Russian Journal of Plant Physiology

, Volume 51, Issue 1, pp 127–137 | Cite as

Aquaporins: Structure, Systematics, and Regulatory Features

  • A. Yu. Shapiguzov


The review describes current views on the molecular structure, systematics, and functional regulation of aquaporins. These recently discovered channel proteins play a principal role in water transport across cell membranes in the majority of living organisms.

aquaporins cell membranes water relations 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Tyerman, S., Bohnert, H., Maurel, C., Steudle, E., and Smith, J., Plant Aquaporins: Their Molecular Biology, Biophysics and Significance for Plant Water Relations, J. Exp. Bot., 1999, vol. 50, pp. 1055-1071.Google Scholar
  2. 2.
    Chrispeels, M., Crawford, N., and Schroeder, J., Proteins for Transport of Water and Mineral Nutrients across the Membranes of Plant Cells, Plant Cell, 1999, vol. 11, pp. 661-676.Google Scholar
  3. 3.
    Agre, P., Preston, G., Smith, B., Jung, J., Raina, S., Moon, C., Guggino, W., and Nielsen, S., Aquaporin CHIP: The Archetypal Molecular Water Channel, Am. J. Physiol., 1993, vol. 265, pp. 463-476.Google Scholar
  4. 4.
    Moura, T., Macey, R., Chien, D., Karan, D., and Santos, H., Thermodynamics of All-or-None Water Channel Closure in Red Cells, J. Membr. Biol., 1984, vol. 81, pp. 105-11.Google Scholar
  5. 5.
    Denker, B., Smith, B., Kuhajda, F., and Agre, P., Identification, Purification, and Partial Characterization of a Novel Mr 28.000 Integral Membrane Protein from Erythrocytes and Renal Tubules, J. Biol. Chem., 1988, vol. 263, pp. 15634-15642.Google Scholar
  6. 6.
    Preston, G. and Agre, P., Isolation of the cDNA for Erythrocyte Integral Membrane Protein of 28 Kilodaltons: Member of an Ancient Channel Family, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 11110-11114.Google Scholar
  7. 7.
    Gorin, M., Yancey, S., Cline, J., Revel, J., and Horwitz, J., The Major Intrinsic Protein (MIP) of the Bovine Lens Fiber Membrane: Characterization and Structure Based on cDNA Cloning, Cell, 1984, vol. 39, pp. 49-59.Google Scholar
  8. 8.
    Johnson, K., Herman, E., and Chrispeels, M., An Abundant, Highly Conserved Tonoplast Protein in Seeds, Plant Physiol., 1992, vol. 91, pp. 1006-1013.Google Scholar
  9. 9.
    Agre, P., Molecular Physiology of Water Transport: Aquaporin Nomenclature Workshop. Mammalian Aquaporins, Biol. Cell, 1997, vol. 89, pp. 255-257.Google Scholar
  10. 10.
    Reizer, J., Reizer, A., and Saier, M., Jr., The MIP Family of Integral Membrane Channel Proteins: Sequence Comparisons, Evolutionary Relationships, Reconstructed Pathway of Evolution and Proposed Functional Differentiation of the Two Repeated Halves of the Proteins, Crit. Rev. Biochem. Mol. Biol., 1993, vol. 28, pp. 235-257.Google Scholar
  11. 11.
    Weig, A., Deswarte, C., and Chrispeels, M., The Major Intrinsic Protein Family of Arabidopsis Has 23 Members That Form Three Distinct Groups with Functional Aquaporins in Each Group, Plant Physiol., 1997, vol. 114, pp. 1347-1357.Google Scholar
  12. 12.
    Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjovall, S., Fraysse, L., Weig, A., and Kjellbom, P., The Complete Set of Genes Encoding Major Intrinsic Proteins in Arabidopsis Provides a Framework for a New Nomenclature for Major Intrinsic Proteins in Plants, Plant Physiol., 2001, vol. 126, pp. 1358-1369.Google Scholar
  13. 13.
    Quigley, F., Rosenberg, J., Shachar-Hill, Y., and Bohnert, H., From Genome to Function: The Arabidopsis Aquaporins, Genome Biol., 2002, vol. 3, pp. RESEARCH0001.Google Scholar
  14. 14.
    Chaumont, F., Barrieu, F., Wojcik, E., Chrispeels, M., and Jung, R., Aquaporins Constitute a Large and Highly Divergent Protein Family in Maize, Plant Physiol., 2001, vol. 125, pp. 1206-1215.Google Scholar
  15. 15.
    Verkman, A., Water Permeability Measurement in Living Cells and Complex Tissues, J. Membr. Biol., 2000, vol. 173, pp. 73-87.Google Scholar
  16. 16.
    Fischbarg, J., Kuang, K., Vera, J., Arant, S., Silverstein, S., Loike, J., and Rosen, O., Glucose Transporters Serve as Water Channels, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, pp. 3244-3247.Google Scholar
  17. 17.
    Zeidel, M., Nielsen, S., Smith, B., Ambudkar, S., Maunsbach, A., and Agre, P., Ultrastructure, Pharmacologic Inhibition, and Transport Selectivity of Aquaporin Channel-Forming Integral Protein in Proteoliposomes, Biochemistry, 1994, vol. 33, pp. 1606-1615.Google Scholar
  18. 18.
    Zeidel, M., Ambudkar, S., Smith, B., and Agre, P., Reconstitution of Functional Water Channels in Liposomes Containing Purified Red Cell CHIP28 Protein, Biochemistry, 1992, vol. 31, pp. 7436-7440.Google Scholar
  19. 19.
    Cheng, A., van Hoek, A., Yeager, M., Verkman, A., and Mitra, A., Three-Dimensional Organization of a Human Water Channel, Nature, 1997, vol. 387, pp. 627-630.Google Scholar
  20. 20.
    Meinild, A., Klaerke, D., and Zeuthen, T., Bidirectional Water Fluxes and Specificity for Small Hydrophilic Molecules in Aquaporins 0–5, J. Biol. Chem., 1998, vol. 273, pp. 32 446-32 451.Google Scholar
  21. 21.
    Maurel, C., Reizer, J., Schroeder, J., and Chrispeels, M. The Vacuolar Membrane Protein Gamma-TIP Creates Water Specific Channels in Xenopus Oocytes, EMBO J., 1993, vol. 12, pp. 2241-2247.Google Scholar
  22. 22.
    Pohl, P., Saparov, S., Borgnia, M., and Agre, P., Highly Selective Water Channel Activity Measured by Voltage Clamp: Analysis of Planar Lipid Bilayers Reconstituted with Purified AqpZ, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 9624-9629.Google Scholar
  23. 23.
    Preston, G., Jung, J., Guggino, W., and Agre, P., The Mercury-Sensitive Residue at Cysteine 189 in the CHIP28 Water Channel, J. Biol. Chem., 1993, vol. 268, pp. 17-20.Google Scholar
  24. 24.
    Daniels, M., Chaumont, F., Mirkov, T., and Chrispeels, M., Characterization of a New Vacuolar Membrane Aquaporin Sensitive to Mercury at a Unique Site, Plant Cell, 1996, vol. 8, pp. 587-599.Google Scholar
  25. 25.
    Barone, L., Shih, C., and Wasserman, B., Mercury-Induced Conformational Changes and Identification of Conserved Surface Loops in Plasma Membrane Aquaporins from Higher Plants. Topology of PMIP31 from Beta vulgaris L., J. Biol. Chem., 1997, vol. 272, pp. 30672-30677.Google Scholar
  26. 26.
    Borgnia, M. and Agre, P., Reconstitution and Functional Comparison of Purified GlpF and AqpZ, the Glycerol and Water Channels from Escherichia coli, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 2888-2893.Google Scholar
  27. 27.
    Cooper, G., Zhou, Y., Bouyer, P., Grichtchenko, I., and Boron, W., Transport of Volatile Solutes through AQP1, J. Physiol., 2002, vol. 542, pp. 17-29.Google Scholar
  28. 28.
    Rivers, R., Dean, R., Chandy, G., Hall, J., Roberts, D., and Zeidel, M., Functional Analysis of Nodulin 26, an Aquaporin in Soybean Root Nodule Symbiosomes, J. Biol. Chem., 1997, vol. 272, pp. 16256-16261.Google Scholar
  29. 29.
    Otto, B. and Kaldenhoff, R., Cell-Specific Expression of the Mercury-Insensitive Plasma-Membrane Aquaporin NtAQP1 from Nicotiana tabacum, Planta, 2000, vol. 211, pp. 167-172.Google Scholar
  30. 30.
    Borgnia, M., Nielsen, S., Engel, A., and Agre, P., Cellular and Molecular Biology of the Aquaporin Water Channels, Annu. Rev. Biochem., 1999, vol. 68, pp. 425-458.Google Scholar
  31. 31.
    Henzler, T. and Steudle, E., Transport and Metabolic Degradation of Hydrogen Peroxide in Chara corallina: Model Calculations and Measurements with the Pressure Probe Suggest Transport of H2O2 across Water Channels, J. Exp. Bot., 2000, vol. 51, pp. 2053-2066.Google Scholar
  32. 32.
    Nakhoul, N., Davis, B., Romero, M., and Boron, W., Effect of Expressing the Water Channel Aquaporin-1 on the CO2 Permeability of Xenopus Oocytes, Am. J. Physiol., 1998, vol. 274, pp. 543-548.Google Scholar
  33. 33.
    Yang, B., Fukuda, N., van Hoek, A., Matthay, M., Ma, T., and Verkman, A., Carbon Dioxide Permeability of Aquaporin-1 Measured in Erythrocytes and Lung of Aquaporin-1 Null Mice and in Reconstituted Proteoliposomes, J. Biol. Chem., 2000, vol. 275, pp. 2686-2692.Google Scholar
  34. 34.
    Fang, X., Yang, B., Matthay, M., and Verkman, A., Evidence against Aquaporin-1-Dependent CO2 Permeability in Lung and Kidney, J. Physiol., 2002, vol. 542, pp. 63-69.Google Scholar
  35. 35.
    Tchernov, D., Helman, Y., Keren, N., Luz, B., Ohad, I., Reinhold, L., Ogawa, T., and Kaplan, A., Passive Entry of CO2 and Its Energy-Dependent Intracellular Conversion to HCO3 in Cyanobacteria Are Driven by a Photosystem I-Generated DeltamuH+, J. Biol. Chem., 2001, vol. 276, pp. 23450-23455.Google Scholar
  36. 36.
    Terashima, I. and Ono, K., Effects of HgCl2 on CO2 Dependence of Leaf Photosynthesis: Evidence Indicating Involvement of Aquaporins in CO2 Diffusion across the Plasma Membrane, Plant Cell Physiol., 2002, vol. 43, pp. 70-78.Google Scholar
  37. 37.
    Reuss, L., Focus on “Effect of Expressing the Water Channel Aquaporin-1 on the CO2 Permeability of Xenopus Oocytes,” Am. J. Physiol., 1998, vol. 274, pp. 297-298.Google Scholar
  38. 38.
    Anthony, T., Brooks, H., Boassa, D., Leonov, S., Yanochko, G., Regan, J., and Yool, A., Cloned Human Aquaporin-1 Is a Cyclic GMP-Gated Ion Channel, Mol. Pharmacol., 2000, vol. 57, pp. 576-588.Google Scholar
  39. 39.
    Boassa, D. and Yool, A., A Fascinating Tail: cGMP Activation of Aquaporin-1 Ion Channels, Trends Pharmacol. Sci., 2002, vol. 23, pp. 558-562.Google Scholar
  40. 40.
    Zampighi, G., Hall, J., and Kreman, M., Purified Lens Junctional Protein Forms Channels in Planar Lipid Films, Proc. Natl. Acad. Sci. USA, 1985, vol. 82, pp. 8468-8472.Google Scholar
  41. 41.
    Ehring, G., Zampighi, G., Horwitz, J., Bok, D., and Hall, J., Properties of Channels Reconstituted from the Major Intrinsic Protein of Lens Fiber Membranes, J. Gen. Physiol., 1990, vol. 96, pp. 631-664.Google Scholar
  42. 42.
    Modesto, E., Lampe, P., Ribeiro, M., Spray, D., and Campos de Carvalho, A., Properties of Chicken Lens MIP Channels Reconstituted into Planar Lipid Bilayers, J. Membr. Biol., 1996, vol. 154, pp. 239-249.Google Scholar
  43. 43.
    Yasui, M., Hazama, A., Kwon, T., Nielsen, S., Guggino, W., and Agre, P., Rapid Gating and Anion Permeability of an Intracellular Aquaporin, Nature, 1999, vol. 402, pp. 184-187.Google Scholar
  44. 44.
    Ikeda, M., Beitz, E., Kozono, D., Guggino, W., Agre, P., and Yasui, M., Characterization of Aquaporin-6 as a Nitrate Channel in Mammalian Cells. Requirement of Pore-Lining Residue Threonine 63, J. Biol. Chem., 2002, vol. 277, pp. 39873-39879.Google Scholar
  45. 45.
    Weaver, C., Shomer, N., Louis, C., and Roberts, D., Nodulin 26, a Nodule-Specific Symbiosome Membrane Protein from Soybean, Is an Ion Channel, J. Biol. Chem., 1994, vol. 269, pp. 17858-17862.Google Scholar
  46. 46.
    Bill, R., Hedfalk, K., Karlgren, S., Mullins, J., Rydstrom, J., and Hohmann, S., Analysis of the Pore of the Unusual Major Intrinsic Protein Channel, Yeast Fps1p, J. Biol. Chem., 2001, vol. 276, pp. 36543-36549.Google Scholar
  47. 47.
    Scheuring, S., Ringler, P., Borgnia, M., Stahlberg, H., Muller, D., Agre, P., and Engel, A., High Resolution AFM Topographs of the Escherichia coli Water Channel Aquaporin Z, EMBO J., 1999, vol. 18, pp. 4981-4987.Google Scholar
  48. 48.
    Verbavatz, J., Brown, D., Sabolic, I., Valenti, G., Ausiello, D., van Hoek, A., Ma, T., and Verkman, A., Tetrameric Assembly of CHIP28 Water Channels in Liposomes and Cell Membranes: A Freeze-Fracture Study, J. Cell Biol., 1993, vol. 123, pp. 605-618.Google Scholar
  49. 49.
    Eskandari, S., Wright, E., Kreman, M., Starace, D., and Zampighi, G., Structural Analysis of Cloned Plasma Membrane Proteins by Freeze-Fracture Electron Microscopy, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11235-11240.Google Scholar
  50. 50.
    Fu, D., Libson, A., Miercke, L., Weitzman, C., Nollert, P., Krucinski, J., and Stroud, R., Structure of a Glycerol-Conducting Channel and the Basis for Its Selectivity, Science, 2000, vol. 290, pp. 481-486.Google Scholar
  51. 51.
    Sui, H., Walian, P., Tang, G., Oh, A., and Jap, B., Crystallization and Preliminary X-Ray Crystallographic Analysis of Water Channel AQP1, Acta Crystallogr. D. Biol. Crystallogr., 2000, vol. 56, pp. 1198-1200.Google Scholar
  52. 52.
    Sui, H., Han, B., Lee, J., Walian, P., and Jap, B., Structural Basis of Water-Specific Transport through the AQP1 Water Channel, Nature, 2001, vol. 414, pp. 872-878.Google Scholar
  53. 53.
    De Groot, B., Engel, A., and Grubmuller, H., The Structure of the Aquaporin-1 Water Channel: A Comparison between Cryo-Electron Microscopy and X-Ray Crystallography, J. Mol. Biol., 2003, vol. 325, pp. 485-493.Google Scholar
  54. 54.
    Thomas, D., Bron, P., Ranchy, G., Duchesne, L., Cavalier, A., Rolland, J., Raguenes-Nicol, C., Hubert, J., Haase, W., and Delamarche, C., Aquaglyceroporins: One Channel for Two Molecules, Biochim. Biophys. Acta, 2002, vol. 1555, pp. 181-186.Google Scholar
  55. 55.
    Jensen, M., Tajkhorshid, E., and Schulten, K., The Mechanism of Glycerol Conduction in Aquaglyceroporins, Structure (Cambridge), 2001, vol. 9, pp. 1083-1093.Google Scholar
  56. 56.
    Tajkhorshid, E., Nollert, P., Jensen, M., Miercke, L., O'Connell, J., Stroud, R., and Schulten, K., Control of the Selectivity of the Aquaporin Water Channel Family by Global Orientational Tuning, Science, 2002, vol. 296, pp. 525-530.Google Scholar
  57. 57.
    Kong, Y. and Ma, J., Dynamic Mechanisms of the Membrane Water Channel Aquaporin-1 (AQP1), Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 14345-14349.Google Scholar
  58. 58.
    Kozono, D., Ding, X., Iwasaki, I., Meng, X., Kamagata, Y., Agre, P., and Kitagawa, Y., Functional Expression and Characterization of an Archaeal Aquaporin: AqpM from Methanothermobacter marburgensis, J. Biol. Chem., 2003, vol. 278, pp. 10649-10656.Google Scholar
  59. 59.
    Park, J. and Saier, M., Jr., Phylogenetic Characterization of the MIP Family of Transmembrane Channel Proteins, J. Membr. Biol., 1996, vol. 153, pp. 171-180.Google Scholar
  60. 60.
    Heymann, J. and Engel, A., Aquaporins: Phylogeny, Structure, and Physiology of Water Channels, News Physiol. Sci., 1999, vol. 14, pp. 187-193.Google Scholar
  61. 61.
    Zardoya, R. and Villalba, S., A Phylogenetic Framework for the Aquaporin Family in Eukaryotes, J. Mol. Evol., 2001, vol. 52, pp. 391-404.Google Scholar
  62. 62.
    Echevarria, M. and Ilundain, A., Aquaporins, J. Physiol. Biochem., 1998, vol. 54, pp. 107-118.Google Scholar
  63. 63.
    Liu, Z., Shen, J., Carbrey, J., Mukhopadhyay, R., Agre, P., and Rosen, B., Arsenite Transport by Mammalian Aquaglyceroporins AQP7 and AQP9, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 6053-6058.Google Scholar
  64. 64.
    Fu, D., Libson, A., and Stroud, R., The Structure of GlpF, a Glycerol Conducting Channel, Novartis. Found. Symp., 2002, vol. 245, pp. 51-61.Google Scholar
  65. 65.
    Elkjaer, M., Nejsum, L., Gresz, V., Kwon, T., Jensen, U., Frokiaer, J., and Nielsen, S., Immunolocalization of Aquaporin-8 in Rat Kidney, Gastrointestinal Tract, Testis, and Airways, Am. J. Physiol. Renal Physiol., 2001, vol. 281, pp. F1047-F1057.Google Scholar
  66. 66.
    Hohmann, I., Bill, R., Kayingo, I., and Prior, B., Microbial MIP Channels, Trends Microbiol., 2000, vol. 8, pp. 33-38.Google Scholar
  67. 67.
    Chaumont, F., Barrieu, F., Jung, R., and Chrispeels, M., Plasma Membrane Intrinsic Proteins from Maize Cluster in Two Sequence Subgroups with Differential Aquaporin Activity, Plant Physiol., 2000, vol. 122, pp. 1025-1034.Google Scholar
  68. 68.
    Maurel, C., Tacnet, F., Guclu, J., Guern, J., and Ripoche, P., Purified Vesicles of Tobacco Cell Vacuolar and Plasma Membranes Exhibit Dramatically Different Water Permeability and Water Channel Activity, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 7103-7108.Google Scholar
  69. 69.
    Jauh, G., Fischer, A., Grimes, H., Ryan, C., Jr., and Rogers, J., Delta-Tonoplast Intrinsic Protein Defines Unique Plant Vacuole Functions, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 12995-12999.Google Scholar
  70. 70.
    Jauh, G., Phillips, T., and Rogers, J., Tonoplast Intrinsic Protein Isoforms as Markers for Vacuolar Functions, Plant Cell, 1999, vol. 11, pp. 1867-1882.Google Scholar
  71. 71.
    Karlsson, M., Johansson, I., Bush M., McCann, M., Maurel, C., Larsson, C., and Kjellbom, P., An Abundant TIP Expressed in Mature Highly Vacuolated Cells, Plant J., 2000, vol. 21, pp. 83-90.Google Scholar
  72. 72.
    Johanson, U. and Gustavsson, S., A New Subfamily of Major Intrinsic Proteins in Plants, Mol. Biol. Evol., 2002, vol. 19, pp. 456-461.Google Scholar
  73. 73.
    Wallace, I., Wills, D., Guenther, J., and Roberts, D., Functional Selectivity for Glycerol of the Nodulin 26 Subfamily of Plant Membrane Intrinsic Proteins, FEBS Lett., 2002, vol. 523, pp. 109-112.Google Scholar
  74. 74.
    Zardoya, R., Ding, X., Kitagawa, Y., and Chrispeels, M., Origin of Plant Glycerol Transporters by Horizontal Gene Transfer and Functional Recruitment, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 14893-14896.Google Scholar
  75. 75.
    Johansson, I., Larsson, C., Ek, B., and Kjellbom, P., The Major Integral Proteins of Spinach Leaf Plasma Membranes Are Putative Aquaporins and Are Phosphorylated in Response to Ca2+ and Apoplastic Water Potential, Plant Cell, 1996, vol. 8, pp. 1181-1191.Google Scholar
  76. 76.
    Phillips, A. and Huttly, A., Cloning of Two Gibberellin-Regulated cDNAs from Arabidopsis thaliana by Subtractive Hybridization: Expression of the Tonoplast Water Channel, Gamma-TIP, Is Increased by GA3, Plant Mol. Biol., 1994, vol. 24, pp. 603-615.Google Scholar
  77. 77.
    Kaldenhoff, R., Kolling, A., and Richter, G., Regulation of the Arabidopsis thaliana Aquaporin Gene AthH2 (PIP1b), J. Photochem. Photobiol. B., 1996, vol. 36, pp. 351-354.Google Scholar
  78. 78.
    Suga, S., Komatsu, S., and Maeshima, M., Aquaporin Isoforms Responsive to Salt and Water Stresses and Phytohormones in Radish Seedlings, Plant Cell Physiol., 2002, vol. 43, pp. 1229-1237.Google Scholar
  79. 79.
    Yamada, S., Katsuhara, M., Kelly, W., Michalowski, C., and Bohnert, H., A Family of Transcripts Encoding Water Channel Proteins: Tissue-Specific Expression in the Common Ice Plant, Plant Cell, 1995, vol. 7, pp. 1129-1142.Google Scholar
  80. 80.
    Morillon, R., Catterou, M., Sangwan, R., Sangwan, B., and Lassalles, J., Brassinolide May Control Aquaporin Activities in Arabidopsis thaliana, Planta, 2001, vol. 212, pp. 199-204.Google Scholar
  81. 81.
