Mechanisms of Adaptation to Salinity in Cultured Glycophyte Cells

  • M. L. Binzel
  • F. D. Hess
  • R. A. Bressan
  • P. M. Hasegawa
Part of the NATO ASI Series book series (volume 19)


Cultured cells of Nicotiana tabacum var Wisconsin 38 can be adapted to grow in levels of NaCl similar to those tolerated by many halophytes. Adaptation of these cells to high levels of salinity is associated with reduced cell expansion even though turgor is maintained, a result similar to that commonly reported for whole plants exposed to salinity and/or drought. Glycophytic cells adapted to salinity apparently utilize many of the same biochemical and physiological processes to deal with salinity as do halophytes. Na+ and Cl- are the principal solutes contributing to the extensive osmotic adjustment these cells undergo in response to salinity, although organic solutes, particularly proline, accumulate as well. Adapted cells accumulate less Na+ than unadapted cells when grown in comparable levels of NaCl, suggesting that the ability to regulate ion accumulation may be an important component of the salinity tolerance of these cells. The majority of Na+ and Cl- accumulated by the cells is compartmentalized in the vacuole, such that cytosolic levels of these ions remain near 100 mM at external NaCl concentrations of 428 mM. Current research is directed at examining changes in membrane transport properties associated with salinity in order to assess their contribution to the ability of the cells to tolerate salt.


Salt Tolerance Salinity Tolerance Tonoplast Vesicle Isobutyl Ester Unadapted Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ben-Hayyim G, Kochba J (1983) Aspects of salt tolerance in a NaCl-selected stable cell line of Citrus sinensis. Plant Physiol 72:685–690PubMedCrossRefGoogle Scholar
  2. Bennett AB, Spanswick RM (1983) Optical measurements of ΔpH and Δψ in corn root membrane vesicles: Kinetic analysis of Cl- effects on a proton translocating ATPase. J Membr Biol 71:95–107CrossRefGoogle Scholar
  3. Binzel ML, Hess FD, Bressan RA, Hasegawa PM (1988) Intracellular compartmentation of ions in salt adapted tobacco cells. Plant Physiol 86:607–614PubMedCrossRefGoogle Scholar
  4. Binzel ML,Hasegawa PM, Rhodes D, Handa S, Handa AK, Bressan RA (1987) Solute accumulation in tobacco cells adapted to NaCl. Plant Physiol 84:1408–1415PubMedCrossRefGoogle Scholar
  5. Binzel ML, Hasegawa PM, Handa AK, Bressan RA (1985) Adaptation of tobacco cells to NaCl. Plant Physiol 79:118–125PubMedCrossRefGoogle Scholar
  6. Blum A (1987) Methods of plant breeding for drought resistance. In: Monti L, Porceddu E (eds) Drought resistance in plants: Physiological and Genetic Aspects. Comm European Commun, Luxembourg, pp 235–254Google Scholar
  7. Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78:163–167PubMedCrossRefGoogle Scholar
  8. Blumwald E, Poole RJ (1985) Nitrate storage and retrieval in Beta vulgaris: Effects of nitrate and chloride on proton gradients in tonoplast vesicles. Proc Natl Acad Sci, USA 82:3683–3687PubMedCrossRefGoogle Scholar
  9. Braun Y, Hassidim M, Lerner HR, Reinhold L (1988) Evidence for a Na+/H+ antiporter in membrane vesicles isolated from roots of the halophyte Atriplex nummularia. Plant Physiol 87:104–108PubMedCrossRefGoogle Scholar
  10. Bressan RA, Singh NK, Handa AK, Mount R, Clithero J, Hasegawa PM (1987) Stability of altered genetic expression in cultured plant cells adapted to salt. In: Monti L, Porceddu E (eds) Drought Resistance in Plants: Physiological and Genetic Aspects. Comm Europ Commun, Luxembourg, pp 41–58Google Scholar
  11. Bressan RA, Singh NK, Handa AK, Kononowicz A, Hasegawa PM (1985) Stable and unstable tolerance to NaCl in cultured tobacco cells. In: Freeling M (ed) UCLA Symposium on Plant Genetics. AR Liss, New York, pp 755–769Google Scholar
  12. Bressan RA, Handa AK, Handa S, Hasegawa PM (1982) Growth and water relations of cultured tomato cells after adjustment to low external water potentials. Plant Physiol 70:1303–1309PubMedCrossRefGoogle Scholar
  13. Cheeseman JM (1988) Mechanisms of salinity tolerance in plants. Plant Physiol 87:547–550PubMedCrossRefGoogle Scholar
