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Ciencia e investigación agraria

versión On-line ISSN 0718-1620

Cienc. Inv. Agr. v.37 n.3 Santiago dic. 2010

http://dx.doi.org/10.4067/S0718-16202010000300006 

Cien. Inv. Agr. 37 (3); 71-81. 2010
www.rcia.uc.cl

RESEARCH PAPER

 

Mitigating effect of salicylic acid and nitrate on water relations and osmotic adjustment in maize, cv. Lluteño exposed to salinity

Efecto mitigante del ácido salicílico y nitrato en las relaciones hídricas y ajuste osmótico en maíz, cv. Lluteño expuesto a salinidad

 

Hugo Escobar1, Richard Bustos1, Felipe Fernández1, Henry Cárcamo1, Herman Silva2, Nicolás Frank2, Liliana Cardemil3

1Laboratorio de Cultivo de Tejidos Vegetales, Facultad de Ciencias Agronómicas, Universidad de Tarapacá, Velásquez 1775, Arica, Chile,
2Laboratorio de Suelo, Agua y Planta, Facultad de Ciencias Agronómicas, Universidad de Chile, Santa Rosa 11315, La Pintana, Santiago, Chile.
3Laboratorio de Biología Molecular Vegetal, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Macul, Santiago, Chile.

Dirección para correspondencia.


Abstract

We analyzed the mitigating effect of NO3 - and salicylic acid (SA) on the detrimental effects of salt stress by studying the water status of plants of maize grown in Hoagland's medium with NaCl 100 mM as the saline component, to which SA and NO3 - were added in different concentrations as mitigating agents. We evaluated water potential Ψw, osmotic potential Ψs, relative water content (RWC), turgor potential (Ψp ), and the osmotic adjustment (OA) of leaves and roots. SA 0.5 mM mitigated the effects of salinity by increasing the Ψs of the leaf, the Ψsof theroot, the Ψpof the leaf, RWC and OA of the leaf; while NO3 was only effective in combination with SA, mitigating the effects of salinity by increasing RWC and OA. However, the interaction SA-NO3 reduced leaf Ψw and Ψs of leaves and roots. Mtigation of salt stress was also detected by a positive effect on plant growth. The greatest effect on growth was produced by the NO3 treatments and SA 0.5 mM combined with NO3.

Key words: nitrate, osmotic potential, osmotic adjustment, salinity mitigation, salicylic acid, water potential, water relative content.


Resumen

Se evaluó el efecto mitigante de NO3 y AS sobre el deterioro fisiológico inducido por salinidad en plantas de maíz crecidas en solución Hoagland con 100 mM de NaCl. La evaluación se realizó mediante determinaciones del potencial hídrico Ψw, potencial osmótico (Ψs), contenido relativo de agua (RWC), potencial de turgor (Ψp ) y el ajuste osmótico (AO). A la solución de Hoagland con 100 mM de NaCl se adicionó AS, NO3 y combinaciones de diferentes concentraciones de ambos mitigadores. AS 0.5 mM puede mitigar el efecto de la salinidad incrementando el Ψs de la hoja, Ψs de la raíz, el Ψp de la hoja, el RWC y el AO de la hoja. El NO3 6 mM solo y la interacción AS-NO3 6 mM puede mitigar el efecto salino incrementando el RWC y el AO. Sin embargo, la interacción AS-NO3 6 mM disminuye el Ψw de la hoja y el Ψs de hojas y raíces. La mitigación del estrés salino puede ser detectada, también, por un efecto positivo en el crecimiento de la planta. El mayor efecto en el crecimiento fue obtemdo cuando las plantas fueron tratadas con NO3 6 mM y con AS 0.5 mM combinado con NO3 6 mM.

Palabras claves: Ácido salicílico, mitigación de salinidad, nitrato, RWC, potencial hídrico, potencial osmótico, potencial de turgencia, ajuste osmótico.


Introduction                                                           

Salinity may cause water stress in plants, which is first manifested as an osmotic stress and then as ionic toxicity, due mainly to an excess of Na+ and Cl- in the tissues. Plants may also have a nutritional deficieNO3- due to the c ompetition of Na+ y Cl- for the ionic nutrient transporters in the external zone of the roots.

Maize, cv. Lluteño, is the main cultivated species in the Lluta Valley, and the most widely cultivated crop in terms of area in the desert of northern Chile. It is especially interesting due to its high tolerance to extreme conditions of salt stress and the excess of boron in the irrigation water. The main drawback with this cultivar is its low yield, which fluctuates between 12.000 and 20.000 ears/ha with a planting density of 30.000-40.000 plants/ha, what means less than one ear per plant. This low yield may be due to an excessive absorption of toxic ions such as boron, and to high concentrations of sodium and chlorine in the irrigation water (Bastías, 2005). In the Lluta valley the water has concentrations of Na+ from 194 to 480 ppm, Cl- from 397 to 900 ppm and B from 11.7 to 28.7 ppm (Sotomayor et al, 1995). How-ever, the concentration of these ions should not be higher than 186, 200 and 0.75 ppm, respectively, to avoid toxic effects on crops, as has been reported by the Chilean Instituto Nacional de Normalización (1987). The toxicity induced by NaCL may be exacerbated by a deficient water absorption generated by the saline stress of the environment. This salinity can decrease the relative water content (RWC) and cause cell dehydration (Hasegawa et al, 2000; Ortíz et al, 2003; Chartzoulakis, 2005). Water stress may activate molecular signals to counteract the physiological damage of stress, such as the sy nthesis of abscisic acid (ABA) causing closure of the stomata to avoid water loss. The closure of stomata, however, decreases CO2 assimilation by plants; this might be a cause of the low yield of maize cv Lluteño (Sharp et al, 1993; Wahbi et al, 2005; Centritto et al, 2005).

Some plants confront salinity by osmotic adjustments to absorb and retain water while maintaining cell turgor (Serraj and Sinclair, 2002; Silva et al, 2007) by means of the accumulation of compatible solutes and osmoregulators (Hasegawa et al, 2000; Chinnusamy et al, 2005; Munns y Tester, 2008).

Due to its biological and physiological actions, SA has been considered as a plant hormone (Canet et al, 2010). As in the case of other plant hormones, SA may act as a plant regulator and signal messenger in plants under stress conditions (Harfouchea, 2008). SA activates defense mechanisms in pathogenicity and tolerance mechanisms to counteract different environmental stress conditions, such as ozone increase, low and high temperatures, salinity, anaerobiosis, etc. (Cakmak, 2003; Sawada et al, 2006; Shi y Zhu, 2008).

The application of SA to cereal plants appears to decrease the concentrations Na+, Cl- and B in plant tissues and significantly improves the nitrogen absorption of these plants when there is high salinity associated with boron (Shakirova et al, 2003; Gunes et al, 2005). However, the signals induced by SA to counteract saline stress of plants are unknown (Gunes et al, 2005; Gunes et al, 2007).

In glycophytic plants the lack of nitrogen produces severe consequences in the synthesis of proteins, nucleic acids, lipids and amino acids. Nitrogen deficiecy also induces the synthesis of compatible solutes in plants to perform osmotic adjustments (Huber and Kaiser, 1996; Viégas and Gomes da Silveira, 2002). The decrease in NO3- is correlated with a high absorption of Cl-. However, the application of NO3- in the soil compensates the decrease of N in leaves caused by an excess Cl- (Tabatabaei, 2006). Salinity may affect nitrogen uptake by a direct competition between Cl- and NO3- ions of the NO3- transport system (Pessarakli et al, 1989; Campbell y Kinghorn, 1990) and/or by alteration of the plasmalemma by affecting the integrity of the proteins of this membrane (Cramer et al, 1985).

Since SA seems to improve nitrogen absorption and nitrogen stimulates plant growth by synthesis of the fundamental biomolecules and reduces water stress by stimulating the synthesis of compatible solutes, it is necessary to test the combined effects of SA and NO3- in the induced salinity tolerance of maize, cv. Lluteño. The objective of this study was to evaluate the combined mitigating effect of SA and NO3- on the detrimental effects cause by salinity on the maize plants. If there is an alleviating effect on salinity stress induced by SA different from that induced by NO3- the combined presence of SA with NO3- will increase the mitigation induced by SA or by NO3- separately, suggesting two interacting routes of transduction signals.

To evaluate this hypothesis, the water status of the plants was determined (water and osmotic potentials, relative water content (RWC), pres-sure potential (turgor potential), and the osmotic adjustment (OA). For this, experiments were performed with 28 days old maize plants. grown in pots and irrigated with Hoagland's medium to which 100 mM NaCl was added. For mitigation of the stress effects caused by salinity, SA, NO3- and combinations of SA and NO3- were added to the Hoagland's medium supplemented with 100 mM NaCl (Acevedo et al, 1998, Munns and Tester, 2008).

Materials and methods

Growth conditions and experimental design

The experiment was performed with plants of Zea mays L., cv Lluteño, in a greenhouse with natural light, mean maximun temperature 27.3° C, mean minimum 11.4° C, PAR 359.8 umol/m2 s-1 and relative humidity 50%-80% (day-night). Plants were established in 15 L pots with a Perlite substrate. Three seeds were planted in each pot. After 10 days, one of the three seedlings of each pot was selected to obtain plants with a uniform size for all the experimental groups; the other two were removed from the pot. During the first 28 days plants were irrigated with 100% Hoagland's solution, pH 6-7 (Hoagland and Arnon, 1950). The plants were watered every two days with one liter of Hoagland's solution per pot when the substrate reached a humidity of 30% of the field capacity (FC) (Fuentes, 2003). To avoid the accumulation of nutrients and salts in the substrate, every third irrigation the substrate was washed with distilled water until the electrical conductivity of the substrate was less than that of the Hoagland's solution. After 28 days the experimental treatments with NaCl, NO3- and SA began. All these chemical compounds were added to the Hogland's medium (Gunes et al, 2007). Treatments are indicated in Table 1; there were 9 treatments with 5 repetitions using 5 plants per treatment. Treatments were continued for 58 days; measurements started after 30 days of treatment. The parameters determined included water potential (Ψw), osmotic potential (Ψ), relative water content (RWC), turgor potential and osmotic adjustment (OA).

 

Measurement of water relations

The water potential (Ψw), the osmotic potential (Ψs) and the relative water content (RWC) were measured at 9:00 inthe sixth completely expanded leaf. At the same time, the root osmotic potential (Ψp) was measured. The reported results are the mean of two values measured two days apart, each measurement performed 16 hours after watering.

Leaf Ψw was measured with a pressure bomb (PMS Model 600, USA) according to Scholander et al. (1965). The osmotic potential of leaves and roots was measured in tissue sections which were frozen at -20° C for 2 hrs and then macerated and centrifuged at 13,200 g for 5 min to extract the cell sap. Osmolality was measured in an osmometer (Roebling Messtechnick D-14129) using 100 μL of sap in an Eppendorf tube calibrated with distilled water. Van't Hoff's equation was used to calculate the osmotic potential (Ψs) of the solution (Nobel, 1991):

Ψs = - C R T                         [1]

C = Concentration of the solution, expressed as molality.
R = Universal gas constant, 0.083 kg bar mol-1 K-1.
T = Absolute temperature in degrees Kelvin (298 °K).
RWC is expressed as:


RWC = 100 x (fresh weight - dry weight)/(turgid weight - dry weight)                              [2]

The turgor potential of leaves (Ψp) was estimated as the difference between the water potential (Ψw) and osmotic potential (Ψs):

Ψp= Ψw - Ψs                          [3]

The leaf osmotic adjustment (OA) was obtained using the value of Ψs at maximun turgidity (Ψs100), which was estimated as the product of the values of Ψsand RWC (Irigoyen et al., 1996):

Ψs = (Ψs x RWC)/100                    [4]

OA was then calculated as the difference between the values of the osmotic potential at maximun turgidity of the plants treated with salts (Ψs100s) and the control plants (Ψs100c). The water condition of the substrate must be optimum for this measurement, to eliminate the possibility of plant dehydration due to a deficieNO3- of irrigation that could mask the effect of the treatment.

OA = (Ψs100c - Ψs100s)                    [5]

Design and statistical analysis

A completely randomized experimental design was established with nine treatments and five replicates for the measurements of the plant water relations parameters. The results obtained were subject to an analysis of variance (ANOVA) and the means were compared according to Tukey's test (P ≤ 0.05)

Results

Water Potential (Ψw)

Water potential decreased after treatment with NaCl. 0.5 mM SA increased the water potential to a similar value to that of the control without salinity, annulling the osmotic effect of NaCl. However, its interaction with NO3- decreased the water potential significantly, as concentrations of SA-NO3- increased. Concentrations inferior or superior to 0.5 mM were not effective in reverting Ψw (Figure 1).

Figure 1. Mitigating effects of SA and SA with 6 mM NO3- on the leaf Ψs of plants of maize, cv. Lluteño. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤ 0.05).

Osmotic Potential (Ψs) of leaves and roots

Treatment with 100 mM NaCl caused a decrease in Ψs in both leaves and roots; the decrease was greater in the leaves (Figures 2 and 3). In leaves, the Y of the treatments with SA and SA-NO3- decreased more than the NaCl treatment. In roots, the treatment with 0.5 mM SA produced a Ψs greater than that of the NaCl treatment and close to the value of the control. The responses of osmotic potential to the treatments were similar to those of the water potential.

Figure 2. Mitigating effects of SA and SA with 6 mM NO3- on the leaf Ψsof plants of maize, cv. Lluteño. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤ 0.05).

Figure 3. Mitigating effects of S A and S A with 6 mM NO3- on the root Ψs of plants of maize, cv. Lluteño. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤0.05).

Relative water content (RWC)

The application of NaCl caused a significant decrease in RWC. The treatments with NO3-, 0.5 mM SA-NO3- and 1.0 mM SA counteracted the effect of NaCl, returning the RWC to the value of the control plants without salinity (Figure 4). Although 0.5 mM SA mitigated the effect of 100 mM NaCl, it did not return RWC to the level of the control.

Figure 4. Mitigating effects of SA and SA with 6 mM NO3- on the leaf RWC of plants of maize, cv. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤ 0.05).

Turgor potential (Ψp)

Turgor potential was significantly affected by the treatment with 100 mM NaCl. Four of the treatments mitigated the effect of salinity: NO3-, 0.1 mM SA, 0.1 mM SA-NO3- and 0.5 mM SA; these all produced a turgor potential greater than that of the control without salt (Figure 5). The greatest positive effect was produced by 0.5 mM SA, however, when combined with NO3- it produced a greater decrease in turgor than that produced by NaCl. The Ψp of the treatment with 0.5 mM SA-NO3- was significantly different from the control without salt; however, the differences between turgor values are small. The three treatments with greatest growth (Table 2) (control, NO3- and 0.5 mM SA-NO3-) had very similar turgor values.

Figure 5. Mitigating effects of S A and S A with 6 mM NO3- on the leaf Ψp of plants of maize, cv. Lluteño. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤ 0.05).



Osmotic adjustment (OA)

OA was lower in the treatment with NaCl 100 mM. All the treatments with SA and NO3- increased the osmotic adjustment significantly above the level of the NaCl treatment. The most efficient conditions of mitigation and increase of OA were found in the treatments with all the combinations SA-NO3- and with 0.5 mM SA (Figure 6).

Figure 6. Mitigating effects of SA and SA with 6 mM NO3- on the leaf OA of plants of maize, cv. Lluteño. The determinations were performed 30 days after treatment. Each dot corresponds to five independent determinations with their SD (vertical bars). Different letters represent significant differences among treatments (Tukey test, P ≤ 0.05).

Discussion

NaCl 100 mM caused a significant decrease in the water relation parameters RWC, Ψw , leaf Ψs, root Ψs, Ψp and OA in maize cv. Lluteño. Our results demónstrate that this decrease may be reverted with an appropriate concentration of SA interacting with 6 mM NO3- applied in the irrigation solution. The mitigating effect of 0.5 mM SA on the effects of salinity was shown by increases in leaf RWC, leaf Ψw , root Ψs leaf Ψp and leaf OA, compared to the treatment with NaCl. The addition of both compounds might favor water absorption and plant growth, and therefore also have a mitigating effect. Thus growth, measured by plant height, leaf rea and fresh weight of greenery and of roots was greater in the treatment with 0.5 mM SA-NO3-, in spite of the decrease in the values of Ψw in leaves and Ψs in leaves and roots.

Water potential (Ψw)

It is knownthat SA with NO3- reduces Ψw (Song et al, 2006, Szepesi et al, 2009). The magnitude of this reduction will depend on how they are applied, their concentrations, and the plant species (Hayat et al, 2008). In the case of maize cv. Lluteño, concentrations lower than 0.5 mM SA were inefficient, while greater concentrations were supraoptimal. This reinforces the idea that SA acts as a hormonal factor with a specific optimum concentration.

In contrast to the action of 0.5 mM SA, its combination with 6 mM NO3- caused a decrease in leaf Ψw and root Ψs . A number of authors (Wahbi etal, 2005; Centritto etal, 2005) have suggested that this decrease favors the absorption of water under saline conditions, and thus this treatment is positive in terms of producing greater growth. Nevertheless, the significant differences between the Ψw of the leaves and the Ψs of the roots favored growth in plants with 0.5 mM SA, with or without NO3-.

Osmotic potential (Ψs) of leaves and roots

Osmotic potential decreased significantly in plants treated with NaCl, which has also been shown for many other species that grow in saline conditions (Cicek and CakMar, 2002; Wahbi et al, 2005, Carillo et al, 2008). As in the case of Ψw , Ψs decreased in plants treated with 0.5 mM SA-NO3- while 0.5 mM SA returned the Ψs of the roots to the values of control plants. However, inthe leaf 0.5 mM SA did not have this effect. 0.5 mM SA alone and in combination with NO3- increased the concentrations of sugars in maize cv. Lluteño (unpublished results), which are osmolytes, favorable for the retention of water in the cell. This retention of water due to increase in sugars may explain the greater growth of plants subjected to these treatments.

Relative water content (RWC)

The decrease in the Ψw of the plant, caused by salinity, produced a reduction in Ψs, which resulted in a reduction in RWC in leaves of the plants of maize cv. Lluteño. These effects of salinity have been reported for other species (Cicek and Cakirlar, 2002; Chartzoulakis, 2005). The high concentration of salt retains water in the substrate, which would imply less water absorption by the roots, aggravated by a loss of water through the roots (Burgess and Bleby, 2006). The consequence of this water loss is a lower RWC. SA and NO3- revert these adverse effects of salinity, possibly by means of an osmotic regulation at the level of the leaf and root (Song et al, 2006). This reversion of the RWC appears to indicate that these mitigating agents favor the entrance of water in the roots and/or avoid water loss by the roots (Carvajal et al, 1999; Hasegawa et al, 2000; Zhu, 2001; Martinez-Ballesta et al, 2006; Burgess and Bleby, 2006). The increase in RWC caused by SA was directly related to its concentration in the experimental range used, supporting the idea that SA may be considered as a hormone. However, its molecular role is unknown (Gunes et al, 2005). NO3- has been considered an osmotic regulator due to its ability to replace other solutes, especially in halophytic plants (VeenandKleinendorst, 1986; Song et al, 2006). If NO3- is an osmotic regulator, it will diminish the negative effects caused by the entrance of NaCl and will facilitate water transpon by the roots, increasing water absorption as well as providing a nutritional effect (Mclntyre et al, 1996; Song et al, 2006). It is interesting to note that in halophytic plants a greater salt concentration induces the expression of aquaporin genes, allowing water to enter the plant (Qi et al, 2009). This may also be the case for NO3-; it might induce the expression of aquaporin genes of maize cv. Lluteño as salinity does for halophytic plants (Qi et al, 2009).

Because the RWC increased significantly in the treatments with 0.5 mM SA, NO3- and with 0.5 mM SA-NO3- compared to the NaCl treatment, the greater growth observed is due to the recovery of the RWC. The reversion of the RWC in plants by these treatments suggests that the mitigation is produced by root water absorption. It may be that these treatments (SA, NO3-, and SA 0.5 mM-NO3-) activate the expression of aquaporins in the plasmalemma of the root and leaves, as it occurs with salt in halophytic plants (Qi et al, 2009).

Turgor potential (Ψp)

According to Hasegawa et al. (2000), a plant cell exposed to a saline medium equilibrates its water potential by decreasing cell water, which causes a decrease in ΨpWe observed this effect in maize cv. Lluteño only in the treatments Table 1 with NaCl and 0.5 mM SA-NO3-. The treatments with NO3-, 0.1 mM SA-NO3-, 0.1 mM S A and 0.5 mM S A caused an increase in turgor. In contrast, treatments with 1.0 mM SA with or without NO3- did not cause variation from control values.

Therefore, the mitigating action of 0.5 mM SA is not only due the increase of Ψw and Ψs, but also because it increases Ψp . The greater turgor induced by SA 0.5 mM was 241.7% of the control value, which may explain the reversion of growth to 50% of the control. The reversion of root growth was even more notable, reaching 80% of the control value. We may speculate that this greater root growth could be induced by an increase in ABA in the root, also induced by SA 0.5mM(Sharpe et al, 1993; Szepesi et al, 2009). The lowest turgor was observed in the treatment 0.5 mM SA-NO3- (61.1 % of the control), which was even lower than the NaCl treatment (83% of control). However, greater growth was produced when 0.5 mM SA interacted with NO3-.

Leaf osmotic adjustment (OA)

100 mM NaCl decreased the leaf OA of maize, cv. Lluteño. All treatments which included SA and SA-NO3- reverted the OA, possibly due to an increase in the osmolyte concentration in the vacuoles. If this is the case, the increase of osmolytes would cause the cell to increase the flow of water towards the vacuole, which would increase its volume without losing water. The result would be an increase in Ψp , and plant growth (Parida and Das, 2005). OA may also be produced by the participation of other organic solutes as well as sugars, by which plants may also recover their Ψw and Ψp (Hasegawa et al, 2000; De Costa et al, 2007). However, in our experiments 0.1 mM SA and NO3- increased OA less than other treatments did. In summary, the rest of the treatments produced a highly significant effect on osmotic regulation of maize, cv. Lluteño, and their mitigating effects led to a recovery of water in the cell.

In summary, ourresults of determinations of water relations in plants of maize cv. Lluteño treated with 100 mM NaCl lead us to conclude that: 1) SA is a good mitigator of the effects of salt stress at a concentration of 0.5 mM. 2) Treatment with 0.5 mM SA in combination with 6 mM NO3- is a better treatment than with only one of them reverting the negative effect of NaCl on growth. 3) The reversion of the deteriorating effects of NaCl by these mitigants implies the reversion of Ψp due to the increase of OA, which induces the uptake of water and plant growth.

 

Acknowledgements

This report is part of the requirements for the Doctoral Degree in Ciencias Silvoagropecu-arias of the Facultad de Ciencias Agronómicas, University of Chile given to Hugo Escobar. The research was funded by the Universidad de Tarapacá and CONICYT through the Centro de Investigación del Hombre en el Desierto (CIHDE). We thank the Convenio de Desempeño Universidad de Tarapacá-MINEDUC, Libertad Carrasco for help with the physiological analyses, Francisco Fuentes and Victor Tello of Universidad Arturo Prat, Iquique for their help with statistical analyses, and Elvis Hurtado for his permanent assistance in physiological analyses and equipment maintenance.

 

References

Acevedo, E., H. Silva, and R Silva. 1998. Tendencias actuales de la investigación en la resistencia al estrés hídrico de las plantas cultivadas. Universidad de Chile, Facultad de Ciencias Agrarias y Forestales. Santiago, Chile. Boletín Técnico 49: 1-28.         [ Links ]

Bastías, E. 2005. Interacción del boro en la tolerancia a la salinidad de Zea mays L. amy lacea originario del Valle de Lluta (Arica-Chile). Tesis de Doctorado. Universidad del País Vasco. España. 314 pp.        [ Links ]

Burgess, S.S.O., and T.M. Bleby. 2006. Redistribution of soil water by lateral roots mediated by stem tissues. Journal of Experimental Botany 57: 3283-3291.        [ Links ]

Cakmak, I. 2003. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. In: Feed the soil to feed the people: the role of potash in sustainable agriculture. International Potash Institute, Basel. pp. 325-343.        [ Links ]

Campbell, W.H., and J.R. Kinghorn. 1990. Functional domains of assimilatory nitrate reductases and nitrite reductases. Trend in Biochemical Science 15:315-319.        [ Links ]

Canet, J.V, A. Dobon, F. Ibañez, L. Perales, and R Tornero. 2010. Resistance and biomass in Arabidopsis: a new model for Salicylic Acid perception. Plant Biotechnology Journal 8: 126-141.        [ Links ]

Carillo, R, G. Mastrolonardo, F. Nacca, and D. Parisi. 2008. Nitrogen metabolism in durum wheat under salinity: acumulation of proline and gly-cinebetaine. Plant Biology 35: 412-426.        [ Links ]

Carvajal, M., V. Martínez, and C.F. Alcaraz. 1999. Physiological function of water-channels, as affected by salinity in roots of paprika pepper Physiology Plantarum 105: 95-101.        [ Links ]

Centritto, M., S. Wahbi, R. Serraj, and Chavez, M. 2005. Effects of partial rootzone drying (PRD) on adult olive tree (Olea europaea) in field conditions under arid climate. II. Photosynthetic responses. Agriculture, Ecosystems and Environment 106: 303-311.        [ Links ]

Chartzoulakis, K. 2005. Salinity and olive: growth, salt tolerance, photosynthesis and yield. Agriculture Water Management 78: 108-121.        [ Links ]

Chinnusamy, V, A. Jagendorf, and J. Zhu. 2005. Understanding and improving salt tolerance in plants. Crop Science 45: 437-448.        [ Links ]

Cicek, N., and H. Cakirlar. 2002. The effect of salinity on some physiological parameters en two maize cultivars. Bulgarian Journal of Plant Physiology 28 (1-2): 66-74.        [ Links ]

Cramer, G., A. Lauchli, and V.S. Polito. 1985. Displacement of Ca2+ by Na+ from the plasmalemma of root cells. A primary response to salt stress? Plant Physiology 79: 207-211.        [ Links ]

De Costa, W., C. Zórb, W. Hartung, and S. Schubert. 2007.  Salt resistance is determined by osmotic adjustment and abscisic acid in newly developed maize hybrids in the first phase of salt stress. Physiologia Plantarum 131: 311-321.        [ Links ]

Fuentes, J. 2003. Técnicas de riego. Ed. MundiPrensa Libros S.A. Madrid, España. 484 pp.        [ Links ]

Gunes, A., A. Inal, M. Alpaslan, N. Cicek, E. Guneri, F. Eraslan, andT. Guzelordu. 2005. Effects of ex-ogenously applied salicylic acid on the induction of multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Archives of Agronomy and Soil Science 51: 687-695.        [ Links ]

Gunes, A., A. Inal, M. Alpaslan, F. Eraslan, E. Guneri, and N.Cicek. 2007. Salicylic acid changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology 164: 728-736.        [ Links ]

Hayat, S., S. Aiman, Q. Fariduddin, and A. Ahmad. 2008.  Growth of tomato (Lycopersicon esculentum) in response to salicylic acid. Journal o Plant Interactions 3: 297-304.        [ Links ]

Harfouchea, A. L., E. Rugini, F. Mencarelli, R. Botondi, andR. Muleo. 2008. Salicylic acid induces H2O2 production and endochitinase gene expression but not ethylene biosynthesis in Castanea sativa in vitro model system. Journal of Plant Physiology 165: 734-744.        [ Links ]

Hasegawa, P, R. Bressan, J. Zhu, and H. Bohnert. 2000. Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51: 463-499.        [ Links ]

Hoagland, D.R., and D.J. Arnon. 1950. The water-culture method for growing plants without soil. Circular 347. California Agricultural Experiment Station. Berkeley, USA.        [ Links ]

Huber, S.C., and W.M. Kaiser. 1996. 5-Aminoimid-azole-4-carboxiamide riboside activates nitrate reductase in darkened spinach and pea leaves. Physiologia Plantarum 98: 833-837.        [ Links ]

Instituto Nacional de Normalización. 1987. Registros de calidad del agua para diferentes usos. Instituto Nacional de Normalización. NCH 1333. Of. 1978. Mod. 1987. Chile.        [ Links ]

Irigoyen, J. J., J. Pérez de San Juan, and M. Sanchez-Diaz. 1996. Drougth enhances chilling tolerant in a Chilling-sensitive mays (Zea mays) variety. The New Phytologist 134: 53-59.        [ Links ]

Mclntyre, G.I., A.J. Cessna, and A.I. Hsiao. 1996. Seed dormaNO3- in Avena fatua: interacting effects of nitrate, water and seed coal injury. Physiologia Plantarum 97: 291-302.        [ Links ]

Martínez-Ballesta, M. del C, C. Silva, C. López-Berenguer, F.J. Cabañero, and M. Carvajal. 2006. Plant Aquaporins: New Perspectives on Water and Nutrient Uptake in Saline Environmental Plant Biology 8: 535-546.        [ Links ]

Munns, R., and M. Tester. 2008. Mechanisms of Salinity Tolerance. Plant Biology 59: 651-81.        [ Links ]

Nobel, PS. 1991. Physicochemical and environmental plant physiology. Academic Press. San Diego, USA. 200 pp.        [ Links ]

Ortíz, M., H. Silva, P Silva, and E. Acevedo. 2003. Estudio de parámetros hídricos foliares en trigo (Triticum aestivum L.) y su uso en selección de genotipos resistentes a sequía. Revista Chilena de Historia Natural 76: 219-233.        [ Links ]

Parida A.K., and A.B. Das. 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicol-ogy and Environmental Safety 60: 324-349.        [ Links ]

Pessarakli, M., J.T. Huber, and T.C. Tucker. 1989. Protein synthesis in green beans under salt stress with two nitrogen sources. Journal of Plant Nutrition 12: 1261-77.        [ Links ]

Qi, C.H., M. Chen, J. Song, and B.S. Wang. 2009. Increase in acuaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Science 176: 200-205.        [ Links ]

Sawada, H, I. Sung, and K. Usui. 2006. Induction of benzoic acid 2-hidroxylase and salicylic acid biosynthesis-Modulation by salt stress in rice seedlings. Plant Science 171: 263-270.        [ Links ]

Scholander, PE, H.T. Hammel, E.D. Bradstreed, EA. Hemmingsen. 1965. Sap pressure in vascular plants. Science 148: 339-346.        [ Links ]

Serraj, R., and T.R. Sinclair. 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell and Environment 2: 333-341.        [ Links ]

Shakirova, F., A. Sakhabutdinova, M. Bezrukova, R. Fatkhutdinova, and D. Fatkhutdinova. 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science 164: 317-322.        [ Links ]

Sharp, R.E, G.S. Voetberg, I.N Saab, and N. Bernstein. 1993. Role of abscisic acid in the regulation of cell expansion in roots at low water potentials. In: Plant Responses to Cellular Dehydration During Environmental Stress. Close T.J. and Bray E.A. (eds.). American Society of Plant Physiologists. Current Topics in Plant Physiology Series 10: 57-66.        [ Links ]

Shi, Q., and Z. Zhu. 2008. Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environmental and Experimental Botany 63: 317-326.        [ Links ]

Silva, H., M. Ortiz, and E. Acevedo. 2007. Hydric relationships and osmotic adjustment in wheat. Agrociencia 41: 23-34. 2007.        [ Links ]

Song, I, X. Ding, G. Feng, and F. Zhang. 2006. Nutritional and osmotic roles of nitrate in a euhalophyte and a xerophyte in saline conditions. The New Phytologist 171: 357-366.        [ Links ]

Sotomayor, E., F. de la Riva, and A. Leiva. 1995. Informe proyecto de introducción de olivo (Olea europaea L.) a los valles costeros de Arica, Primera Región y sur del país. Proyecto FONDEC YT. Instituto de Agronomía, Universidad de Tarapacá, Arica, Chile. 136 pp.        [ Links ]

Szepesi, A., J. Csiszar, K. Gemes, E. Horvath, F. Horvath, M.L. Simon, and I. Tari. 2009. Salicilyc acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology 166: 914-925.        [ Links ]

Tabatabaei, S. 2006. Effects of salinity and N on the growth, photosynthesis and N status of olive (Olea europaea L.) trees. Scientia Horticulturae 108: 432-438.        [ Links ]

Veen, B.W., andA. Kleinendorst. 1986. The rol of nitrate in osmoregulation on Italian ryegrass. Plant and Soil 91: 433-436.        [ Links ]

Viégas, R. and J. Gomes da Silveira 2002. Activation of nitrate reductase of cashew leaf by exogenus nitrite. Brazilian Journal of Plant Physiology 14:1-9        [ Links ]

Wahbi, S. R. Wakrim, B. Aganchich, H. Tahí, and R. Serraj. 2005. Effects of partial rootzone drying (PRD) on adult olive tree (Olea europaea) in field conditions under arid climate. I. Physiological and agronomic responses. Agriculture, Ecosystems and Environment 106: 289-301.        [ Links ]

Zhu, J.K. 2001. Plant salt tolerance: regulatory path-ways, genetic improvement and model systems. Trends in Plant Science 6: 66-71.        [ Links ]

 

Received: August 18, 2009. Accepted: November 10, 2009.

Corresponding author: hescobar@uta.cl         

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