Abstract
Photoautotrophic tobacco (Nicotiana tabacum var. Wisconsin 38) cell cultures were gradually adapted to grow in media containing the normally inhibitory concentration of 20 g l−1 NaCl. Both salt-adapted cultures maintained in 20 g l−1 NaCl (P20) and salt-unadapted (P0) cultures demonstrated similar chloroplast morphology and similar growth characteristics on a dry weight basis, but P20 cells showed reduced growth on a fresh weight basis compared to P0 cells. Compared to P0 cells, intracellular sucrose levels were significantly higher in P20 cells while starch levels in P0 cells were significantly higher than in P20 cells. Levels of intracellular and extracellular reducing sugars, and chlorophyll accumulated to the same degree in P20 and P0 cells, but accumulation was delayed by approximately 13 days in P20 cells. O2 evolution and14[CO2] fixation was more resistant to inhibition by NaCl in P20 cells than in P0 cells. However, significant changes in the abundance of thylakoid membrane proteins could not be demonstrated between P20 and P0 cells although higher levels of Rubisco on a per milligram chlorophyll basis were observed in P0 compared to P20 chloroplasts.
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Abbreviations
- DW :
-
Dry weight
- FW :
-
Fresh weight
References
Ackerson RC, Hebert RR (1981) Osmoregulation in cotton in response to water stress. I. Alterations in photosynthesis, leaf conductance, translocation, and ultrastructure. Plant Physiol 67:484–488
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase inBeta vulgaris. Plant Physiol 24:1–15
Binzel ML, Hasegawa PM, Handa AK, Bressan RA (1985) Adaptation of tobacco cells to NaCl. Plant Physiol 79:118–125
Binzel ML, Hasegawa PM, Rhodes D, Handa S, Handa AK, Bressan RA (1987) Solute accumulation in tobacco cells adapted to NaCl. Plant Physiol 84:1408–1415
Boag S, Portis AR (1984) Inhibited light activation of fructose and sedoheptulose bisphosphatase in spinach chloroplasts exposed to osmotic stress. Planta 160:33–40
Bohnert HJ, Ostrem JA, Cushman JC, Michalowski CB, Rickets J, Meyer G, Derocher EJ, Vernon DM, Krueger M, Vazquez-Moreno L, Elten J, Hoefner R, Schmitt JM (1988)Mesembryan-themum crystallinum, a higher plant model for the study of environmentally induced changes in gene expression. Plant Mol Biol Rep 6:10–28
Bressan RA, Nelson DE, Iraki NM, Larosa PC, Singh NK, Hasegawa PM, Carpita NC (1990) Reduced cell expansion and changes in cell walls of plant cells adapted to NaCl. In: Katterman F (eds) Environmental injury to plants. Academic Press, New York, pp 137–171
Briens M, Lather F (1982) Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell Environ 5:287–292
Dickinson C, Altabella T, Chrispeels MJ (1991) Slow-growth phenotype of transgenic tomato expressing apoplastic invertase. Plant Physiol 95:420–425
Downton WS, Grant WJ, Robinson SP (1985) Photosynthetic and stomatal responses of spinach leaves to salt stress. Plant Physiol 77:85–88
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121
Flowers TJ, Yeo AR (1989) Effects of salinity on plant growth and crop yields. In: Cherry JH (ed) Environmental stress in plants. NATO ASI Series vol 19. Springer, Berlin Heidelberg New York, pp 101–120
Fougere F, Le Roudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236
Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448
Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Anon Rev Plant Physiol 31:149–190
Hasegawa PM, Bressan RA, Handa AK (1986) Cellular mechanisms of salinity tolerance. Hort Science 21:1317–1324
Handa S, Bressan RA, Handa AK, Carpita NC, Hasegawa PM (1983) Solutes contributing to osmotic adjustment in cultured plant cells adapted to water stress. Plant Physiol 73:834–843
Horn ME, Sherrard JH, Widholm JM (1983) Photoautotropic growth of soybean cells in suspension culture. 1. Establishment of photoautotrophic cultures. Plant Physiol 72:426–429
Hosono K (1992) Effect of salt stress on lipid composition and membrane fluidity of the salt-tolerant yeastZygosaccharomyces rouxii. J Gen Microbiol 138:91–96
Huber SC (1989) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol 91:656–662
Huber SC, Huber JLA, McMichael RW Jr (1993) The regulation of sucrose synthesis in leaves. In: Pollock CJ, Farrar JF, Gordon AJ (eds) Carbohydrate partitioning within and between organisms. BIOS Scientific, Oxford, pp 1–26
Kaiser WM (1984) Sites and mechanisms for the inhibition of photosynthesis by water stress. In: Sybesma C (ed) Advances in photosynthesis research, vol 4. Nijhoff Junk, Dordrecht, pp 341–348
Kaiser WM, Kaiser G, Wildman SG, Heber U (1981) Photosynthesis under osmotic stress: effect of high solute concentrations on the permeability properties of the chloroplast envelope and on activity of stroma enzymes. Planta 153:423–429
Keys AJ, Parry MA (1990) Ribulose bisphosphate carboxylase/oxygenase and carbon anhydrase. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry, vol 3. Academic Press, San Diego, pp 1–14
Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685
LaRosa PC, Hasegawa PM, Bressan RA (1984) Photoautotrophic potato cells: transition from heterotrophic to autotrophic growth. Physiol Plant 61:279–286
Locy RD, Chang C-C, Nielsen BL, Singh NK (1996) Photosynthesis in salt-adapted heterotrophic tobacco cells and regenerated plants. Plant Physiol 110:321–328
Mathews MA, Boyer JS (1984) Acclimation of photosynthesis to low water potential. Plant Physiol 74:161–166
Muller M, Santarius KA (1978) Changes in chloroplast membrane lipids during adaptation of barley to extreme salinity. Plant Physiol 62:326–329
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 15:473–497
Murota K, Ohshita Y, Watanabe A, Aso S, Sato F, Yamada Y (1994) Changes related to salt tolerance in thylakoid membranes of photoautotrophically cultured green tobacco cells. Plant Cell Physiol 35:107–113
Neumann K, Bender L (1987) Photosynthesis in cell and tissue culture systems. In: Somers DA, Gengenbach BG, Hackett WP (eds) Plant tissue and cell culture. Proc VIth IAPTC Congress. Liss, New York, pp 151–165
Pham TT, Ferrari IR, Vieira SJ (1984) Effects of water stress on the fatty acid and lipid composition of cotton chloroplasts. In: Sybesma C (ed) Advances in photosynthesis research, vol 4. Nijhoff/Junk, Dordrecht, pp 387–390
Plaut Z, Bachmann E, Oertli J (1991) The effect of salinity on light and dark CO2-fixation of salt-adapted and unadapted cell cultures ofAtriplex and tomato. J Exp Bot 42:531–535
Potter JR, Boyer JS (1973) Chloroplast response to low leaf water potentials. 2. Role of osmotic potential. Plant Physiol 51:993–997
Quick WP, Chaves MM, Wendler R, David M, Rodriques ML, Passaharinho JA, Pereira JS, Adcock MD, Leegood RC, Stitt M (1992) The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions. Plant Cell Environ 15:25–35
Rains DW (1989) Plant tissue and protoplast culture: applications to stress physiology and biochemistry. In: Jones HG, Flowers TJ, Jones MB (eds) Plants under stress. Soc Exp Biol Semin Ser, vol 39. Cambridge University Press, New York, pp 181–196
Rascio A, Platani C, Scalfati G, Tonti A, Difonzo N (1994) The accumulation of solutes and water binding strength in durum wheat. Physiol Plant 90:715–721
Robinson SP (1985) Osmotic adjustment by intact isolated chloroplasts in response to osmotic stress and its effect on photosynthesis and chloroplast volume. Plant Physiol 79:996–1002
Rodgers SMD, Ogren WL, Widholm JM (1987) Photosynthetic characteristics of a photoautotrophic cell suspension culture of soybean. Plant Physiol 84:1451–1456
Rose R, Rose CL, Omi SK, Forty KR, Durall DM, Bigg WL (1991) Starch determination by perchloric acid vs enzymes: evaluating the accuracy and precision of six calorimetric methods. J Agr Food Chem 38:2–11
Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of a salt-sensitive species,Phaseolus vulgaris L. Planta 164:151–162
Seemann JR, Sharkey TD (1986) Salinity and nitrogen effects on photosynthesis, ribulose-1,5-bisphosphate carboxylase and metabolite pool sizes inPhaseolus vulgaris L. Plant Physiol 82:555–560
Sharkey TD (1987) Carbon reduction cycle intermediates in water stressed, intact leaves. In: Randall DD, Sharp EE, Novacky AJ, Blevins DG (eds) Current Topics in Plant Biochemistry and Physiology, vol 6. University of Missouri Press, Columbia, pp 88–103
Sharkey TD, Badger MR (1982) Effects of water stress on photosynthetic electron transport, photophosphorylation, and metabolite levels ofXanthium strumarium mesophyll cells. Planta 156:199–206
Sheen J (1994) Feedback control of gene expression. Photosyn Res 39:427–438
Somogyi M (1945) A new reagent for the determination of sugars. J Biol Chem 160:61–71
Thomas JC, De Armond RL, Bohnert HJ (1992) Influence of NaCl on growth, proline, and phosphoenolpyruvate carboxylase levels inMesembryanthemum crystallinum suspension cultures. Plant Physiol 98:626–631
Von Schaewen A, Stitt M, Schmidt R, Sonnewald U, Willmitzer L (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J 9:3033–3044
Walker DA, Cerovic ZG, Robinson SP (1987) Isolation of intact chloroplasts: general principles and criteria of integrity. Methods Enzymol 148:145–187
Watad A, Reinhold L, Lerner H (1983) Comparison between a stable NaCl-selectedNicotiana cell line and the wild type. Plant Physiol 73:624–629
Widholm JM (1992) Properties and uses of photoautotrophic plant cell cultures. Int Rev Cytol 132:109–175
Winicov I, Seemann JR (1990) Expression of genes for photosynthesis and the relationship to salt tolerance of alfalfa (Medicago sativa) cells. Plant Cell Physiol 31:1155–1161
Zrenner R, Stitt M (1991) Comparison of the effect of rapidly and gradually developing water-stress on carbohydrate metabolism in spinach leaves. Plant Cell Environ 14:939–946
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Communicated by I. K. Vasil
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Chang, C.C., Locy, R.D., Smeda, R. et al. Photoautotrophic tobacco cells adapted to grow at high salinity. Plant Cell Reports 16, 495–502 (1997). https://doi.org/10.1007/BF01092773
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DOI: https://doi.org/10.1007/BF01092773