Abstract
C4 carbon fixation or the Hatch–Slack pathway is a photosynthetic process in some plants. It is the first step in extracting carbon from carbon dioxide to be able to use it in sugar and other biomolecules. It is one of three known processes for carbon fixation. The C4 in one of the names refers to the four-carbon molecule that is the first product of this type of carbon fixation. C4 fixation is an elaboration of the more common C3 carbon fixation and is believed to have evolved more recently. C4 overcomes the tendency of the enzyme RuBisCO to wastefully fix oxygen rather than carbon dioxide in the process of photorespiration.
The C4 photosynthetic cycle supercharges photosynthesis by concentrating CO2 around ribulose-1,5-bisphosphate carboxylase and significantly reduces the oxygenation reaction. Therefore engineering C4 feature into C3 plants has been suggested as a feasible way to increase photosynthesis and yield of C3 plants, such as rice, wheat, and potato. To identify the possible transition from C3 to C4 plants, the systematic comparison of C3 and C4 metabolism is necessary.
References
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40. Mechin V, Thevenot C, Le Guilloux M, Prioul JL, Damerval C. Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol. 2007;143:1203–1219. doi: 10.1104/pp.106.092148. [PMC free article] [PubMed] [Cross Ref]
41. Oberhuber W, Dai Z-Y, Edwards GE. Light dependence of quantum yields of Photosystem II and CO2 fixation in C3 and C4 plant. Photosythesis research. 1993;35:265–274. doi: 10.1007/BF00016557. [PubMed] [Cross Ref]
42. Kanai R, Edwards GE. The biochemistry of C4 photosynthesis. Chapter 3 in C4 Plant Biology. . 1999.
43. Fravolini A, Williams DG, Thompson TL. Carbon isotope discrimination and bundle sheath leakiness in three C4 subtypes grown under variable nitrogen, water and atmospheric CO2 supply. Journal of Experimental Botany. 2002;53:2261–2269. doi: 10.1093/jxb/erf084. [PubMed] [Cross Ref]
44. Bowman WD. Inputs and Storage of Nitrogen in Winter Snowpack in an Alpine Ecosystem. Arctic and Alpine Research. 1992;24:211–215. doi: 10.2307/1551659. [Cross Ref]
45. Buchman N, Brooks JR, Rapp KD, Ehleringer JR. Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant, Cell & Environment. 1996;19:392–402. doi: 10.1111/j.1365-3040.1996.tb00331.x. [Cross Ref]
46. Taub DR, Lerdau MT. Relationship between leaf nitrogen and photosynthetic rate for three NAD-ME and three NADP-ME C4 grasses. Am J Bot. 2000;87:412–417. doi: 10.2307/2656637. [PubMed] [Cross Ref]
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48. Caemmerer SV. Modeling C4 photosynthesis. In Biochemical models of leaf photosynthesis. 2000. pp. 91–122.
