Feedforward non-Michaelis-Menten mechanism for CO2 uptake by Rubisco: Contribution of carbonic anhydrases and photorespiration to optimization of photosynthetic carbon assimilation

BioSystems

Volumn 107, Issue 3, 2012, Pages 158-166

  Igamberdiev, Abir U ^a   Roussel, Marc R ^b  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Carbonic anhydrase; Non Michaelis Menten enzyme kinetics; Photosynthesis; Redox balance; Rubisco

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE; OXYGEN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

BICARBONATE; BIOLOGICAL UPTAKE; BIOMASS; CARBON DIOXIDE; CARBON FLUX; CATALYSIS; CHLOROPLAST; CONCENTRATION (COMPOSITION); ELECTRON; ENZYME ACTIVITY; FLUX MEASUREMENT; MAGNITUDE; OPTIMIZATION; PHOTOSYNTHESIS; PROTEIN; REACTION KINETICS; REDOX POTENTIAL;

ARTICLE; CARBON DIOXIDE FIXATION; CARBON FIXATION; CHLOROPLAST; CONCENTRATION (PARAMETERS); ELECTRON TRANSPORT; MICHAELIS MENTEN KINETICS; PHOTORESPIRATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; STROMA; THYLAKOID; THYLAKOID MEMBRANE;

EMBRYOPHYTA;

EID: 84856618188     PISSN: 03032647     EISSN: 18728324     Source Type: Journal    
DOI: 10.1016/j.biosystems.2011.11.008     Document Type: Article

References (87)

