Diversity in forms and functions of carbonic anhydrase in terrestrial higher plants

Russian Journal of Plant Physiology

Volumn 54, Issue 2, 2007, Pages 143-162

  Ivanov, B N ^a   Ignatova, L K ^a   Romanova, A K ^a  

^a INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

Author keywords

Carbonic anhydrase; CO2; Concentrating system; Molecular forms; Photosynthesis; Properties; Terrestrial phototrophs

Indexed keywords

EMBRYOPHYTA;

EID: 34147123572     PISSN: 10214437     EISSN: None     Source Type: Journal    
DOI: 10.1134/S102144370702001X     Document Type: Review

References (143)

1. Faurholt, C., Ètudes sur les Solutions Aqueuses d'Anhydride Carbonique et d'Acide Carbonique, J. Chim. Physiq., 1924, vol. 21, pp. 400-455.
2. 2 in Water, Biophysics and Physiology of Carbon Dioxide, Bauer, C., Gros, G., and Bartels, H., Eds., New York: Springer-Verlag, 1980, pp. 3-11.
3. Rabinowitch, E.I., Photosynthesis and Related Processes, vol. 1, Chemistry of Photosynthesis, Chemosynthesis and Related Processes In Vitro and In Vivo, New York: Intersci. Publ., 1945.
4. Gutknecht, J., Bisson, M.A., and Tosteson, D.C., Diffusion of Carbon Dioxide through Lipid Bilayer Membranes. Effects of Carbonic Anhydrase, Bicarbonate and Unstirred Layers, J. Gen. Physiol., 1977, vol. 69, pp. 779-794.
5. Mitz, M.A., Biodinamics: A New Concept of Cellular Control, J. Theor. Biol., 1979, vol. 80, pp. 537-551.
6. Lawlor, D.W., Photosynthesis: Metabolism, Control, and Physiology, New York: John Wiley and Sons, 1987.
7. Smith, R.G., Inorganic Carbon Transport in Biological Systems, Comp. Biochem. Physiol., 1988, vol. 90B, pp. 639-654.
8. 4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis, Oxford: Blackwell, 1983.
9. Romanova, A.K., Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase, Usp. Biol. Khim., 1991, vol. 32, pp. 87-113.
10. Moroney, J.V., Bartlett, S.J., and Samuelson, G., Carbonic Anhydrases in Plants and Algae, Plant, Cell Environ., 2001, vol. 24, pp. 141-153.
11. Tripp, B.C., Smith, K., and Ferry, J.G., Carbonic Anhydrase: New Insights for an Ancient Enzyme, J. Biol. Chem., 2001, vol. 276, pp. 48 615-48 618.
12. So, A.K.-C. and Espie, G.S., Cyanobacterial Carbonic Anhydrase, Can. J. Bot., 2005, vol. 83, pp. 721-734.
13. Hewett-Emmett, D. and Tashian, R.E., Functional Diversity, Conservation, and Convergence in the Evolution of the Alpha, Beta, and Gamma Carbonic Anhydrase Families, Mol. Phylogen. Evol., 1996, no. 5, pp. 52-77.
14. Liljas, A. and Lauberg, M.A., Weel Invented Three Times. The Molecular Structure of the Three Carbonic Anhydrases, EMBO J., 2000, vol. 19, pp. 16-17.
15. Kruft, V., Eubel, H., Jansch, L., Werdhahn, W., and Braun, H.-P., Proteomic Approach to Identify Novel Mitochondrial Proteins in Arabidopsis, Plant Physiol., 2001, vol. 127, pp. 1694-1710.
16. 2, EMBO J., 1998, vol. 17, pp. 1208-1216.
17. Coleman, J.E., Zinc Proteins: Enzymes, Storage Proteins, Transcription Factors, and Replication Proteins, Annu. Rev. Biochem., 1992, vol. 61, pp. 897-946.
