Skip to main content
SpringerLink
Log in

Chapter 13 C4-Phosphoenolpyruvate Carboxylase

  • Chapter
  • First Online:
Book cover C4 Photosynthesis and Related CO2 Concentrating Mechanisms

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

Summary

Phosphoenolpyruvate carboxylase (PEPC, EC 4.1.1.31) is one of the enzymes indispensable for all variants of the C4 photosynthetic pathway. C4 photosynthesis evolved polyphyletically implying that the genes encoding the C4 PEPC originated several times independently from non-photosynthetic ancestral genes. During the evolution of C4 photosynthesis the photosynthetic PEPCs acquired distinct properties that distinguish them considerably from other PEPCs of higher plants. These changes include the modification of kinetic and regulatory properties of the enzyme as well as the high and cell-specific expression of C4 PEPC genes. In this review, beside a brief introduction to general aspects of plant PEPCs, we discuss the evolutionary origin of C4 PEPCs and how their specific properties might have been realised on the molecular level.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

DCDP:

3,3-Dichloro-2-dihydroxyphosphinomethy-2-propenoate, a PEP analogue

MEM1:

Mesophyll expression module 1

PEP:

Phosphoenolpyruvate

PEPC:

Phosphoenolpyruvate carboxylase

PEPCK:

PEPC-kinase

ppc:

PEPC gene

References

  • Akyildiz M (2007). Identification of Cis- and Trans-Regulatory Factors Controlling the Expression of the C4 Phosphoenolpyruvate Carboxylase Gene of the C4 Dicot Flaveria trinervia. Thesis, Heinrich-Heine University Düsseldorf.

    Google Scholar 

  • Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M and Westhoff P (2007). Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. Plant Cell 19: 3391–3402.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Arndt K and Fink GR (1986). GCN4 protein, a positive transcription factor in yeast, binds general promoters at all 5¢ TGACTC 3¢ sequences. Proc Natl Acad Sci U S A 83: 8516–8520.

    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 

  • Bandurski RS and Greiner CM (1953). The enzymatic synthesis of oxaloacetate from phosphoryl-enolpyruvate and carbon dioxide. J Biol Chem 204: 781–786.

    PubMed  CAS  Google Scholar 

  • Bauwe H (1986). An efficient method for the determination of Km values for HCO3- of phosphoenolpyruvate carboxylase. Planta 169: 356–360.

    Article  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • Besnard G, Pincon G, D’Hont A, Hoarau JY, Cadet F and Offmann B (2003). Characterisation of the phosphoenolpyruvate carboxylase gene family in sugarcane (Saccharum spp.). Theor Appl Genet 107: 470–478.

    Article  PubMed  CAS  Google Scholar 

  • Bläsing OE, Westhoff P and Svensson P (2000). Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria, a conserved serine residue in the carboxyl-terminal part of the enzyme is a major determinant for C4-specific characteristics. J Biol Chem 275: 27917–27923.

    PubMed  Google Scholar 

  • Bläsing OE, Ernst K, Streubel M, Westhoff P and Svensson P (2002). The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia - implications for the evolution of C4 photosynthesis. Planta 215: 448–456.

    Article  PubMed  Google Scholar 

  • Brown NJ, Parsley K and Hibberd JM (2005). The future of C4 research – maize, Flaveria or Cleome? Trends Plant Sci 10: 215–221.

    Article  PubMed  CAS  Google Scholar 

  • Chen L-M, Li K-Z, Miwa T and Izui K (2004). Overexpression of a cyanobacterial phosphoenolpyruvate carboxylase with diminished sensitivity to feedback inhibition in Arabidopsis changes amino acid metabolism. Planta 219: 440–449.

    PubMed  CAS  Google Scholar 

  • Chitty JA, Furbank RT, Marshall JS, Chen Z and Taylor WC (1994). Genetic transformation of the C4 plant, Flaveria bidentis. Plant J 6: 949–956.

    Article  CAS  Google Scholar 

  • Chollet R, Vidal J and O’Leary MH (1996). Phosphoenolpyruvate carboxylase: A ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273–298.

    Article  PubMed  CAS  Google Scholar 

  • Christin P-A, Salamin N, Savolainen V, Duvall MR and Besnard G (2007). C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr Biol 17: 1241–1247.

    Article  PubMed  CAS  Google Scholar 

  • Cushman JC and Bohnert HJ (1999). Crassulacean acid metabolism: Molecular genetics. Annu Rev Plant Physiol Plant Mol Biol 50: 305–332.