  14. Croughan TP, Stavarek SJ, Rains DW (1978) Selection of a NaCl tolerant line of cultured alfalfa cells. Crop Sci 18:959–963CrossRefGoogle Scholar
  15. Dix PJ, Street HE (1975) Sodium chloride-resistant cultured cell lines from Nicotiana sylvestris and Capsicum annuum. Plant Sci Lett 5:231–237CrossRefGoogle Scholar
  16. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121CrossRefGoogle Scholar
  17. Garbarino J, DuPont FM (1988) NaCl induces a Na+/H+ antiport in tonoplast vesicles from barley roots. Plant Physiol 86:231–236Google Scholar
  18. Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  19. Grumet R, Hanson AD (1986) Genetic evidence for an osmoregulatory function of glycinebetaine accumulation in barley. Aust J Plant Physiol 13:353–364CrossRefGoogle Scholar
  20. Harvey DMR (1985) The effects of salinity on ion concentrations within the root cells ofZea mays L. Planta 165:242–248CrossRefGoogle Scholar
  21. Hasegawa PM, Bressan RA, Handa AK (1986) Cellular mechanisms of salinity tolerance. HortScience 21:317–324Google Scholar
  22. Hasegawa PM, Bressan RA, Handa AK (1980) Growth characteristics of NaCl selected and nonselected cells of Nicotiana tabacum L. Plant Cell Physiol 21:1347–1355Google Scholar
  23. Hess SR, Hasegawa PM, Bressan RA (1985) Sucrose optima for growth of salt-adapted tobacco cells. HortScience 20(3):522Google Scholar
  24. Iraki N, Bressan RA, Hasegawa PM, Carpita NC (1988) Alteration of the physical and chemical structure of the primary cell wall of growth limited plant cells adapted to osmotic stress. Plant Physiol(In press)Google Scholar
  25. Jeschke WD (1984) K+-Na+ exchange at cellular membranes, intracellular compartmentation of cations and salt tolerance. In: Staples RC, Toenniessen GH (eds) Salinity Tolerance in Plants. Strategies for Crop improvement. John Wiley and Sons, New York, pp 37–66Google Scholar
  26. Kochba J, Ben-Hayyim G, Spiegel-Roy P, Saad S, Neumann H (1982) Selection of stable salt-tolerant callus cell lines and embryos in Citrus sinensis and C. aurantium. Z Pflanzenphysiol 106:111–118Google Scholar
  27. Ladyman JAR, Ditz KM, Grumet R, Hanson AD (1983) Genotypic variation for glycinebetaine accumulation by cultivated and wild barley in relation to water stress. Crop Sci 23:465–468CrossRefGoogle Scholar
  28. Lowe R, Hamilton T (1967) Rapid method for determination of nitrate in plant and soil extracts. J Agric Food Chem 15:359–361CrossRefGoogle Scholar
  29. Leigh RA, Wyn Jones RG (1984) An hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13CrossRefGoogle Scholar
  30. Matsuda K, Riazi A (1981) Stress-induced osmotic adjustment in growing regions of barley leaves. Plant Physiol 68:571–576PubMedCrossRefGoogle Scholar
  31. McHughen A (1987) Salt tolerance through increased vigor in a flax line (STS-II) selected for salt tolerance in vitro. Theor Appl Genet 74:727–732CrossRefGoogle Scholar
  32. Meyer RF, Boyer JS (1981) Osmoregulation, solute distribution, and growth in soybean seedlings having low water potentials. Planta 151:482–489CrossRefGoogle Scholar
  33. Michelena VA, Boyer JS (1982) Complete turgor maintenance at low water potentials in the elongating region of maize leaves. Plant Physiol 69:1145–1149PubMedCrossRefGoogle Scholar
  34. Nabors MW, Daniels A, Nadolny L, Brown C (1975) Sodium chloride tolerant lines of tobacco cells. Plant Sci Lett 4:155–159CrossRefGoogle Scholar
  35. Pallaghy CK,Scott BIH (1969) The electrochemical state of cells of broad bean roots II.Potassium kinetics in excised root tissue. Aust J Biol Sci 22:585–600Google Scholar
  36. Poljakoff-Mayber A (1982) Biochemical and physiological responses of higher plants to salinity stress. In: San Pietro A (ed) Biosaline Research, A Look to the Future. Plenum Press, New York, pp 245–269Google Scholar
  37. Rangan TS, Vasil IK (1983) Sodium chloride tolerant embryogenic cell lines of Pennisetum americanum (L.) K. Schum. Ann Bot 52:59–64Google Scholar
  38. Reuvini M, Bennett AB, Bressan RA, Hasegawa PM (1988) Activity changes in tonoplast ATPase of NaCl adapted cells. Plant Physiol 86S:76Google Scholar
  39. Rhodes D, Myers AC, Jamieson G (1981) Gas chromatography-mass spectro-mometry of N-heptafluorobutyryl isobutyl esters of amino acids in the analysis of the kinetics of [15N]H4 + assimilation in Lemna minor L. Plant Physiol 68:1197–1205PubMedCrossRefGoogle Scholar
  40. Rietveld RC, Singh NK, Hasegawa PM, Bressan RA (1988) A selectable mtDNA polymorphism is found in salt tolerant tobacco mitochondria. Plant Physiol 86S:136Google Scholar
  41. Sacher RF, Staples RC, Robinson RA (1982) Saline tolerance in hybrids of Lycopersicon esculentum x Solanum penellii and selected breeding lines. In: San Petro A (ed) Biosaline Research: A Look to the Future. Plenum Press, New York, pp 325–336Google Scholar
  42. Schales O, Schales SS (1941) A simple and accurate method for the determination of chloride in biological fluids. J Biol Chem 140:879–884Google Scholar
  43. Schroppel-Meier G, Kaiser WM (1988) Ion homeostasis in chloroplasts under salinity and mineral deficiency I. Solute concentrations in leaves and chloroplasts from spinach plants under NaCl or NaNO3 salinity. Plant Physiol 87:822–827PubMedCrossRefGoogle Scholar
  44. Schumaker KS, Sze H (1987) Decrease of pH gradients in tonoplast vesicles by NO3 - and Cl-: Evidence for H+-coupled anion transport. Plant Physiol 83:490–496PubMedCrossRefGoogle Scholar
  45. Shannon MC (1984) Breeding, selection and the genetics of salt tolerance. In: Staples RC, Toenniessen GH (eds) Salinity Tolerance in Plants. Strategies for Crop Improvement. John Wiley and Sons, New York, pp 231–255Google Scholar
  46. Singh NK, LaRosa PC, Nelson D, Iraki N, Carpita NC, Hasegawa PM, Bressan RA (1988) Reduced growth rate and changes in cell walls of plant cells adapted to NaCl. (this volume)Google Scholar
  47. Somogyi M (1952) Notes on sugar determinations. J Biol Chem 195:19–23Google Scholar
  48. Storey R, Pitman MG, Stelzer R, Carter C (1983) X-ray micro-analysis of cells and cell compartments of Atriplex spongiosa. J Exp Bot 34:778–794CrossRefGoogle Scholar
  49. Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657CrossRefGoogle Scholar
  50. Termaat A, Passioura JB, Munns R (1985) Shoot turgor does not limit shoot growth of NaCl-affected wheat and barley. Plant Physiol 77:869–872PubMedCrossRefGoogle Scholar
  51. Van Volkenburgh E, Boyer JS (1985) Inhibitory effects of water deficit on maize leaf elongation. Plant Physiol 77:190–194PubMedCrossRefGoogle Scholar
  52. Watad A -EA, Pesci P-A, Reinhold L, Lerner HR (1986) Proton fluxes as a response to external salinity in wild type and NaCl-adapted Nicotiana cell lines. Plant Physiol 81:454–459PubMedCrossRefGoogle Scholar
  53. Watad AA, Reinhold L, Lerner HR (1983) Comparison between a stable NaCl-selected Nicotiana cell line and the wild type. K+, Na+, and proline as a function of salinity. Plant Physiol 73:624–629PubMedCrossRefGoogle Scholar
  54. Wyn Jones RG, Gorham J, McDonnell E (1984) Organic and inorganic solute contents as selection criteria for salt tolerance in the Tritícea. In: Staples RC, Toenniessen GH (eds) Salinity Tolerance in Plants. Strategies for Crop Improvement. John Wiley and Sons, New York, pp 189–203Google Scholar
  55. Wyn Jones RG (1981) Salt tolerance. In: Johnson CB (ed) Physiology Processes Limiting Plant Productivity. Butterworth, London, pp 271–292Google Scholar
  56. Wyn Jones RG, Gorham J (1980) Aspects of salt and drought tolerance in higher plants. In: Kosuge T, Meredith CP, Hollaender A (eds) Genetic Engineering of Plants, An Agricultural Perspective. Plenum Press, New York, pp 355–370Google Scholar
  57. Yeo AR, Flowers TJ (1984) Mechanisms of salinity resistance in rice and their role as physiological criteria in plant breeding. In: Staples RC, Toenniessen GH (eds) Salinity Tolerance in Plants. Strategies for Crop Improvement. John Wiley and Sons, New York, pp 151–170Google Scholar
  58. Yeo AR (1981) Salt tolerance in the halophyte Suaeda maritima L. Dum.: intracellular compartmentation of ions. J Exp Bot 32:487–497CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • M. L. Binzel
    • 1
  • F. D. Hess
    • 1
    • 2
  • R. A. Bressan
    • 1
  • P. M. Hasegawa
    • 1
  1. 1.Center for Plant Environmental Stress Physiology, Department of HorticulturePurdue UniversityW. LafayetteUSA
  2. 2.Zoecon Research Institute, Sandoz Crop Protection InstitutePalo AltoUSA

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