Russian Journal of Plant Physiology

, Volume 58, Issue 2, pp 197–209 | Cite as

Carbonic anhydrase: Enzyme that has transformed the biosphere

Reviews

Abstract

The bases of modern type biosphere were laid down about two billion years ago during the predominance of prokaryotes on the Earth. Cyanobacteria changed radically the composition of the Proterozoic atmosphere by saturating it with photosynthetic oxygen. At the same time, large quantities of atmospheric CO2 became sequestered in carbonates owing to mineralization of ancient cyano-bacterial communities; the latter have reached us in the form of laminated limestone deposits, termed stromatolites. The mechanism of carbonate depositing by cyanobacteria is still poorly understood. It is not yet clear whether physiological processes are involved in cell mineralization or if the outer membranes of cyanobacteria serve as a kind of crystallization center and arrange the structure for natural accumulation of sediments. We proposed that a key role in the mechanism of biomineralization belongs to the enzyme carbonic anhydrase (CA), which regulates the equilibrium between the inorganic carbon forms (Ci), including bicarbonate that participates in natural sedimentation of calcium. Since the deposition of calcium carbonate by prokaryotes occurs in the pericellular space and this deposition is controlled by pH, it seems likely that CA, localized on the periphery of cyanobacterial cells, is involved in stabilizing the external pH and in promoting cell mineralization. This review summarizes information concerning possible mechanisms of biogenic calcification (CaCO3 deposition). The function of CA in the living cell and the role of this enzyme in biological processes are considered, and the data on localization of CA in cyano-bacterial cells are presented. Based on available evidence, a scheme is suggested to describe the role of extracellular CA in photosynthetic carbon assimilation and to relate this process with CaCO3 deposition during mineralization of cyanobacteria.

Keywords

cyanobacteria mineralization stromatolites carbonic anhydrase 

Abbreviations

CA

carbonic anhydrase

CCM

CO2-concentrating mechanism

Ci

inorganic carbon (CO2 + HCO3)