49. Ziska LH, Bunce JA. Influence of increasing carbon dioxide concentration on the photosynthetic and growth stimulation of selected C4 crops and weeds. Photosynthesis Research. 1997;54:199–208. doi: 10.1023/A:1005947802161. [Cross Ref]
50. Price ND, Schellenberger J, Palsson BO. Uniform sampling of steady-state flux spaces: means to design experiments and to interpret enzymopathies. Biophys J. 2004;87:2172–2186. doi: 10.1529/biophysj.104.043000. [PMC free article] [PubMed] [Cross Ref]
51. Schellenberger J, Lewis NE, Palsson BO. Elimination of thermodynamically infeasible loops in steady-state metabolic models. Biophys J. 2011;100:544–553. doi: 10.1016/j.bpj.2010.12.3707. [PMC free article] [PubMed] [Cross Ref]
2. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, van Wijk KJ. Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell. 2010;22:3509–3542. doi: 10.1105/tpc.110.079764. [PMC free article] [PubMed] [Cross Ref]
3. Hibberd JM, Sheehy JE, Langdale JA. Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. CurrOpin Plant Biol. 2008;11:228–231. doi: 10.1016/j.pbi.2007.11.002. [PubMed] [Cross Ref]
4. Taniguchi Y, Ohkawa H, Masumoto C, Fukuda T, Tamai T, Lee K, Sudoh S, Tsuchida H, Sasaki H, Fukayama H, Miyao M. Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J Exp Bot. 2008;59:1799–1809. [PubMed]
5. Evans JR. Enhancing C3 photosynthesis. Plant Physiol. 2010;154:589–592. doi: 10.1104/pp.110.160952. [PMC free article] [PubMed] [Cross Ref]
6. Sweetlove LJ, Last RL, Fernie AR. Predictive metabolic engineering: a goal for systems biology. Plant Physiol. 2003;132:420–425. doi: 10.1104/pp.103.022004. [PMC free article] [PubMed] [Cross Ref]
7. Gutierrez RA, Shasha DE, Coruzzi GM. Systems biology for the virtual plant. Plant Physiol. 2005;138:550–554. doi: 10.1104/pp.104.900150. [PMC free article] [PubMed] [Cross Ref]
8. DellaPenna D. Plant metabolic engineering. Plant Physiol. 2001;125:160–163. doi: 10.1104/pp.125.1.160. [PMC free article] [PubMed] [Cross Ref]
9. Kitano H. Standards for modeling. Nat Biotechnol. 2002;20:337. [PubMed]
10. Kitano H. Systems biology: a brief overview. Science. 2002;295:1662–1664. doi: 10.1126/science.1069492. [PubMed] [Cross Ref]
11. Dennis C, Surridge C. Arabidopsis thaliana genome. Introduction. Nature. 2000;408:791. [PubMed]
12. 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. et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457:551–556. doi: 10.1038/nature07723. [PubMed] [Cross Ref]
13. Becker SA, Feist AM, Mo ML, Hannum G, Palsson BØ, Herrgard MJ. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Nature Protocols. 2007;2:727–738. doi: 10.1038/nprot.2007.99. [PubMed] [Cross Ref]
14. Boyle NR, Morgan JA. Flux balance analysis of primary metabolism in Chlamydomonasreinhardtii. BMC SystBiol. 2009;3:4. [PMC free article] [PubMed]
15. Pramanik J, Keasling JD. Stoichiometric model of Escherichia coli metabolism: incorporation of growth-rate dependent biomass composition and mechanistic energy requirements. BiotechnolBioeng. 1997;56:398–421. [PubMed]
16. Varma A, Palsson BO. Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl Environ Microbiol. 1994;60:3724–3731. [PMC free article] [PubMed]
17. Price ND, Papin JA, Schilling CH, Palsson BO. Genome-scale microbial in silico models: the constraints-based approach. Trends Biotechnol. 2003;21:162–169. doi: 10.1016/S0167-7799(03)00030-1. [PubMed] [Cross Ref]
