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Chapter 14 C4 Decarboxylases: Different Solutions for the Same Biochemical Problem, the Provision of CO2 to Rubisco in the Bundle Sheath Cells

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C4 Photosynthesis and Related CO2 Concentrating Mechanisms

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 32))

Summary

The decarboxylation of C4 acids in the bundle sheath cells (BSCs) is a key step in the C4 photosynthetic carbon assimilation pathway. Depending on the particular subtype of C4-species, this process can be mediated by different enzymes: NADP-malic enzyme (NADP-ME), NAD-malic enzyme (NAD-ME) and/or phosphoenolpyruvate carboxykinase (PEPCK), and each enzyme has a different subcellular compartmentalization within the BSCs. Thus, the C4 subtype cycle mediated by each decarboxylase displays distinguishing features in leaf anatomy, biochemistry and physiology. In some cases, the operation of more than one type of decarboxylating enzyme in the C4 photosynthetic process has been described. During the last few years, remarkable advances have been made in the characterization of different isoforms of each C4 decarboxylase. In most cases, non-photosynthetic isoforms of the C4-decarboxylating enzymes involved in primary and/or secondary metabolisms were characterized. These non-C4 isoforms were for sure the starting point for the evolution of the C4-specific decarboxylases through the gaining of characteristics that make them more suitable to fulfill the requirements of the photosynthetic process. For each decarboxylating enzyme, the analysis of phylogenetic relationships reveals several features of the molecular evolution of the C4 process which accomplished the same biochemical aim: the generation of CO2 in the vecinity of Rubisco in BSCs, reducing photorespiration and enhancing photosynthesis.

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Abbreviations

3-PGA:

3-Phosphoglycerate

BSC:

Bundle sheath cell

CAM:

Crassulacean acid metabolism

MC:

Mesophyll cell

NAD-ME:

NAD-malic enzyme

NADP-ME:

NADP-malic enzyme

OAA:

Oxaloacetate

PEP:

Phosphoenolpyruvate

PEPC:

Phosphoenolpyruvate carboxylase

PEPCK:

Phosphoenolpyruvate carboxykinase

PPDK:

Pyruvateorthophosphate dikinase

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

TCA:

Tricarboxylic acid cycle

References

  • Agostino A, Heldt HW and Hatch MD (1996) Mitochondrial respiration in relation to photosynthetic C4 acid decarboxylation in C4 species. Aust J Plant Physiol 23: 1–7

    Article  CAS  Google Scholar 

  • Aich S, Imabayashi F and Delbaere LTJ (2003) Crystallization and preliminary X-ray crystallographic studies of phosphoenolpyruvate carboxykinase form Corynebacterium glutamicum. Acta Cryst 59: 1640 –1641

    Google Scholar 

  • Artus NN and Edwards GE (1985) NAD-malic enzyme from plant. FEBS Lett 182: 225–233

    Article  CAS  Google Scholar 

  • Ashton AR (1997) NADP-malic enzyme from the C4 plant Flaveria bidentis: Nucleotide substrate specificity. Arch Biochem Biophys 345: 251–258

    Article  PubMed  CAS  Google Scholar 

  • Bahrami AR, Chen Z-H, Walker RP, Leegood RC and Gray JE (2001) Ripening-related occurrence of phosphoenolpyruvate carboxykinase in tomato fruit. Plant Mol Biol 47: 499–506

    Article  PubMed  CAS  Google Scholar 

  • Bailey KJ, Gray JE, Walker RP and Leegood RC (2007) Coordinate regulation of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxykinase by light and CO2 during C4 photosynthesis. Plant Physiol 144: 479–486

    Article  PubMed  CAS  Google Scholar 

  • Bakrim N, Echeverria C, Crétin C, Arrio-Dupont M, Pierre JN, Vidal J, Chollet R and Nadal P (1992) Regulatory phosphorylation of Sorghum leaf phosphoenolpyruvae carboxylase: identification of the protein-serine kinase and some elements of the signal transduction cascade. Eur J Biochem 204: 821–830

    Article  PubMed  CAS  Google Scholar 

  • Borland AM, Tecsi LI, Leegood RC and Walker RP (1998) Inducibility of Crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta 205: 342–351

    Article  CAS  Google Scholar 

  • Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt MM, Klein PE and Mullet JE (2005) Shorgum bicolor´s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58: 699–720

    Article  PubMed  CAS  Google Scholar 

  • Burnell JN (1986) Purification and properties of phosphoenolpyruvate carboxykinase from C4 plants. Aust J Plant Physiol 13: 577–587

    Article  CAS  Google Scholar 

  • Burnell JN (1987) Photosynthesis in Phosphoenolpyruvate carboxykinase-type C4 species: Properties of NAD-malic enzyme from Urochloa panicoides. Aust J Plant Physiol 14: 517–525

    Article  CAS  Google Scholar 

  • Burnell JN and Hatch MD (1988) Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: Pathways of C4 acid decarboxylation in bundle sheath cells of Urochloa panicoides. Arch Biochem Biophys 260: 187–199

    Article  PubMed  CAS  Google Scholar 

  • Cabello-Pasini A, Swift H, Smith GJ and Alberte RS (2001) Phosphoenolpyruvate carboxykinase from the marine diatom Skeletonema costatum and the paheophyte Laminaria setchellii.II. Immunological characterization and subcellular localization. Bot Mar 44: 199–207

    Article  CAS  Google Scholar 

  • Calsa T and Filgueira A (2007) Serial analysis of gene expression in sugarcane (Saccharum spp.) leaves revealed alternative C(4) metabolism and putative antisense transcripts. Plant Mol Biol 63: 745–762

    Article  PubMed  CAS  Google Scholar 

  • Cannata JJB and Stoppani AOM (1963) Phosphoenolpyruvate carboxylase from baker’s yeast: II Properties of the enzyme. J Biol Chem 238: 1208–1212

    PubMed  CAS  Google Scholar 

  • Cardemil E, Encinas MV and Jabalquinto AM (1990) Reactive sulfhydryl groups in Saccharomyces cerevisiae phosphoenolpyruvate carboxykinase. Biochim Biophys Acta 1040: 71–76

    Article  PubMed  CAS  Google Scholar 

  • Carter PJ, Nimmo HG, Fewson CA and Wilkins MB (1990) Bryophyllum fedtschenkoi protein phosphatase 2A can dephosphorylate phosphoenolpyruvate carboxylase. FEBS Lett 263: 233–236

    Article  CAS  Google Scholar 

  • Casati P, Andreo CS and Edwards GE (1999a) Characterization of NADP-malic enzyme from two species of Chenopodiaceae: Haloxylon persicum (C4) and Chenopodium album (C3). Phytochemistry 52: 985–992

    Article  CAS  Google Scholar 

  • Casati P, Drincovich MF, Edwards GE and Andreo CS (1999c) Malate metabolism by NADP-malic enzyme in plant defence. Photosynth Res 61: 99–105

    Article  CAS  Google Scholar 

  • Casati P, Fresco AG, Andreo CS and Drincovich MF (1999b) An intermediate form of NADP-malic enzyme from C3 C4 intermediate species Flaveria floridana. Plant Sci 147: 101–109

    Article  CAS  Google Scholar 

  • Casati P, Lara MV and Andreo CS (2000) Induction of a C4-Like mechanism of CO2 fixation in Egeria densa, a submersed aquatic species. Plant Physiol 123: 1611–1621

    Article  PubMed  CAS  Google Scholar 

  • Casati P, Spampinato C and Andreo CS (1997) Characteristics and physiological function of NADP+-malic enzyme from wheat. Plant Cell Physiol 38: 928–934

    Article  CAS  Google Scholar 

  • Chang HC and Lane MD (1966) The enzymatic carboxylation of phosphoenolpyruvate: II. Purification and properties of liver mitochondrial phosphoenolpyruvate carboxykinase. J Biol Chem 241: 2421–2430

    PubMed  CAS  Google Scholar 

  • Chang G-G and Tong L (2003) Structure and function of malic enzymes, a new class of oxidative decarboxylases. Biochemistry 42: 12721–12733

    Article  PubMed  CAS  Google Scholar 

  • Chen Z-H, Walker R, Técsi LI, Lea PJ and Leegood RC (2004) Phosphoenolpyruvate carboxykinase in cucumber plants is increased both by ammonium and by acidification, and is present in the phloem. Planta 219: 48–58

    Article  PubMed  CAS  Google Scholar 

  • Chen Z-H, Walker RP, Acheson RM and Leegood RC (2002) Phosphoenolpyruvate carboxykinase assayed at physiological concentrations of metal ions as a high affinity for CO2. Plant Physiol 128: 160–164

    Article  PubMed  CAS  Google Scholar 

  • Chen Z-H, Walker RP, Acheson RM, Técsi LI, Wingler A, Lea PJ and Leegood RC (2000) Are Isocitrate Lyase and Phosphoenolpyruvate Carboxykinase Involved in Gluconeogenesis during Senescence of Barley Leaves and Cucumber Cotyledons? Plant Cell Physiol 41: 960–967

    Article  PubMed  CAS  Google Scholar 

  • Chi W, Yang J, Wu N and Zhang F (2004) Four rice genes encoding NADP-malic enzyme exhibit distinct expression profiles. Biosci Biotechnol Biochem 68: 1865–1874

    Article  PubMed  CAS  Google Scholar 

  • Coleman DE, Jagannatha Rao GS, Goldsmith EJ, Cook PF and Harris BG (2002) Crystal structure of the malic enzyme from Ascaris suum complexed with nicotinamide adenine dinucleotide at 2.3 A resolution. Biochemistry 41: 6928–6938

