THE EFFECT OF SALT AND OSMOTIC STRESS ON THE RETENTION OF POTASSIUM BY EXCISED BARLEY AND BEAN ROOTS
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1 New Phytol (1975) 75, ^; THE EFFECT OF SALT AND OSMOTIC STRESS ON THE RETENTION OF POTASSIUM BY EXCISED BARLEY AND BEAN ROOTS BY H. Department of Biology, Pahlavi University, Shiraz, Iran {Received 16 December 1974) SUMMARY The effect of different concentrations of NaCl, mannitol and CaCIj on the retention of potassium ion by preloaded roots of barley, Hordeum vulgare, and bean, Phaseolus vulgaris, indicated that 10 mm NaCl had no effect on potassium loss, but 50 mm NaCl or more increased the rate of efflux. Barley roots appeared 10 be more sensitive to salt stress than bean roots since 100 mm NaCl caused 78% potassium loss over 6.5 h by barley as compared with 40% loss by bean roots. Mannitol up to 200 mm had no eifect on the retention of potassium by barley roots but slightly increased the potassium loss from bean roots (26%). The results suggested that salt stress is more effective than osmotic stress in disrupting the membrane permeability and calcium ions can prevent the increased permeability caused by osmotic or ionic stress. INTRODUCTION Salt avoidance which results from the impermeability of the cytoplasmic and vacuolar membranes to salt is thought to be one of the controlling mechanisms involved in resistance of plants to saline habitats, thus it is suggested that glycophytes may have a higher degree of permeability to Na"*" than halophytes, making them less resistant to salt (Levitt, 1972). Many authors have demonstrated that a reduction in uptake or an increase in efflux of ions or both results when plant tissues are subjected to water or salt stress (Sutcliffe, 1954; Greenway, Klepper and Hughes, 1968; Minchin and Baker, 1969; Dessimoni Pinto and Flowers, 1970; Smith, St John and Parrondo, 1973; Nassery and Baker, 1974). The work of Smith and colleagues (1973) demonstrated that the water stress induced by mannitol affects primarily the uptake mechanism rather than the efflux in maize roots. However, the permeability changes resulting from the osmotic stress have often not been differentiated from the salt or ionic stress. The present work aims at distinguishing the effect of salt and osmotic stress on permeability changes of barley and bean roots which are known to differ in their salt resistance. MATERIALS AND METHODS Barley seeds {Hordeum vulgare var. valki) and white bean seeds {Phaseolus vulgaris var. Marmari) were grown in o.i mm Ca (NO 3)2 as described by Nassery (1971 and 1972). When their root-systems had grown to about 4 cm, they were placed in a solution 63
2 H. NASSERY containing io mm KCl + o.i mm Ca(NO3)2 overnight for i6 h. After this loading period, about 1500 mg fresh roots were excised and washed for 15 min in three changes of O.I mm HCl (ph = 4.0) to allow a complete free space wash (Nassery, 1971 and 1972). The loss of potassium was measured over 6.5 h in three replicates each of 100 mg fresh root that were placed in a 125 ml ffask containing 75 ml of the required solution in the presence of o.i mm Ca (NO3)2. The temperature of the loading and the efflux solutions was maintained at 25 C. During efflux, the ffasks were shaken at about 180 strokes per min in a Grant shaking bath. After the efflux period, the roots were washed with 2 litres of running distilled water followed by 2 litres of running 0.1 mm HCl, the approximate washing time being 1.5 min. The quantity of potassium lost from the roots or that of sodium absorbed was measured after the dry-ashing of the roots by flame photometry as described by Nassery (1971 and 1972). RESULTS Fig. I demonstrates the effect of different concentrations of sodium chloride upon the retention of potassium ion by preloaded barley roots. It is evident that NaCl at 10 mm does not increase the permeability of barley roots to potassium but, 50 and 100 mm NaCl increases the potassium loss by 29% and 78% respectively. There is no further significant increase at 250 mm NaCl. It is also clear from Table i that there is an internal accumulation of sodium above the external concentration at 10 and 50 mm NaCl but hardly at 100 mm, and none at 250 mm NaCl. This observation supports the pattern of potassium loss and indicates that a breakdown of the permeability barrier to potassium and sodium ion occurs at 100 mm NaCl in barley roots. Fig. 2 which is the result of a similar treatment given to bean roots indicates that, at 10 and 50 mm NaCl, bean roots also behave as barley. However, contrary to the behaviour of barley roots, bean roots resist any increase in permeability to potassium ion when NaCl concentration is raised I50Q 01 g 1000 D O 1000 cr io Fig. 1 Fig. 2 Fig. I. The effect of different concentrations of sodium chloride upon absorption of sodium (O) and retention of potassium ( ) by excised barley roots. Vertical bars indicate ± S.E.M. Fig. 2. The effect of different concentrations of sodium chloride upon absorption of sodium (O) and retention of potassium ( ) by excised bean roots. Vertical bars indicate + S.E.M.
3 Table 2 demonstrates the effect of mannitol concentrations approximately iso-osmotic to those of NaCl which increased the permeability of barley and bean roots to potassium ion. It is evident by contrast that barley roots resisted changes of permeability up to 200 mm mannitol, (which is iso-osmotic to 100 mm NaCl that increased potassium efflux by 78%). Although mannitol at 500 mm increased the potassium efflux to 66% that is considerably lower than 85% loss induced by 250 mm NaCl. Table 2 also demonstrates that bean roots lose 20%, 26% and 53% of their potassium at 100, 200 and 500 mm mannitol which are considerably lower than the corresponding losses induced by equiosmotic NaCl concentrations (35%, 60% and 90%). The reslilts of Table 2 also indicate that bean root is more sensitive than barley root to osmotic stress induced by 100 and 200 mm mannitol. Retention of potassium 65 Table i. The accumulation factor for sodium absorption hy barley and bean roots calculated from the values given in Figs, i and 2 NaCl mm Tissue concentration (// equiv./g fresh wt) Solution concentration {fx equiv./ml) Bean Barley 3-O I.I 0.26 from 50 to 100 mm. It is also clear from Table i that the accumulation factor for sodium absorption by bean roots is greater than barley, particularly at concentrations of NaCl above 50 mm. Thus, an accumulation factor of 1.3 at 100 mm NaCl for bean roots gives support to the pattern of potassium retention and indicates that 100 mm NaCl does not increase the permeability to the point of complete breakdown as observed in barley roots. Table 2. The effect of different concentrations of mannitol upon the retention of potassium by excised bean and barley roots. Figures in parentheses are retentions as % of control Mannitol cone. (mm) fi equiv retained/g dry Bean 1483 ±43 (100) ii9o±55 (80) (74) 701 ±57 (47). K root/6.5 h Barley I43O±I39 (100) i334±75 (93) i562± 105 (109) 486 ±43 (34)
4 ,.s,;:.'v^,:,!i-.s.5:.vsf;';;;:;'' :/,,,.; 66 H. NASSERY Table 3 shows that CaCl2 concentrations up to 250 mm do not affect the retention of potassium ion by excised barley or bean roots, suggesting that calcium ions prevent the disruption of membrane permeability that would be caused by low water potential or by destructive concentrations of the chloride ion. Table 3. The effect of different concentrations of calcium chloride upon the retention of potassium by excised bean and barley roots. Figures in parentheses are retentions as % of zero CaCl2 addition H equiv. K retained/g dry root/6.s h CaCl2 cone. (mm) Bean Barley (100) (100) is99±i9o (90) (112) ± (107) (109) IOO ±57 (98) (100) ±51 (99) (121) DISCUSSION The effect of salt and osmotic stress on the retention of potassium by excised bean and barley roots indicates that salt stress increased the permeability more than the equiosmotic stress caused by mannitol. This indicates that salt has an additional effect on permeability to that caused by its osmotic potential. Levitt (1972, p ) reviewed the work of many authors who have shown a greater inhibition of growth, yield and seed germination by salt stress than by iso-osmotic organic substances. Flowers and Hanson (1969) found that the reduced phosphorylation rate of soybean mitochondria that could be induced by water potentials lower than 15 bars was not removed by hydrostatic pressure, they suggested that KCl had other effects than reduction of water potential per se. Similarly, the observation of Greenway and Osmond (1972) that mannitol at iso-osmotic concentrations with NaCl and KCl had less inhibitory effect on the activity of malate dehydrogenase from bean leaves is also of interest in demonstrating the kind of way in which salt stress can be more destructive than the osmotic stress. It is likely that the observation of Smith et al. (1973) that mannitol inhibited absorption more than retention may not apply to salt stress. The observation that 10 mm NaCl did not increase the permeability to potassium ion indicates that plasmalemma does not become permeable at system 2 range of concentrations as is believed by Epstein and colleagues (see Epstein, 1972) and also supports our previous observations on bean and barley roots (Nassery and Baker, 1974; Nassery and Didehvar, 1975). The experiments with CaClj indicated that even at 250 mm CaCl2, where plants were subjected to both a water potential lower than 500 mm mannitol and Cl~ concentration
5 Retention of potassium 67 twice that of 250 mm NaCl, no loss of permeability occurred. This effect of calcium ion on maintenance of cell permeability has been suggested to involve a non-metabolic as well as a metabolic pathway (Jennings, 1964; Handley, Metwally and Overstreet, 1965; Mengel and Helal, 1967; Nassery, 1971; Epstein, 1972; Simon and Raja Harum, 1972). The observation of Lahaye and Epstein (1971) that calcium at few mm increased the resistance of i week-old bean plants to 50 mm NaCl and moreover reduced the level of sodium in the shoot and root of bean plants supports our short-term observation on the effect of calcium ion on maintenance of membrane permeability. The recent work of Frota and O'Leary (1973) further demonstrates that at high sodium chloride concentrations (some 100 mm) bean roots become leaky and calcium loss from the cell interior could cause physiological disturbances contributing to salt injury. ACKNOWLEDGMENT I would like to thank Mr A. A. Siadat-Pour for his interest and assistance in the experimental work of this investigation. REFERENCES DESSIMONI PINTO, C. M. & FLOWERS, T. J. (1970). The effect of water deficits on slices of beetroot and potato tissue. II. Changes in respiration and permeability to solutes. J. exp. Bot., 21, 754. EPSTEIN, E. (1972). Mineral Nutrition of Plants: Principles and Perspectives. John Wiley & Sons, Inc., FLOWERS, T. J. & HANSON, J. B. (1969). The effect of reduced water potential on soybean mitochodria. FROTA,^J. N.'^ ''& O'LEARY, J. W. (1973). Calcium loss from plant roots during osmotic adjustment. GREENWIY, H.,'KLEPPE'R! B. & HUGHES, P. G. (1968). Effects of low water potential on ion uptake and loss for excised roots. P/a«to, 80, 129..,...,^., GREENWAY, H. & OSMOND, C. B. (1972). Salt responses of enzymes from species differing in salt tolerance. HANDLE? R^^METW^AVL^^'A. & OVERSTREET, R. (1965). Effects of Ca upon metabolic and non-metabolic uptakeoinaandrhhy root segments oi Zea mays. Plant Phystol. Lancaster, 40, 513- JENNINGS, D. H. (1964). The effect of cations on absorption of phosphate by beech mycorrhizal roots. r/rtepstetn', E. (1971). Calcium and salt toleration by bean plants. Physiol. Plant,25, 213 I1V^7T ] {j972).respones of Plants to Environmental Stresses. Academic Press, New York and London MENGEL K & HELAL M (1967). The influence of the exchangeable Ca++ of young barley roots on the fluxes of K^ and phosphate-an interpretation of the Viets effect. Z. PflansenphystoL,p, MINCHS' F. R. & BAKER, D. A. (1969). Water dependent and water independent fluxes of potassium in eii.uamg root systems oi Ricinus communis. Pianta, %g, 211. p;,,,^/ -«,1-. NASSERY H (IQ7I) Some aspects of potassium loss from excised barley roots. New Phytol., ^o, 113. NASSERY', H! (1972): ThTloss of potassium and sodium from excised barley and bean roots. New Phytol,." & BAKER, D. A. (1974). Extrusion of sodium by barley roots. III. The effect of high salinity t ^^ of ions by meristematic V WtRAiT^ARUM ^^t^. ^J^i^^^^^^^on. y. exp. Bot., , t^z: I: a," IT. Jo^HN B H.' & PARRON'D'O,^ R. (1973). Influence of mannitol on absorption and retention of'rubidium by excised corn roots. ^mer.j.-bol, 60, 839. SUTCLIFFE, J. F. (1954). The absorption of potassium ions by plasmolysed cells. J. exp. Bot., 5, 2i>
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