18. Lindskog, S., Structure and Mechanism of Carbonic Anhydrase, Pharmacol. Theraupeutics, 1997, vol. 74, pp. 1-20.
19. 2" Utilized by Ribulose Diphosphate Carboxylase, J. Biol. Chem., 1969, vol. 244, pp. 1018-1083.
20. - and to Carbon Isotopic Discrimination, New Phytol., 1980, vol. 86, pp. 245-259.
21. Pfanz, H., Apoplastic and Symplastic Proton Concentrations and Their Significance for Metabolism, Ecophysiology of Photosynthesis. Ecological Studies, Schulze, E.-D. and Coldwele, M.M., Eds., Berlin: Springer-Verlag, 1994, pp. 103-122.
22. Watson, R.T., Rodhe, H., Oescheger, H., and Siegenthaler, U., Greenhouse Gases and Aerosols, Climate Changes: The IPCC Scientific Assessment, Houghton, J.T., Jenkins, G.J., and Ephranums, J.J., Eds., Cambridge: Cambridge Univ. Press, 1990, pp. 1-40.
23. 2 Assimilation, Plant Cell Physiol., 1985, vol. 26, pp. 881-891.
24. 2 Excess, Fiziol. Rast. (Moscow), 1992, vol. 39, pp. 82-88 (Sov. Plant Physiol., Engl. Transl.).
25. Enser, U. and Heber, U., Metabolic Regulation by pH Gradients. Inhibition of Photosynthesis by Indirect Proton Transfer across the Chloroplast Envelope, Biochim. Biophys. Acta, 1980, vol. 592, pp. 577-591.
26. 2 Evolution Rate and Parameters of Chlorophyll Fluorescence Quenching, Plant Physiol. Biochem., 1993, vol. 31, pp. 295-301.
27. 3 Plant Leaf Cell, Aust. J. Plant Physiol., 1998, vol. 25, pp. 673-677.
28. 4 Plants, Physiol. Plant., 1993, vol. 88, pp. 413-419.
29. Ignatova, L.K., Moskvin, O.V., and Ivanov, B.N., Effects of Carbonic Anhydrase Inhibitors on Proton Exchange and Photosynthesis in Pea Protoplasts, Russ. J. Plant Physiol., 2001, vol. 48, pp. 467-472.
30. - Transport in Isolated Pea Mesophyll Protoplasts, Plant Physiol., 1981, vol. 67, pp. 1119-1123.
31. Kachru, R.B. and Anderson, L., Chloroplast and Cytoplasmic Enzymes: 5. Pea-Leaf Carbonic Anhydrase, Planta, 1974, vol. 118, pp. 235-240.
32. Rumeau, D., Cuiné, S., Fina, L., Gault, N., Nicole, M., and Peltier, G., Subcellular Distribution of Carbonic Anhydrase in Solanum tuberosum L. Leaves, Planta, 1996, vol. 199, pp. 79-88.
33. Fett, J.P. and Coleman, J.R., Characterization and Expression of Two cDNA Encoding Carbonic Anhydrase in Arabidopsis thaliana, Plant Physiol., 1994, vol. 105, pp. 707-713.
34. Reed, M.L., Intracellular Location of Carbonate Dehydratase (Carbonic Anhydrase) in Leaf Tissue, Plant Physiol., 1979, vol. 63, pp. 216-217.
35. 2 Fixation in Intact Chloroplasts, Phytochemistry, 1970, vol. 9, pp. 25-32.
36. Werdan, K. and Heldt, K.W., Accumulation of Bicarbonate in Intact Chloroplast Following a pH Gradient, Biochim. Biophys. Acta, 1972, vol. 283, pp. 430-441.
37. Poincelot, R.P., Intracellular Distribution of Carbonic Anhydrase in Spinach Leaves, Biochim. Biophys. Acta, 1972, vol. 258, pp. 637-642.
38. Douce, R., Holtz, R.B., and Benson, A.A., Isolation and Properties of the Envelope of Spinach Chloroplasts, J. Biol. Chem., 1973, vol. 248, pp. 7215-7222.
39. Heldt, H.W., Metabolite Transport in Intact Spinach Chloroplast, The Intact Chloroplast , Barber, J., Ed., Amsterdam: Elsevier and North-Holland Biomed., 1976, pp. 215-234.
40. 2 Concentrating in Plants, Fiziol. Rast. (Moscow), 1988, vol. 35, pp. 429-437 (Sov. Plant Physiol., Engl. Transl.).
41. Poincelot, R.P., Carbonic Anhydrase, Encyclopedia of Plant Physiology. New Ser., Gibbs, M. and Latzko, E., Eds., Berlin: Springer-Verlag, 1979, vol. 6, pp. 230-238.
42. Reed, M.L. and Graham, D., Carbonic Anhydrase in Plants: Distribution, Properties and Possible Physiological Roles, Progress in Phytochemistry, Reinhold, L., Harborne, J.B., and Swain, T., Eds., Oxford: Pergamon, 1981, pp. 47-94.
43. Graham, D., Reed, M.L., Patterson, B.D., Hockley, D.G., and Dwyer, M.R., Chemical Properties, Distribution and Physiology of Plant and Algal Carbonic Anhydrase, Ann. New York Acad. Sci., 1984, vol. 429, pp. 222-237.
44. Aliev, D.A. and Guliev, N.M., Karboangidraza rastenii (Plant Carbonic Anhydrase), Moscow: Nauka, 1990.
45. Tiwari, A., Kumar, P., Singh, S., and Ansari, S.A., Carbonic Anhydrase in Relation to Higher Plants, Photosynthetica, 2005, vol. 43, pp. 1-11.
46. Silverman, D.N., The Catalytic Mechanism of Carbonic Anhydrase, Can. J. Bot., 1991, vol. 69, pp. 1070-1078.
47. Badger, M.R. and Price, G.D., The Role of Carbonic Anhydrase in Photosynthesis, Annu. Rev. Plant Physiol. Plant. Mol. Biol., 1994, vol. 45, pp. 369-392.
48. Neish, A.G., Studies in Chloroplasts: 2. Their Chemical Composition and the Distribution of Certain Metabolites between the Chloroplasts and the Remainder of the Leaf, Biochemistry, 1939, vol. 33, pp. 300-307.
49. 2: Chemical, Biochemical, and Physiological Aspects, Forster, R.E., Edsall, J.T., Otis, A.B., and Haughton, F.J.W., Eds., Washington: NASA, 1969, pp. 131-138.
50. Pocker, Y. and Ng, J.C.Y., Plant Carbonic Anhydrase: Properties and Carbon Dioxide Kinetics, Biochemistry, 1973, vol. 12, pp. 5127-5134.
51. Tobin, A.J., Carbonic Anhydrase from Parsley Leaves, J. Biol. Chem., 1970, vol. 245, pp. 2656-2666.
52. Kisiel, W. and Graf, G., Purification and Characterization of Carbonic Anhydrase from Pisum sativum, Phytochemistry, 1972, vol. 11, pp. 113-117.
53. Walk, A.R. and Metzner, H., Reinigung und Characterisierung von Chloroplasten-Carbonat-Dehydratase (Isoenzym I) aus Blättern von Lactuca sativa, Hoppe-Seyler's Z. Physiol. Chem., 1975, vol. 356, pp. 1733-1741.
54. Firus, O.K. and Romanova, A.K., Extraction and Some Properties of Carbonic Anhydrase from Nicotiana tabacum, Dokl. Akad. Nauk Tadzh. SSR, 1983, vol. 26, pp. 795-797.
55. Guliev, N.M., Mamedov, T.G., Yusufov, E.F., Bairamov, Sh.M., and Aliev, D.A., Crystallization of Carbonic Anhydrase in Cicer arietinum, Izv. Akad. Nauk SSSR, Ser. Biol. Nauk, 1987, no. 4, pp. 3-4.
56. Aliev, D.A., Guliev, N.M., and Idayatov, R.B., Extraction and Some Properties of Carbonic Anhydrase from Wheat Leaves, Izv. Akad. Nauk Az. SSR, Ser. Biol. Nauk, 1989, no. 1, pp. 15-17.
57. Okabe, K., Yang, S.-Y., Tsusuki, M., and Miyachi, S., Carbonic Anhydrase: Its Content in Spinach Leaves and Its Taxonomic Diversity Studied with Anti-Spinach Leaf Carbonic Anhydrase Antibody, Plant Sci. Lett., 1984, vol. 33, pp. 145-153.
58. Kimber, M.S. and Pai, E.F., The Active Centre Architecture of Pisum sativum Beta Carbonic Anhydrase Is a Mirror Image of That of Alpha Carbonic Anhydrases, EMBO J., 2000, vol. 19, pp. 1407-1418.
59. Pocker, Y. and Ng, J.C.Y., Plant Carbonic Anhydrase: Hydrase Activity and Its Reversible Inhibition, Biochemistry, 1974, vol. 13, pp. 5116-5120.
60. Chang, C.W., Carbonic Anhydrase of the Cotton Plant, Phytochemistry, 1975, vol. 14, pp. 119-121.
61. M of Carbonic Anhydrase from the Cotton Plant, Plant Sci. Lett., 1975, vol. 4, pp. 109-113.
62. Atkins, C.A., Patterson, B.D., and Graham, D., Plant Carbonic Anhydrases: 1. Distribution of Types among Species, Plant Physiol., 1972, vol. 50, pp. 214-217.
63. Atkins, C.A., Patterson, B.D., and Graham, D., Plant Carbonic Anhydrases: 2. Preparation and Some Properties of Monocotyledon and Dicotyledon Enzyme Types, Plant Physiol., 1972, vol. 50, pp. 218-223.
64. Kositsin, A.V., Plant Carbonic Anhydrase, Usp. Sovrem. Biol., 1977, vol. 83, pp. 86-96.
65. Burnell, J.N., Gibbs, M.J., and Mason, J.G., Spinach Chloroplastic Carbonic Anhydrase, Plant Physiol., 1990, vol. 92, pp. 37-40.
66. Fawsett, T.W., Browse, J.A., Volokita, M., and Bartlett, S.G., Spinach Carbonic Anhydrase Primary Structure Deduced from Sequence of a cDNA Clone, J. Biol. Chem., 1990, vol. 265, pp. 5414-5417.
67. Roeske, C.A. and Ogren, W.L., Nucleotide Sequence of Pea cDNA Encoding Chloroplastic Carbonic Anhydrase, Nucleic Acids Res., 1990, vol. 18, p. 3413.
68. Majeau, N. and Coleman, J.R., Isolation and Characterization of a cDNA Coding for Pea Chloroplastic Carbonic Anhydrase, Plant Physiol., 1991, vol. 95, pp. 264-268.
69. 2 on mRNA Levels, Plant Mol. Biol., 1992, vol. 20, pp. 1143-1148.
70. Johanson, I.M. and Forsman, C., Processing of Chloroplast Transit Peptide of Pea Carbonic Anhydrase in Chloroplasts and in Esherichia coli. Identification of Two Cleavage Sites, FEBS Lett., 1992, vol. 34, pp. 232-236.
71. 2? Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 609-639.
72. 2, Russ. J. Plant Physiol., 2005, vol. 52, pp. 112-126.
73. 2 Concentration on Carbonic Anhydrase and Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Expression in Pea, Plant Physiol., 1996, vol. 112, pp. 569-574.
74. 2, Russ. J. Plant Physiol., 2005, vol. 52, pp. 158-164.
75. Majeau, N. and Coleman, J.R., Nucleotide Sequence of a Complementary DNA Encoding Tobacco Chloroplastic Carbonic Anhydrase, Plant Physiol., 1992, vol. 100, pp. 1077-1078.
76. Kim, H.J., Bracey, M.H., and Bartlett, S.G., Nucleotide Sequence of a Gene Encoding Carbonic Anhydrase in Arabidopsis thaliana, Plant Physiol., 1994, vol. 105, p. 449.
77. Aliev, D.A., Guliev, N.M., Mamedov, T.G., and Tsuprun, V.L., Physical and Chemical Properties and Quarternary Structure of Carbonic Anhydrase in Chick-Pea, Biokhimiya, 1986, vol. 51, pp. 1785-1794.
78. 2 Hydration Catalyzed by Human Carbonic Anhydrase I, Biochim. Biophys. Acta, 1992, vol. 1120, pp. 81-86.
79. Johanson, I.M. and Forsman, C., Kinetic Studies of Pea Carbonic Anhydrase, Eur. J. Biochem., 1993, vol. 21, pp. 439-446.
80. Pocker, Y. and Miksch, R.R., Plant Carbonic Anhydrase: Properties and Bicarbonate Dehydration Kinetics, Biochemistry, 1978, vol. 17, pp. 1119-1125.
81. Walker, D.A. and Jones, M.E., Carbonic Anhydrase of Microorganisms: 1. An Enzyme from Baker's Yeast Catalyses the Formation of Carbamate from Ammonium Bicarbonate Solutions, Arch. Biochem. Biophys., 1970, vol. 130, pp. 130-142.
82. Guliev, N.M., Bairamov, Sh.M., and Aliev, D.A., Functional Organization of Carbonic Anhydrase in Higher Plants, Fiziol. Rast. (Moscow), 1992, vol. 39, pp. 186-195 (Sov. Plant Physiol., Engl. Transl.).
83. Porter, M.A. and Grodzinski, B., Regulation of Chloroplastic Carbonic Anhydrase, Plant Physiol., 1983, vol. 72, pp. 604-605.
84. Jacobson, B.S., Fong, F., and Heath, R.I., Carbonic Anhydrase of Spinach. Studies of Its Location, Inhibition, and Physiological Function, Plant Physiol., 1975, vol. 55, pp. 468-474.
85. 2 Fixation in the Light and Dark, Biochim. Biophys. Acta, 1975, vol. 396, pp. 276-292.
86. 2 Assimilation, Planta, 1994, vol. 193, pp. 331-340.
87. Majeau, N., Arnoldo, M.A., and Coleman, J.R., Modification of Carbonic Anhydrase Activity by Antisense and Over-Expression Constructs in Transgenic Tobacco, Plant Mol. Biol., 1994, vol. 25, pp. 377-385.
88. 16O in Tobacco Plants Modified by an Antisense Construct to Have Low Chloroplastic Carbonic Anhydrase, Plant Physiol., 1996, vol. 112, pp. 319-326.
89. Graham, D. and Reed, M.L., Carbonic Anhydrase and the Regulation of Photosynthesis, Nature New Biol., 1971, vol. 231, pp. 81-83.
90. Vermaas, W.F.J., Govindjee, Bicarbonate or Carbon Dioxide as a Requirement for Efficient Electron Transport on the Acceptor Side of Photosystem II, Photosynthesis, vol. II, Development, Carbon Metabolism, and Plant Productivity, Govindjee, Ed., New York: Academic, 1982, pp. 541-558.
91. Stemler, A.J. and Jursinic, P., The Effect of Carbonic Anhydrase Inhibitors Formate, Bicarbonate, Acetazolamide, and Imidazole on Photosystem II in Maize Chloroplast, Arch. Biochem. Biophys., 1983, vol. 221, pp. 227-237.
92. - to Photosystem II in Chloroplast Thylakoids, Photobiochem. Photobiophys., 1984, vol. 8, pp. 289-304.
93. Klimov, V.V., Allakhverdiev, S.I., Feiziev, Ya.M., and Baranov, S.V., Bicarbonate Requirement for the Donor Side of Photosystem II, FEBS Lett., 1995, vol. 363, pp. 251-255.
94. Klimov, V.V., Baranov, S.V., and Allakhverdiev, S.I., Bicarbonate Protects the Donor Side of Photosystem II against Photoinhibition and Thermoinactivation, FEBS Lett., 1997, vol. 418, pp. 243-246.
95. Van Rensen, J.J.S., Role of Bicarbonate in Photosystem II, the Water-Plastoquinone Oxido-Reductase of Plant Photosynthesis, Physiol. Plant., 1999, vol. 105, pp. 585-592.
96. Vaklinova, S.G., Goushtina, L.M., and Lazova, G.N., Carbonic Anhydrase Activity in Chloroplasts and Chloroplast Fragments, C. R. Acad. Bulg. Sci., 1982, vol. 35, pp. 1721-1724.
97. Komarova, Yu.M., Doman, N.G., and Shaposhnikov, G.L., Two Carbonic Anhydrase Forms in Bean Chloroplasts, Biokhimiya, 1982, vol. 47, pp. 1027-1134.
98. Moskvin, O.V., Ignatova, L.K., Ovchinnikova, V.I., and Ivanov, B.N., Membrane-Bound Carbonic Anhydrase in Pea Thylakoids, Biokhimiya, 1995, vol. 60, pp. 859-864.
99. Moskvin, O.V., Shutova, T.V., Khristin, M.S., Ignatova, L.K., Villarejo, A., Samuelsson, G., Klimov, V.V., and Ivanov, B.N., Carbonic Anhydrase Activities in Pea Thylakoids, Photosynth. Res., 2004, vol. 79, pp. 93-100.
100. Pronina, N.A., Allakhverdiev, S.I., Kupriyanova, E.V., Klyachko-Gurvich, G.L., and Klimov, V.V., Carbonic Anhydrase in Subchloroplast Particles of Pea Plants, Russ. J. Plant Physiol., 2002, vol. 49, pp. 303-310.
101. Lu, Y.-K. and Stemler, A.J., Extrinsic Photosystem II Carbonic Anhydrase in Maize Mesophyll Chloroplasts, Plant Physiol., 2002, vol. 128, pp. 643-649.
102. Khristin, M.S., Ignatova, L.K., Rudenko, N.N., Ivanov, B.N., and Klimov, V.V., Photosystem II Associated Carbonic Anhydrase Activity in Higher Plants Is Situated in Core Complex, FEBS Lett., 2004, vol. 577, pp. 1208-1216.
103. Ignatova, L.K., Rudenko, N.N., Khristin, M.S., and Ivanov, B.N., Heterogeneity of Carbonic Anhydrase Activity in Membrane Thylakoids, Biokhimiya, 2006, vol. 71, pp. 651-659.
104. Lu, Y.-K., Theg, S.M., and Stemler, A.J., Carbonic Anhydrase Activity of the Photosystem II OEC33 Protein from Pea, Plant Cell Physiol., 2005, vol. 49, pp. 1944-1953.
105. Rudenko, N.N., Ignatova, L.K., Kamornitskaya, V.B., and Ivanov, B.N., The Presence of Several Carbonic Anhydrases in Thylakoids from Pea Leaves, Dokl. Akad. Nauk, 2006, vol. 408, pp. 553-555.
106. Vilarejo, A., Shutova, T., Moskvin, O., Forssén, M., Klimov, V.V., and Samuelsson, G., A Photosystem II-Associated Carbonic Anhydrase Regulates the Efficiency of Photosynthetic Oxygen Evolution, EMBO J., 2002, vol. 21, pp. 1930-1938.
107. Moskvin, O.V., Ivanov, B.N., Ignatova, L.K., and Kollmeier, M.A., Light-Induced Stimulation of Carbonic Anhydrase Activity in Pea Thylakoids, FEBS Lett., 2000, vol. 470, pp. 375-377.
108. 4 Plants, Aust. J. Plant Physiol., 1995, vol. 22, pp. 45-49.
109. Parisi, G., Perales, M., Fornasari, M.S., Colaneri, A., González-Shain, N., Gómez-Casati, D., Zimmermann, S., Brennicke, A., Araya, A., Ferry, J.G., Echave, J., and Zabaleta, E., Gamma Carbonic Anhydrases in Plant Mitochondria, Plant Mol. Biol., 2004, vol. 55, pp. 193-207.
110. Perales, M., Parisi, G., Fornasari, M.S., Colaneri, A., González-Shain, N., Gómez-Casati, D., Zimmermann, S., Brennicke, A., Araya, A., Ferry, J.G., Echave, J., and Zabaleta, E., Gamma Carbonic Anhydrases Like Complex Interact with Plant Mitochondria, Plant Mol. Biol., 2005, vol. 56, pp. 47-57.
111. Pavlovets, V.V. and Romanova, A.K., Intermolecular Interaction of NADP-Malic Enzyme and Carboxylation Phase Enzymes in Maize Leaf Extracts, Russ. J. Plant Physiol, 1997, vol. 44, pp. 279-283.
112. Burnell, J.N., Suzuki, I., and Sugiyama, T., Light Induction and the Effect of Nitrogen Status upon the Activity of Carbonic Anhydrase in Maize Leaves, Plant Physiol., 1990, vol. 94, pp. 384-387.
113. 4 Plants Using Antibodies to Maize Cytosolic and Spinach Chloroplastic Carbonic Anhydrase, Plant Cell Physiol., 1990, vol. 31, pp. 423-427.
114. 4 Photosynthesis, Plant Physiol., 1990, vol. 93, pp. 825-828.
115. Burnell, J.N. and Ludwig, M., Characterization of Two cDNAs Encoding Carbonic Anhydrase in Maize Leaves, Aust. J. Plant Physiol., 1997, vol. 24, pp. 451-458.
116. 4 Pathway Operation, Plant Physiol., 1988, vol. 86, pp. 1252-1256.
117. 2-Concentrating Mechanism, Plant Physiol., 1998, vol. 117, pp. 1071-1081.
118. Guliev, N.M., Babaev, G.G., Bairamov, Sh.M., and Aliev, D.A., Purification, Properties, and Localization of Two Carbonic Anhydrases from Amaranthus cruentus Leaves, Russ. J. Plant Physiol., 2003, vol. 50, pp. 213-219.
119. Ludwig, M. and Burnell, J., Molecular Comparison of Carbonic Anhydrase from Flaveria Species Demonstrating Different Photosynthetic Pathways, Plant Mol. Biol., 1995, vol. 29, pp. 353-365.
120. Stemler, A.J., Carbonic Anhydrase: Molecular Insights Applied to Photosystem II Research in Thylakoid Membranes, Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, Lucas, W.J. and Berry, J.A., Eds., Washington: American Society of Plant Physiologists, 1985, pp. 376-387.
121. 2+, Photosynthesis: Mechanisms and Effects, Garab, G., Ed., Dordrecht: Kluwer, 1998, vol. 2, pp. 1193-1196.
122. Moubarak-Milad, M. and Stemler, A., Oxidation-Reduction Dependence of Photosystem II Carbonic Anhydrase in Maize Thylakoids, Biochemistry, 1994, vol. 33, pp. 4432-4438.
123. Stemler, A.J., The Case for Chloroplast Thylakoid Carbonic Anhydrase, Physiol. Plant., 1997, vol. 99, pp. 348-353.
124. 2 Concentrating Mechanisms in Algae: Mechanisms, Environmental Modulation, and Evolution, Annu. Rev. Physiol., 2005, vol. 56, pp. 99-131.
125. Pronina, N.A. and Semenenko, V.E., Localization of Membrane-Bound and Soluble Carbonic Anhydrases in Chlorella Cells, Fiziol. Rast. (Moscow), 1984, vol. 31, pp. 241-251 (Sov. Plant Physiol., Engl. Transl.).
126. 2 Concentration in Algal Cells, Current Research in Photosynthesis, Baltcheffsky, M., Ed., Dordrecht: Kluwer, 1990, vol. 4, pp. 489-492.
127. 2 Concentrating Mechanism: Investigation by Means of Photosystem-Deficient and Carbonic Anhydrase-Deficient Mutants of Chlamydomonas reinhardtii, Photosynthetica, 1993, vol. 28, pp. 515-522.
128. 2-Concentrating Mechanism: A Direct Role for Thylakoid Lumen Acidification, Plant, Cell Environ., 1997, vol. 20, pp. 147-154.
129. 2 Uptake, J. Exp. Bot., 1985, vol. 36, pp. 1835-1841.
130. 2 Exchange, J. Exp. Bot., 1985, vol. 36, pp. 1542-1550.
131. 3 Plants: Physics, Physiology, and Rate Limitations, Bot. Rev., 1985, vol. 51, pp. 53-105.
132. 2Effect on Light and Temperature, Aust. J. Plant Physiol., 1991, vol. 10, pp. 75-85.
133. 3 Plants), Moscow: Nauka, 1977.
134. Nobel, P., Plant Cell Physiology: A Physicochemical Approach, San Francisco: Freeman and Co., 1970.
135. 2 Surplus, Prikl. Biokhim. Mikrobiol., 1998, vol. 34, pp. 332-336.
136. Anderson, L.T., Gibbons, J.T., and Wang, X., Distribution of Ten Enzymes of Carbon Metabolism in Pea (Pisum sativum) Chloroplasts, Int. J. Plant Sci., 1996, vol. 157, pp. 525-538.
137. Jebanathirajah, J.A. and Coleman, J.R., Association of Carbonic Anhydrase with a Calvin Cycle Complex in Nicotiana tabacum, Planta, 1998, vol. 204, pp. 177-182.
138. Mori, H., Takabe, T., and Akazawa, T., Loose Association of Ribulose-1,5-Bisphosphate Carboxylase/Oxyganase with Chloroplast Thylakoid Membranes, Photosynth. Res., 1984, vol. 5, pp. 17-28.
139. Makino, A. and Osmond, B., Solubilization of Ribulose-1,5-Bisphosphate Carboxylase from the Membrane Fraction of Pea Leaves, Photosynth. Res., 1991, vol. 29, pp. 79-85.
140. Süss, K.-H., Arkona, C., Manteufel, R., and Adler, K., Calvin Cycle Multienzyme Complexes Are Bound to Chloroplast Thylakoid Membranes of Higher Plants In Situ, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 5514-5518.
141. Aliev, K.A., Vasil'eva, V.N., and Nasyrov, Yu.S., Properties of Free and Membrane-Bound Ribulose-1,5-Bisphosphate Carboxylases during Chloroplast Biogenesis, Fiziol. Rast. (Moscow), 1984, vol. 31, pp. 124-129 (Sov. Plant Physiol., Engl. Transl.).
142. Babadzhanova, M.P., Babadzhanova, M.A., and Aliev, K.A., Free and Membrane-Bound Multienzyme Complexes with Calvin Cycle Activities in Cotton Leaves, Russ. J. Plant Physiol., 2002, vol. 49, pp. 592-597.
143. Chugunova, N.G., Kartashov, I.M., Kholodenko, N.Ya., and Muzafarov, E.N., Effects of Kinetin on Soluble and Membrane-Bound Ribulose-1,5-Bisphosphate Carboxylases in Pea Chloroplasts, Fiziol. Rast. (Moscow), 1993, vol. 40, pp. 16-21 (Sov. Plant Physiol., Engl. Transl.).