1. 2 unidirectional fluxes in plants: I. Regulation of pre-industrial atmosphere. Biosystems 2011, 103:239-251.
2. 2 unidirectional fluxes in plants: II. Analysis of Rubisco evolution. Biosystems 2011, 103:252-264.
3. Bar-Even A., Noor E., Lewis N.E., Milo R. Design and analysis of synthetic carbon fixation pathways. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8889-8894.
4. Baeyer A.D. Ueber die Wasserentziehung und ihre Bedeutung für das Pflanzenleben und die Gährung. Ber. Deutsch. Chem. Ges. 1870, 3:63-75.
5. Bauer E.S. Theoretical Biology 1982, Akadémiai Kiadó, Budapest, (Originally published 1935).
6. Borghans J.A.M., De Boer R.J. Extending the quasi-steady state approximation by changing variables. Bull. Math. Biol. 1996, 58:43-63.
7. Briggs G.E., Haldane J.B.S. A note on the kinetics of enzyme action. Biochem. J. 1925, 19:338-339.
8. Butlerow A. Bildung einer zuckerartigen Substanz durch Synthese. Ann. Chem. Pharm. 1861, 44:295-298.
9. Côme G.M. Mechanistic modelling of homogeneous reactors: a numerical method. Comput. Chem. Eng. 1979, 3:603-609.
10. Dolmetsch R.E., Xu K., Lewis R.S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998, 392:933-936.
11. 2 concentration in wheat (Triticum aestivum). Physiol. Plant. 1979, 46:299-306.
12. - transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5990-5995.
13. 2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol. Rev. 2004, 28:353-376.
14. Easterby J.S. The analysis of metabolite channelling in multienzyme complexes and multifunctional proteins. Biochem. J. 1989, 264:605-607.
15. cat is regulated in balance with photosynthetic electron transport. J. Exp. Bot. 2009, 60:4077-4088.
16. Ellis R.J. The most abundant protein in the world. Trends Biochem. Sci. 1979, 4:241-244.
17. Farazdaghi H., Edwards G.E. A model for photosynthesis and photorespiration in C3 plants based on the biochemistry and stoichiometry of the pathways. Plant Cell Environ. 1988, 11:799-809.
18. 4 photosynthesis from gas exchange. Biosystems 2011, 103:265-284.
19. Farquhar G.D. Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase. Arch. Biochem. Biophys. 1979, 193:456-468.
20. 3 plants. Planta 1980, 149:78-90.
21. 2 concentration mechanism in chloroplasts of C3 plants. Role of carbonic anhydrase. Gen. Physiol. Biophys. 1987, 6:617-632.
22. 3 plants and estimation of their efficiency. Sov. Plant Physiol. 1988, 35:333-339.
23. 2 concentration mechanis in chloroplasts of C3 plants. Photosynthesis: From Light to Biosphere 1995, vol. 5:559-562. Kluwer, Netherlands.
24. 2 and possible mechanisms of this phenomenon. Sov. Plant Physiol. 1992, 39:504-507.
25. 2 fixation as an example for general control mechanisms in metabolic cycles. Biosystems 1999, 51:79-93.
26. Giordano M., Norici A., Forssen M., Eriksson M., Raven J.A. An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol. 2003, 132:2126-2134.
27. Gontero B., Mulliert G., Rault M., Giudici-Orticoni M.-T., Ricard J. Structural and functional properties of a multi-enzyme complex from spinach chloroplasts. 2. Modulation of the kinetic properties of enzymes in the aggregated state. Eur. J. Biochem. 1993, 217:1075-1082.
28. Hahn H.-S., Nitzan A., Ortoleva P., Ross J. Threshold excitations, relaxation oscillations, and effect of noise in an enzyme reaction. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:4067-4071.
29. 2 supply to Rubisco and not photosystem II function in vivo. Plant Physiol. 2003, 132:2267-2275.
30. Hanson S.M., Schnell S. Reactant stationary approximation in enzyme kinetics. J. Phys. Chem. A 2008, 112:8654-8658.
31. Harris G.C., Königer M. The 'high' concentrations of enzymes within the chloroplast. Photosynth. Res. 1997, 54:5-23.
32. Henri V. Théorie générale de l'action de quelques diastases. C. R. Acad. Sci. 1902, 135:916-919.
33. Igamberdiev A.U., Bykova N.V., Kleczkowski L.A. Origins and metabolism of formate in higher plants. Plant Physiol. Biochem. 1999, 37:503-513.
34. Igamberdiev A.U., Bykova N.V., Lea P.J., Gardeström P. The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol. Plant. 2001, 111:427-438.
35. Igamberdiev A.U., Gardeström P. Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta 2003, 1606:117-125.
36. 2+ are interconnected via adenylate kinase equilibrium in plant cells. Biochim. Biophys. Acta 2003, 1607:111-119.
37. Igamberdiev A.U., Mikkelsen T.N., Ambus P., Bauwe H., Lea P.J., Gardeström P. Photorespiration contributes to stomatal regulation and carbon isotope fractionation: a study with barley, potato and Arabidopsis plants deficient in glycine decarboxylase. Photosynth. Res. 2004, 81:139-152.
38. Igamberdiev A.U., Kleczkowski L.A. Equilibration of adenylates in the mitochondrial intermembrane space maintains respiration and regulates cytosolic metabolism. J. Exp. Bot. 2006, 57:2133-2141.
39. 2 concentrations in the atmosphere. Photosynth. Res. 2006, 87:177-194.
40. Igamberdiev A.U., Kleczkowski L.A. Metabolic systems maintain stable non-equilibrium via thermodynamic buffering. Bioessays 2009, 31:1091-1098.
41. 2 fixation in photosynthetic cells via thermodynamic buffering. Biosystems 2011, 103:224-229.
42. 2 assimilation by C3 plants in the light. Biofizika 1989, 34:887-891.
43. Kursar T.A., Coley P.D. Photosynthetic induction times in shade-tolerant species with long and short-lived leaves. Oecologia 1993, 93:165-170.
44. Laisk A. Kinetics of Photosynthesis and Photorespiration in C3-Plants 1977, Nauka, Moscow.
45. Lindner B., García-Ojalvo J., Neiman A., Schimansky-Geier L. Effects of noise in excitable systems. Phys. Rep. 2004, 392:321-424.
46. Loreto F., Delfine S., DiMarco G. Estimation of photorespiratory carbon dioxide recycling during photosynthesis. Aust. J. Plant Physiol. 1999, 26:733-736.
47. McNevin D., von Caemmerer S., Farquhar G. Determining RuBisCO activation kinetics and other rate and equilibrium constants by simultaneous multiple non-linear regression of a kinetic model. J. Exp. Bot. 2006, 57:3883-3900.
48. Michaelis L., Menten M. Die Kinetik der Invertinwirkung. Biochem. Z. 1913, 49:333-369.
49. Moskvin O.V., Ivanov B.N., Ignatova L.K., Kollmeier M.A. Light-induced stimulation of carbonic anhydrase activity in pea thylakoids. FEBS Lett. 2000, 470:375-377.
50. Mueller-Cajar O., Badger M.R. New roads lead to Rubisco in Archaebacteria. Bioessays 2007, 29:722-724.
51. Ngo L.G., Roussel M.R. A new class of biochemical oscillator models based on competitive binding. Eur. J. Biochem. 1997, 245:182-190.
52. Park Y.I., Karlsson J., Rojdestvenski I., Pronina N., Klimov V., Oquist G., Samuelsson G. Role of a novel photosystem II-associated carbonic anhydrase in photosynthetic carbon assimilation in Chlamydomonas reinhardtii. FEBS Lett. 1999, 444:102-105.
53. Pedersen M.G., Bersani A.M. Introducing total substrates simplifies theoretical analysis at non-negligible enzyme concentrations: pseudo first-order kinetics and the loss of zero-order ultrasensitivity. J. Math. Biol. 2010, 60:267-283.
54. Pettersson G., Ryde-Pettersson U. Effects of metabolite binding to ribulosebisphosphate carboxylase on the activity of the Calvin photosynthesis cycle. Eur. J. Biochem. 1988, 177:351-355.
55. Pierce J., Andrews T.J., Lorimer G.H. Reactions intermediate partitioning by ribulose-bisphosphate carboxylases with differing substrate specificities. J. Biol. Chem. 1986, 261:10248-10256.
56. Pons T.L., Pearcy R.W., Seemann J.R. Photosynthesis in flashing light in soybean leaves grown in different conditions. I. Photosynthetic induction state and regulation of ribulose-1,5-bisphosphate carboxylase activity. Plant Cell Environ. 1992, 15:569-576.
57. Portis A.R. The regulation of Rubisco by Rubisco activase. J. Exp. Bot. 1995, 46:1285-1291.
58. 2 diffusion. J. Exp. Bot. 2006, 57:3195-3207.
59. Pronina N.A., Semenenko V.E. Localization of bound carbonic anhydrase in membranes of Chlorella cells. Sov. Plant Physiol. 1988, 35:38-46.
60. 2 concentration in algae cells. Current Research in Photosynthesis 1990, vol. IV:489-492. Kluwer Academic Publishers, The Netherlands.
61. Rault M., Giudici-Orticoni M.-T., Gontero B., Ricard J. Structural and functional properties of a multi-enzyme complex from spinach chloroplasts. 1. Stoichiometry of the polypeptide chains. Eur. J. Biochem. 1993, 217:1065-1073.
62. 2-grown cells of Chlamydomonas reinhardtii. Plant Cell Environ. 2001, 24:261-265.
63. 2 and carbonic anhydrase. Physiol. Plant. 2006, 128:763-772.
64. Richter P.H., Ross J. Concentration oscillations and efficiency: glycolysis. Science 1981, 211:715-717.
65. Robinson S.P., Portis A.R. Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase/oxygenase by Rubisco activase. FEBS Lett. 1988, 233:413-416.
66. Roussel M.R. The use of delay differential equations in chemical kinetics. J. Phys. Chem. 1996, 100:8323-8330.
67. 2. J. Plant Physiol. 2007, 164:1188-1196.
68. Roussel M.R., Igamberdiev A.U. Dynamics and mechanisms of oscillatory photosynthesis. Biosystems 2011, 103:230-238.
69. Rudenko N.N., Ignatova L.K., Ivanov B.N. Multiple sources of carbonic anhydrase activity in pea thylakoids: soluble and membrane-bound forms. Photosynth. Res. 2007, 91:81-89.
70. Servaites J.C. Inhibition of ribulose 1,5-bisphosphate carboxylase/oxygenase by 2-carboxyarabinitol-1-phosphate. Plant Physiol. 1990, 92:867-870.
71. 2 evolution rate by proton removal. EMBO J. 2008, 27:782-791.
72. Stépán G. Retarded Dynamical Systems: Stability and Characteristic Functions 1989, Longman, NewYork.
73. Stucki J.W. The thermodynamic-buffer enzymes. Eur. J. Biochem. 1980, 109:257-267.
74. Sunderhaus, Dudkina S., Jansch N.V., Klodmann L., Heinemeyer J., Perales J., Zabaleta M., Boekema E., Braun E.J.H.-P. Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J. Biol. Chem. 2006, 281:6482-6488.
75. Tabita F.R., Hanson T.E., Satagopan S., Witte B.H., Kreel N.E. Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Phil. Trans. R. Soc. B 2008, 363:2629-2640.
76. Tcherkez G.G., Farquhar G.D., Andrews T.J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:7246-7251.
77. Tzafriri A.R. Michaelis-Menten kinetics at high enzyme concentrations. Bull. Math. Biol. 2003, 65:1111-1129.
78. Tzafriri A.R., Edelman E.R. Quasi-steady-state kinetics at enzyme and substrate concentrations in excess of the Michaelis-Menten constant. J. Theor. Biol. 2007, 245:737-748.
79. Viil J., Ivanova H., Pärnik T. Estimation of rate constants of the partial reactions of carboxylation of ribulose-1,5-bisphosphate in vivo. Photosynth. Res. 1999, 60:247-256.
80. Viil Yu, Ivanova H., Pärnik T., Pärsim E. Measurement of the concentration of the active centers of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo. Russ. J. Plant Physiol. 2001, 48:116-121.
81. 2 with enzyme-bound ribulose 1,5-bisphosphate in vivo. J. Exp. Bot. 1995, 46:1301-1307.
82. Villarejo A., Shutova T., Moskvin O., Forssén M., Klimov V.V., Samuelsson G. A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J. 2002, 21:1930-1938.
83. 4 photosynthesis in Miscanthus×giganteus relative to Zea mays be explained by differences in activities and thermal properties of Rubisco?. J. Exp. Bot. 2008, 59:1779-1787.
84. Wienkoop S., Weiss J., May P., Kempa S., Irgang S., Recuenco-Munoz L., Pietzke M., Schwemmer T., Rupprecht J., Egelhofer V., Weckwerth W. Targeted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analyses. Mol. Biosyst. 2010, 6:1018-1031.
85. 2 fixation in C3 plants. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 1988, 39:533-594.
86. Woodrow I.E., Kelly M.E., Mott K.A. Limitation of the rate of ribulosebisphosphate carboxylase activation by carbamylation and ribulosebisphosphate carboxylase activase activity: development and tests of a mechanistic model. Aust. J. Plant Physiol. 1996, 23:141-149.
87. 3 photosynthesis: a sensitivity analysis of the photosynthetic carbon-reduction cycle. Planta 1993, 191:421-432.