    Article  PubMed  CAS  Google Scholar 

  • Colombo SL, Andreo CS and Podestá FE (1997) Carbon metabolism in germinating Ricinus communis cotyledons. Purification, characterization and developmental profile of NADP-dependent malic enzyme. Physiol Plant 101: 821–826

    Article  CAS  Google Scholar 

  • Cotelesage JJ, Prasad L, Zeikus JG, Laivenieks M and Delbaere LT (2005) Crystal structure of Anaerobiospirillum succiniciproducens PEP carboxykinase reveals an important active site loop. Int J Biochem Cell Biol 37: 1829–1837

    Article  PubMed  CAS  Google Scholar 

  • Cotelessage JJM, Puttick J, Goldie H, Rajabi B, Novkovski B and Delbaere LTJ (2007) How does an enzyme recognize CO2? Int J Biochem Cell Biol 39: 1204–1210

    Article  CAS  Google Scholar 

  • Croninger CM, Olswang Y, Reschef L, Kalhan SC, Tilghman SM and Hanson RW (2002) Phosphoenolpyruvate carboxykinase revisited: insights into its metabolic role. Biochem Mol Biol Educ 30: 14–20

    Article  Google Scholar 

  • Delgado Alvarado A, Walker RP and Leegood RC (2007) Phosphoenolpyruvate carboxykinase in developing pea seed is associated with tissues involve in solute transport and is nitrogen-responsive. Plant Cell Environ 30: 225–235

    Article  PubMed  CAS  Google Scholar 

  • Detarsio E, Gerrard Wheeler MC, Campos Bermúdez VA, Andreo CS and Drincovich MF (2003) Maize C4 NADP-malic enzyme. Expression in Escherichia coli and characterization of site-directed mutants at the putative nucleotide-binding sites. J Biol Chem 278: 13757–13764

    Article  PubMed  CAS  Google Scholar 

  • Detarsio E, Andreo CS and Drincovich MF (2004) Basic residues play key roles in catalysis and NADP-specificity in maize (Zea mays L.) photosynthetic NADP-dependent malic enzyme. Biochem J 382: 1025–1030

    Article  PubMed  CAS  Google Scholar 

  • Detarsio E, Alvarez C, Saigo M, Andreo, CS and Drincovich­ MF (2007) Identification of domains implicated in tetramerization and malate inhibition of maize C4 NADP-malic enzyme by analysis of chimerical proteins. J Biol Chem 282: 6053–6060

    Article  PubMed  CAS  Google Scholar 

  • Detarsio E, Maurino VG, Alvarez C, Muller G, Andreo CS and Drincovich MF (2008) Maize cytosolic NADP-malic enzyme (ZmCytNADP-ME): a phylogenetically distant isoform specifically expressed in embryo and emerging root. Plant Mol Biol 68: 355–367

    Google Scholar 

  • Dever LV, Pearson M, Ireland RJ, Leegood RC and Lea PJ (1998) The isolation and characterization of a mutant of the C4 plant Amaranthus edulis deficient in NAD-malic enzyme activity. Planta 206: 449–656

    Article  Google Scholar 

  • Dittrich P, Campbell WH and Black CC (1973) Phosphoenolpyruvate carboxykinase in plants exhibiting Crassulacean acid metabolism. Plant Physiol 52: 357–361

    Article  PubMed  CAS  Google Scholar 

  • Drincovich MF, Iglesias AA and Andreo CS (1991) Interaction of divalent metal ions with the NADP-malic enzyme from maize leaves. Physiol. Plantarum 81: 462–466

    Google Scholar 

  • Drincovich MF, Spampinato CP and Andreo CS (1992) Evidence for the existence of two essential and proximal cysteinyl residues in NADP-malic enzyme from maize leaves. Plant Physiol 100: 2035–2040

    Article  PubMed  CAS  Google Scholar 

  • Drincovich MF and Andreo CS (1994) Redox regulation of maize NADP-malic enzyme by thiol-disulfide interchange. Biochem Biopys Acta 1206: 10–16

    Article  CAS  Google Scholar 

  • Drincovich MF, Casati P, Andreo CS, Franceschi V, Edwards GE and Ku MSB (1998) Evolution of C4 photosynthesis in Flaveria species. Isoforms of NADP-malic enzyme. Plant Physiol 117: 733–744

    Article  PubMed  CAS  Google Scholar 

  • Drincovich MF, Casati P, Andreo CS (2001) NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett 490: 1–6

    Article  PubMed  CAS  Google Scholar 

  • Dunten P, Belunis C, Crowther R, Hollfelder K, Kammlott U, Levin W, Michel H, Ramsey GB, Sawain A, Weber D and Wertheimer SJ (2002) Crystal structure of human cytosolic phosphoenolpyruvate carboxykinase reveals a new GTP-binding site. J Mol Biol 316: 257–264