    Article  PubMed  CAS  Google Scholar 

  • Danker T, Dreesen B, Offermann S, Horst I and Peterhänsel C (2008). Developmental information but not promoter activity controls the methylation state of histone H3 lysine 4 on two photosynthetic genes in maize. Plant J 53: 465–474.

    Article  PubMed  CAS  Google Scholar 

  • Doebley J and Lukens L (1998). Transcriptional regulators and the evolution of plant form. Plant Cell 10: 1075–1082.

    PubMed  CAS  Google Scholar 

  • Dong LY, Masuda T, Kawamura T, Hata S and Izui K (1998). Cloning, expression, and characterization of a root-form phosphoenolpyruvate carboxylase from Zea mays: Comparison with the C4-form enzyme. Plant Cell Physiol 39: 865–873.

    Article  PubMed  CAS  Google Scholar 

  • Duff SMG and Chollet R (1995). In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation. Plant Physiol 107: 775–782.

    PubMed  CAS  Google Scholar 

  • Ehleringer JR, Cerling TE and Helliker BR (1997). C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285–299.

    Article  Google Scholar 

  • Engelmann S, Bläsing OE, Westhoff P and Svensson P (2002). Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phosphoenolpyruvate carboxylase of Flaveria trinervia. FEBS Lett 524: 11–14.

    Article  PubMed  CAS  Google Scholar 

  • Engelmann S, Bläsing OE, Gowik U, Svensson P and Westhoff P (2003). Molecular evolution of C4 phosphoenolpyruvate carboxylase in the genus Flaveria - a gradual increase from C3 to C4 characteristics. Planta 217: 717–725.

    Article  PubMed  CAS  Google Scholar 

  • Ernst K, and Westhoff P. (1996). The phosphoenolpyruvate carboxylase (ppc) gene family of Flaveria trinervia (C4) and F. pringlei (C3): molecular characterization and expression analysis of the ppcB and ppcC genes. Plant Mol Biol 34: 427–443.

    Article  Google Scholar 

  • Ettema TJG, Makarova KS, Jellema GL, Gierman HJ, Koonin EV, Huynen MA, de Vos WA and van der Oost J (2004). Identification and functional verification of archaeal-type phosphoenolpyruvate carboxylase, a missing link in archaeal central carbohydrate metabolism. J Bacteriol 186: 7754–7762.

    Article  PubMed  CAS  Google Scholar 

  • Fukayama H, Hatch M, Tamai T, Tsuchida H, Sudoh S, Furbank R and Miyao M (2003). Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants. Photosynth Res 77: 227–239.

    Article  PubMed  CAS  Google Scholar 

  • Furumoto T, Izui K, Quinn V, Furbank RT and von Caemmerer S (2007). Phosphorylation of phosphoenolpyruvate carboxylase is not essential for high photosynthetic rates in the C4 species Flaveria bidentis. Plant Physiol 144: 1936–1945.

    Article  PubMed  CAS  Google Scholar 

  • Gehrig H, Heute V and Kluge M (2001). New partial sequences of phosphoenolpyruvate carboxylase as molecular phylogenetic markers. Mol Phylogenet Evol 20: 262–274.

    Article  PubMed  CAS  Google Scholar 

  • Gehrig HH, Heute V and Kluge M (1998). Toward a better knowledge of the molecular evolution of phosphoenolpyruvate carboxylase by comparison of partial cDNA sequences. J Mol Evol 46: 107–114

    Article  PubMed  CAS  Google Scholar 

  • Gennidakis S, Rao S, Greenham K, Uhrig RG, O´Leary B, Snedden WA, Lu C and Plaxton WC (2007). Bacterial- and plant-type phosphoenolpyruvate carboxylase polypeptides interact in the hetero-oligomeric Class-2 PEPC complex of developing castor oil seeds. Plant J 52: 839–849.

    Article  PubMed  CAS  Google Scholar 

  • Gowik U, Engelmann S, Bläsing O, Raghavendra A and Westhoff P (2006). Evolution of C4 phosphoenolpyruvate carboxylase in the genus Alternanthera: gene families and the enzymatic characteristics of the C4 isozyme and its orthologues in C3 and C3/C4 Alternantheras. Planta 223: 359–368.

    Article  PubMed  CAS  Google Scholar 

  • Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M and Westhoff P (2004). cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16: 1077–1090.

    Article  PubMed  CAS  Google Scholar 

  • Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins GL and Nimmo HG (1999). Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J 20: 333–342.

    Article  PubMed  CAS  Google Scholar 

  • Hermans J and Westhoff P (1992). Homologous genes for the C4 isoform of phosphoenolpyruvate carboxylase in a C3- and a C4-Flaveria species. Mol Gen Genet 234: 275–284.

    Article  PubMed  CAS  Google Scholar 

  • Izui K, Matsumura H, Furumoto T and Kai Y (2004). Phosphoenolpyruvate carboxylase: A new era of structural biology. Annu Rev Plant Biol 55: 69–84.

    Article  PubMed  CAS  Google Scholar 

  • Jacobs B, Engelmann S, Westhoff P and Gowik U (2008). Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria determinants for high tolerance towards the inhibitor L-malate. Plant Cell Environ 31: 793–803.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kai Y, Matsumura H and Izui K (2003). Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch Biochem Biophys 414: 170–179.

    Article  PubMed  CAS  Google Scholar 

  • Kai Y, Matsumura H, Inoue T, Terada K, Nagara Y, Yoshinaga T, Kihara A, Tsumura K and Izui K (1999). Three-dimensional structure of phosphoenolpyruvate carboxylase: A proposed mechanism for allosteric inhibition. Proc Natl Acad Sci USA 96: 823–828.

    Article  PubMed  CAS  Google Scholar 

  • Lara MV, Chuong SDX, Akhani H, Andreo CS, and Edwards GE (2006). Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiol 142: 673–684.

    Article  PubMed  CAS  Google Scholar 

  • Latzko E and Kelly J (1983). The multi-faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiol Vég 21: 805–815.

    CAS  Google Scholar 

  • Leegood RC and Walker RP (1999). Regulation of the C4 pathway. In C4 Plant Biology, R.F. Sage and R.K. Monson, Eds. Academic, San Diego, CA. pp. 89–131.

    Chapter  Google Scholar 

  • Lepiniec L, Vidal J, Chollet R, Gadal P and Crétin C (1994). Phosphoenolpyruvate carboxylase: Structure, regulation and evolution. Plant Sci 99: 111–124.

    Article  CAS  Google Scholar 

  • Li JJ and Herskowitz I (1993). Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science 262: 1870–1874.

    Article  PubMed  CAS  Google Scholar 

  • Mamedov TG, Moellering ER and Chollet R (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 J 42: 832–843.

    Article  PubMed  CAS  Google Scholar 

  • Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF and Hibberd JM (2007). Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J 51: 886–896.

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Izui K and Mizuguchi K (2006). A novel mechanism of allosteric regulation of archaeal phosphoenolpyruvate carboxylase: a combined approach to structure-based alignment and model assessment. Protein Eng Des Sel 19: 409–419.

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Xie Y, Shirakata S, Inoue T, Yoshinaga T, Ueno Y, Izui K and Kai Y (2002). Crystal structures of C4 form maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10: 1721–1730.

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka M, Kyozuka J, Shimamoto K and Kano-Murakami Y (1994). The promoters of two carboxylases in a C4 plant (maize) direct cell-specific, light-regulated expression in a C3 plant (rice). Plant J 6: 311–319.

    Article  PubMed  CAS  Google Scholar 

  • Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Munch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S and Wingender E (2003). TRANSFAC: transcriptional regulation, from patterns to profiles. Nucl Acid Res 31: 374–378.

    Article  CAS  Google Scholar 

  • McKown AD, Moncalvo JM and Dengler NG (2005). Phylogeny of Flaveria (Asteraceae) and of C4 photosynthesis evoution. Am J Bot 92: 1911–1928.

    Article  PubMed  CAS  Google Scholar 

  • Melzer E and O’Leary MH (1987). Anaplerotic CO2 fixation by phosphoenolpyruvate carboxylase in C-3 Plants. Plant Physiol 84: 58–60.

    Article  PubMed  CAS  Google Scholar 

  • Monson RK (2003). Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. Int J Plant Sci 164 Suppl: S43–S54.

    Google Scholar 

  • Muhaidat R, Sage RF and Dengler NG (2007). Diversity of Kranz anatomy and biochemistry in C-4 eudicots. Am J Bot 94: 362–381.

    Article  PubMed  CAS  Google Scholar 

  • Nimmo GA, Wilkins MB and Nimmo HG (2001). Partial purification and characterization of a protein inhibitor of phosphoenolpyruvate carboxylase kinase. Planta 213: 250–257.