    Yamamoto, Y., Taylor, C., Acedo, G., Cheng, C., and Conkling, M., Characterization of Cis-Acting Sequences Regulating Root-Specific Gene Expression in Tobacco, Plant Cell, 1991, vol. 3, pp. 371-82.Google Scholar
  82. 82.
    Siefritz, F., Biela, A., Eckert, M., Otto, B., Uehlein, N., and Kaldenhoff, R., The Tobacco Plasma Membrane Aquaporin NtAQP1, J. Exp. Bot., 2001, vol. 52, pp. 1953-1957.Google Scholar
  83. 83.
    Morillon, R. and Chrispeels, M., The Role of ABA and the Transpiration Stream in the Regulation of the Osmotic Water Permeability of Leaf Cells, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 14138-14143.Google Scholar
  84. 84.
    Ohshima, Y., Iwasaki, I., Suga, S., Murakami, M., Inoue, K., and Maeshima, M., Low Aquaporin Content and Low Osmotic Water Permeability of the Plasma and Vacuolar Membranes of a CAM Plant Graptopetalum paraguayense: Comparison with Radish, Plant Cell Physiol., 2001, vol. 42, pp. 1119-1129.Google Scholar
  85. 85.
    Sarda, X., Tousch, D., Ferrare, K., Legrand, E., Dupuis, J., Casse-Delbart, F., and Lamaze, T., Two TIP-Like Genes Encoding Aquaporins Are Expressed in Sunflower Guard Cells, Plant J., 1997, vol. 12, pp. 1103-1111.Google Scholar
  86. 86.
    Weaver, C., Crombie, B., Stacey, G., and Roberts, D., Calcium-Dependent Phosphorylation of Symbiosome Membrane Proteins from Nitrogen-Fixing Soybean Nodules, Plant Physiol., 1991, vol. 95, pp. 222-227.Google Scholar
  87. 87.
    Inoue, K., Takeuchi, Y., Nishimura, M., and Hara-Nishimura, I., Characterization of Two Integral Membrane Proteins Located in the Protein Bodies of Pumpkin Seeds, Plant Mol. Biol., 1995, vol. 28, pp. 1089-1101.Google Scholar
  88. 88.
    Higuchi, T., Suga, S., Tsuchiya, T., Hisada, H., Morishima, S., Okada, Y., and Maeshima, M., Molecular Cloning, Water Channel Activity and Tissue Specific Expression of Two Isoforms of Radish Vacuolar Aquaporin, Plant Cell Physiol., 1998, vol. 9, pp. 905-913.Google Scholar
  89. 89.
    Johansson, I., Karlsson, M., Johanson, U., Larsson, C., and Kjellbom, P. The Role of Aquaporins in Cellular and Whole Plant Water Balance, Biochim. Biophys. Acta, 2000, vol. 1465, pp. 324-342.Google Scholar
  90. 90.
    Gouraud, S., Laera, A., Calamita, G., Carmosino, M., Procino, G., Rossetto, O., Mannucci, R., Rosenthal, W., Svelto, M., and Valenti, G., Functional Involvement of VAMP/Synaptobrevin-2 in CAMP-Stimulated Aquaporin 2 Translocation in Renal Collecting Duct Cells, J. Cell Sci., 2002, vol. 115, pp. 3667-3674.Google Scholar
  91. 91.
    Nielsen, S., Chou, C., Marples, D., Christensen, E., Kishore, B., and Knepper, M., Vasopressin Increases Water Permeability of Kidney Collecting Duct by Inducing Translocation of Aquaporin-CD Water Channels to Plasma Membrane Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 1013-1017.Google Scholar
  92. 92.
    Kirch, H., Vera-Estrella, R., Golldack, D., Quigley, F., Michalowski, C., Barkla, B., and Bohnert, H., Expression of Water Channel Proteins in Mesembryanthemum crystallinum, Plant Physiol., 2000, vol. 123, pp. 111-124.Google Scholar
  93. 93.
    Wayne, R. and Tazawa, M., The Actin Cytoskeleton and Polar Water Permeability in Characean Cells, Protoplasma, 1988, vol. 2, pp. 116-130.Google Scholar
  94. 94.
    Girsch, S. and Peracchia, C., Calmodulin Interacts with a C-Terminus Peptide from the Lens Membrane Protein MIP26, Curr. Eye Res., 1991, vol. 10, pp. 839-849.Google Scholar
  95. 95.
    Swamy-Mruthinti, S., Glycation Decreases Calmodulin Binding to Lens Transmembrane Protein, MIP, Biochim. Biophys. Acta, 2001, vol. 1536, pp. 64-72.Google Scholar
  96. 96.
    Chen, T., Hsu, C., Tsai, P., Ho, Y., and Lin, N., Heterotrimeric G-Protein and Signal Transduction in the Nematode-Trapping Fungus Arthrobotrys dactyloides, Planta, 2001, vol. 212, pp. 858-863.Google Scholar
  97. 97.
    Fotiadis, D., Suda, K., Tittmann, P., Jeno, P., Philippsen, A., Muller, D., Gross, H., and Engel, A., Identification and Structure of a Putative Ca2+-Binding Domain at the C Terminus of AQP1, J. Mol. Biol., 2002, vol. 318, pp. 1381-1394.Google Scholar
  98. 98.
    Lorenz, A., Kaldenhoff, R., and Hertel, R., A Major Integral Protein of the Plant Plasma Membrane Binds Flavin, Protoplasma, 2003, vol. 221, pp. 19-30.Google Scholar
  99. 99.
    Kuwahara, M., Fushimi, K., Terada, Y., Bai, L., Marumo, F., and Sasaki, S., cAMP-Dependent Phosphorylation Stimulates Water Permeability of Aquaporin-Collecting Duct Water Channel Protein Expressed in Xenopus Oocytes, J. Biol. Chem., 1995, vol. 270, pp. 10 384-10 387.Google Scholar
  100. 100.
    Maurel, C., Kado, R., Guern, J., and Chrispeels, M., Phosphorylation Regulates the Water Channel Activity of the Seed-Specific Aquaporin Alpha-TIP, EMBO J., 1995, vol. 14, pp. 3028-3035.Google Scholar
  101. 101.
    Miao, G., Hong, Z., and Verma, D., Topology and Phosphorylation of Soybean Nodulin-26, an Intrinsic Protein of the Peribacteroid Membrane, J. Cell Biol., 1992, vol. 118, pp. 481-490.Google Scholar
  102. 102.
    Johnson, K. and Chrispeels, M., Tonoplast-Bound Protein Kinase Phosphorylates Tonoplast Intrinsic Protein, Plant Physiol., 1992, vol. 100, pp. 1787-1795.Google Scholar
  103. 103.
    Johansson, I., Karlsson, M., Shukla, V., Chrispeels, M., Larsson, C., and Kjellbom, P., Water Transport Activity of the Plasma Membrane Aquaporin PM28A Is Regulated by Phosphorylation, Plant Cell, 1998, vol. 10, pp. 451-459.Google Scholar
  104. 104.
    Kjellbom, P., Larsson, C., Johansson, I., Karlsson, M., and Johanson, U., Aquaporins and Water Homeostasis in Plants, Trends Plant Sci., 1999, vol. 4, pp. 308-314.Google Scholar
  105. 105.
    Maurel, C., Javot, H., Lauvergeat, V., Gerbeau, P., Tournaire, C., Santoni, V., and Heyes, J., Molecular Physiology of Aquaporins in Plants, Int. Rev. Cytol., 2002, vol. 215, pp. 105-148.Google Scholar
  106. 106.
    Tyerman, S., Niemietz, C., and Bramley, H., Plant Aquaporins: Multifunctional Water and Solute Channels with Expanding Roles, Plant Cell Environ., 2002, vol. 25, pp. 173-194.Google Scholar
  107. 107.
    Baiges, I., Schaffner, A., Affenzeller, M., and Mas, A., Plant Aquaporins, Physiol.Plant., 2002, vol. 115, pp. 175-182.Google Scholar
  108. 108.
    Allakhverdiev, S., Sakamoto, A., Nishiyama, Y., and Murata, N., Inactivation of Photosystems I and II in Response to Osmotic Stress in Synechococcus. Contribution of Water Channels, Plant Physiol., 2000, vol. 122, pp. 1201-1208.Google Scholar
  109. 109.
    Barrowclough, D., Peterson, C., and Steudle, E., Radial Hydraulic Conductivity along Developing Onion Roots, J. Exp. Bot., 2000, vol. 51, pp. 547-557.Google Scholar
  110. 110.
    Martre, P., North, G., and Nobel, P., Hydraulic Conductance and Mercury-Sensitive Water Transport for Roots of Opuntia acanthocarpa in Relation to Soil Drying and Rewetting, Plant Physiol., 2001, vol. 126, pp. 352-362.Google Scholar
  111. 111.
    Tazawa, M., Sutou, E., and Shibasaka, M., Onion Root Water Transport Sensitive to Water Channel and K+ Channel Inhibitors, Plant Cell Physiol., 2001, vol. 42, pp. 28-36.Google Scholar
  112. 112.
    Siefritz, F., Tyree, M., Lovisolo, C., Schubert, A., and Kaldenhoff, R., PIP1 Plasma Membrane Aquaporins in Tobacco: From Cellular Effects to Function in Plants, Plant Cell, 2002, vol. 14, pp. 869-876.Google Scholar
  113. 113.
    Javot, H., Lauvergeat, V., Santoni, V., Martin-Laurent, F., Guclu, J., Vinh, J., Heyes, J., Franck, K., Schaffner, A., Bouchez, D., and Maurel, C., Role of a Single Aquaporin Isoform in Root Water Uptake, Plant Cell, 2003, vol. 15, pp. 509-522.Google Scholar
  114. 114.
    Maggio, A. and Joly, R., Effects of Mercuric Chloride on the Hydraulic Conductivity of Tomato Root Systems (Evidence for a Channel-Mediated Water Pathway), Plant Physiol., 1995, vol. 109, pp. 331-335.Google Scholar
  115. 115.
    Daniels, M., Mirkov, T., and Chrispeels, M., The Plasma Membrane of Arabidopsis thaliana Contains a Mercury-Insensitive Aquaporin That Is a Homolog of the Tonoplast Water Channel Protein TIP, Plant Physiol., 1994, vol. 106, pp. 1325-1333.Google Scholar
  116. 116.
    Hasegawa, H., Ma, T., Skach, W., Matthay, M., and Verkman, A., Molecular Cloning of a Mercurial-Insensitive Water Channel Expressed in Selected Water-Transporting Tissues, J. Biol. Chem., 1994, vol. 269, pp. 5497-5500.Google Scholar
  117. 117.
    Kaldenhoff, R., Grote, K., Zhu, J., and Zimmermann, U., Significance of Plasmalemma Aquaporins for Water-Transport in Arabidopsis thaliana, Plant J., 1998, vol. 14, pp. 121-128.Google Scholar
  118. 118.
    Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., and Galili, G., Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress, Plant Cell, 2003, vol. 15, pp. 439-447.Google Scholar
  119. 119.
    Dixit, R., Rizzo, C., Nasrallah, M., and Nasrallah, J., The Brassica MIP-mod Gene Encodes a Functional Water Channel that Is Expressed in the Stigma Epidermis, Plant Mol. Biol., 2001, vol. 45, pp. 51-62.Google Scholar
  120. 120.
    Hukin., D., Doering-Saad, C., Thomas, C., and Pritchard, J., Sensitivity of Cell Hydraulic Conductivity to Mercury Is Coincident with Symplasmic Isolation and Expression of Plasmalemma Aquaporin Genes in Growing Maize Roots, Planta, 2002, vol. 215, pp. 1047-1056.Google Scholar
  121. 121.
    Ikeda, S., Nasrallah, J., Dixit, R., Preiss, S., and Nasrallah, M., An Aquaporin-Like Gene Required for the Brassica Self-Incompatibility Response, Science, 1997, vol. 276, pp. 1564-1566.Google Scholar
  122. 122.
    Marin-Olivier, M., Chevalier, T., Fobis-Loisy, I., Dumas, C., and Gaude, T., Aquaporin pip Genes Are Not Expressed in the Stigma Papillae in Brassica oleracea, Plant J., 2000, vol. 24, pp. 231-240.Google Scholar
  123. 123.
    Steudle, E. and Peterson, C., How Does Water Get through Roots?, J. Exp. Bot., 1998, vol. 49, pp. 775-788.Google Scholar
  124. 124.
    Santoni, V., Gerbeau, P., Javot, H., and Maurel, C., The High Diversity of Aquaporins Reveals Novel Facets of Plant Membrane Functions, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 476-481.Google Scholar
  125. 125.
    Javot, H. and Maurel, C., The Role of Aquaporins in Root Water Uptake, Ann. Bot., 2002, vol. 90, pp. 301-313.Google Scholar
  126. 126.
    Henzler, T., Waterhouse, R., Smyth, A., Carvajal, M., Cooke, D., Schaffner, A., Steudle, E., and Clarkson, D., Diurnal Variations in Hydraulic Conductivity and Root Pressure Can Be Correlated with the Expression of Putative Aquaporins in the Roots of Lotus japonicus, Planta, 1999, vol. 210, pp. 50-60.Google Scholar
  127. 127.
    Carvajal, M., Cooke, D., Clarkson, D., Responses of Wheat Plants to Nutrition Deprivation May Involve the Regulation of Water-Channel Function, Planta, 1996, vol. 199, pp. 372-381.Google Scholar
  128. 128.
    Clarkson, D., Carvajal, M., Henzler, T., Waterhouse, R., Smyth, A., Cooke, D., and Steudle, E., Root Hydraulic Conductance: Diurnal Aquaporin Expression and the Effects of Nutrient Stress, J. Exp. Bot., 2000, vol. 51, pp. 61-70.Google Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2004

Authors and Affiliations

  • A. Yu. Shapiguzov
    • 1
  1. 1.Timiryazev Institute of Plant Physiology, Russian Academy of SciencesMoscowRussia

Personalised recommendations