    Article  PubMed  CAS  Google Scholar 

  • Edwards GE, Kanai R and Black CC (1971) Phosphoenolpyruvate carboxykinase in leaves of certain plants which fix CO2 by the C4-dicarboxylic acid cycle of photosynthesis. Biochem Biophys Res Commun 45: 278–285

    Article  PubMed  CAS  Google Scholar 

  • Edwards GE and Andreo CS (1992) NADP-malic enzyme from plants. Phytochemistry 31: 1845–1857

    Article  PubMed  CAS  Google Scholar 

  • Edwards GE, Franceschi VR and Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55: 173–196

    Article  PubMed  CAS  Google Scholar 

  • Fahnenstich H, Saigo S, Niessen M, Zanor MI, Andreo CS, Fernie AR, Drincovich MF, Flügge U-I, and Maurino VG (2007) Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol 145: 640–652

    Article  PubMed  CAS  Google Scholar 

  • Falcone L, Andreo CS and Podestá FE (2003) Purification and physical and kinetic characterization of a photosynthetic NADP-dependent malic enzyme from the CAM plant Aptenia cordifolia. Plant Sci 164: 95–102

    Article  Google Scholar 

  • Famiani F, Walker RP, Técsi L, Chen ZH, Proietti P and Leegood RC (2000) An immunohistochemical study of the compartmentation of metabolism during the development of grape (Vitis vinifera L.) berries. J Exp Bot 51: 675–683

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP – phylogeny inference package (version 3.2). Cladistics 5: 164–166

    Google Scholar 

  • Finnegan PM and Burnell JN (1995) Isolation and sequence analysis of cDNAs encoding phosphoenolpyruvate carboxykinase from the PCK-type C4 grass Urochloa panicoides. Plant Mol Biol 27: 365–376

    Article  PubMed  CAS  Google Scholar 

  • Finnegan PM, Suzuki S, Ludwig M and Burnell JN (1999) Phosphoenolpyruvate carboxykinase in the C4 monocot Urochloa panicoides is encoded by four differentially expressed genes. Plant Physiol 120: 1033–1042

    Article  PubMed  CAS  Google Scholar 

  • Foster DO, Lardy HA, Ray PD and Johnston JB (1967) Alteration of rat liver phosphoenolpyruvate carboxykinase activity by l-tryptophan in vivo and metals in vivo. Biochemistry 6: 2120–2128

    Article  PubMed  CAS  Google Scholar 

  • Furbank RT, Jenkins CLD and Hatch MD (1990) C4 photosynthesis: Quantum requirement, C4 acid overcycling and Q-cycle involvement. Aust J Plant Physiol 17: 1–7

    Article  CAS  Google Scholar 

  • Furumoto T, Hata S and Izui K (1999) cDNA cloning and characterization of maize phosphoenolpyruvate carboxykinase, a bundle sheath cell-specific enzyme. Plant Mol Biol 41: 301–311

    Article  PubMed  CAS  Google Scholar 

  • Gerrard Wheeler MC, Tronconi MA, Drincovich MF, Andreo CS, Flügge U-I. and Maurino VG (2005) A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis thaliana. Plant Physiol 139: 39–51

    Article  CAS  Google Scholar 

  • Gerrard Wheeler MC, Arias L, Tronconi MA, Maurino VGM, Andreo CS and Drincovich MF (2008) Arabidopsis thaliana NADP-malic enzyme isoforms: high degree of identity but clearly distinct properties. Plant Mol Biol 67: 231–242

    Article  CAS  Google Scholar 

  • Girodano M, Beardall J and Raven JA (2005) CO2 concen­tration mechanisms in algae: mechanisms, ­environmental modulation, and evolution. Annu Rev Plant Biol 56: 99–131

    Article  CAS  Google Scholar 

  • Grover SD, Canellas PF and Wedding RT (1981). Purification of NAD-malic enzyme from potato and investigation of some physiological and kinetic properties. Arch Biochem Biophys 209: 396–407

    Article  PubMed  CAS  Google Scholar 

  • Grover SD and Wedding RT (1982) Kinetic ramifications of the association-dissociation behaviour of NAD-malic enzyme. Plant Physiol 70: 1169–1172

    Article  PubMed  CAS  Google Scholar 

  • Grover SD and Wedding RT (1984) Modulation of the activity of the NAD-malic enzyme from Solanum tuberosum by changes in oligomeric state. Arch Biochem Biophys 234: 418–425

    Article  PubMed  CAS  Google Scholar 

  • Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochem Biophys Acta 895: 81–106

    Article  CAS  Google Scholar 

  • Hatch MD and Mau SL (1977) Properties of Phosphoenolpyruvate carboxykinase operative in C4 pathway photosynthesis. Aust J Plant Physiol 4: 207–216

