Journal of Experimental Botany, Vol. 52, No. 364, pp. 2207-2211,
November 1, 2001
© 2001 Oxford University Press
Original Papers |
Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation
Plant Physiology Laboratory, Faculty of Agricultural Engineering, Technion-Israel Institute of Technology, Haifa 32000, Israel
Received 5 April 2001; Accepted 29 June 2001
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Abstract |
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The transition from reversible to permanent wilting, in whole tomato seedlings (Lycopersicon esculentum Mill. cv. M82) following severe salt-stress by root exposure to 300 mM NaCl, was investigated. Salinized seedlings wilted rapidly but recovered if returned to non-saline nutrient solution within 6 h. However, after 9 h of salt-treatment 100% of the seedlings remained wilted and died. Remarkably, the addition of an anti-oxidant (0.5 mM ascorbic acid) to the root medium, prior to and during salt-treatment for 9 h, facilitated the subsequent recovery and long-term survival of c. 50% of the wilted seedlings. Other organic solutes without known anti-oxidant activity were not effective. Salt-stress increased the accumulation in roots, stems and leaves, of lipid peroxidation products produced by interactions with damaging active oxygen species. Additional ascorbic acid partially inhibited this response but did not significantly reduce sodium uptake or plasma membrane leakiness.
Key words: NaCl-stress, ascorbic-acid, lipid-peroxidation, tomato, survival.
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Introduction |
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Adverse plant responses to salinity-stress depend on the osmotic and toxic effects of salt and on the level and duration of the stress. Responses range from growth inhibition and accelerated leaf senescence under moderate stress, to permanent wilting of shoots with subsequent plant death, under severe stress. The mechanisms underlying these different responses to salinity are still far from clear (see reviews by Munns, 1993
; Flowers and Yeo, 1995; Neumann, 1997; Glenn et al., 1999). This report investigates the rapid transition from reversible to permanent wilting in hydroponically grown tomato seedlings (Lycopersicon esculentum Mill. cv. M82) exposed to high levels of NaCl salinity. One possibility was that salt-induced cellular accumulation of damaging active-oxygen species (AOS) might be involved.
AOS can damage essential membrane lipids as well as proteins and nucleic acids (reviewed by Inzé and Van Montague, 1995; Becana et al., 1998; Noctor and Foyer, 1998). Levels of AOS in plant cells are normally controlled by protective antioxidant activity. However, under environmental stress AOS production can increase and protective activity may then become inadequate. Various associations between saline or drying environments and endogenous levels of water-soluble anti-oxidants and/or anti-oxidative enzymes have been reported (Smirnoff, 1993; Gosset et al., 1994; Zhang and Kirkham, 1996; Gueta-Dahan et al., 1997; Lechno et al., 1997; Shalata and Tal, 1998; Tsugane et al., 1999). For example, Tsugane et al. determined that wild-type Arabidopsis seedlings could not survive in 200 mM NaCl (Tsugane et al., 1999). However, they isolated a recessive deletion mutant which showed c. 20% survival under these saline conditions. As compared with the wild type, the mutant showed higher anti-oxidative activities of superoxide dismutase and ascorbate peroxidase. Tsugane et al. suggested that the full potential for anti-oxidative activity and associated resistance to salinity, might be blocked in wild-type plants (Tsugane et al., 1999). If so, artificially induced increases in anti-oxidative activity might increase resistance to salinity stress.
The activity of anti-oxidant enzymes associated with the detoxification of active oxygen species can be increased via appropriate gene transfer and the possible effects of such transformations on plant resistance to environmental stresses have been investigated (Inzé and Van Montague, 1995; Noctor and Foyer, 1998; McKersie et al., 1999). However, this approach does not always lead to the expected physiological results. Thus, overproduction of ascorbate peroxidase or of enzymes involved in glutathione synthesis, did not increase and even decreased plant resistance to oxidative stresses (Torsethaugen et al., 1997; Creissen et al., 1999).
Another approach would be to increase the cellular level of enzyme substrates such as ascorbic acid (vitamin C). Ascorbic acid is a small, water-soluble anti-oxidant molecule which acts as a primary substrate in the cyclic pathway for enzymatic detoxification of hydrogen peroxide. In addition, it acts directly to neutralize superoxide radicals, singlet oxygen or superoxide and as a secondary anti-oxidant during reductive recycling of the oxidized form of 
-tocopherol, another lipophilic anti-oxidant molecule (Noctor and Foyer, 1998). There appear to have been no quantitative investigations of the effects of an additional supply of ascorbic acid on plant resistance to severe salt stress.
This report investigates (a) whether the onset of permanent wilting in whole tomato seedlings during root exposure to severe salt-stress, is associated with salt-induced increases in cellular levels of damaging active-oxygen species and (b) whether an additional supply of ascorbic acid to seedlings might decrease the build-up of active oxygen species and thereby increase resistance to salt-stress.
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Materials and methods |
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Plant growth
Seeds of cultivated tomato (Lycopersicon esculentum Mill. cv. M82) were germinated in the dark for 2 d and then grown on polystyrene floats with the roots held in aerated 0.1 strength modified Hoagland solution plus 5 mM CaCl2 in order to maintain calcium activity at adequate levels (Zidan et al., 1991
). The growth chamber was at 27±2 °C with a 12 h day and 150 µmol s-1 m-2 light intensity. Relative humidity was 35% by day and 60% by night. After 14 d, seedlings at the stage of third leaf opening were assayed.
Seedling survival
Before salt-treatment, 10–14 uniform seedlings were incubated with their roots in 5.0 l of mineral nutrient solution with or without the addition of freshly prepared 0.5 mM ascorbic acid, for 24 h. The optimal concentration was chosen after preliminary experiments with 0.1 and 1.0 mM ascorbic acid. After 24 h, seedlings were again transferred to fresh nutrient solution ±300 mM NaCl ±0.5 mM ascorbic acid (or other organic solutes where indicated). NaCl at 300 mM (-1.35 MPa osmotic potential) rapidly induced complete wilting of the shoots. Where indicated, solutions of polyethylene glycol (PEG 6000 at 293 g l-1) were used to simulate the osmotic effects of 300 mM NaCl. PEG 6000 is a polymeric osmoticum which, unlike NaCl, does not penetrate plant cells and is relatively non-toxic (Chazen and Neumann, 1994). The equivalent osmotic potential of solutions of NaCl and PEG 6000 were based on standard tables for NaCl and the calibration of Money for PEG 6000 (Money, 1989). Survival results are means±SE for three separate experiments with batches of 10 or more plants per treatment.
Ascorbic acid
The effect of exogenous supply on tissue levels of ascorbic acid was determined. Seedlings were incubated with or without 0.5 mM ascorbic acid for 24 h and then for an additional 9 h with or without 300 mM NaCl. After rinsing in 0.5 mM CaCl2, root, stem and leaf tissues were frozen with liquid nitrogen and ground in a mortar and pestle. Ground tissue was mixed with 10 ml of 10% TCA and the supernatent obtained after centrifugation at 18 000 g for 15 min at 4 °C was analysed for total ascorbic acid (according to Walker and McKersie, 1993). Briefly, any dehydroascorbic acid was reduced to ascorbate with ß-mercaptoethanol and excess mercaptoethanol was complexed with N-ethylmaleimide. Total ascorbate was then assayed under acid conditions by measuring the reduction of Fe2+ to Fe3+ and the formation of a pink coloured bipiridyl–Fe complex at 525 nm. Results are means±SD, n=3.
Lipid peroxidation
The comparative rates of lipid peroxidation were assayed by determining the levels of malondialdehyde in 1 g aliquots of root, stem (hypocotyl tissue from below the cotyledons) or leaf tissue. Malondialdehyde is a product of lipid peroxidation and was assayed by the thiobarbituric acid reaction (Heath and Packer, 1968). Addition of extra ascorbic acid or NaCl to the extraction medium did not affect the measurements and significant readings were not obtained without addition of the reactive TBA (thiobarbituric acid). Results for roots, stems and leaves are each means±SE for three separate experiments with batches of 10 or more plants per treatment.
Salt-induced membrane damage
The roots of intact seedlings were gently rinsed for 5 min in large volumes of 0.5 mM CaCl2 and then with water prior to incubation under dim light in small vials containing 5 ml of deionized water. After incubation for 1 h the electrical conductivity (EC) of the bathing solution was measured using an El Hama conductivity meter. The roots were then killed by immersion in 5 ml of fresh water at 95 °C for 5 min, cooled and incubated for 1 h more, prior to an additional measurement of EC. The EC resulting from ion leakage from live roots was expressed as a percentage of total conductivity (EC live root plus EC killed root). The resultant value was taken as a comparative measure of treatment effects on root cell-membrane integrity.
Sodium accumulation
The possible effects of ascorbate on sodium accumulation in the stems of salinized seedlings were assayed. Intact seedlings were rinsed in 0.5 mM CaCl2 and a 2 cm segment was excised from the base of the stem, oven-dried for 72 h at 70 °C, weighed, powdered and incubated in 10 ml 0.1 N HCl for 48 h prior to filtration and determination of ion content by ICP analysis. Representative results are a mean of five plants per treatment ±SE.
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Results |
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Exogenous ascorbic acid increases seedling capacity to recover from salt stress
Root exposure to severe salt stress (300 mM NaCl) rapidly caused complete wilting with the visible collapse of stems and leaves. Resistance was assayed by determining the recovery of the wilted tomato seedlings after transfer back to non-saline root medium. Complete recovery was routinely observed c. 60 min after the return of seedlings treated with NaCl for 5 h or 6 h, to non-saline medium (Fig. 1
). Recovery was characterized by the restoration of a vertical position in the previously horizontal and completely wilted stems and leaves and subsequent plant survival. However, longer exposure to salinity (for 7, 8 or 9 h) resulted in progressive decreases in recovery. Thus, after 9 h, seedlings remained wilted and later died (0% survival) despite the transfer back to non-saline conditions.
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In order to differentiate between possible osmotic and toxic effects, seedlings were exposed to a similar osmotic stress using a non-penetrating polyethylene glycol (PEG 6000) instead of NaCl. Seedlings treated with PEG solution at -1.35 MPa osmotic potential wilted completely, but showed 100% recovery when moved back to nutrient solution without PEG after 9 h (not shown). Thus, the seedling mortality caused by NaCl treatment for 9 h was not merely a response to osmotic effects on the external availability of water.
Most importantly, the addition of exogenous ascorbic acid to the root medium remarkably increased seedling survival of treatments with 300 mM NaCl for 7, 8 or 9 h (Fig. 1
). Thus, seedlings treated for 9 h with 300 mM NaCl alone showed 0% recovery. However, c. 50% of seedlings treated for 9 h with 300 mM NaCl and 0.5 mM ascorbic acid showed rapid shoot recovery after the return to non-saline medium. Recovered seedlings eventually produced new lateral roots and leaves.
Chemical analyses showed that root addition of exogenous ascorbic acid (0.5 mM) for 33 h (24+9 h) increased seedling levels from 2.4±0.2 µmol g-1 FW to 3.1±0.3 µmol g-1 FW in salinized seedlings and from 2.3±0.2 µmol g-1 FW to 3.1±0.2 µmol g-1 FW in non-salinized seedlings.
Comparisons were made between the protective effect of ascorbic acid on survival and that of other small organic compounds without known anti-oxidant activity. Addition to the root medium of glucose, glycine-betaine, leucine or proline, each at 0.5 mM, had little or no effect on seedling survival of 300 mM NaCl treatment for 9 h: percentage recoveries were 0%, 9%, 10%, and 0%, respectively, as compared to 0% survival with no addition and 50% survival with the addition of ascorbic acid.
Progressive increases in peroxidation of lipids during severe salt stress are partially inhibited by exogenous ascorbic acid
One of the expected consequences of stress-induced cellular build-up of active oxygen species (AOS) is an increase in lipid peroxidation. The assay of cellular accumulation of lipid peroxidation products, in the form of thiobarbituric acid reactive substances (TBARS), can provide a comparative indication of such activity. Salt stress induced progressive increases in accumulation of TBARS in roots, stems and leaves of salt-stressed seedlings at 6 h and 9 h. Exogenous ascorbic acid partially inhibited these increases (Table 1).
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Exogenous ascorbic acid does not reduce membrane leakiness or sodium accumulation
Damage to plasma membranes, as a result of lipid peroxidation in plants treated for 9 h with 300 mM NaCl, could interfere with essential tissue capacity to retain water and exclude sodium ions thereby inhibiting recovery from wilting. The possibility that additional ascorbic acid acted to inhibit such events was investigated by comparing the effects of 9 h treatments with NaCl or NaCl+ascorbic acid on electrolyte leakage from the roots and on sodium accumulation in the stems. Salt treatment without exogenous ascorbic acid induced leakage of 44% of root electrolytes, i.e. less than the leakage of 49% in roots treated with NaCl plus ascorbic acid. Moreover, the addition of ascorbic acid gave only non-significant reductions in sodium accumulation in stems of salinized seedlings (40±5 µg Na g-1 DW without additional ascorbate and 34±6 µg Na g-1 DW with ascorbate).
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Discussion |
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Completely wilted tomato seedlings showed an amazing capacity for shoot recovery after up to 6 h of severe salt-stress treatment with 300 mM NaCl. Netting et al. observed a similar capacity for shoot recovery in tomato seedlings after inducing one or more daily cycles of wilting by air-drying for 30 min and then returning the roots to aqueous media (Netting et al., 1997
). However, the loss of capacity to recover from severe salt-stress and the transition to permanent wilting, do not appear to have been previously investigated. These results show clearly that the permanent wilting of 100% of the seedlings induced by 9 h of salt treatment was related to the uptake and toxicity of NaCl (rather than simple osmotic reductions in water availability to the roots). Thus, comparable treatment of seedlings for 9 h with solutions of non-penetrating PEG 6000 in place of NaCl did not induce permanent wilting.
The exogenous supply of ascorbic acid increased tissue levels in tomato seedlings, as in a previous report showing plant uptake of exogenous ascorbic acid (Arrigoni et al., 1997). The additional ascorbic acid increased the percentage of tomato seedlings able to survive the toxic effects of a 9 h exposure to NaCl, from 0% to c. 50%. Alternative organic carbon sources without direct anti-oxidant activity, such as glucose, glycine-betaine, leucine or proline, did not provide equivalent protection. The remarkable protective effect of exogenous ascorbic acid therefore appeared to be specifically related to its anti-oxidant activity, rather than its possible utility as an organic substrate for respiratory energy metabolism.
Several findings indicated that the salt-induced transition to permanent wilting was associated with increases in the cellular activity of damaging active oxygen species (AOS) and that the effect of additional ascorbic acid on seedling-survival was associated with the partial inhibition of these increases. (a) The level of TBARS (indicative of lipid peroxidation by AOS) in root, stem and leaf tissues, increased progressively during salt stress. (b) The provision of exogenous ascorbic acid consistently reduced salt-induced accumulation of TBARS and reduced seedling mortality. Interestingly, a relationship between higher vitamin C (ascorbic acid) intake and reduced mortality has also been found in humans (Enstrom et al., 1992).
The inhibitory effect of additional ascorbic acid on the accumulation of TBARS in the roots, stems and leaves of salinized plants (Table 1) was apparent after 6 h of NaCl treatment, when all the wilted seedlings still retained the capacity for rapid recovery, i.e. the tissues were still alive. The additional ascorbic acid did not therefore inhibit lipid peroxidation only in killed cells (cf. Smirnoff, 1993).
Zhang and Kirkham reported similar inhibitory effects of exogenous ascorbic acid on lipid peroxidation in sunflower seedlings exposed to osmotically induced water-stress (PEG 8000 at -0.21 MPa for 24 h) (Zhang and Kirkham, 1996). Water stress increased TBARS accumulation, and as with salt stress, this increase was partially inhibited when seedlings were supplied with exogenous ascorbic acid. However, the level of osmotic stress was too low to allow a parallel investigation of the effects on seedling survival.
Although the inhibitory effect of ascorbic acid on lipid peroxidation and increased seedling survival appear to be related, the actual mechanism(s) are not yet clear. One possibility was that additional ascorbic acid would inhibit stress-induced increases in the leakage of essential electrolytes following peroxidative damage to plasma membranes (Lechno et al. 1997; McKersie et al., 1999). However, additional ascorbic acid did not inhibit increases in leakage of electrolytes from roots of salt-stressed tomato seedlings. Nor did additional ascorbic acid significantly reduce the undesirable accumulation of sodium in the stems of salt-stressed plants. Possibly, the protective effect of ascorbic acid is more related to reduced AOS damage to essential proteins and/or nucleic acids (Inzé and Van Montague 1995; Becana et al., 1998; Noctor and Foyer, 1998).
Finally, the fact that new roots and leaves were produced by the seedlings which recovered from 9 h of salt treatment with ascorbic acid suggests that additional ascorbic acid may have affected meristematic cells in the salt-stressed root and shoot tissues. Low ascorbic acid levels have been associated with mitotic quiescence in root meristems (Kerk et al., 2000). Conversely, treatment with exogenous ascorbic acid (0.1 mM) was associated with an increase from 34% to 58% in normal root and shoot emergence from somatic embryos (Stassola and Yeung, 1999).
In conclusion, this report shows for the first time that root treatment with exogenous ascorbic acid can remarkably increase the capacity of tomato seedlings to survive the otherwise lethal effects of a 9 h exposure to severe salt-stress. The increase in plant resistance to salt-stress was associated with the anti-oxidant activity of ascorbic acid and a partial inhibition of salt-induced increases in lipid peroxidation by active oxygen species.
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Acknowledgments |
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Abed Shalata was supported by a post-doctoral grant from the Israel Ministry of Science.
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Notes |
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1 To whom correspondence should be addressed. Fax: +972 4 8221529. E-mail: agpetern{at}tx.technion.ac.il
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