    Article  PubMed  CAS  Google Scholar 

  • Nimmo HG (2000). The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5: 75–80.

    Article  PubMed  CAS  Google Scholar 

  • Nomura M, Higuchi T, Katayama K, Taniguchi M, Miyao-Tokutomi M, Matsuoka M and Tajima S (2005a). The Promoter for C4-type mitochondrial aspartate aminotransferase does not direct bundle sheath-specific expression in transgenic rice plants. Plant Cell Physiol. 46: 743–753.

    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 (2005b). Differential expression pattern of C4 bundle sheath expression genes in rice, a C3 plant. Plant Cell Physiol 46: 754–761.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Offermann S, Danker T, Dreymüller D, Kalamajka R, Topsch S, Weyand K and Peterhänsel C (2006). Illumination is necessary and sufficient to induce histone acetylation independent of transcriptional activity at the C4-specific phosphoenolpyruvate carboxylase promoter in maize. Plant Physiol 141: 1078–1088.

    Article  PubMed  CAS  Google Scholar 

  • Olson EN (2006). Gene regulatory networks in the evolution and development of the heart. Science 313: 1922–1927.

    Article  PubMed  CAS  Google Scholar 

  • Oñate L, Vicente-Carbajosa J, Lara P, Díaz I and Carbonero P (1999). Barley BLZ2, a seed-specific bZIP protein that interacts with BLZ1 in vivo and activates transcription from the GCN4-like motif of B-hordein promoters in barley endosperm. J Biol Chem 274: 9175–9182.

    Article  PubMed  Google Scholar 

  • Patel HM, Kraszewski JL and Mukhopadhyay B (2004). The phosphoenolpyruvate carboxylase from Methanothermobacter thermautotrophicus has a novel structure. J Bacteriol 186: 5129–5137.

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J and Rokhsar DS (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551–556.

    Google Scholar 

  • Rademacher T, Hausler RE, Hirsch HJ, Zhang L, Lipka V, Weier D, Kreuzaler F and Peterhänsel C (2002). An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 32: 25–39.

    Article  PubMed  CAS  Google Scholar 

  • Rajagopalan AV, Devi MT and Raghavendra AS (1994). Molecular biology of C4 phosphoenolpyruvate carboxylase: Structure, regulation and genetic engineering. Photosynth Res 39: 115–135.

    Article  CAS  Google Scholar 

  • Sage RF (2004). The evolution of C4 photosynthesis. New Phytol 161: 341–370.

    Article  CAS  Google Scholar 

  • Sánchez R and Cejudo FJ (2003). Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132: 949–957.

    Article  PubMed  Google Scholar 

  • Saze H, Ueno Y, Hisabori T, Hayashi H and Izui K (2001). Thioredoxin-mediated reductive activation of a protein kinase for the regulatory phosphorylation of C4-form phosphoenolpyruvate carboxylase from maize. Plant Cell Physiol 42: 1295–1302.

    Article  PubMed  CAS  Google Scholar 

  • Schnarrenberger C and Martin W (2002). Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants – A case study of endosymbiotic gene transfer. Eur J Biochem 269: 868–883.

    Article  PubMed  CAS  Google Scholar 

  • Schuller KA, Plaxton WC and Turpin DH (1990). Regulation of phosphoenolpyruvate carboxylase from the green alga Selenastrum minutum. Properties associated with replenishment of tricarboxylic acid cycle intermediates during ammonium assimilation. Plant Physiol 93: 1303–1311.

    Article  PubMed  CAS  Google Scholar 

  • Sheen J (1999). C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50: 187–217.

    Article  PubMed  CAS  Google Scholar 

  • Stockhaus J, Poetsch W, Steinmüller K and Westhoff P (1994). Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 dicot Flaveria trinervia: an expression analysis in the C3 plant tobacco. Mol Gen Genet 245: 286–293.

    Article  PubMed  CAS  Google Scholar 

  • Stockhaus J, Schlue U, Koczor M, Chitty JA, Taylor WC and Westhoff P (1997). The promoter of the gene encoding the C4 form of phosphoenolpyruvate carboxylase directs mesophyll specific expression in transgenic C4 Flaveria spp. Plant Cell 9: 479–489.

    PubMed  Google Scholar 

  • Sullivan S, Jenkins GI and Nimmo HG (2004). Roots, cycles and leaves. Expression of the phosphoenolpyruvate carboxylase kinase gene family in soybean. Plant Physiol 135: 2078–2087.

