Abstract
There is evidence that the plasma membrane (PM) permeability alterations might be involved in plant salt tolerance. This review presents several lines of evidence demonstrating that PM permeability is correlated with salt tolerance in plants. PM injury and hence changes in permeability in salt sensitive plants is brought about by ionic effects as well as oxidative stress induced by salt imposition. It is documented that salinity enhances lipid peroxidation as well as protein oxidative damage, which in turn induces permeability impairment. PM protection, and thus retained permeability, in tolerant plants under salt imposition could be achieved through increasing antioxidative systems and thereby reducing lipid peroxidation and protein oxidative damage of PM. It appears that specific membrane proteins and/or lipids are constitutive or induced under salinity, which may contribute to maintenance of membrane structure and function in salt tolerant plant species. Furthermore, protecting agents (e.g., glycinebetaine, proline, polyamines, trehalose, sorbitol, mannitol) accumulated in salt tolerant species/cultivars may also contribute to PM stabilization and protection under salinity. Based on the presented evidence that PM permeability correlates with plant salt tolerance, we suggest that PM permeability is an easy and useful parameter for selection of genotypes of agriculture crops adapted to salt stress.
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Abbreviations
- EC:
-
electrical conductivity
- PA:
-
phosphatidic acid
- PC:
-
phosphatidylcholine
- PE:
-
phosphatidylethanolamine
- PEG:
-
polyethyleneglycol
- PG:
-
phosphatidylglycerol
- PI:
-
phosphatidylinositol
- PM:
-
plasma membrane
- ROS:
-
reactive oxygen species
References
Abdul Kader, M., Seidel, T., Golldack, D., Lindberg, S.; Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under salt stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. — J. exp. Bot. 57: 4257–4268, 2006.
Aghaei, K., Ehsanpour, A.A., Komatsu, S.: Potato responses to salt stress was mitigated by induced activity of antioxidant enzymes. — J. Integr. Plant Biol. 51: 1095–1103, 2009.
Alvarez-Pizarro, A., Gomes-Filho, E., De Lacerda, C., Alencar, N.L., Prisco, J.T.: Salt-induced changes on H+-ATPase activity, sterol and phospholipid content and lipid peroxidation of root plasma membrane from dwarf-cashew (Anacardium occidentale L.) seedlings. — Plant Growth Regul. 59: 125–135, 2009.
Amtmann, A, Beilby, M.: The role of ion channels in plant salt tolerance. — In: Demidchik, V., Maathuis, F. (ed.): Ion Channels and Plant Stress responses. — Springer-Verlag, Berlin 2010.
Arzani, A.: Improving salinity tolerance in crop plants: a biotechnological review. — In Vitro cell. dev. Biol. Plant 44; 373–383, 2008.
Ashraf, M., Foolad, M.R.: Roles of glycinebetaine and proline in improving plant abiotic stress resistance. — Environ. exp. Bot. 59: 206–216, 2007.
Ashraf, M., Ali, Q.: Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). — Environ. exp. Bot. 63: 266–273, 2008.
Ashraf, M.: Biotechnological approach of improving plant salt tolerance using antioxidants as markers. — Biotechnol. Adv. 27: 84–93, 2009.
Attia, H., Karray, N., Msilini, N., Lachaal, M.: Effect of salt stress on gene expression of superoxide dismutases and copper chaperone in Arabidopsis thaliana. — Biol. Plant. 55; 159–163, 2011.
Avery, S.V.: Molecular targets of oxidative stress. — Biochem. J. 434: 201–210, 2011.
Bao, A.K., Wang, S., Wu, G., Xi, J., Zhang, J., Wang, C.; Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). — Plant Sci. 176: 232–240, 2009.
Bargmann, B.O., Laxalt, A., Riet, B., Schooten, B., Merquiol, E., Testerink, C., Haring, M., Bartels, D., Munnik, T.; Multiple PLDs required for high salinity tolerance and water deficit tolerance in plants. — Plant Cell Physiol. 50; 78–89, 2009.
Ben Amor, N., Megiche, W., Jimenez, A., Sevilla, F., Abdelly, C.: The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress. — Acta Physiol. Plant. 32: 453–461, 2010.
Bishop, D.G.: Functional role of plant membrane lipids. — In; Thomson, W.W., Mudd, J.B., Gibbs, M. (ed.): Biosynthesis and Function of Plant Lipids. Pp. 81–103. Univ. California, Riverside 1983.
