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Aquaporins and cell growth

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Abstract

This review covers the data concerning the relationship between cell growth and aquaporins in the cell membranes, the plasmalemma and tonoplast. Genes of aquaporins, water channel-forming proteins, are actively expressed before the onset and during cell elongation, thus providing accumulation of aquaporin protein and higher membrane hydraulic conductivity. As a result, an additional water uptake favors cell vacuolation and elongation. The review gives information on all growing plant organs. In actively dividing plant cells, only plasmalemma aquaporins are synthesized, whereas in elongating cells, tonoplast aquaporins are synthesized as well. The review includes also the findings of aquaporin research after growth completion.

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References

  1. Chaumont, F., Barrieu, F., Wojcic, E., Chrispeels, M.J., and Jung, R., Aquaporins Constitute a Large and Highly Divergent Protein Family in Maize, Plant Physiol., 2001, vol. 125, pp. 1206–1215.

    Article  CAS  PubMed  Google Scholar 

  2. Tyerman, S.D., Bohnert, H.J., Maurel, C., Steudle, E., and Smith, J.A.C., Plant Aquaporins: Their Molecular Biology, Biophysics and Significance for Plant Water Relation, J. Exp. Bot., 1999, vol. 50, pp. 1055–1071.

    Article  CAS  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. Postaire, O., Verdoucq, L., and Maurel, C., Aquaporins in Plants: From Molecular Structure to Integrated Functions, Adv. Bot. Res., 2008, vol. 46, pp. 76–136.

    Google Scholar 

  5. Shapiguzov, A.Yu., Aquaporins: Structure, Systematics, and Regulatory Features, Russ. J. Plant Physiol., 2004, vol. 51, pp. 127–137.

    Article  CAS  Google Scholar 

  6. Maurel, C., Verdoucq, L., Luu, D.T., and Santoni, V.P., Plant Aquaporins. Membrane Channels with Multiple Integrated Functions, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 595–624.

    Article  CAS  PubMed  Google Scholar 

  7. Maurel, C. and Chrispeels, M.J., Aquaporins: A Molecular Entry into Plant Water Relations, Plant Physiol., 2001, vol. 125, pp. 135–138.

    Article  CAS  PubMed  Google Scholar 

  8. Tornroth-Horesefield, S., Wang, Y., Hedfolk, K., Johanson, U., Karlson, M., Tajkhordshid, E., Neutze, R., and Kjellbom, P., Structural Mechanism of Plant Aquaporin Gating, Nature, 2006, vol. 439, pp. 688–694.

    Article  Google Scholar 

  9. Fujiyoshi, Y., Mitsuoka, K., de Groot, B.L., Philippsen, A., Grubmüller, H., Agre, P., and Engel, A., Structure and Function of Water Channels, Curr. Opin. Struct. Biol., 2002, vol. 12, pp. 509–515.

    Article  CAS  PubMed  Google Scholar 

  10. Maurel, C., Plant Aquaporins: Novel Function and Regulation Properties, FEBS Lett., 2007, vol. 581, pp. 2227–2236.

    Article  CAS  PubMed  Google Scholar 

  11. Javot, H. and Maurel, C., The Role of Aquaporins in Root Water Uptake, Ann. Bot., 2002, vol. 90, pp. 301–313.

    Article  CAS  PubMed  Google Scholar 

  12. Trofimova, M.S., Zhestkova, I.M., Andreev, I.M., Svinov, M.M., Bobylev, Yu.S., and Sorokin, E.M., Osmotic Water Permeability of Vacuolar and Plasma Membranes Isolated from Maize Roots, Russ. J. Plant Physiol., 2001, vol. 48, pp. 287–293.

    Article  CAS  Google Scholar 

  13. Harvengt, P., Vlerick, A., Fuks, B., Wattiez, R., Ruysschaert, J.-M., and Homble, F., Lentil Seed Aquaporins Form a Hetero-Oligomer Which Is Phosphorylated by a Mg2+-Dependent and Ca2+-Regulated Kinase, Biochem. J., 2000, vol. 352, pp. 183–190.

    Article  CAS  PubMed  Google Scholar 

  14. Hachez, C., Moshelion, M., Zelazny, E., Cavez, D., and Chaumont, F., Localization and Quantification of Plasma Membrane Aquaporin Expression in Maize Primary Root: A Clue to Understanding Their Role as Cellular Plumbers, Plant Mol. Biol., 2006, vol. 62, pp. 305–323.

    Article  CAS  PubMed  Google Scholar 

  15. Kaldenhoff, R. and Fisher, M., Functional Aquaporin Diversity in Plants, Biochim. Biophys. Acta, 2006, vol. 1758, pp. 1134–1141.

    Article  CAS  PubMed  Google Scholar 

  16. Hachez, C., Heinen, R.B., Draye, X., and Chaumont, F., The Expression Pattern of Plasma Membrane Aquaporins in Maize Leaf Highlights Their Role in Hydraulic Regulation, Plant Mol. Biol., 2008, vol. 68, pp. 337–353.

    Article  CAS  PubMed  Google Scholar 

  17. Schuurmans, J.A.M.J., van Dongen, J.T., Rutjens, B.P.S., Boonman, A., Pieterse, C.M.J., and Borstlap, A.C., Members of the Aquaporin Family in the Developing Pea Seed Coat Include Representatives of the PIP, TIP, and NIP Subfamilies, Plant Mol. Biol., 2003, vol. 53, pp. 655–667.

    Article  Google Scholar 

  18. Barrouclough, D., Peterson, C., and Steudle, E., Radial Hydraulic Conductivity along Developing Onion Roots, J. Exp. Bot., 2000, vol. 51, pp. 547–557.

    Article  Google Scholar 

  19. Wan, X., Steudle, E., and Hartung, W., Gating of Water Channels (Aquaporins) in Cortical Cells of Young Corn Roots by Mechanical Stimuli (Pressure Pulses): Effects of ABA and HgCl2, J. Exp. Bot., 2004, vol. 55, pp. 411–422.

    Article  CAS  PubMed  Google Scholar 

  20. O’Brien, M., Bertrand, C., and Matton, D.P., Characterization of a Fertilization-Induced and Developmentally Regulated Plasma-Membrane Aquaporin Expressed in Reproductive Tissues, in the Wild Potato Solanum chacoense Bitt., Planta, 2002, vol. 215, pp. 485–493.

    Article  PubMed  Google Scholar 

  21. Ciavatta, V.T., Morillon, R., Pullman, G.S., Chrispeels, M.J., and Cairney, J., An Aquaglyceroporin Is Abundantly Expressed Early in the Development of the Suspensor and the Embryo Proper of Loblolly Pine, Plant Physiol., 2001, vol. 127, pp. 1556–1567.

    Article  CAS  PubMed  Google Scholar 

  22. Johnson, K.D., Herman, E.M., and Chrispeels, M.J., An Abundant, Highly Conserved Tonoplast Protein in Seeds, Plant Physiol., 1989, vol. 91, pp. 1006–1013.

    Article  CAS  PubMed  Google Scholar 

  23. Höfte, H. and Chrispeels, M.J., Protein Sorting to the Vacuolar Membrane, Plant Cell, 1992, vol. 4, pp. 995–1001.

    Article  PubMed  Google Scholar 

  24. Maeshima, M., Hara-Nishimura, I., Takeuchi, Y., and Nishimura, M., Accumulation of Vacuolar H+-Pyrophosphatase and H+-ATPase during Reformation of the Central Vacuole in Germinating Pumpkin Seeds, Plant Physiol., 1994, vol. 106, pp. 61–69.

    CAS  PubMed  Google Scholar 

  25. Oliviusson, P. and Hakman, I., A Tonoplast Intrinsic Protein (TIP) Is Present in Seeds, Roots and Somatic Embryos of Norway Spruce (Picea abies), Physiol. Plant., 1995, vol. 95, pp. 288–295.

    Article  CAS  Google Scholar 

  26. Melroy, D.L. and Herman, E.M., TIP, an Integral Membrane Protein of the Protein-Storage Vacuoles of the Soybean Cotyledon Undergoes Developmentally Regulated Membrane Accumulation and Removal, Planta, 1991, vol. 184, pp. 113–122.

    Article  CAS  Google Scholar 

  27. 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.

    Article  CAS  PubMed  Google Scholar 

  28. Mäer, M. and Chrispeels, M.J., Synthesis of an Integral Protein of the Protein-Body Membrane in Phaseolus vulgaris Cotyledons, Planta, 1984, vol. 160, pp. 330–340.

    Article  Google Scholar 

  29. Maurel, C., Kado, R.T., Guern, J., and Chrispeels, M.J., Phosphorylation Regulates the Water Channel Activity of the Seed-Specific Aquaporin α-TIP, EMBO J., 1995, vol. 14, pp. 3028–3035.

    CAS  PubMed  Google Scholar 

  30. Jauh, G.Y., Philips, T.E., and Rogers, J.C., Tonoplast Intrinsic Protein Isoforms as Markers for Vacuolar Functions, Plant Cell, 1999, vol. 11, pp. 1867–1882.

    Article  CAS  PubMed  Google Scholar 

  31. Willigen, V.C., Postaire, O., Tournair-Roux, C., Boursiac, Y., and Maurel, C., Expression and Inhibition of Aquaporins in Germinating Arabidopsis Seeds, Plant Cell Physiol., 2006, vol. 47, pp. 1241–1250.

    Article  Google Scholar 

  32. Shizhneva, I.A., Involvement of Aquaporins in Water Influx to Axial Organs of Germinating Seeds, Cand. Sci. (Biol.) Dissertation, Moscow: Timiryazev Inst. Plant Physiol. Russ. Acad. Sci., 2007.

    Google Scholar 

  33. Gao, Y.P., Young, L., Bonham-Smith, P., and Gusta, L.V., Characterization and Expression of Plasma and Tonoplast Membrane Aquaporins in Primed Seed of Brassica napus during Germination under Stress Conditions, Plant Mol. Biol., 1999, vol. 40, pp. 635–644.

    Article  CAS  PubMed  Google Scholar 

  34. Fukuhara, T., Kirch, H.-H., and Bohnert, H.J., Expression of Vap1 and Water Channel Proteins during Seed Germination, Plant Cell Environ., 1999, vol. 22, pp. 417–424.

    Article  CAS  Google Scholar 

  35. Liu, H.Y., Yu, X., Cui, D.Y., Sun, M.H., Sun, W.N., Tang, Z.C., Kwak, S.S., and Su, W.A., The Role of Water Channel Proteins and Nitric Oxide Signaling in Rice Seed Germination, Cell Res., 2007, vol. 17, pp. 638–649.

    Article  CAS  PubMed  Google Scholar 

  36. Obroucheva, N.V., Seed Germination: A Guide to the Early Stages, Leiden: Backhuys Publ., 1999.

    Google Scholar 

  37. Obroucheva, N.V. and Antipova, O.V., Physiology of the Initiation of Seed Germination, Russ. J. Plant Physiol., 1997, vol. 44, pp. 250–264.

    CAS  Google Scholar 

  38. Veselova, T.V. and Veselovsky, V.A., Possible Involvement of Aquaporins in Water Uptake by Pea Seeds Differing in Quality, Russ. J. Plant Physiol., 2006, vol. 53, pp. 96–101.

    Article  CAS  Google Scholar 

  39. Obroucheva, N.V., Kovadlo, L.S., and Prokof’ev, A.A., Water Content as a Trigger of Starch and Protein Mobilization during Pea Seed Germination, Sov. Plant Physiol., 1988, vol. 35, pp. 322–328.

    Google Scholar 

  40. Herman, E.M. and Larkins, B.A., Protein Storage Bodies and Vacuoles, Plant Cell, 1999, vol. 11, pp. 601–613.

    Article  CAS  PubMed  Google Scholar 

  41. Shizhneva, I.A., Novikova, G.V., and Obroucheva, N.V., Tonoplast and Plasmalemma Aquaporins in Axial Organs of Bean Seeds during Germination, Dokl. Akad. Nauk, 2007, vol. 413, pp. 116–119.

    Google Scholar 

  42. Penfield, S., Li, Yi., Gilday, A.D., Graham, S., and Graham, I.A., Arabidopsis ABA INSENSITIVE4 Regulates Lipid Mobilization in the Embryo and Reveals Repression of Seed Germination by the Endosperm, Plant Cell, 2006, vol. 18, pp. 1887–1899.

    Article  CAS  PubMed  Google Scholar 

  43. Daniels, M.J., Chaumont, F., Mirkov, E.T., and Chrispeels, M.J., Characterization of New Vacuolar Membrane Aquaporin Sensitive to Mercury at a Unique Site, Plant Cell, 1996, vol. 8, pp. 587–599.

    Article  CAS  PubMed  Google Scholar 

  44. Karlsson, M., Johansson, I., Bush, M., McCann, M.C., Maurel, C., Larsson, C., and Kjellbom, P., An Abundant TIP Expressed in Mature Highly Vacuolated Cells, Plant J., 2000, vol. 21, pp. 83–90.

    Article  CAS  PubMed  Google Scholar 

  45. Ludevid, D., Höfte, H., Himelblau, E., and Chrispeels, M.J., The Expression Pattern of the Tonoplast Intrinsic Protein γ-TIP in Arabidopsis thaliana Is Correlated with Cell Enlargement, Plant Physiol., 1992, vol. 100, pp. 1633–1639.

    Article  CAS  PubMed  Google Scholar 

  46. Hukin, D., Doering-Saad, C., Thomas, C.R., 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.

    Article  CAS  PubMed  Google Scholar 

  47. Suga, S., Murai, M., Kuwagata, T., and Maeshima, M., Differences in Aquaporin Levels among Cell Types of Radish and Measurement of Osmotic Water Permeability of Individual Protoplasts, Plant Cell Physiol., 2003, vol. 44, pp. 277–286.

    Article  CAS  PubMed  Google Scholar 

  48. Barrieu, F., Chaumont, F., and Chrispeels, M.J., High Expression of Tonoplast Aquaporin ZmTIP in Epidermal and Conducting Tissues of Maize, Plant Physiol., 1998, vol. 117, pp. 1153–1163.

    Article  CAS  PubMed  Google Scholar 

  49. Kaldenhoff, R., Kölling, A., Meyers, J., Karmann, U., Ruppel, G., and Richter, G., The Blue Light-Responsive AthH2 Gene of Arabidopsis thaliana Is Primarily Expressed in Expanding as Well as in Differentiating Cells and Encodes a Putative Channel Protein of the Plasmalemma, Plant J., 1995, vol. 7, pp. 87–95.

    Article  CAS  PubMed  Google Scholar 

  50. Javot, H., Lauvergeat, V., Santoni, V., Martin-Laurent, F., Guclu, J., Vinh, J., Heyes, J., Franck, K.I., Schäffner, A.R., Bouchez, D., and Maurel, C., Role of Single Aquaporin Isoform in Root Water Uptake, Plant Cell, 2003, vol. 15, pp. 509–522.

    Article  CAS  PubMed  Google Scholar 

  51. Chaumont, F., Barrieu, F., Herman, E.M., and Chrispeels, M.J., Characterization of a Maize Tonoplast Aquaporin Expressed in Zone of Cell Division and Elongation, Plant Physiol., 1998, vol. 117, pp. 1143–1152.

    Article  CAS  PubMed  Google Scholar 

  52. Barrieu, F., Thomas, D., Marty-Mazars, D., Charbonnier, M., and Marty, F., Tonoplast Intrinsic Proteins from Cauliflower (Brassica oleracea L. var. botrytis): Immunological Analysis, cDNA Cloning and Evidence for Expression in Meristematic Tissues, Planta, 1998, vol. 204, pp. 335–334.

    Article  CAS  PubMed  Google Scholar 

  53. 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.

    Article  CAS  PubMed  Google Scholar 

  54. Bots, M., Feron, R., Uehlein, N., Weterings, K., Kaldenhoff, R., and Mariani, T., PIP1 and PIP2 Aquaporins Are Differentially Expressed during Tobacco Anther and Stigma Development, J. Exp. Bot., 2005, vol. 56, pp. 113–121.

    CAS  PubMed  Google Scholar 

  55. Eisenbarth, D.A. and Weig, A.R., Dynamics of Aquaporins and Water Relations during Hypocotyls Elongation in Ricinus communis L. Seedlings, J. Exp. Bot., 2005, vol. 56, pp. 1831–1842.

    Article  CAS  PubMed  Google Scholar 

  56. Yooyongwech, S., Horigane, A.K., Yoshida, M., Yamaguchi, M., Sekozawa, Y., Sugaya, S., and Gemma, H., Changes in Aquaporin Gene Expression and Magnetic Resonance Imaging of Water Status in Peach Tree Flower Buds during Dormancy, Physiol. Plant., 2008, vol. 134, pp. 522–533.

    Article  CAS  PubMed  Google Scholar 

  57. Cui, X.H., Hao, F.S., Chen, J., and Wang, X.C., Expression of the Vicia faba VfPIP Gene in Arabidopsis thaliana Plants Improves Their Drought Resistance, J. Plant Res., 2008, vol. 121, pp. 207–214.

    Article  CAS  PubMed  Google Scholar 

  58. Schünmann, P.H.D. and Ougham, H.J., Identification of Three cDNA Clones Expressed in the Leaf Extension Zone and with Altered Patterns of Expression in the Slender Mutant of Barley: A Tonoplast Intrinsic Protein, a Putative Structural Protein and Protochlorophyllide Oxidoreductase, Plant Mol. Biol., 1996, vol. 31, pp. 529–537.

    Article  PubMed  Google Scholar 

  59. Frangue, N., Maeshima, M., Schäffner, A.R., Mandel, T., Martinoia, E., and Bonnemain, J.L., Expression and Distribution of Vacuolar Aquaporin in Young and Mature Leaf Tissues of Brassica napus in Relation to Water Fluxes, Planta, 2001, vol. 212, pp. 270–278.

    Article  Google Scholar 

  60. Volkov, V., Hachez, C., Moshelion, M., Draye, X., Chaumont, F., and Fricke, W., Water Permeability Differs between Growing and Nongrowing Barley Leaf Tissues, J. Exp. Bot., 2007, vol. 58, pp. 377–390.

    Article  CAS  PubMed  Google Scholar 

  61. Ma, N., Xue, J., Li, Y., Liu, X., Dai, F., Jia, W., Luo, Y., and Gao, J., Rh-PIP2;1 a Rose Aquaporin Gene, Is Involved in Ethylene-Regulated Petal Expansion, Plant Physiol., 2008, vol. 148, pp. 894–907.

    Article  CAS  PubMed  Google Scholar 

  62. 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.

    Article  CAS  PubMed  Google Scholar 

  63. Ozga, J.A., van Huizen, R., and Reinecke, D.M., Hormone and Seed-Specific Regulation of Pea Fruit Growth, Plant Physiol., 2002, vol. 128, pp. 1379–1389.

    Article  CAS  PubMed  Google Scholar 

  64. Schlosser, J., Olsson, N., Weis, M., Reid, K., Peng, F., Lund, S., and Bowen, P., Cellular Expansion and Gene Expression in the Developing Grape (Vitis vinifera L.), Protoplasma, 2008, vol. 232, pp. 255–265.

    Article  CAS  PubMed  Google Scholar 

  65. Zhou, Y., Setz, N., Niemietz, C., Offler, C.E., Tyerman, S.D., and Patrick, J.W., Aquaporins and Unloading of Phloem-Imported Water in Coats of Developing Bean Seeds, Plant Cell Environ., 2007, vol. 30, pp. 1566–1577.

    Article  CAS  PubMed  Google Scholar 

  66. Smart, L.B., Vojdani, F., Maeshima, M., and Wilkins, T.A., Genes Involved in Osmoregulation during Turgor-Driven Cell Expansion of Developing Cotton Fibers Are Differentially Regulated, Plant Physiol., 1998, vol. 116, pp. 1539–1549.

    Article  CAS  PubMed  Google Scholar 

  67. Phillips, A.L. and Huttly, A.K., Cloning of Two Gibberellin-Regulated cDNAs from Arabidopsis thaliana by Subtractive Hybridization: Expression of the Tonoplast Water Channel, γ-TIP, Is Increased by GA3, Plant Mol. Biol., 1994, vol. 24, pp. 603–615.

    Article  CAS  PubMed  Google Scholar 

  68. Ogawa, M., Hanada, A., Yamauchi, Y., Kuwahara, A., Kamiya, Y., and Yamaguchi, S., Gibberellin Biosynthesis and Response during Arabidopsis Seed Germination, Plant Cell, 2003, vol. 15, pp. 1591–1604.

    Article  CAS  PubMed  Google Scholar 

  69. Uehlein, N., Otto, B., Hanson, D.T., Fisher, M., McDowell, N., and Kaldenhoff, R., Function of Nicotiana tabacum Aquaporins as Chloroplast Gas Pores Challenges the Concept of Membrane CO2 Permeability, Plant Cell, 2008, vol. 20, pp. 648–657.

    Article  CAS  PubMed  Google Scholar 

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  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276, Russia

    N. V. Obroucheva & I. A. Sin’kevich

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  1. N. V. Obroucheva
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  2. I. A. Sin’kevich
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Original Russian Text © N.V. Obroucheva, I.A. Sin’kevich, 2010, published in Fiziologiya Rastenii, 2010, Vol. 57, No.2, pp. 163–176.

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Obroucheva, N.V., Sin’kevich, I.A. Aquaporins and cell growth. Russ J Plant Physiol 57, 153–165 (2010). https://doi.org/10.1134/S1021443710020019

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