    Article  PubMed  CAS  Google Scholar 

  • Svensson P, Bläsing O and Westhoff P (1997). Evolution of the enzymatic characteristics of C4 phosphoenolpyruvate carboxylase: a comparison of the orthologous ppcA phosphoenolpyruvate carboxylases of Flaveria trinervia (C4) and F. pringlei (C3). Eur J Biochem 246: 452–460.

    Article  PubMed  CAS  Google Scholar 

  • Svensson P, Bläsing OE and Westhoff P (2003). Evolution of C4 phosphoenolpyruvate carboxylase. Arch Biochem Biophys 414: 180–188.

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002). PAUP*: Phylogenetic Analysis Using Parsimony (and other methods) 4.0. Sinauer Associates, Inc., Sunderland, MA.

    Google Scholar 

  • Takahashi-Terada A, Kotera M, Ohshima K, Furumoto T, Matsumura H, Kai Y and Izui K (2005). Maize phosphoenolpyruvate carboxylase: Mutations at the putative binding site for glucose 6-phosphate caused desensitization and abolished responsiveness to regulatory phosphorylation. J Biol Chem 280: 11798–11806.

    Article  PubMed  CAS  Google Scholar 

  • Tetu SG, Tanz SK, Vella N, Burnell JN and Ludwig M (2007). The Flaveria bidentis beta-carbonic anhydrase gene family encodes cytosolic and chloroplastic isoforms demonstrating distinct organ-specific expression patterns. Plant Physiol 144: 1316–1327.

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F and Higgins DG (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acid Res 25: 4876–4882.

    Article  CAS  Google Scholar 

  • Ting IP and Osmond CB (1973a). Multiple forms of plant phosphoenolpyruvate carboxylase associated with different metabolic pathways. Plant Physiol 51: 448–453.

    Article  PubMed  CAS  Google Scholar 

  • Ting IP and Osmond CB (1973b). Photosynthetic phosphoenolpyruvate carboxylase. Characteristics of allozymes from leaves of C3 and C4 plants. Plant Physiol 51: 439–447.

    Article  PubMed  CAS  Google Scholar 

  • Tovar-Mendez A, Rodriguez-Sotres R, Lopez-Valentin DM and Munoz-Clares RA (1998). Re-examination of the roles of PEP and Mg2+ in the reaction catalysed by the phosphorylated and non-phosphorylated forms of phosphoenolpyruvate carboxylase from leaves of Zea mays - Effects of the activators glucose 6-phosphate and glycine. Biochem J 332: 633–642.

    PubMed  CAS  Google Scholar 

  • Tovar-Méndez A, Mújica-Jiménez C and Muñoz-Clares RA (2000). Physiological implications of the kinetics of maize leaf phosphoenolpyruvate carboxylase. Plant Physiol 123: 149–160.

    Article  PubMed  Google Scholar 

  • Vidal J and Chollet R (1997). Regulatory phosphorylation of C4 PEP carboxylase. Trends Plant Sci 2: 230–237.

    Article  Google Scholar 

  • Wang X, Gowik U, Tang H, Bowers J, Westhoff P and Paterson A (2009). Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol 10: R68.

    Article  PubMed  Google Scholar 

  • Winter K (1985). Crassulacean acid metabolism. In Photosynthetic Mechanisms and the Environment, J. Barber and N.R. Baker, Eds. Elsevier Science Publsihers B.V. (Biomedical Division), Amsterdam/New York/Oxford. pp. 329–387.

    Google Scholar 

  • Yuan JP, Sayegh J, Mendez J, Sward L, Sanchez N, Sanchez S, Waldrop G and Grover S (2006). The regulatory role of residues 226-232 in phosphoenolpyruvate carboxylase from maize. Photosynth Res 88: 73–81.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Entwicklungs- und Molekularbiologie der Pflanzen, Heinrich-Heine Universität Düsseldorf, Universitätsstrasse 1, D-40225, Düsseldorf, German

    Udo Gowik & Peter Westhoff

Authors
  1. Udo Gowik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Westhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Udo Gowik .

Editor information

Editors and Affiliations

  1. School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Agepati S. Raghavendra

  2. Dept. Botany, University of Toronto, Willcocks Street 25, Toronto, M5S 3B2, Ontario, Canada

    Rowan F. Sage

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Gowik, U., Westhoff, P. (2010). Chapter 13 C4-Phosphoenolpyruvate Carboxylase. 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_13

Download citation

Publish with us

Policies and ethics

Search

Navigation