References

  1. 1.
    Zavarzin, G.A., Biosphere Formation, Vestn. Ross. Akad. Nauk, 2001, vol. 71, pp. 988–1001.Google Scholar
  2. 2.
    Zavarzin, G.A., Evolution of Geosphere-Biosphere System, Priroda (Moscow), 2003, vol. 1, pp. 27–35.Google Scholar
  3. 3.
    Zavarzin, G.A., Microbial Geochemical Calcium Cycle, Microbiology (Moscow), 2002, vol. 71, pp. 1–17.CrossRefGoogle Scholar
  4. 4.
    Sorokhtin, O.G. and Ushakov, S.A., Razvitie zemli (Earth Development), Moscow: Mosk. Gos. Univ., 2002.Google Scholar
  5. 5.
    Es’kov, K.Yu., Udivitel’naya paleontologiya: istoriya zemli i zhizni na nei (Surprising Paleonthology: Earth History and Life on It), Moscow: ENAS, 2008.Google Scholar
  6. 6.
    Konhauser, K., Biogeochemistry: Deepening the Early Oxygen Debate, Nature GeoSci., 2009, vol. 2, pp. 241–242.CrossRefGoogle Scholar
  7. 7.
    Walter, M.R., Introduction, Stromatolites, Walter, M.R., Ed., Amsterdam: Elsevier, 1976.Google Scholar
  8. 8.
    Sergeev, V.N., Gerasimenko, L.M., and Zavarzin, G.A., The Proterozoic History and Present State of Cyanobacteria, Microbiology (Moscow), 2002, vol. 71, pp. 623–638.CrossRefGoogle Scholar
  9. 9.
    Zavarzin, G.A., Gerasimenko, L.M., and Zhilina, T.N., Cyano-bacterial Communities in Hypersaline Lagoons of the Lake Sivash, Mikrobiologiya, 1993, vol. 62, pp. 1113–1126.Google Scholar
  10. 10.
    Zavarzin, G.A. and Zhilina, T.N., Soda Lake — a Natural Model of the Ancient Biosphere on the Continent, Priroda (Moscow), 2000, vol. 2, pp. 45–55.Google Scholar
  11. 11.
    Gerasimenko, L.M., Mityushina, L.L., and Namsaraev, B.B., Microcoleus Mats from Alcaliphilic and Halophilic Communities, Microbiology (Moscow), 2003, vol. 72, pp. 71–79.CrossRefGoogle Scholar
  12. 12.
    Zavarzin, G.A., Orleanskii, V.K., Gerasimenko, L.M., Pushko, S.N., and Ushatinskaya, G.T., Laboratory Simulationd of Cyano-bacterial Mats of the Alkaline Geochemical Barrier, Microbiology, (Moscow), 2003, vol. 72, pp. 80–85.CrossRefGoogle Scholar
  13. 13.
    Zaitseva, L.V., Orleanskii, V.K., Gerasimenko, L.M., and Ushatinskaya, G.T., Role of Cyano-Bacterium in Crystallization of Magnesia Tiffs, Paleontol. Zh., 2006, vol. 40, pp. 14–20.Google Scholar
  14. 14.
    Stolz, J.F., Feinstein, T.N., Salsi, J., Visscher, P.T., and Reid, R.P., TEM Analysis of Microbial Mediated Sedimentation and Lithification an Modern Marine Stromatolites, Am. Mineral., 2001, vol. 86, pp. 826–833.Google Scholar
  15. 15.
    Bilan, M.I. and Usov, A.I., Polysaccharides in Calcareous Algae and Their Effects Calcification, Bioorg. Khim., 2001, vol. 27, pp. 4–20.PubMedGoogle Scholar
  16. 16.
    Arp, G., Reimer, A., and Reitner, J., Photosynthesis-Induced Biofilm Calcification and Calcium Concentrations in Phanerozoic Oceans, Science, 2001, vol. 292, pp. 1701–1704.PubMedCrossRefGoogle Scholar
  17. 17.
    Planavsky, N., Reid, R.P., Lyons, T.W., Myshrall, K.L., and Visscher, P.T., Formation and Diagenesis of Modern Marine Calcified Cyanobacteria, Geobiology, 2009, vol. 7, pp. 566–576.PubMedCrossRefGoogle Scholar
  18. 18.
    Kupriyanova, E., Villarejo, A., Markelova, A., Gerasimenko, L., Zavarzin, G., Samuelsson, G., Los, D., and Pronina, N., Extracellular Carbonic Anhydrases of the Stromatolite-Forming Cyanobacterium Microcoleus chthonoplastes, Microbiology, 2007, vol. 153, pp. 1149–1156.PubMedCrossRefGoogle Scholar
  19. 19.
    Khalifah, R.G., The Carbon Dioxide Hydration Activity of Carbonic Anhydrase. Stop-Flow Kinetic Studies on the Native Human Isoenzymes B and C, J. Biol. Chem., 1971, vol. 246, pp. 2561–2573.PubMedGoogle Scholar
  20. 20.
    Rabinowitch, E.I., Photosynthesis and Related Processes, New York: Intersciences, 1945, vol. 1.Google Scholar
  21. 21.
    Meldrum, N.N. and Rounghton, F.J.W., Carbonic Anhydrase: Its Preparation and Properties, Nature, 1933, vol. 80, pp. 113–142.Google Scholar
  22. 22.
    Stadie, W.C. and O’Brien, H., The Catalysis of the Hydration of Carbonic Dioxide and Dehydration of Carbonic Acid by the Enzyme from Red Blood Cells, J. Biochem., 1933, vol. 103, pp. 521–529.Google Scholar
  23. 23.
    Neish, A.C., Studies on Chloroplasts. Their Chemical Composition and the Distribution of Certain Metabolites between the Chloroplasts and the Remainder of the Leaf, Biochem. J., 1939, vol. 33, pp. 300–308.PubMedGoogle Scholar
  24. 24.
    Veitch, F.P. and Blankenship, L.C., Carbonic Anhydrase Activity in Bacteria, Nature, 1963, vol. 197, pp. 76–77.PubMedCrossRefGoogle Scholar
  25. 25.
    Karrasch, M., Bott, M., and Thauer, R.K., Carbonic Anhydrase Activity in Acetate Grown Methanosarcina barkeri, Arch. Microbiol., 1989, vol. 151, pp. 137–142.CrossRefGoogle Scholar
  26. 26.
    Hewett-Emmett, D. and Tashian, R.E., Functional Diversity, Conservation and Convergence in the Evolution of α, β and γ-Carbonic Anhydrase Gene Families, Mol. Phylogenet. Evol., 1996, vol. 5, pp. 50–77.PubMedCrossRefGoogle Scholar
  27. 27.
    Coleman, J.R., Carbonic Anhydrase and Its Role in Photosynthesis, Photosynthesis: Physiology and Metabolism, Leegood, R.C., Sharkey, T.D., and Caemmerer, S., Eds., Dordrecht: Kluwer, 2000, pp. 353–367.Google Scholar
  28. 28.
    Smith, K.S. and Ferry, J.G., Prokaryotic Carbonic Anhydrases, FEMS Microbiol. Rev., 2000, vol. 24, pp. 335–366.PubMedCrossRefGoogle Scholar
  29. 29.
    Supuran, C.T., Carbonic Anhydrases: Catalitic and Inhibition Mechanisms, Distribution and Physiological Roles, Carbonic Anhydrase. Its Inhibitors and Activators, Supuran, C.T., Scozzafava, A., and Conway, J., Eds., Boca Raton: CRC, 2004, pp. 1–24.CrossRefGoogle Scholar
  30. 30.
    Ferry, J.G., The Gamma Class of Carbonic Anhydrases, Biochim. Biophys. Acta, 2010, vol. 1804, pp. 374–381.PubMedGoogle Scholar
  31. 31.
    Zimmerman, S.A. and Ferry, J.G., The Beta and Gamma Classes of Carbonic Anhydrase, Curr. Pharm. Des., 2008, vol. 14, pp. 716–721.PubMedCrossRefGoogle Scholar
  32. 32.
    Xu, Y., Feng, L., Jeffrey, P.D., Shi, Y., and Morel, F.M., Structure and Metal Exchange in the Cadmium Carbonic Anhydrase of Marine Diatoms, Nature, 2008, vol. 452, pp. 56–61.PubMedCrossRefGoogle Scholar
  33. 33.
    Mitsuhashi, S., Mizushima, T., Yamashita, E., Yamamoto, M., Kumasaka, T., Moriyama, H., Ueki, T., Miyachi, S., and Tsukihara, T., X-Ray Structure of β-Carbonic Anhydrase from the Red Alga, Porphyridium purpureum, Reveals a Novel Catalytic Site for CO2 Hydration, J. Biol. Chem., 2000, vol. 275, pp. 5521–5526.PubMedCrossRefGoogle Scholar
  34. 34.
    Iverson, T.M., Alber, B.E., Kisker, C., Ferry, J.G., and Rees, D.C., A Closer Look at the Active Site of Gamma-Class Carbonic Anhydrases: High-Resolution Crystallographic Studies of the Carbonic Anhydrase from Methanosarcina thermophila, Biochemistry, 2000, vol. 39, pp. 9222–9231.PubMedCrossRefGoogle Scholar
  35. 35.
    Strop, P., Smith, K.S., Iverson, T.M., Ferry, J.G., and Rees, D.C., Crystal Structure of the “cab”-Type Beta Class Carbonic Anhydrase from the Archaeon Methanobacterium thermoautotrophicum, J. Biol. Chem., 2001, vol. 276, pp. 10 299–10 305.CrossRefGoogle Scholar
  36. 36.
    Supuran, C.T., Carbonic Anhydrases-An Overview, Curr. Pharm. Des., 2008, vol. 14, pp. 603–614.PubMedCrossRefGoogle Scholar
  37. 37.
    Roberts, S.B., Lane, T.W., and Morel, F.M.M., Carbonic Anhydrase in the Marine Diatom Thalassiosira weissflogii (Bacillariophyceae), J. Phycol., 1997, vol. 33, pp. 845–850.CrossRefGoogle Scholar
  38. 38.
    Cox, E.H., McLendon, G.L., Morel, F.M., Lane, T.W., Prince, R.C., Pickering, I.J., and George, G.N., The Active Site Structure of Thalassiosira weissflogii Carbonic Anhydrase 1, Biochemistry, 2000, vol. 39, pp. 12128–12130.PubMedCrossRefGoogle Scholar
  39. 39.
    Soto, A.R., Zheng, H., Shoemaker, D., Rodriguez, J., Read, B.A., and Wahlund, T.M., Identification and Preliminary Characterization of Two cDNAs Encoding Unique Carbonic Anhydrases from the Marine Alga Emiliania huxleyi, Appl. Environ. Microbiol., 2006, vol. 72, pp. 5500–5511.PubMedCrossRefGoogle Scholar
  40. 40.
    Lapointe, M., Mackenzie, T.D., and Morse, D., An External Delta-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition, Plant Physiol., 2008, vol. 147, pp. 1427–1436.PubMedCrossRefGoogle Scholar
  41. 41.
    McGinn, P.J. and Morel, F.M., Expression and Regulation of Carbonic Anhydrases in the Marine Diatom Thalassiosira pseudonana and in Natural Phytoplankton Assemblages from Great Bay, New Jersey, Physiol. Plant., 2008, vol. 133, pp. 78–91.PubMedCrossRefGoogle Scholar
  42. 42.
    So, A.K., Espie, G.S., Williams, E.B., Shively, J.M., Heinhorst, S., and Cannon, G.C., A Novel Evolutionary Lineage of Carbonic Anhydrase (Epsilon Class) Is a Component of the Carboxysome Shell, J. Bacteriol., 2004, vol. 186, pp. 623–630.PubMedCrossRefGoogle Scholar
  43. 43.
    Sawaya, M.R., Cannon, G.C., Heinhorst, S., Tanaka, S., Williams, E.B., Yeates, T.O., and Kerfeld, C.A., The Structure of Beta-Carbonic Anhydrase from the Carboxysomal Shell Reveals a Distinct Subclass with One Active Site for the Price of Two, J. Biol. Chem., 2006, vol. 17, pp. 7546–7555.CrossRefGoogle Scholar
  44. 44.
    Henry, R.P., Multiple Roles of Carbonic Anhydrase in Cellular Transport and Metabolism, Annu. Rev. Physiol., 1996, vol. 58, pp. 523–538.PubMedCrossRefGoogle Scholar
  45. 45.
    Kozliak, E.I., Guilloton, M.B., Fuchs, J.A., and Anderson, P.M., Bacterial Carbonic Anhydrases, EXS, 2000, vol. 90, pp. 547–565.PubMedGoogle Scholar
  46. 46.
    Pronina, N.A., The Organization and Physiological Role of the CO2-CM in Microalgal Photosynthesis, Russ. J. Plant Physiol., 2000, vol. 47, pp. 706–714.Google Scholar
  47. 47.
    Raven, J.A., Photosynthetic and Non-Photosynthetic Roles of Carbonic Anhydrase in Algae and Cyanobacteria, Phycologia, 1995, vol. 34, pp. 93–101.CrossRefGoogle Scholar
  48. 48.
    Supuran, C.T., Carbonic Anhydrases as Drug Targets — An Overview, Curr. Top. Med. Chem., 2007, vol. 7, pp. 825–833.PubMedCrossRefGoogle Scholar
  49. 49.
    Badger, M.R. and Price, G.D., CO2 Concentrating Mechanisms in Cyanobacteria: Molecular Components, Their Diversity and Evolution, J. Exp. Bot., 2003, vol. 54, pp. 609–622.PubMedCrossRefGoogle Scholar
  50. 50.
    Holtum, J.A.M., Summons, R., Roeske, C.A., Comins, H.N., and Oleary, M.H., Oxygen-18 Incorporation into Malic-Acid during Nocturnal Carbon Dioxide Fixation in Crassulacean Acid Metabolism Plants: A New Approach to Estimating In Vivo Carbonic Anhydrase Activity, J. Biol. Chem., 1984, vol. 259, pp. 6870–6881.PubMedGoogle Scholar
  51. 51.
    Badger, M.R., Kaplan, A., and Berry, J.A., Internal Inorganic Carbon Pool of Chlamydomonas reinhardtii. Evidence for a Carbon Dioxide Concentrating Mechanism, Plant Physiol., 1980, vol. 66, pp. 407–413.PubMedCrossRefGoogle Scholar
  52. 52.
    Pronina, N.A., Avramova, S., Georgiev, D., and Semenenko, V.E., Dynamics of Carbonic Anhydrase Activity in Chlorella and Scenedesmus during Cell Adaptation to High Light and Low CO2 Concentration, Sov. Plant Physiol., 1981, vol. 28, pp. 43–52.Google Scholar
  53. 53.
    Aizawa, K. and Miyachi, S., Carbonic Anhydrase and CO2-Concentrating Mechanism in Microalgae and Cyanobacteria, Fed. Eur. Microbiol. Soc., Microbiol. Rev., 1986, vol. 39, pp. 215–233.Google Scholar
  54. 54.
    Price, G.D., Badger, M.R., Woodger, F.J., and Long, B.M., Advances in Understanding the Cyanobacterial CO2-Concentrating Mechanism (CCM): Functional Components, Ci Transporters, Diversity, Genetic Regulation and Prospects for Engineering into Plants, J. Exp. Bot., 2008, vol. 59, pp. 1441–1461.PubMedCrossRefGoogle Scholar
  55. 55.
    Moroney, J.V. and Ynalvez, R.A., Proposed Carbon Dioxide Concentrating Mechanism in Chlamydomonas reinhardtii, Eukaryotic Cell, 2007, vol. 6, pp. 1251–1259.PubMedCrossRefGoogle Scholar
  56. 56.
    Spalding, M.H., Microalgal Carbon-Dioxide-Concentrating Mechanisms: Chlamydomonas Inorganic Carbon Transporters, J. Exp. Bot., 2008, vol. 59, pp. 1463–1473.PubMedCrossRefGoogle Scholar
  57. 57.
    Kupriyanova, E.V., Lebedeva, N.V., Dudoladova, M.V., Gerasimenko, L.M., Alekseeva, S.G., Pronina, N.A., and Zavarzin, G.A., Carbonic Anhydrase Activity of Alkaliphilic Cyanobacteria from Soda Lakes, Russ. J. Plant Physiol., 2003, vol. 50, pp. 532–539.CrossRefGoogle Scholar
  58. 58.
    Markelova, A.G., Sinetova, M.P., Kupriyanova, E.V., and Pronina, N.A., Distribution and Functional Role of Carbonic Anhydrase Cah3 Associated with Thylakoid Membranes in the Chloroplast and Pyrenoid of Chlamydomonas reinhardtii, Russ. J. Plant Physiol., 2009, vol. 56, pp. 761–768.CrossRefGoogle Scholar
  59. 59.
    Drews, G. and Niklowitz, W., Cytology of Cyanophycea. II. Centroplasm and Granular Inclusions of Phormidium uncinatum, Arch. Mikrobiol., 1956, vol. 24, pp. 147–162.PubMedCrossRefGoogle Scholar
  60. 60.
    Yeates, T.O., Kerfeld, C.A., Heinhorst, S., Cannon, G.C., and Shively, J.M., Protein-Based Organelles in Bacteria: Carboxysomes and Related Microcompartments, Nat. Rev. Microbiol., 2008, vol. 6, pp. 681–691.PubMedCrossRefGoogle Scholar
  61. 61.
    Markelova, A.G., Vladimirova, M.G., and Semenenko, V.E., Ultrastructural Localization of RBC in Algal Cells, Sov. Plant Physiol., 1990, vol. 37, pp. 907–911.Google Scholar
  62. 62.
    Karlsson, J., Clarke, A.K., Chen, Z.Y., Hugghin, S.Y., Par, Y.I., Husic, H.D., Moroney, J.V., and Samuelsson, G., A Novel Alpha-Type Carbonic Anhydrase Associated with the Thylakoid Membrane in Chlamydomonas reinhardtii Is Required at Ambient CO2, EMBO J., 1998, vol. 17, pp. 1208–1216.PubMedCrossRefGoogle Scholar
  63. 63.
    Park, Y.I., Karlsson, J., Rojdestvenski, I., Pronina, N., Klimov, V., Oquist, G., and Samuelsson, G., Role of a Novel Photosystem II-Associated Carbonic Anhydrase in Photosynthetic Carbon Assimilation in Chlamydomonas reinhardtii, FEBS Lett., 1999, vol. 444, pp. 102–105.PubMedCrossRefGoogle Scholar
  64. 64.
    South, G.R. and Whittick, A., Introduction to Phycology, Oxford: Blackwell, 1987.Google Scholar
  65. 65.
    Quinn, P., Bowers, R.M., Zhang, X., Wahlund, T.M., Fanelli, M.A., Olszova, D., and Read, B.A., cDNA Microarrays as a Tool for Identification of Biomineralization Proteins in the Coccolithophorid Emiliania huxleyi (Haptophyta), Appl. Environ. Microbiol., 2006, vol. 72, pp. 5512–5526.PubMedCrossRefGoogle Scholar
  66. 66.
    Furla, P., Galgani, I., Durand, I., and Allemand, D., Sources and Mechanisms of Inorganic Carbon Transport for Coral Calcification and Photosynthesis, J. Exp. Biol., 2000, vol. 203, pp. 3445–3457.PubMedGoogle Scholar
  67. 67.
    Moya, A., Tambutté, S., Bertucci, A., Tambutté, E., Lotto, S., Vullo, D., Supuran, C.T., Allemand, D., and Zoccola, D., Carbonic Anhydrase in the Scleractinian Coral Stylophora pistillata: Characterization, Localization, and Role in Biomineralization, J. Biol. Chem., 2008, vol. 283, pp. 25475–25484.PubMedCrossRefGoogle Scholar
  68. 68.
    Soltes-Rak, E., Mulligan, M.E., and Coleman, J.R., Identification and Characterization of Gene Encoding a Vertebrate-Type Carbonic Anhydrase in Cyanobacteria, J. Bacteriol., 1997, vol. 179, pp. 769–774.PubMedGoogle Scholar
  69. 69.
    So, A.K., Spall, N.G.S., Coleman, J.R., and Espie, O.S., Catalytic Exchange of 18O from 13C18O-Labelled CO2 by Wild Type Cells and ecaA, ecaB, and ccaA Mutants of the Cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803, Can. J. Bot., 1998, vol. 76, pp. 1153–1160.CrossRefGoogle Scholar
  70. 70.
    Dudoladova, M.V., Kupriyanova, E.V., Markelova, A.G., Sinetova, M.P., Allakhverdiev, S.I., and Pronina, N.A., The Thylakoid Carbonic Anhydrase Associated with Photosystem II Is the Component of Inorganic Carbon Accumulating System in Cells of Halo- and Alkaliphilic Cyanobacterium Rhabdoderma lineare, Biochim. Biophys. Acta, 2007, vol. 1767, pp. 616–623.PubMedCrossRefGoogle Scholar
  71. 71.
    Fukuzawa, H., Suzuki, E., Komukai Y., and Miyachi, S., A Gene Homologous to Chloroplast Carbonic Anhydrase (icfA) Is Essential to Photosynthetic Carbon Dioxide Fixation by Synechococcus PCC7942, Proc. Natl. Acad. Sci. USA, 1992, vol. 89, pp. 4437–4441.PubMedCrossRefGoogle Scholar
  72. 72.
    So, A.K. and Espie, G.S., Cloning, Characterization and Expression Carbonic Anhydrase from the Cyanobacterium Synechocystis PCC6803, Plant Mol. Biol., 1998, vol. 37, pp. 205–215.PubMedCrossRefGoogle Scholar
  73. 73.
    Price, G.D., Howitt, S.M., Harrison, K., and Badger, M.R., Analysis of a Genomic DNA Region from the Cyanobacterium Synechococcus sp. Strain PCC7942 Involved in Carboxysome Assembly and Function, J. Bacteriol., 1993, vol. 175, pp. 2871–2879.PubMedGoogle Scholar
  74. 74.
    Price, G.D., Sultemeyer, D., Klughammer, B., Ludwig, M., and Badger, M.R., The Functioning of the CO2-Concentrating Mechanism in Several Cyanobacterial Strains: A Review of General Physiological Characteristics, Genes, Proteins and Recent Advances, Can. J. Bot., 1998, vol. 76, pp. 973–1002.CrossRefGoogle Scholar
  75. 75.
    Peña, K.L., Castel, S.E., de Araujo, C., Espie, G.S., and Kimber, M.S., Structural Basis of the Oxidative Activation of the Carboxysomal Gamma-Carbonic Anhydrase, CcmM, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 2455–2460.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations