 369–376.
- 30 A.N. Dodd, K. Parkinson and A.A.R. Webb (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytologist 162, 63–70.
- 31 J.T. Marsh, S. Sullivan, J. Hartwell and H.G. Nimmo (2003) Structure and expression of phosphoenolpyruvate carboxylase kinase genes in Solanaceae. A novel gene exhibits alternative splicing. Plant Physiology 133, 2021–2028.
- 32 G.A. Nimmo, G.A.L. McNaughton, C.A. Fewson, M.B. Wilkins and H.G. Nimmo (1987) Changes in the kinetic properties and phosphorylation state of phosphoenolpyruvate carboxylase in Zea mays leaves in response to light and dark. FEBS Letters 213, 18–22.
- 33 N. Giglioli-Guivarc'h, J-N. Pierre, S. Brown, R. Chollet, J. Vidal and P. Gadal (1996) The light-dependent transduction pathway controlling the regulatory phosphorylation of C4 phosphoenolpyruvate carboxylase in protoplasts from Digitaria sanguinalis . Plant Cell 8, 573–586.
- 34 S. Coursol, N. Giglioli-Guivarc'h, J. Vidal and J-N. Pierre (2000) An increase in phosphoinositide-specific phospholipase C activity precedes induction of C4 phosphoenolpyruvate carboxylase phosphorylation in illuminated and NH4Cl-treated protoplasts from Digitaria sanguinalis . Plant Journal 23, 497–506.
- 35 E.M. Hrabak, C.W.M. Chan, M. Gribskov et al. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology 132, 666–680.
- 36 L. Osuna, S. Coursol, J.N. Pierre and J. Vidal (2004) A Ca2+-dependent protein kinase with characteristics of protein kinase C in leaves and mesophyll cell protoplasts from Digitaria sanguinalis: possible involvement in the C4-phosphoenolpyruvate carboxylase phosphorylation cascade. Biochemical and Biophysical Research Communications 314, 428–433.
- 37 Y. Ueno, E. Imanari, J. Emura et al. (2000) Immunological analysis of the phosphorylation state of maize C4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide. Plant Journal 21, 17–26.
- 38 C. Echevarria, S. Garcia-Mauriño, R. Alvarez, A. Soler and J. Vidal (2001) Salt stress increases the Ca2+-independent phosphoenolpyruvate carboxylase kinase activity in Sorghum leaves. Planta 214, 283–287.
- 39 S. Garcia-Mauriño, J.A. Monreal, R. Alvarez, J. Vidal and C. Echeverria (2003) Characterization of salt stress-enhanced phosphoenolpyruvate carboxylase kinase activity in leaves of Sorghum vulgare: independence from osmotic stress, involvement of ion toxicity and significance of dark phosphorylation. Planta 216, 648–655.
- 40 U. Lüttge (2000) The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211, 761–769.
- 41 K. Winter and J.D. Tenhunen (1982) Light-stimuated burst of carbon dioxide uptake following nocturnal acidification in the Crassulacean acid metabolism plant Kalanchoë daigremontiana . Plant Physiology 70, 1718–1722.
- 42 A. Fischer and M. Kluge (1984) Studies on carbon flow in Crassulacean acid metabolism during the initial light period. Planta 160, 121–128.
- 43 A.M. Borland and H. Griffiths (1997) A comparative study on the regulation of C3 and C4 carboxylation processes in the constitutive crassulacean acid metabolism (CAM) plant Kalanchoë daigremontiana and the C3-CAM intermediate Clusia minor. Planta, 201, 368–378.
- 44 A.M. Borland, J. Hartwell, G.I. Jenkins, M.B. Wilkins and H.G. Nimmo (1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in Crassulacean acid metabolism. Plant Physiology 121, 889–896.
- 45 C.R. McClung (2001) Circadian rhythms in plants. Annual Reviews of Plant Physiology and Plant Molecular Biology 52, 139–162.
- 46 M.E. Eriksson and A.J. Millar (2003) The circadian clock. A plant's best friend in a spinning world. Plant Physiology 132, 732–738.
- 47 J. Hartwell, G.A. Nimmo, M.B. Wilkins, G.I. Jenkins and H.G. Nimmo (2002) Probing the circadian control of phosphoenolpyruvate carboxylase kinase expression in Kalanchoë fedtschenkoi . Functional Plant Biology 29, 663–668.
- 48 T. Taybi, H.G. Nimmo and A.M. Borland (2004) Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic capacity and phenotypic plasticity in the expression of Crassulacean acid metabolism. Plant Physiology 135, 587–598.
- 49 B. Blasius, R. Neff, F. Beck and U. Lüttge (1999) Oscillatory model of Crassulacean acid metabolism with a dynamic hysteresis switch. Philosophical Transactions of the Royal Society of London, Series B 266, 93–101.
- 50 T.P. Wyka, A. Bohn, H.M. Duarte, F. Kaiser and U.E. Lüttge (2004) Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalanchoë daigremontiana: testing the tonoplast-as-oscillator model. Planta 219, 705–713.
- 51 S.F. Boxall, J.M. Foster, H.J. Bohnert, J.C. Cushman, H.G. Nimmo and J. Hartwell (2005) Conservation and divergence of circadian clock operation in a stress-inducible crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiology 137, 969–982.
- 52 A.N. Dodd, H. Griffiths, T. Taybi, J.C. Cushman and A.M. Borland (2003) Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum . Planta 216, 789–797.
- 53 J. Hartwell (2005) The circadian clock in CAM plants. In: Annual Plant Reviews: Endogenous plant rhythms (eds A. Hall and H.G. McWatters), pp. 211–236. Blackwell Publishing, Oxford, UK.
- 54 N. Bakrim, J. Brulfert, J. Vidal and R. Chollet (2001) Phosphoenolpyruvate carboxylase kinase is controlled by a similar signalling cascade in CAM and C4 plants. Biochemical and Biophysical Research Communications 286, 1158–1162.
- 55 H.G. Nimmo, V. Fontaine, J. Hartwell, G.I. Jenkins, G.A. Nimmo and M.B. Wilkins (2001) PEP carboxylase kinase is a novel protein kinase controlled at the level of expression. New Phytologist 151, 91–97.
- 56 K.M. Paterson and H.G. Nimmo (2000) Effects of pH on the induction of phosphoenolpyruvate carboxylase kinase in Kalanchoe fedtschenkoi . Plant Science 154, 135–141.
- 57 A.A.R. Webb (2003) The physiology of circadian rhythms in plants. New Phytologist 160, 281–303.
- 58 M. Agetsuma, T. Furumoto, S. Yanagisawa and K. Izui (2005) The ubiquitin-proteasome pathway is involved in rapid degradation of phosphoenolpyruvate carboxylase kinase for C4 photosynthesis. Plant and Cell Physiology 46, 389–398.
- 59 R. Sanchez and F.J. Cejudo (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiology 132, 949–957.
- 60 T.G. Mamedov, E.R. Moellering and R. Chollet (2005) Identification and expression analysis of two inorganic C- and N-responsive genes encoding novel and distinct molecular forms of eukaryotic phosphoenolpyruvate carboxylase in the green microalga Chlamydomonas reinhardtii . Plant Journal 42, 832–843.
- 61 J. Rivoal, S. Trzos, D.A. Gage, W.C. Plaxton and D.H. Turpin (2001) Two unrelated phosphoenolpyruvate carboxylase polypeptides physically interact in the high molecular mass isoforms of this enzyme in the unicellular green alga Selenastrum minutum . Journal of Biological Chemistry 276, 12588–12597.
- 62 J. Rivoal, W.C. Plaxton and D.H. Turpin (1998) Purification and characterization of high- and low-molecular-mass isoforms of phosphoenolpyruvate carboxylase from Chlamydomonas reinhardtii . Biochemical Journal 331, 201–209.
- 63 K.A. Schuller, W.C. Plaxton and D.H. Turpin (1990) Regulation of phosphoenolpyruvate carboxylase from the green alga Selenastrum minutum . Plant Physiology 93, 1301–1311.
- 64 G.C. Vanlerberghe, K.A. Schuller, R.G. Smith, R.Feil, W.C. Plaxton and D.H. Turpin (1990) Relationship between NH4 + assimilation rate and in vivo phosphoenolpyruvate carboxylase activity. Plant Physiology 94, 284–290.
- 65 J. Rivoal, D.H. Turpin and W.C. Plaxton (2002) In vitro phosphorylation of phosphoenolpyruvate carboxylase from the green alga Selenastrum minutum . Plant and Cell Physiology 43, 785–792.
- 66 M.S.B. Ku, S. Agarie, M. Nomura et al. (1999) High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nature Biotechnology 17, 76–80.
- 67 M. Jeanneau, J. Vidal, A. Gousset-Dupont et al. (2002) Manipulating PEPC levels in plants. Journal of Experimental Botany 53, 1837–1845.
- 68 L.M. Chen, K.Z. Li, T. Miwa and K. Izui (2004) Over-expression of a cyanobacterial phosphoenolpyruvate carboxylase with diminished sensitivity to feedback inhibition in Arabidopsis changes amino acid metabolism. Planta 219, 440–449.
- 69 H. Rolletschek, L. Borisjuk, R. Radchuk et al. (2004) Seed-specific expression of a bacterial phosphoenolpyruvate carboxylase in Vicia narbonensis increases protein content and improves carbon economy. Plant Biotechnology Journal 2, 214–219.
Browse other articles of this reference work:
