This view shows enzymes only for those organisms listed below, in the list of taxa known to possess the pathway. If an enzyme name is shown in bold, there is experimental evidence for this enzymatic activity.
Synonyms: PCA cycle, C4 photosynthesis, NADP-ME type
|Superclasses:||Generation of Precursor Metabolites and Energy → Photosynthesis|
Some taxa known to possess this pathway include : Zea mays
Expected Taxonomic Range: Embryophyta
The main CO2 fixation enzyme in plants, EC 18.104.22.168, ribulose-bisphosphate carboxylase/oxygenase (RuBisCO), has both carboxylase (photosynthetic CO2 fixation) and oxygenase (photorespiration) activities. The carboxylase activity is favored at high CO2/O2 ratio, whereas the oxygenase activity predominates at a decreased CO2/O2 ratio.
At the time when RuBisCO first evolved, atmospheric CO2 concentration was very high and thus the enzyme's carboxylase activity was favored. However, later in evolution, atmospheric O2 concentration began to rise and RuBisCO's oxygenase activity increased at the expense of the carboxylase activity. At current CO2 levels, photorespiration can reduce photosynthesis by more than 40%.
C4 plants have evolved to respond to lowered CO2 levels. The C4 photosynthetic carbon assimilation cycle starts with carbon fixation in the mesophyll cells by a combination of EC 22.214.171.124, carbonic anhydrase, which converts the gasous CO2 to soluble hydrogen carbonate, and EC 126.96.36.199, phosphoenolpyruvate carboxylase, which incorporates the latter, forming the C4 acid oxaloacetate. Oxaloacetate or a derivative thereof (L-aspartate) is then transported from the mesophyll cells to bundle sheath cells. Once inside the bundle sheath cells, CO2 is released from the C4 acids, generating a micro-environment with a much higher concentration of CO2, suitable for an efficient carboxylation by RuBisCO.
There are at least three variations of the C4 photosynthetic carbon assimilation cycle in plants, namely the NADP-ME (NADP-malic enzyme), NAD-ME (NAD-malic enzyme), or PEPCK (phosphoenolpyruvate carboxykinase) types. The NADP-ME variant does not involve L-aspartate and utilizes an NADP-dependent malic enzyme to releases CO2 from (S)-malate. The NAD-ME variant does involve L-aspartate and utilizes an NAD-dependent malic enzyme. The PEPCK variant contains an additional route for CO2 release by EC 188.8.131.52, phosphoenolpyruvate carboxykinase (ATP), which usually operates to supplement the NADP-ME variant.
However, recent research indicates a flexibility between the three subtypes of C4 photosynthesis (see also C4 photosynthetic carbon assimilation cycle, NAD-ME type and C4 photosynthetic carbon assimilation cycle, PEPCK type) which is documented by the occurrence of mixed C4 decarboxylation pathways in carious plants previously considered to belong to exclusively one C4 photosynthetic type [Wang14d]. For instance, Zea mays has been shown to use both L-aspartate and oxaloacetate for the generation of CO2 [Chapman81]. In addition, it has been demonstrated that maize leaves exhibit the corresponding aspartate aminotransferase activity to maintain an efficient flow-rate. Moreover, the phosphoenol carboxykinase (PEPCK), considered the hallmark of the PEPCK pathway, is also active in maize and shown to support L-aspartate-driven photosynthesis [Pick11]. Similar results have been reported from the NADP-ME type plant Flaveria bidentis which also utilized both L-aspartate and oxaloacetate equally and demonstrated aspartate aminotransferase activity [Meister96]. In general, current discussion of the C4 photosynthetic pathway types move in a direction favoring the existence of only two subtypes, i.e. NADP-ME and NAD-ME which may both contain the supplementary PEPCK cycle [Wang14d].
About This Pathway
C4 photosynthesis basically represents a CO2 concentrating mechanism (CCM) which independently originated more than 60 times in plants indicating the evolutionary drive to optimize photosynthetic CO2 fixation as an tool to keep pace with an ever-changing environment [Ludwig12].This MetaCyc pathway describes the NADP-ME variant, found in major C4 crops such as maize, sorghum, and sugar cane. Note that the pathway spans two cell types, mesophyll and bundle sheath cells.
The roles and sub-cellular locations of carbonic anhydrases (CA) in plants differ and are metabolically integrated in a rather complex manner regardless of the seemingly simple reaction they catalyze, i.e. the reversible hydration of CO2 to hydrogen carbonate [Badger03, Moroney01]. In C3 plants CA's are ambivalent enzymes and contribute to increased CO2 concentration in micro-compartments creating a more efficient environment for the carbon fixating role of RuBisCO in the chloroplast, and also have non-photosynthetic functions as in lipid biosynthesis and operating as antioxidant [Rowlett14]. However, in C4 plants β-carbonic anhydrases operating in the cytoplasm of mesophyll cells are considered essential for the operation of the pathway by providing the PEP-carboxylase substrate hydrogen carbonate for CO2 fixation into oxaloacetate [Burnell88]. Corresponding β-carbonic anhydrases characterized in Zea mays, i.e. CA2 [Tems10, Burnell97] and in Flaveria bidentis [Tetu07], i.e. CA3 are part of a small CA family in this plants where only one member is directly involved in the first reaction of C4 photosynthesis [Monti13, Burnell90]. However, it appears that even those β-carbonic anhydrases have only a limited role in C4 photosynthesis under current climate conditions and are more essential when C4 plants are stressed by high temperature and drought [Studer14].
The initial CO2 fixation occurs in the mesophyll cells, producing oxaloacetate that is subsequently converted to (S)-malate. Malate is transported into bundle sheath cells and CO2 is released there by an NADP-dependent malic enzyme. Pyruvate reenters the mesophyll cells and replenishes phosphoenolpyruvate.
Experimental evidence indicates that CO2 fixation in cyanobacteria is mediated by the C3 pathway, and although C4 acids are among the initial products of photosynthesis, these organisms do not have the enzymatic capacity for the operation of a C4 pathway [Colman89].
Burnell90: Burnell JN (1990). "Immunological Study of Carbonic Anhydrase in C3 and C4 Plants Using Antibodies to Maize Cytosolic and Spinach Chloroplastic Carbonic Anhydrase." Plant Cell Physiol. 31(4):423-427.
Chapman81: Chapman KSR, Hatch MD (1981). "Aspartate Decarboxylation in Bundle Sheath Cells of Zea mays and its possible Contribution to C4 Photosynthesis." Australian Journal of Plant Physiology 8(2):237-248.
Monti13: Monti SM, De Simone G, Dathan NA, Ludwig M, Vullo D, Scozzafava A, Capasso C, Supuran CT (2013). "Kinetic and anion inhibition studies of a β-carbonic anhydrase (FbiCA 1) from the C4 plant Flaveria bidentis." Bioorg Med Chem Lett 23(6);1626-30. PMID: 23414801
Pick11: Pick TR, Brautigam A, Schluter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber AP (2011). "Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation." Plant Cell 23(12);4208-20. PMID: 22186372
Studer14: Studer AJ, Gandin A, Kolbe AR, Wang L, Cousins AB, Brutnell TP (2014). "A Limited Role for Carbonic Anhydrase in C4 Photosynthesis as Revealed by a ca1ca2 Double Mutant in Maize." Plant Physiol 165(2);608-617. PMID: 24706552
Tetu07: Tetu SG, Tanz SK, Vella N, Burnell JN, 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(3);1316-27. PMID: 17496111
Bologna07: Bologna FP, Andreo CS, Drincovich MF (2007). "Escherichia coli malic enzymes: two isoforms with substantial differences in kinetic properties, metabolic regulation, and structure." J Bacteriol 189(16);5937-46. PMID: 17557829
Brown81: Brown DA, Cook RA (1981). "Role of metal cofactors in enzyme regulation. Differences in the regulatory properties of the Escherichia coli nicotinamide adenine dinucleotide phosphate specific malic enzyme, depending on whether magnesium ion or manganese ion serves as divalent cation." Biochemistry 1981;20(9);2503-12. PMID: 7016178
Ferte86: Ferte N, Jacquot JP, Meunier JC (1986). "Structural, immunological and kinetic comparisons of NADP-dependent malate dehydrogenases from spinach (C3) and corn (C4) chloroplasts." Eur J Biochem 154(3);587-95. PMID: 3948869
Gennidakis07: Gennidakis S, Rao S, Greenham K, Uhrig RG, O'Leary B, Snedden WA, Lu C, 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(5);839-49. PMID: 17894783
Izui et al., 1981: Izui K, Taguchi M, Morikawa M, Katsuki H (1981). "Regulation of Escherichia coli phosphoenolpyruvate carboxylase by multiple effectors in vivo. II. Kinetic studies with a reaction system containing physiological concentrations of ligands." J Biochem 90(5);1321-31. PMID: 7040354
Izui et al., 1983: Izui K, Matsuda Y, Kameshita I, Katsuki H, Woods AE (1983). "Phosphoenolpyruvate carboxylase of Escherichia coli. Inhibition by various analogs and homologs of phosphoenolpyruvate." J Biochem (Tokyo) 1983;94(6);1789-95. PMID: 6368527
Kagawa88: Kagawa T, Bruno PL (1988). "NADP-malate dehydrogenase from leaves of Zea mays: purification and physical, chemical, and kinetic properties." Arch Biochem Biophys 260(2);674-95. PMID: 3341761
Kai et al., 1999: Kai Y, Matsumura H, Inoue T, Terada K, Nagara Y, Yoshinaga T, Kihara A, Tsumura K, Izui K (1999). "Three-dimensional structure of phosphoenolpyruvate carboxylase: a proposed mechanism for allosteric inhibition." Proc Natl Acad Sci U S A 96(3);823-8. PMID: 9927652
Kameshita et al., 1979: Kameshita I, Tokushige M, Izui K, Katsuki H (1979). "Phosphoenolpyruvate carboxylase of Escherichia coli. Affinity labeling with bromopyruvate." J Biochem (Tokyo) 1979;86(5);1251-7. PMID: 42643
Matsumura99: Matsumura H, Nagata T, Terada M, Shirakata S, Inoue T, Yoshinaga T, Ueno Y, Saze H, Izui K, Kai Y (1999). "Crystallization and preliminary x-ray diffraction studies of C4-form phosphoenolpyruvate carboxylase from maize." Acta Crystallogr D Biol Crystallogr 1999;55(11);1937-8. PMID: 10531501
Matsuoka88: Matsuoka M, Ozeki Y, Yamamoto N, Hirano H, Kano-Murakami Y, Tanaka Y (1988). "Primary structure of maize pyruvate, orthophosphate dikinase as deduced from cDNA sequence." J Biol Chem 263(23);11080-3. PMID: 2841317
Showing only 20 references. To show more, press the button "Show all references".
©2015 SRI International, 333 Ravenswood Avenue, Menlo Park, CA 94025-3493