18. Grafahrend-Belau E, Schreiber F, Koschutzki D, Junker BH. Flux balance analysis of barley seeds: a computational approach to study systemic properties of central metabolism. Plant Physiol. 2009;149:585–598. doi: 10.1104/pp.108.129635. [PMC free article] [PubMed] [Cross Ref]
19. de Oliveira Dal'Molin CG, Quek LE, Palfreyman RW, Brumbley SM, Nielsen LK. AraGEM, a Genome-Scale Reconstruction of the Primary Metabolic Network in Arabidopsis. Plant Physiology. 2009;152:579–589. [PMC free article] [PubMed]
20. Poolman MG, Miguet L, Sweetlove LJ, Fell DA. A genome-scale metabolic model of Arabidopsis and some of its properties. Plant Physiol. 2009;151:1570–1581. doi: 10.1104/pp.109.141267. [PMC free article] [PubMed] [Cross Ref]
21. Radrich K, Tsuruoka Y, Dobson P, Gevorgyan A, Swainston N, Baart G, Schwartz JM. Integration of metabolic databases for the reconstruction of genome-scale metabolic networks. BMC SystBiol. 2010;4:114. [PMC free article] [PubMed]
22. Williams TC, Poolman MG, Howden AJ, Schwarzlander M, Fell DA, Ratcliffe RG, Sweetlove LJ. A genome-scale metabolic model accurately predicts fluxes in central carbon metabolism under stress conditions. Plant Physiol. 2010;154:311–323. doi: 10.1104/pp.110.158535. [PMC free article] [PubMed] [Cross Ref]
23. Knoop H, Zilliges Y, Lockau W, Steuer R. The metabolic network of Synechocystis sp. PCC 6803: systemic properties of autotrophic growth. Plant Physiol. 2010;154:410–422. doi: 10.1104/pp.110.157198. [PMC free article] [PubMed] [Cross Ref]
24. Golomysova A, Gomelsky M, Ivanov PS. Flux balance analysis of photoheterotrophic growth of purple nonsulfur bacteria relevant to biohydrogen production. International Journal of Hydrogen Energy. 2010;35:12751–12760. doi: 10.1016/j.ijhydene.2010.08.133. [Cross Ref]
25. de Oliveira Dal'Molin CG, Quek LE, Palfreyman RW, Brumbley SM, Nielsen LK. C4GEM, a Genome-Scale Metabolic Model to Study C4 Plant Metabolism. Plant Physiology. 2010;154:1871–1885. doi: 10.1104/pp.110.166488. [PMC free article] [PubMed] [Cross Ref]
26. Mrvar A, Batagelj V. Exploratory network analysis with pajek. Mark Granovetter: Cambridge University Press; 2005.
27. Albert R, DasGupta B, Hegde R, Sivanathan GS, Gitter A, Gürsoy G, Paul P, Sontag E. A new computationally efficient measure of topological redundancy of biological and social networks. Physical Review E. 2011;84:036117. [PubMed]
28. Farquhar GD, Berry JA. A Biochemical Model of Photosynthetic CO2 Assimilation in Leaves of C3 Species. Planta. 1980;149:78–90. doi: 10.1007/BF00386231. [PubMed] [Cross Ref]
29. Marri L, Sparla F, Pupillo P, Trost P. Co-ordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase, and CP12 in Arabidopsis thaliana. J Exp Bot. 2005;56:73–80. [PubMed]
30. GeneBank Database. http://www.ncbi.nlm.nih.gov/gene/
31. Quick WP, Schurr U, Fichtner K, Schulze E-D, Rodermel SR, Bogorad L, Stitt M. The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. The Plant Journal. 1991;1:51–58. doi: 10.1111/j.1365-313X.1991.00051.x. [Cross Ref]
32. Sicher RC, Bunce JA. Relationship of photosynthetic acclimation to changes of Rubisco activity in field-grown winter wheat and barley during growth in elevated carbon dioxide. PHOTOSYNTHESIS RESEARCH. 1997;52:27–38. doi: 10.1023/A:1005874932233. [Cross Ref]
33. Debnam PM, Emes MJ. Subcellular distribution of enzymes of the oxidative pentose phosphate pathway in root and leaf tissues. Journal of Experimental Botany. 1999;50:1653–1661.
34. Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP. High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiol. 2009;149:195–204. doi: 10.1104/pp.108.128439. [PMC free article] [PubMed] [Cross Ref]
35. CLORE SMD AM, TINNIRELLO SMN. Increased levels of reactive oxygen species and expression of a cytoplasmic aconitase/iron regulatory protein 1 homolog during the early response of maize pulvini to gravistimulation. Plant, Cell & Environment. 2008;31:144–158. [PubMed]
36. Schwarte S, Bauwe H. Identification of the photorespiratory 2-phosphoglycolate phosphatase, PGLP1, in Arabidopsis. Plant Physiol. 2007;144:1580–1586. doi: 10.1104/pp.107.099192. [PMC free article] [PubMed] [Cross Ref]
37. Lunn JE, Ashton AR, Hatch MD, Heldt HW. Purification, molecular cloning, and sequence analysis of sucrose-6F-phosphate phosphohydrolase from plants. PNAS. 2000;97:12914–12919. doi: 10.1073/pnas.230430197. [PMC free article] [PubMed] [Cross Ref]
38. Hernández JMGM, Castignolles P, Gidley MJ, Myers AM, Gilbert RG. Mechanistic investigation of a starch-branching enzyme using hydrodynamic volume SEC analysis. Biomacromolecules. 2008;9:954–965. doi: 10.1021/bm701213p. [PubMed] [Cross Ref]
39. Monreal JA, McLoughlin F, Echevarria C, Garcia-Maurino S, Testerink C. Phosphoenolpyruvate carboxylase from C4 leaves is selectively targeted for inhibition by anionic phospholipids. Plant Physiol. 2010;152:634–638. doi: 10.1104/pp.109.150326. [PMC free article] [PubMed] [Cross Ref]
40. Mechin V, Thevenot C, Le Guilloux M, Prioul JL, Damerval C. Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol. 2007;143:1203–1219. doi: 10.1104/pp.106.092148. [PMC free article] [PubMed] [Cross Ref]
41. Oberhuber W, Dai Z-Y, Edwards GE. Light dependence of quantum yields of Photosystem II and CO2 fixation in C3 and C4 plant. Photosythesis research. 1993;35:265–274. doi: 10.1007/BF00016557. [PubMed] [Cross Ref]
42. Kanai R, Edwards GE. The biochemistry of C4 photosynthesis. Chapter 3 in C4 Plant Biology. . 1999.
43. Fravolini A, Williams DG, Thompson TL. Carbon isotope discrimination and bundle sheath leakiness in three C4 subtypes grown under variable nitrogen, water and atmospheric CO2 supply. Journal of Experimental Botany. 2002;53:2261–2269. doi: 10.1093/jxb/erf084. [PubMed] [Cross Ref]
44. Bowman WD. Inputs and Storage of Nitrogen in Winter Snowpack in an Alpine Ecosystem. Arctic and Alpine Research. 1992;24:211–215. doi: 10.2307/1551659. [Cross Ref]
45. Buchman N, Brooks JR, Rapp KD, Ehleringer JR. Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant, Cell & Environment. 1996;19:392–402. doi: 10.1111/j.1365-3040.1996.tb00331.x. [Cross Ref]
46. Taub DR, Lerdau MT. Relationship between leaf nitrogen and photosynthetic rate for three NAD-ME and three NADP-ME C4 grasses. Am J Bot. 2000;87:412–417. doi: 10.2307/2656637. [PubMed] [Cross Ref]
47. Zhu XG, Shan L, Wang Y, Quick WP. C4 rice - an ideal arena for systems biology research. J Integr Plant Biol. 2010;52:762–770. doi: 10.1111/j.1744-7909.2010.00983.x. [PubMed] [Cross Ref]
48. Caemmerer SV. Modeling C4 photosynthesis. In Biochemical models of leaf photosynthesis. 2000. pp. 91–122.
49. Ziska LH, Bunce JA. Influence of increasing carbon dioxide concentration on the photosynthetic and growth stimulation of selected C4 crops and weeds. Photosynthesis Research. 1997;54:199–208. doi: 10.1023/A:1005947802161. [Cross Ref]
50. Price ND, Schellenberger J, Palsson BO. Uniform sampling of steady-state flux spaces: means to design experiments and to interpret enzymopathies. Biophys J. 2004;87:2172–2186. doi: 10.1529/biophysj.104.043000. [PMC free article] [PubMed] [Cross Ref]
51. Schellenberger J, Lewis NE, Palsson BO. Elimination of thermodynamically infeasible loops in steady-state metabolic models. Biophys J. 2011;100:544–553. doi: 10.1016/j.bpj.2010.12.3707. [PMC free article] [PubMed] [Cross Ref]
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