Bittisnich, D., Robinson, D., Whitecross, M.: Membrane-associated and intracellular free calcium levels in root cells under NaCl stress. — In: De Michelis, M., Marre, D., Rasi-Caldogno, S. (ed.): Plant Membrane Transport: the Current Position. Pp 681–683. Elsevier, Amsterdam 1989.
Blits, K.C., Gallagher, J.L.: Effect of NaCl on lipid content of plasma membranes isolated from root and cell suspension of the dicot. Halophyte Kosteletzkya virginica L. Preal. — Plant Cell Rep. 9: 156–159, 1990.
Blumwald, E.: Sodium transport and salt tolerance in plants. — Curr. Opin. Cell Biol. 12: 431–434, 2000.
Bouchereau, A., Azia, A., Larher, F., Martin-Tanguy, J.; Polyamines and environmental challenges: recent development. — Plant Sci. 140: 103–125, 1999.
Brown, D. J., DuPont, F.M.: Lipid composition of plasma membranes and endomembranes prepared from roots of barley (Hordeum vulgaris L.). Effect of salt. — Plant Physiol. 90: 472–478, 1989.
Carruthers, A., Melchior, D.J.: How bilayer lipids affect membrane protein activity. — Trends Biochem. Sci. 11: 331–335, 1989.
Chen, T.H., Murata, N.: Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. — Plant Cell Environ. 34: 1–20, 2011.
Chen, Z., Tracy, A.C., Zhou, M., Twomey, A., Naidu, B., Shabala, S.: Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. — J. exp. Bot. 58: 4245–4255, 2007.
Chinnusamy, V., Jagendrof, A., Zhu, J.K.: Understanding and improving salt tolerance in plants. — Crop Sci. 45: 437–448, 2005.
Collado, M., Arture, M., Aulicino, M., Molina, M.; Identification of salt tolerance in seedlings of maize (Zea mays L.) with the cell membrane stability trait. — Int. Res. J. Plant Sci. 5: 126–132, 2010.
Cosentino, C., Fisher-Schliebs, E., Adam, B., Thiel, G., Homann, U.: Na+/H+ antiporters are differentially regulated in response to NaCl stress in leaves and roots of Mesembryanthemum crystalinum. — New Phytol. 186: 669–680, 2010.
Cramer, R.C., Lauchli, A., Polito, V.S.: Displacement of Ca2+ by Na+ from the plasmalemma of root cells. A primary response to salt stsress? — Plant Physiol. 79: 207–211, 1985.
Cuin, T.A., Shabala, S.: Compatible solutes mitigate damaging effects of salt stress by reducing the impact of stressinduced reactive oxygen species. — Plant Signal. Behav. 3; 207–218, 2008.
Cullis, R.C., De Kruijf, B.: Lipid polymorphism and the functional roles of lipid in biological membranes. — Biochim. biophys. Acta 559: 399–420, 1979.
Daneshmand, F., Arvin, M.J., Kalantari, K.M.: Physiological responses to NaCl stress in three wild species of potato in vitro. — Acta Physiol. Plant. 32: 91–101, 2010.
Dias, A.S., Barreiro, M.G., Campos, P., Ramalho, J.C., Lidon, F.C.: Wheat cellular membrane thermotolerance under heat stress. — J. Agron. Crop Sci. 196: 100–108, 2010.
Douglas, T.J., Walker, R.P.: Phospholpids, free sterols and adenosine triphosphatase of plasma membrane-enriched preparations from roots of citrus genotypes differing in chloride exclusion ability. — Physiol. Plant. 62: 51–58, 1984.
Douglas, T.J.: NaCl effects on 4-desmethylsterol composition of plasma membrane enriched preparations from citrus roots. — Plant Cell Environ. 8: 687–692, 1985.
Dwivedi, R., Snehi, Y., Toshi, A., Qadar, E.: Membrane permeability in tetraploid and hexaploid wheats under salinity stress. — Curr. Sci. 50: 194–197, 1981.
Farooq, S., Azam, F.: The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties. — J. Plant Physiol. 163: 629–637, 2006.
Flowers, T.J., Flowers, S.A.: Why does salinity pose such a difficult problem for plant breeders. — Agr. Water Manage. 78: 15–24, 2005.
Flowers, T.J., Galal, H.K., Bromhaml, M.: Evaluation of halophytes: multiple origins of salt tolerance in land plants. — Funct. Plant Biol. 37: 604–612, 2010.
Gagne, J., Stamatatos, L., Diacovo, T., Hui, S., Yeagel, P.L., Silvius, J.P.: Physical properties and surface interactions of bilayer membranes containing N-methylated phosphatidylethanolamine. — Biochemistry 24: 4400–4408, 1985.
Gao, T., Gao, Q., Duan, X., Yue, G., Yang, A.F., Zhang, J.R.; Cloning of H+-PPase gene from Thellungiela halophila and its heterologous expression to improve tobacco salt tolerance. — J. exp. Bot. 57: 3259–3270, 2006.
Garg, A.K., Kim, J., Owens, T., Ranwala, A.P., Choi, Y., Kochian, L.V., Wu, R. J.: Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. — Proc. nat. Acad. Sci. USA 99: 15898–15903, 2002.
Ghanti, S.K., Sujata, K.G., Kumar, B.M., Karba, N.N., Reddy, K.J.: Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. — Biol. Plant. 55: 634–640, 2011.
Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. — Plant Physiol. Biochem. 48: 909–930, 2010.
Goncalo, A., Filho, S., Ferreira, B. S., Dias, J., Queiroz, K., Branco, A.T., Bressan, R.A., Smith, D., Oliveira, J., Garcia, B.: Accumulation of SALT protein in rice plants as response to environmental stresses. — Plant Sci. 164: 623–628, 2003.
Hajlaoui, H., Denden, M., Elyeb, N.: Changes in fatty acids composition, hydrogen peroxide generation and lipid peroxidation of salt-stressed corn (Zea mays L.) root. — Acta Physiol. Plant. 31: 33–34, 2009.
Hanson, A.D., Grumet, R.: Betaine accumulation: metabolic pathways and genetics. — In: Key, J.L., Kosuge, T. (ed.); Cellular and Molecular Biology of Plant Stress. Pp. 71–92. Alan Liss, New York 1985.
Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J.: Plant cellular and molecular responses to high salinity. — Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 463–499, 2000.
Hirayama, O., Mihara, M.: Characterization of membrane lipids of higher plants different in salt tolerance. — Agr. biol. Chem. 51: 3215–3221, 1987.
Hirshi, K.D.: The calcium conundrum. Both versital nutrient and specific signal. — Plant Physiol. 136: 2438–2442, 2004.
Hong, J.K., Hawang, B.K.: The promoter of the pepper pathogen-induced membrane gene CaPIMP1 mediates environmental stress responses in plants. — Planta 229: 249–259, 2009.
Hu, X.J., Zhang, Z., Xu, P., Fu, Z.Y., Hu, S. B., Song, W.Y.; Multifunctional genes: the cross-talk among the regulation networks of abiotic stress responses. — Biol. Plant. 54: 213–223, 2010.
Hurkman, W. J., Tanaka, C.K, DuPont, F.M.: The effects of salt stress on polypeptides in membrane fractions from barley roots. — Plant Physiol. 88: 1263–1273, 1988.
Jackson, P.C., John, J.B.: Changes in membrane lipids of roots associated with changes in permeability. 1. Effects of undissociated organic acids. — Plant Physiol. 66: 801–804, 1980.
Jacobs, A., Ford, K., Kretschmer, J., Tester, M.: Rice plants expressing the moss sodium pumping ATPase PpENA1 maintain greater biomass production under salt stress. — Plant Biotechnol. J. 9: 838–847, 2011.
Kent, L.M., Lauchli, A.: Germination and seedling growth of cotton: salinity-calcium interaction. — Plant Cell Environ. 80: 651–654, 1985.
Kerkeb, L., Donaire, J.P., Rodriguez-Rosales, M.P.: Plasma membrane H+-ATPase activity is involved in adaptation of tomato to NaCl. — Physiol. Plant. 111: 483–490, 2001.
Khan, M.H., Panda, S.K.: Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaC-salinity stress. — Acta Physiol. Plant. 30: 81–89, 2008.
Khan, M.S., Tawaraya, K., Sekimoto, H., Koyama, H., Kobayashi, Y., Mirayama, T., M. Chuba, Y. Shiono, M. Uemura, M. Kambayashi, S. Ishikawa, Wagatsuma, T.; Relative abundance of Δ5-sterol in plasma membrane lipids of root-tip cells correlates with aluminum tolerance of rice. — Physiol. Plant. 135: 73–83, 2009.
Kholova, J., Sairam, R.K., Meena, R.C., Srivastava, G.S.; Response of maize genotypes to salinity stress in relation to osmolytes and metal ions contents, oxidative stress and antioxidant enzymes activity. — Biol. Plant. 53: 249–256, 2009.
Kholova, J., Sairam, R.K, Meena, R.C.: Osmolytes and metal ions accumulation, oxidative stress and antioxidant enzyme activity as determinants of salinity stress tolerance in maize. — Acta Physiol. Plant. 32: 477–486, 2010.
Kononowicz, A.K., Raghothama, K.G., Casas, A., Nelson, N.K., Liu D., Narasimhan, M., LaRose, P.C., Singh, N.K., Bressan, R.A., Hasegawa, P.M.: Structural regulation and function of the osmotin gene. — In: Cherry, J.H. (ed.); Biochemical and Cellular Mechanisms of Stress Tolerance in Plants. Pp. 381–413. Springer, Berlin 1994.
Kuiper, P.J.C.: Functioning of plant cell membranes under saline conditions. Membrane lipid composition and ATPases. — In: Staples, R.C., Toenniessen, G.H., (ed.); Salinity Tolerance in Plants. Pp. 77–91. Wiley, New York 1984.
Lauchli, A.: Calcium, salinity and the plasma membrane. In; Leonard, R.T., Hepler, P.K. (ed.): Calcium in Plant Growth and Development. Pp. 26–35. Amer. Soc. Plant Physiol., Riverside 1990.
Leopold, A.C., Willing, R.P.; Evidence for toxicity effects of salt on membranes. — In: Staples, R.C., Toenniessen, G.H. (ed.): Salinity Tolerance in Plants. Pp. 67–76. Wiley, New York 1984.
Levitt, J.: Responses of plants to environmental stresses. Vol. 2, Water, Radiation, Salt and other Stresses. Academic Press, New York 1980.
Maas, E.V., Nieman, R.H.: Physiology of plant tolerance to salinity. — In: Jung, G.E. (ed.): Crop Tolerance to Suboptimal Conditions. Pp. 277–299. Amer. Soc. Agron., Madison 1987.
Magin, R.L., Niesman, M., Basic, G.: Influence of fluidity on membrane permeability: correspondence between studies of membrane models and simple biological systems. — In; Aloia, R.C., Curtain, J., Gordon, L.M. (ed.): Membrane Transport and Information Storage. Pp. 221–237. Liss Inc., New York 1990.
Malik, S., Nayak, M., Sahu, B.B., Panigrahi, A.K., Shaw, B.P.; Response of antioxidant enzymes to high NaCl concentration in different salt-tolerant plants. — Biol. Plant. 55: 191–195, 2011.
Mansour, M.M.F.: NaCl alteration of plasma membrane of Allium cepa epidermal cells. Alleviation by calcium. — J. Plant Physiol. 145: 726–730, 1995a.
Mansour, M.M.F.: Changes in cell membrane permeability and lipid content of wheat root cortex cells induced by NaCl. — Biol. Plant. 37: 143–145, 1995b.
Mansour, M.M.F.: Cell permeability under salt stress. — In; Jaiwal, P.K., Singh, R.P., Gulati, A. (ed.): Strategies for Improving Salt Tolerance in Higher Plants. Pp. 87–110. Science Publ., Enfield 1997.
Mansour M.M.F.: Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. — Plant Physiol. Biochem. 36: 767–772, 1998.
Mansour, M.M.F.: Nitrogen containing compounds and adaptation of plants to salinity stress. — Biol. Plant. 43: 491–500, 2000.
Mansour, M.M.F., Al-Mutawa, M.M.: Stabilization of plasma membrane by polyamines against salt stress. — Cytobios 100: 7–17, 1999.
Mansour, M.M.F., Al-Mutawa, M.M., Salama, K.H.A., Abou Hadid, A.F.: Salt acclimation of wheat salt sensitive cultivar by polyamines. — In: Ahmad, R., Malik, K.A. (ed.); Prospects for Saline Agriculture. Pp. 155–160. Kluwer, Dordrecht 2002a.
Mansour, M.M.F., Al-Mutawa, M.M., Salama, K.H.A, Abou Hadid, A.F.: Effect of NaCl and polyamines on plasma membrane lipids of wheat roots. — Biol. Plant. 45: 235–239, 2002b.
Mansour, M.M.F., Lee-Stadelmann, O.Y., Stadelmann, E.J.; Salinity stress and cytoplasmic factors. A comparison of cell permeability and lipid partiality in salt sensitive and salt resistant cultivars and lines of Triticum aestivum and Hordeum vulgare. — Physiol. Plant. 88: 141–148, 1993.
Mansour, M.M.F., Salama, K.H.A.: Comparative responses to salinity in wheat genotypes differing in salt tolerance. 2. Cell permeability, osmotic potential and cytoplasmic viscosity. — Egypt. J. Physiol. 20: 17–32, 1996.
Mansour, M.M.F., Salama, K.H.A.: Cellular basis of salinity tolerance in plants. — Environ. Exp. Bot. 52: 113–122, 2004.
Mansour, M.M.F., Salama, K.H.A., Al-Mutawa, M.M.; Transport proteins and salt tolerance in plants. — Plant Sci. 164: 891–900, 2003.
Mansour, M.M.F., Stadelmann, E.J.: NaCl-induced changes in protoplasmic characteristics of Hordeum vulgare cultivars differing in salt tolerance. — Physiol. Plant. 91: 389–394, 1994.
Mansour, M.M.F., Van Hasselt, P.R., Kuiper, P.J.C.: Plasma membrane lipid alterations induced by NaCl in winter wheat roots. — Physiol. Plant. 92: 473–478, 1994.
Mansour, M.M.F., Van Hasselt, P.R., Kuiper, P.J.C.: Ca2+- and Mg2+-ATPase activities in winter wheat root plasma membranes as affected by NaCl stress during growth. — J. Plant Physiol. 153: 181–187, 1998.
Mansour, M.M.F., Van Hasselt, P.R., Kuiper, P.J.C.: NaCl effects on root plasma membrane ATPase of salt tolerant wheat. — Biol. Plant. 43: 62–66, 2000.
McElhaney, R.N., De Gier, J., Van der Neut-Kok, C.M.: The effect of alterations in fatty acid composition and cholesterol content on the nonelectrolyte permeability of Acholeplasma laidlawii B cells and derived liposomes. — Biochim. biophys. Acta 298: 169–175, 1973.
Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.
Munns, R.: Plant salt tolerance. — In: Sunkar R. (ed.): Methods in Molecular Biology. Pp. 25–38. Springer, Berlin 2010.
Munns, R., Termaat, A.: Whole plant response to salinity. — Aust. J. Plant Physiol. 13: 143–160, 1986.
Munns, R., Tester, M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.
Norberg, P., Liljenberg, C.: Lipid of plasma membranes prepared from oat root cells. Effect of induced water-deficit tolerance. — Plant Physiol. 96: 1136–1141, 1991.
Olias, R., Eljakaoui, Z., Li J., Morales, P., Marin-Manzano, M., Pardo, J. Belver, A.: The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. — Plant Cell Environ. 32: 904–916, 2009.
Panda, S.K., Khan M.H.: Growth, oxidative damage and antioxidant responses in greengram (Vigna radiate L.) under short-term salinity stress and its recovery. — J. Agron. Crop Sci. 195: 442–454, 2009.
Poovaiah, B.W., Leopold, A.C.: Effects of inorganic salts on tissue permeability. — Plant Physiol. 40: 229–234, 1976.
Qadir, M., Tubeilch, A, Akhtam, J., Larbi, A., Minhas, P., Khan, M.: Productivity enhancement of salt-affected environments through crop diversification. — Land Degradation Develop. 19: 429–453, 2008.
Qiu, N., Chen, M., Guo, J., Bao, H., Ma, X., Wang, B.; Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa. — Plant Sci. 172: 1218–1225, 2007.
Quinn, P.J.: Models for adaptive changes in cell membranes. — Biochem. Soc. Trans. 11: 329–331, 1983.
Racagni, G., Pedranzani, A., Taleisnik, E., Abdala, G.: Effect of short-term salinity on lipid metabolism and ion accumulation in tomato roots. — Biol. Plant. 47: 373–377, 2003.
Rochester, C. P., Kjellbom, P., Larrson, C.: Lipid composition of plasma membranesfrom barley leaves and roots, spinach leaves and cauliflower inflorescences. — Physiol. Plant. 71; 257–263, 1987.
Roshandel, P., Flowers, T.: The ionic effects of NaCl on physiology and gene expression in rice genotypes differing in salt tolerance. — Plant Soil 315: 135–147, 2009.
Russell, N.J.: Functions of lipids: structural roles and membrane functions. — In: Ratledge, C., Wilkinson, S.C. (ed.); Microbial Lipids. Pp. 279–365. Academic Press, London 1989.
Sade, N., Gebretsadik, M., Seligmann, R., Schwartz, A., Wallach, R., Moshelion, M.: The role of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity and yield production under salt stress. — Plant Physiol. 152, 245–254, 2010.
Sairam, R.K., Veerabhadra, R.K., Srivastava, G.C.: Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. — Plant Sci. 163: 1037–1046, 2002.
Salama, K.H.A.: Amelioration of NaCl-induced alterations on the plasma membrane of Allium cepa L. by ascorbic acid. — Aust. J. basic appl. Sci. 3: 990–994, 2009.
Salama, K.H.A. Mansour, M.M.F., Ali, F.Z.M., Abou Hadid, A.F.: NaCl-induced changes in plasma membrane lipids and proteins of Zea mays L. cultivars in their response to salinity. — Acta Physiol. Plant. 29: 351–359, 2007.
Senadheera, P., Singh, R., Maathuis, F.J.: Differentially expressed membrane transporters in rice roots may contribute cultivar dependent salt tolerance. — J. exp. Bot. 60: 2553–2563, 2009.
Senaratna, T., McKersie, B.D., Stinson, R.: Association between membrane phase properties and dehydration injury in soybean axes. — Plant Physiol. 76: 759–762, 1984.
Serrano, R., Mulet, J.M., Gabino, R., Maquez, J.A., de Larrinoa, I.F., Leube, M.P., Mendizabal, I., Pascual-Ahuir, A., Proft, M., Ros, R., Montesinos C.: A glimpse of the mechanisms of ion homeostasis during salt stress. — J. exp. Bot. 50: 1023–1036, 1999.
Shalata, A., Neumann, P.M.: Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. — J. exp. Bot. 52: 2207–2211, 2001.
Shinitzky, M.: Membrane fluidity and cellular functions. — In; Shinitzky, M. (ed.): Physiology of Membrane Fluidity. Pp. 1–51. CRC Press, Boca Raton 1984.
Simon, E.W.: Phospholipids and plant membrane permeability. — New Phtytol. 73: 377–420, 1974.
Singh, N.K., Bracken, C.A., Hasegawa, P.M., Handa, A.K., Buckel, S., Mermodoson, M.A., Pfankoch, F., Regnier, F., Bressan, R.A.: Characterization of osmotin. A thaumatinlike protein associated with osmotic adjustment in plant cells. — Plant Physiol. 85: 529–536, 1987.
Stadelmann, E.J., Lee-Stadelmann, O.Y.: Passive permeability. — Methods Enzymol. 174: 246–266, 1989.
Sung, D., Kaplan, F., Guy, C.: Plant HSP70 molecular chaperons: protein structure, gene family, expression and function. — Physiol. Plant. 85: 529–536, 1996.
Surjus, A., Durand, M.: Lipid changes in soybean root membranes in response to salt treatment. — J. exp. Bot. 47; 17–23, 1996.
Takahashi, T., Kakehi, T.I.: Polyamines: ubiquitous polycations with unique roles in growth and stress responses. — Ann. Bot. 105: 1–6, 2010.
Tarchoune, I., Sgherric, C., Izzo, R., Lachaal, M., Ouerghi, Z., Navari-Izzo, F.: Antioxidative response of Ocimum basilicum to sodium chloride and sodium sulphate salinization. — Plant Physiol. Biochem. 48: 772–777, 2010.
Termaat, A., Pasioura, J.B., Munns, R.: Shoot turgor does not limit growth of NaCl affected wheat and barley. — Plant Physiol. 77: 869–872, 1985.
Thompson, J.E., Pauls, K., Chia, L.S, Sridhara, S.: Free radicalmediated changes in the organization of membrane lipid bilayers: a simulation of the effects of senescence. — In; Thomson W.W., Mudd J.B., Gibbs M. (ed.): Biosynthesis and Function of Plant Lipids. Pp. 173–194. Univ. California, Reverside 1983.
Tiwari, J.K., Munshi, A., Kumar, R., Pandey, R.N., Arora, A., Bhat, J., Sureja, A.: Effect of salt stress on cucumber: Na+- K+ ratio, osmolyte concentration, phenols, chlorophyll content. — Acta Physiol. Plant. 32: 103–114, 2010.
Tuna, A.L., Kaya, C., Ashraf, M., Altunlu, H., Yokas, I., Yagmur, B.: The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato grown under salt stress. — Environ. exp. Bot. 59: 173–178, 2009.
Uitert, I., Le Gac, S., Berg, A.: The influence of different membrane components on the electrical stability of bilayer lipid membranes. — Biochim. biophys. Acta 179: 21–31, 2010.
Van Zoelen, E. J., De Jesus, C.H., De Jonge, E., Mulder, M., Block, M.C., De Gier, J.: Non-electrolyte permeability as a tool for studying membrane fluidity. — Biochem. biophys. Acta 511: 335–347, 1978.
Vercesi, A.E., Kowaltowski, A., Grijalba, M., Meinicke, A.R., Castilho, R.F.: The role of reactive oxygen species in mitochondrial permeability transition. — Biosci. Rep. 17: 43–52, 1997.
Very, A.A., Sentenac, H.: Cation channels in the Arabidopsis plasma membrane. — Trends Plant Sci. 7: 168–175, 2002.
Wang, W., Kohler, B., Cao, F., Liu, L.: Molecular and physiological aspects of urea transport in higher plants. — Plant Sci. 175: 467–477, 2008.
Wassall, S.R., Stillwell, W.: Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. — Biochim. Biophys. Acta 1788: 24–32, 2009.
Winicov I.: New molecular approaches to improving salt tolerance in crop plants. — Ann. Bot. 82: 703–710, 1998.
Wu, J., Seliskar, D.M., Gallagher, J.L.: Stress tolerance in the march plant Spartina patens: impact of NaCl on growth and root plasma membrane lipid composition. — Physiol. Plant. 102: 307–317, 1998.
Wu, J., Seliskar, D.M., Gallagher, J.L.: The response of plasma membrane lipid composition in callus of the halophyte, Spartina patens, to salinity stress. — Amer. J. Bot. 92: 852–858, 2005.
Yahya, A., Liljenberg, C., Nilsson, R., Lindberg, S., Banas, A.; Effects of pH and minerals nutrition supply on lipid composition and protein pattern of plasma membranes from sugar beet roots. — J. Plant Physiol. 146: 81–87, 1995.
Yang, F., Xiao, X., Zhang, S., Karpelainen, J.: Salt stress responses in Populus cathayana Rehder. — Plant Sci. 176; 667–677, 2009.
Zamani, S., Bybordi, A., Khorshidi, S., Nezami, T.: Effects of NaCl salinity levels on lipids and proteins of canola (Brassica napus L.) cultivars. — Adv. environ. Biol. 4: 397–403, 2010.
Zenoff, A.N., Hilal, M., Galo, M., Moreno, H.: Changes in lipid composition and inhibition of the extrusion of proton during salt stress in two genotypes of soybeanresistant or susceptible to salt stress. Varietal differences. — Plant Cell Physiol. 35: 729–735, 1994.
Zhao, J., Guo, S., Chen, S., Zhang, H., Zhao, Y.: Expression of yeast YAP1 in transgenic Arabidopsis results in increased salt tolerance. — J. Plant Biol. 52: 56–64, 2009.
Zhang, J.S., Xie, C., Li, Z.Y., Chen, S.Y.: Expression of the plasma membrane ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety. — Theor. appl. Genet. 99: 1006–1011, 1999.
Zhu, J.K.: Plant salt tolerance. — Trends Plant Sci. 6: 15–24, 2001.
Zongli, W., Xiaozhong, L., Zhixia, W.: Physiological studies on salt tolerance in rice. II. Changes in plasmalemma permeability and its relation with membrane lipid peroxidation in leaves under salinity. — J. agr. Sci. 3: 1–9, 1987.
Zwiazek, J.J., Shay, J.M.: The effect of sodium fluoride on cytoplasmic leakage and lipid and fatty acid composition of Jack pine (Pinus banksiana) seedlings. — Can.. J. Bot. 66; 535–541, 1988.
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Mansour, M.M.F. Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant 57, 1–10 (2013). https://doi.org/10.1007/s10535-012-0144-9
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DOI: https://doi.org/10.1007/s10535-012-0144-9