    Article  CAS  Google Scholar 

  • Hatch MD, Mau SL and Kagawa T (1974) Properties of leaf NAD-malic enzyme from plants with C4 pathway photosynthesis. Arch. Biochem. Biophys. 165: 188–200

    Article  CAS  Google Scholar 

  • Hibberd JM and Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415: 451–454

    Article  PubMed  CAS  Google Scholar 

  • Honda H, Akagi H and Shimada H (2000) An isozyme of the NADP-malic enzyme of a CAM plant, Aloe arborescens, with variation on conservative aminoacid residues. Gene 243: 85–92

    Article  PubMed  CAS  Google Scholar 

  • Hundal RS, Krassak M, Dufour S, Laurent D, Lebon V, Chandramouli V, Inzucchi SE, Schumann WC, Petersen KF, Landau BR, Shulman GI (2000) Mechanism by which metformin reduces glucose production in Type 2 diabetes. Diabetes 49: 2063–2069

    Article  PubMed  CAS  Google Scholar 

  • Iglesias AA and Andreo CS (1990) Kinetic and Structural Properties of NADP-Malic Enzyme from Sugarcane Leaves. Plant Physiol 92: 66–72

    Article  PubMed  CAS  Google Scholar 

  • Iglesias AA and Andreo CS (1989) Purification of NADP-malic enzyme and phosphoenolpyruvate carboxylase from sugar cane leaves. Plant Cell Physiol 30: 399–405

    CAS  Google Scholar 

  • Jenner HL, Winning BM, Millar H, Tomlinson KL, Leaver CJ and Hill SA (2001) NAD-Malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126: 1139–1149

    Article  PubMed  CAS  Google Scholar 

  • Kim D-J and Smith SM (1994) Molecular cloning of cucumber phosphoenolpyruvate carboxykinase and developmental regulation of gene expression. Plant Mol Biol 26: 423–434

    Article  PubMed  CAS  Google Scholar 

  • Ku MSB, Kano-Murakami YM and Matsuoka M (1996) Evolution and expression of C4 photosynthesis genes. Plant Physiol 111: 949–957

    Article  PubMed  CAS  Google Scholar 

  • Lai LB, Lin W and Nelson TM (2002a) Distinct but conserved functions for two chloroplastic NADP-malic isoforms in C3 and C4 Flaveria species. Plant Physiol 128: 125–139

    Article  PubMed  CAS  Google Scholar 

  • Lai LB, Tausta SL and Nelson TM (2002b) Differential regulation of transcripts encoding cytosolic NADP-malic enzymes in C3 and C4 Flaveria species. Plant Physiol 128: 140–149

    Article  PubMed  CAS  Google Scholar 

  • Lara MV, Casati P and Andreo CS (2002) CO2 concentration mechanisms in Egeria densa, a submersed aquatic species. Physiol Plant 115: 487–495

    Article  PubMed  CAS  Google Scholar 

  • Lara MV, Drincovich MF, Müller GL, Maurino VG and Andreo CS (2005) NADP-malic enzyme and Hsp70: co-purification of both proteins and modification of NADP-malic enzyme properties by association with Hsp70. Plant Cell Physiol 46: 997–1006

    Article  PubMed  CAS  Google Scholar 

  • Lea PJ, Chen Z-H, Leegood RC and Walker RP (2001) Does phosphoenolpyruvate carboxykinase have a role in both amino acid and carbohydrate metabolism? Amino Acids 20: 225–241

    Article  PubMed  CAS  Google Scholar 

  • Leduc YA, Prasad L, Zeikus JG, Laivenieks M and Delbaere LTJ (2005) Structure of PEP carboxykinase from the succinate-producing Actinobacillus succinogenes: a new conserved active-site motif. Acta Cryst 61: 903–912

    Google Scholar 

  • Leegood RC and ap Rees T (1978) Identification of the regulatory steps in gluconeogenesis in cotyledons of Cucurbita pepo. Biochim Biophys Acta 524: 207–218

    Google Scholar 

  • Leegood RC and Walker RP (2003) Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Biochem Biophys 414: 204–210

    Article  PubMed  CAS  Google Scholar 

  • Leegood RC, von Caemmerer S and Osmond CB (1996) Metabolite transport and photosynthetic regulation in C4 and CAM plants. In: Dennis DT, Turpin DH, Layzell DD and Lefebvre DK (eds) Plant Metabolism, pp 341–369. Longman, London

    Google Scholar 

  • Leegood RC, Walker RP (1999) Phosphoenolpyruvate carboxykinase in plants: its role and regulation. In: Bryant JA, Burrell MM and Kruger NJ (eds). Plant Carbohydrate Biochemistry, pp 201–213. BIOS Scientific Publishers, Oxford

    Google Scholar 

  • Lewis CT, Seyer JM, Cassell RG and Carlson GM (1993) Identification of vicinal thiols of phosphoenolpyruvate carboxykinase (GTP). J Biol Chem 268: 1628–1636

    PubMed  CAS  Google Scholar 

  • Liu S, Cheng Y, Zhang X, Guan Q, Nishiuchi S, Hase K and Takano T (2007) Expression of an NADP-malic enzyme gene in rice (Oryza sativa L.) is induced by environmental stresses; overexpression of the gene in Arabidopsis confers salt and osmotic stress tolerance. Plant Mol Biol 64: 49–58

    Article  PubMed  CAS  Google Scholar 

  • Long JL, Wang JL and Berry JO (1994) Cloning and analysis of the C4 NAD-dependent malic enzyme of amaranth mitochondria. J Biol Chem 269: 2827–2833

    PubMed  CAS  Google Scholar 

  • Long JL and Berry JO (1996) Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of Amaranth mitochondria. Plant Physiol 112: 473–482

    PubMed  CAS  Google Scholar 

  • Lopez Becerra E, Puigdomenech P and Stiefel V (1998) A gene coding for a malic enzyme expressed in embryo root epidermis from Zea mays. Plant Physiol 117: 332

    Google Scholar 

  • Magnin NC, Cooley BA, Reiskind JB and Bowes G (1997) Regulation and localization of key enzymes during the induction of kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiol 115: 1681–1689

    PubMed  CAS  Google Scholar 

  • Malone S, Chen Z-H, Bahrami A, Walker RP, Gray JE and Leegood RC (2007) Phosphoenolpyruvate carboxykinase in Arabidopsis: changes in gene expression, protein and activity during vegetative and reproductive development. Plant Cell Physiol 48: 441–450

    Article  PubMed  CAS  Google Scholar 

  • Marshall JS, Stubbs JD and Taylor WC (1996) Two genes encode highly similar chloroplastic NADP-Malic enzymes in Flaveria. Implication for the evolution of C4 photosynthesis. Plant Physiol 111: 1251–1261

    Article  PubMed  CAS  Google Scholar 

  • Marshall JS, Stubbs JD, Chitty JA, Surin B and Taylor WC (1997) Expression of the C4 Me1 gene from Flaveria bidentis requires an interaction between 5¢ and 3¢ sequences. Plant Cell 9: 1515–1525

    Google Scholar 

  • Martinoia E and Rentsch D (1994) Malate compartmentation-responses to a complex metabolism. Annu Rev Plant Physiol Plant Mol Biol 45: 447–467

    Article  CAS  Google Scholar 

  • Matte A, Goldie H, Sweet RM, Delbaere LTJ (1996) crystal structure of Escherichia coli phosphoenolpyruvate carboxykinase: A new structural family with the P-loop nucleoside tryphosphate hydrolase fold. J Mol Biol 256: 126–143

    Article  PubMed  CAS  Google Scholar 

  • Matte A, Tari LW, Goldie H and Delbaere LTJ (1997) Structure and mechanism of phosphoenolpyruvate carboxykinase. J Biol Chem 272: 8105–8108

    Article  PubMed  CAS  Google Scholar 

  • Maurino VG, Drincovich MF and Andreo CS (1996) NADP-Malic enzyme isoforms in maize leaves. Biochem Mol Biol Int 38: 239–250

    PubMed  CAS  Google Scholar 

  • Maurino VG, Drincovich MF, Casati P, Andreo CS, Ku MSB, Gupta SK, Edwards GE and Franceschi VR (1997) NADP-malic enzyme: Inmunolocalization in different tissues of the C4 plant maize and the C3 plant wheat. J Exp Bot 48: 799–811

    Article  CAS  Google Scholar 

  • Maurino VG, Saigo M, Andreo CS and Drincovich MF (2001) Non-photosynthetic malic enzyme from maize: a constitutively expressed enzyme that responds to plant defence inducers. Plant Mol Biol 45: 409–420

    Article  PubMed  CAS  Google Scholar 

  • Meister M, Agostino A and Hatch MD (1996) The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta 199: 262–269

    Article  CAS  Google Scholar 

  • Muhaidat R, Sage RF and Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94: 362–381

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Oshugi R, Matsuoka M and Nakamoto M (1989) Purification and characterization of NAD-ME from leaves of Eleusine coracana and Panicum dichotomiflorum. Plant Physiol 89: 316–324

    Article  PubMed  CAS  Google Scholar 

  • Nomura M, Higuchi T, Ishida Y, Ohta S, Komari T, Imaizumi N, Miyao-Tokutomi M, Matsuoka M and Tajima S (2005) Differential expression pattern of C4 bundle sheath expression genes in rice, a C3. Plant Cell Physiol. 46: 754–761

    Article  PubMed  CAS  Google Scholar 

  • Oshui R and Murata T (1980) Leaf anatomy, post-illumination CO2 burst and NAD-malic enzyme activity in Panicum dichotomiflorum. Plant Cell Physiol 21: 1329–1333

    Google Scholar 

  • Penfield S, Ryllot EL, Gilday AD, Graham S, Larson TR and Graham IA (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyls elongation in the dark, is independent of abscisic acid, and requires phosphoenolpyruvate carboxykinase1. Plant Cell 16: 2705–2718

    Article  PubMed  CAS  Google Scholar 

  • Ray TB and Black CC Jr (1976) Characterization of phosphoenolpyruvate carboxykinase from Panicum maximum. Plant Physiol 58: 603–607

    Article  PubMed  CAS  Google Scholar 

  • Reiskind JB and Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88: 2883–2887

    Article  PubMed  CAS  Google Scholar 

  • Roberts K, Granum E, Leegood RC and Raven JA (2007) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145: 230–235

    Article  PubMed  CAS  Google Scholar 

  • Rothermel BA and Nelson T (1989) Primary structure of the maize NADP-dependent malic enzyme. J Biol Chem 264: 19587–19592

    PubMed  CAS  Google Scholar 

  • Ryllot EL, Gilday AD and Graham IA (2003) The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment. Plant Physiol 131: 1834–1842

    Article  CAS  Google Scholar 

  • Saez-Vasquez J, Raynal M, Delseny M (1995) A rapeseed cold-inducible transcript encodes a phosphoenolpyruvate carboxykinase. Plant Physiol 109: 611–618

    Article  PubMed  CAS  Google Scholar 

  • Saigo M, Bologna FP, Maurino VG, Detarsio E, Andreo CS and Drincovich MF (2004) Maize recombinant non-C4 NADP-malic enzyme: A novel dimeric malic enzyme with high specific activity. Plant Mol Biol 55: 97–107

    Article  PubMed  CAS  Google Scholar 

  • Sheen J (1991) Molecular mechanisms underling the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3: 225–245

    PubMed  CAS  Google Scholar 

  • Suzuki S and Burnell JN (2003) The pck1 promoter from Urochloa panicoides (a C4 plant) directs expression differently in rice (a C3 plant) and maize (a C4 plant). Plant Sci 165: 603–611

    Article  CAS  Google Scholar 

  • Takeuchi Y, Akagi H, Kamasawa N, Osumi M and Honda H (2000) Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211: 265–274

    Article  PubMed  CAS  Google Scholar 

  • Taub DR and Lerdau MT (2000) Relationship between leaf nitrogen and photosynthetic rate for three NAD-ME and three NADP-ME grasses. Am J Bot 87: 412–417

    Article  PubMed  CAS  Google Scholar 

  • Tausta S-L, Coyle HM, Rothermel B, Stiefel V and Nelson T (2002) Maize C4 and non-C4 NADP-dependent malic enzymes are encoded by distinct genes derived from a plastid-localized ancestor. Plant Mol Biol 50: 635–652

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG and Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Trapani S, Linss J, Goldenberg S, Fischer H, Craievich AF and Oliva G (2001) Crystal structure of the dimeric phosphoenolpyruvate carboxykinase (PEPCK) from Trypanosoma cruzi at 2 A resolution. J Mol Biol 313: 1059–1072

    Article  PubMed  CAS  Google Scholar 

  • Trevanion SJ, Brooks AL and Leegood RC (1995) Control of gluconeogenesis by phosphoenolpyruvate carboxykinase in cotyledons of Cucurbita pepo L. Planta 196: 653–658

    Article  CAS  Google Scholar 

  • Tronconi MA, Fahnenstich H, Gerrard Weehler MC, Andreo CS, Flugge U-I, Drincovich MF, and Maurino VG (2008) Arabidopsis thaliana NAD-malic enzyme functions as a homo- and heterodimer and has a major impact on nocturnal metabolism. Plant Physiol 146: 1540–1552

    Article  PubMed  CAS  Google Scholar 

  • Tsuchida H, Tamai T, Fukayama H, Agarie S, Nomura M, Onodera H, Ono K, Nishizawa Y, Lee B-H., Hirose S, Toki S, Ku M, Matsuoka M and Miyao M (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol 452: 138–145

    Article  Google Scholar 

  • Ueno O, Yoshimura Y and Sentoku N (2005) Variation in activity of some enzymes of photorespiratory metabolism in C4 grasses. Ann Bot 96: 863–869

    Article  PubMed  CAS  Google Scholar 

  • Urbina JA and Avilan L (1989) The kinetic mechanism of phosphoenolpyruvate carboxykinase from Panicum maximum. Phytochemistry 28: 1349–1353

    Article  CAS  Google Scholar 

  • Utter MF and Kolenbrander HM (1972) Formation of oxaloacetate by CO2 fixation on phosphoenolpyruvate. In: Boyer PD (ed) The Enzymes, Vol 6 pp 136–153. Academic, New York

    Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Pyankov VI and Edwards GE (1999) Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae). J Exp Bot 50: 1779–1795

    CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Chuong SDX and Edwards GE (2006) Functional characterization of phosphoenolpyruvate carboxykinase-type C4 leaf anatomy: immuno-, cytochemical and ultrastructural analyses. Ann Bot 98: 77–91

    Article  PubMed  CAS  Google Scholar 

  • Walker RP and Chen Z-H (2002) Phosphoenolpyruvate carboxykinase: structure, function and regulation. Adv Bot Res 38: 93–189.

    Article  CAS  Google Scholar 

  • Walker RP and Leegood RC (1996) Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds. Biochem J 317: 653–658

    PubMed  CAS  Google Scholar 

  • Walker RP, Acheson RM, Tecsi LI and Leegood RC (1997) Phosphoenolpyruvate carboxykinase in C4 plants: its role and regulation. Aust J Plant Physiol 24: 459–468

    Article  CAS  Google Scholar 

  • Walker RP, Chen ZH, Tecsi LI, Famiani F and Lea PJ (1999) Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development. Planta 210: 9–18

    Article  PubMed  CAS  Google Scholar 

  • Walker RP, Chen ZH, Johnson KE, Famiani F, Tecsi L and Leegood RC (2001) Using immunohistochemistry to study plant metabolism: the examples of its use in the localization of amino acids in plant tissues, and of phosphoenolpyruvate carboxykinase and its possible role in pH regulation. J Exp Bot 52: 565–576

    Article  PubMed  CAS  Google Scholar 

  • Walker RP, Chen Z-H, Acheson RM and Leegood RC (2002) Effects of Phosphorylation on phosphoenolpyruvate carboxykinase from the C4 plant Guinea grass. Plant Physiol 128: 165–172

    Article  PubMed  CAS  Google Scholar 

  • Walker RP and Leegood RC (1995) Purification, and phosphorylation in vivo and in vitro, of phosphoenolpyruvate carboxykinase from cucumber cotyledons. FEBS Lett 362: 70–74

    Article  PubMed  CAS  Google Scholar 

  • Walker RP, Trevanion SJ and Leegood RC (1995).Phosphoenolpyruvate carboxykinase from higher plants: purification from cucumber and evidence of rapid proteolytic cleavage in extracts from a range of plant tissues. Planta 195: 58–63

    Google Scholar 

  • Wedding RT and Black MK (1983) Physical and kinetic properties and regulation of the NAD-malic enzyme purified from leaves of Crassula argentea. Plant Physiol 72: 1021–1028

    Article  PubMed  CAS  Google Scholar 

  • Wedding RT and Whatley FR (1984) Malate oxidation by Arum spadix mitochondria: Participation and characteristics of NAD-malic enzyme New Phytol 96: 505–517

    Article  CAS  Google Scholar 

  • Wedding RT (1989) Malic enzyme of higher plants. Plant Physiol 90: 367–371

    Article  PubMed  CAS  Google Scholar 

  • Willeford KO and Wedding RT (1987) Evidence for a multiple subunit composition of plant NAD-malic enzyme. J Biol Chem 262: 8423–8429

    PubMed  CAS  Google Scholar 

  • Wingler A, Walker RP, Chen Z and Leegood RC (1999) Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol 120: 539–545

    Article  PubMed  CAS  Google Scholar 

  • Winning BM, Bourguignon J and Leaver CJ (1994) Plant mitochondrial NAD-dependent Malic Enzyme. cDNA cloning, deduced primary structure of the 59–and 62–kDa subunit, import, gene complexity and expression analysis. J Biol Chem 269: 4780–4786

    PubMed  CAS  Google Scholar 

  • Xu Y, Bhargava G, Wu H, Loeber G and Tong L (1999) Crystal structure of human mitochondrial NAD(P).dependent malic enzyme: a new class of oxidative decarboxylases. Structure 7: 877–889

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Zhang H, Hung H-H, Kuo C-C, Tsai L-C, Yuan HS, Chou W-Y, Chang G-G and Tong L (2002) Structural studies of the pigeon liver cytosolic NADP-dependent malic enzyme. Protein Sci 11: 332–341

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The work of the authors is funded by grants from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and the Deutsche Forschungsgemeinschaft. MVL, MFD and CSA are members of the Researcher Career of CONICET.

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Drincovich, M.F., Lara, M.V., Andreo, C.S., Maurino, V.G. (2010). Chapter 14 C4 Decarboxylases: Different Solutions for the Same Biochemical Problem, the Provision of CO2 to Rubisco in the Bundle Sheath Cells. In: Raghavendra, A., Sage, R. (eds) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, vol 32. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9407-0_14

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