Abstract
The plant plasma membrane is the the major barrier to water flow between cells and their surroundings. Water movement across roots involves pathways comprising many cells and their walls. There are three possible pathways which water can follow, (i) a trans-cellular pathway, which involves serial movement into and out from radial files of cells, (ii) a symplasmic pathway through the plasmodesmata, which creates a cytoplasmic continuum and (iii) a tortuous, extracellular pathway through the cell walls, the apoplasmic pathway. In each of these pathways water movement across cell membranes occurs at some stage. The possible role of water-channels in membranes is discussed in relation to this movement. The molecular identity of water-channel proteins in plasma membranes of plants has been confirmed but there remain a number of unresolved questions about their role in cell and tissue water relations, their interaction with the lipid components of membranes and the relationship between water movement through membranes by diffusion in the bilayer.
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Abrami L, Capurro C, Ibarra C, Parisi M, Buhler MJ and Ripoche P (1995) Distribution of mRNA encoding the FACHIP water channel in amphibian tissues: effect of salt adaptation. J Membane Biol 143: 199-205
Barthés L, Bousser A, Hoarau J and Deléens E (1995) Reassessment of the relationship between nitrogen supply and xylem exudation in detopped maize seedlings. Plant Physiol Biochem 33: 173-183
Carvajal M, Cooke DT &; Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199: 372-381
Chapin FS III (1990) Effects of nutrient deficiency on plant growth: evidence for a centralized stress-response system. In: Davies WJ and Jeffcoat B (eds) Importance of root to shoot communication in the responses to environmental stress, pp 135-148. British Society for Plant Growth Regulation, Monograph 21, Bristol
Chrispeels MJ and Agre P (1994) Aquaporins: Water channel protein of plant and animal cells. TIBS 19: 421-425
Chrispeels MJ and Maurel C (1994) Aquaporins: The molecular basis of facilitated water movement through living plant cells?. Plant Physiol 105: 9-13
Clarkson DT (1993) Roots and the delivery of solutes to the xylem. Phil Trans Roy Soc London B 341: 5-17
Clarkson DT, Waterhouse R, Schaeffner T, Carvajal M and Cooke DT (1996) Water channels and root hydraulic conductivity. Plant Physiol Biochem (spec. iss.): 162-163
Dainty J (1963) Water relations of plant cells. Adv Bot Res 1: 179-326
Daniels MJ, Mirkov TE and Chrispeels MJ (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is the homologue of the tonoplast water channel protein TIP. Plant Physiol 106: 1325-1333
Denker BM, Smith B, Kuhaja FP and Agre P (1988) Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein erythrocytes. J Biol Chem 263: 15634-15642
Disalero EA and Gier J (1983) Contribution of aqueous interphases to the permeability barrier of lipid bilayer for non-electrolytes. Chem Phys Lipids 32: 39-47
Ernst JA, Clubb RT, Zhou HX, Gronenborn AM and Clore GM (1995) Demonstration of potentially disordered water within a protein hydrophobic cavity by NMR. Science 267: 1813-1817
Faust M, Liu D, Millard MM and Stutte GW (1991) Bound versus free water dormant apple buds A theory for the endormancy. Hort Sci 26: 887-890
Finkelstein A (1987) Water movement though lipid bilayer, pores and plasma membranes. Theory and reality. John Wiley and Sons, New York
Fullerton GD (1988) Physiologic basis of magnetic relaxation. In: Stark D and Bradley WG Jr. (eds) Magnetic resonance imaging, pp 35-55. CV Mosby, St. Louis
Gorin MB, Yancey SB, Cline J, Revel JP and Horwitz J (1984) The major intrinsic protein (MIP) of the bovine lens fiber membrane characterization and structure based on cDNA cloning. Cell 39: 49-59
Hawes CR, Coleman JOD and Evans DE (1991) Endocytosis, exocytosis and vesicle traffic in plants. Society for Experimental Biology, Seminar Series 45, Cambridge University Press, Cambridge. 252 pp
Hasegawa H, Ma T, Skach W, Matthay MA and Verkman AS (1994) Molecular cloning of a mercurial-insensitive water channel expresed in selected water-transporting tissues. J Biol Chem 269: 5497-5500
Henzler T and Steudle E (1995) Reversible closing of water channels in chara internodes provides evidence for a composite transport of the plasma membrane. J Exp Bot 46: 199-209
Hertel A and Steudle E (1997) The function of water channels in Chara: The temperature dependence of water and solute flows provides evidence for composite membrane transport and for a slippage of small organic solutes across water channels. Planta 202: 324-335
Ho C, Kelly MB and Stubbs CD (1994) The effects of phospholipid unsaturation and alcohol perturbation at the protein/ lipid interface probed using fluorophore lifetime heterogeneity. Biochim Biophys Acta 1193: 307-315
Hoarau J, Barthés L, Bousser A, Deléens EE and Prioul JL (1996) Effect of nitrate on water transfer across roots of nitrogen prestarved maize seedlings. Planta 200: 405-415
Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM and Chrispeels MJ (1992) Vegetative and seedspecific isoforms of a putative solute transporter in the tonoplast of Arabidopsis thaliana. Plant Physiol 99: 561-570
House CR (1974) Water transport in cells and tissues, Edward Arnold, London, 562 pp
Kammerloher W, Fischer U, Piechottka GP and Schäffner R (1994) Water channels in the plant plasma membrane cloned by immunoselection from amammalian expresion system. The Plant J 6: 187-199
Karmoker JL, Clarkson DT, Saker LR, Rooney JM and Purves JV(1991) Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L) roots. Planta 185: 269-278
Knepper MA and Inoue T (1997) Regulation of aquaporin2 water channel trafficking by vasopressin. Curr Opinion Cell Biol 9: 560-564
Lampe PD and Johnson RG (1990) Amino acid sequence of in vivo phosphorylation sites in the main intrinsic protein (MIP) of lens membranes. Eur J Biochem 194: 541-547
Leshem YY (1992) Plant membranes: A biophysical approach to structure, development and senescence. Kluwer Academic Publishers, Dordrecht, Boston, London
Maurel C, Kado RT, Guern J and Chrispeels J (1995) Phosphorylation regulates thewater channel activity of the seedspecific aquaporin aTIP. EMBO J 14: 3028-3035
Maurel C, Tacnet F, Guclu J. Guern J and Riproche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci USA 94: 7103- 7108
Os CH, Deen PMT and Dempster JA (1994) Aquaporins: water selective channels in biological membranes. Molecular structure and tissue distribution. Biochim Biophys Acta 1197: 291-309
Pao GM, Wu LF, Johnson KD, Höfte H, Chrispeels MJ, Sweet G, Sandal NN and Saier MJ (1991) Evolution of the MIP family of integral membranetransport protein. Mol Microbiol 5: 33-37
Preston GM, Carroll TP, Guggino WB and Agre P (1992) Appearance of water channels in Xenopus oocyted expresing red cell CHIP28 protein. Science 256: 385-387
Preston GM, Jung JS, Guggino WB and Agre P (1994) Membrane topology of aquaporin CHIP. J Biol Chem 269: 1668-1673
Qui X, Tai CY and Wasserman BP (1995) Plasma membrane intrinsic proteins of Beta vulgaris L. Plant Physiol 108: 387- 392
Radin JW and Matthews MA (1989) Water transport properties of cortical cells in roots of nitrogen and phosphorus-deficient cotton seedlings. Plant Physiol 89: 264-268
Reizer J, Reizer A and Saier MH (1993) The MIP family of integral membrane channel proteins-sequence comparisons, evolutionary relationships, reconstructed pathways of the evolution and proposed functional differentiation of the 2 repeated halves of proteins. Crit Rev Biochem Mol Biol 28: 235-257
Rich GT, Sha'afi RI, Barton TC and Solomon AK (1968) Permeability studies on red cell membranes of dog, cat and beef. J Gen Phys 50: 2391-2405
Robinson DG, Sieber H, Kammerloher W and Schaeffner AR (1996) PIP1aquaporins are concentrated in plasmalemmasomes of Arabidopsis thaliana mesophyll. Plant Physiol 111: 645-649
Sabolic I, Katsura T, Verbavatz JM and Brown D (1995) The AQP2 water channel: effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats. J Membrane Biol 143: 163-175
Smith BL and Agre P (1991) Erythrocyte Mr 28,000 trans-membrane protein exist as a multisubunit oligomer similar to channels proteins. J Biol Chem 266: 6407-6415
Steudle E (1995) Water transport across the roots. In: Baluska F et al (eds) Structure and Function of Roots, pp 197-208. Kluwer Academic Publishers, The Netherlands
Steudle E and Henzler T (1995) Water channels in plants: do basic principles of water transport change. J Exp Bot 46: 1067-1076
Steudle E and Jeschke WD (1983) Water transport in barley root. Planta 158: 237-248
Vaadia Y (1960) Autonomic diurnal fluctuations in rate of exudation and root pressure of decapitated sunflowers plants. Physiol Plant 13: 701-717
Walz T, Hiri T, Murata K, Heymann JB, Mitsuoka K, Fujyoshi Y, Smith VL, Agre P and Engel A (1997) The three-dimensional structure of aquaporin1. Nature 387: 624-627
Yamada S, Katsuhara M, Kelly WB, Michalowski CB and Bohnert HJ (1995) A family of transcripts encoding water channel proteins: Tissue-specific expression in the common ice plant. The Plant Cell 7: 1129-1142
Yamaguchi Shinozaqui K, Koizumi M, Urao S and Shinozaki K (1992) Molecular cloning and characterizarion of 9 cDNAs for genes that are responsive of desiccation in Arabidopsis thaliana: sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 33(3): 217-224
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Carvajal, M., Cooke, D.T. & Clarkson, D.T. The lipid bilayer and aquaporins: parallel pathways for water movement into plant cells. Plant Growth Regulation 25, 89–95 (1998). https://doi.org/10.1023/A:1005918305552
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DOI: https://doi.org/10.1023/A:1005918305552