Advertisement

Plant Growth Regulation

, Volume 63, Issue 1, pp 55–62 | Cite as

Alleviation of salinity stress in broccoli using foliar urea or methyl-jasmonate: analysis of growth, gas exchange, and isotope composition

  • Francisco M. del AmorEmail author
  • Paula Cuadra-Crespo
Original Research

Abstract

We studied the effects of foliar application of urea or methyl-jasmonate (MeJA) on the salinity tolerance of broccoli plants (Brassisca oleracea L. var. italica). Plant dry weight, leaf CO2 assimilation, and root respiration were reduced significantly under moderate saline stress (40 mM NaCl) but application of either urea or MeJA maintained growth, gas exchange parameters, and leaf N–NO3 concentrations at values similar to those of non-salinized plants. Additionally, when these two foliar treatments were applied leaf Na+ concentration was reduced compared with control plants grown at 40 mM NaCl. However, at a higher salt concentration (120 mM NaCl), no effect of the foliar applications was found on these parameters. Salinity also decreased leaf δ15N but increased δ13C. Our study shows the feasibility of using foliar urea or MeJA to improve tolerance under moderate saline stress.

Keywords

Broccoli Foliar application Urea Isotope composition Methyl-jasmonate Salinity 

Introduction

Salinity is a major environmental factor limiting plant growth and crop productivity, and salinization of irrigated and surrounding areas in the arid tropics and sub-tropics has not diminished (Tuna et al. 2008b). The loss of farmable land due to salinisation is in direct conflict with the growing population, posing a major challenge for maintaining world food supplies (Purty et al. 2008). The reduction in plant growth and yield is mainly due to an osmotic effect of the accumulation of salts near the root zone whereas the build up of toxic saline ions in plant tissues is responsible for the progressive impairment of several physiological processes (Munns 2002). In a saline environment, ion homeostasis can be disturbed by excessive uptake of Na+ and Cl. Competition between these and other anions and cations are well documented and may result in reduced growth (De Pascale et al. 2005). Thus, in saline environments, plants have developed different adaptative mechanisms (Borsani et al. 2003). One adaptive plant response to salt stress is synthesis and accumulation of low-molecular weight organic compounds in the cytosol and organelles (Bartels and Sunkar 2005). Compatible osmolytes reported to be affected by salinity stress include simple sugars, alcohols or polyols, amino acids, quaternary amino acid derivatives, and sulfonium compounds (Zhu 2001).

Salinity can reduce N accumulation in plants (Pessarakli 1991) and an increase in Cl uptake and accumulation is often accompanied a decrease in NO3 concentration. Many authors attributed this reduction to Cl antagonism of NO3 uptake (Kafkafi et al. 1992; Bar et al. 1997). Inhibition of nitrogen uptake may occur by NO3 /Cl interaction at the sites of ion transport (Cram 1983), because sodium results in severe membrane depolarization in plants (Suhayda et al. 1990)—which has been linked to non-competitive inhibition of nitrate uptake (Hawkins and Lewis 1993). However, the method of N application (via soil or leaves) influences growth and storage of N (Habib et al. 1993); thus, when N supply to the roots is impaired, applications of foliar urea can be used effectively (Nicoulaud and Bloom 1996; del Amor et al. 2009). Urea is one of the most widely-used foliar-N fertilizers, characterized by high leaf penetration rate and low cost and most plants can absorb rapidly and hydrolyze urea in the cytosol (Witte et al. 2002). Urea can also increase the level of storage N compounds such as amino acids and proteins (Dong et al. 2004); thus, foliar urea could directly affect N metabolism under saline conditions and therefore amino acids synthesis. Moreover, the application of fertilizer N directly to leaves, especially urea, can be a potential alternative to conventional soil fertilization and does not contribute to soil salinity or potential groundwater contamination (Embleton et al. 1986).

In addition to the foliar supply of N-fertilizer, exogenous application of some phytohormones could also affect directly the plant response to salinity (Tuna et al. 2008a). Jasmonates are ubiquitously-occurring lipid-derived compounds with signal functions in plant responses to abiotic and biotic stresses, as well as in plant growth and development (Wasternack 2007), and recent studies pointed out a number of salinity and jasmonates-regulated genes induced by wounding (Cheong et al. 2002). Applied exogenously, they can induce physiological changes identical to characteristic parts of the stress responses (Tsonev et al. 1998). Thus, jasmonates have been identified as stress modulators suppressing or enhancing the stress responses of plants. Jasmonate levels were increased with high salinity in Iris hexagona (Wang et al. 2001) and rice, resulting in the induction of genes involved in stress-related jasmonates biosynthesis (Tani et al. 2008). Fedina and Benderliev (2000) found that exogenously-applied MeJA supplied simultaneously with NaCl helped algae to counteract salt stress; therefore, the toxic ion effects due to salinity could cause membrane damage and hence trigger the release of the lipid pre-cursors for jasmonate synthesis. Moreover, Parra-Lobato et al. (2009) concluded that exogenous MeJA may be involved in the oxidative stress processes by regulating antioxidant enzyme activities. These results suggest a role for MeJA in the plant response to saline stress. However, relatively little is known about its involvement in the response to abiotic stress in broccoli, especially salinity stress.

The analysis of the natural abundances of stable carbon isotopes in plant dry matter (δ13C) provides information on the long-term water use efficiency (WUE) of plants, and values of δ13C are determined mainly by three processes: diffusion of CO2 through stomata, CO2 assimilation by carboxylase, and metabolism of compounds (Farquhar et al. 1989). In contrast to gas exchange techniques that provide measurements at a single point in time, the leaf carbon isotopic composition integrates the ratio of the intercellular to the ambient CO2 concentrations for longer periods (all the saline-stress period). The basis of the biochemical discrimination against 13C in C3 plants lies with the primary carboxylating enzyme (Rubisco), which discriminates against 13C because of the intrinsically lower reactivity of 13C compared with 12C (Brugnoli and Farquhar 2000). δ13C also gives information about how the nitrogen is used by the plant under water and nutritional (N) stress conditions (Cabrera-Bosquet et al. 2007). Additionally, other studies considered the natural abundance of δ15N as an index of genotypic performance under given stress conditions, specifically water stress (Robinson et al. 2000) and salinity (Handley and Scrimgeour 1997). Carbon stable isotope composition (δ13C) is seen as an index of the integrated response of a physiological characteristic to environmental factors (Choi et al. 2005). However, little is known about correlations between stable isotope composition and salinity in broccoli, especially when foliar treatments are applied.

Broccoli is a crop moderately-sensitive to salinity but has greater salt tolerance than most other common vegetables including melons, corn, lettuce, peppers, onions, and carrots (LeStrange et al. 1996). Salt stress induced detrimental effects on growth and yield depend on several factors such as the level of stress experienced, the time of exposure to the stress, and the soil physical–chemical properties (Maas and Grattan 1999). Additionally, broccoli is a nitrogen-demanding crop and N supply is a determining factor for its productivity and quality (Everaarts and De Willigen 1999); a lower supply of nitrate to growing leaves may be responsible for the inhibition of growth under saline conditions (Hu and Schmidhalter 1998). Therefore, foliar application of fertilizers could alleviate or neutralize growth inhibition due to salinization (Sultana et al. 2001).

The aim of this study was to test the hypothesis that exogenous, foliar application of N-fertilizer (urea) or a phytohormone (methyl-jasmonate) could diminish or counteract the metabolic imbalance produced by a high NaCl concentration in the nutrient solution. We aimed to provide an insight into the physiological significance and usefulness of δ13C and δ15N signatures under saline conditions and to elucidate their responses when foliar N-fertilizer or a phytohorme are applied to broccoli plants.

Materials and methods

Plant material, growth conditions and treatments

Broccoli plants (Brassisca oleracea L. var. italica cv. Lord) were grown in 12-L black containers filled with coconut coir fiber. Plants were irrigated with a solution with the following composition in meq L−1; NO3 : 12.0; H2PO4 : 1.0; SO4 2−: 7.0; K+: 7.0; Ca2+: 9.0; Mg2+: 4.0. Irrigation was supplied by self-compensating drippers (2 lh−1) and fresh nutrient solution was applied to avoid salt accumulation, with a minimum of 35% drainage. Plants were grown in a climate chamber designed by our department specifically for plant research proposes (del Amor et al. 2010), with fully-controlled environmental conditions: 70% RH, 16/8 h day/night photoperiod, 22/18°C, and a photosynthetically-active radiation (PAR) of 250 μmol m−2 s−1 provided by a combination of fluorescent lamps (Philips TL-D Master reflex 830 and 840) and high-pressure sodium lamps (Philips Son-T Agro). Fifteen days after transplanting (DAT) treatments were begun by adding NaCl to the nutrient solution (40 or 120 mM) and spraying foliar urea (10 gl−1) or methyl-jasmonate (5 mM) onto the plants. Triton X-10 (0.125%) and ethanol (0.04%) were added to the foliar applications as surfactant and solvent respectively. Hormonal treatment was applied once, 11 DAT, whilst foliar urea was applied every 2 weeks. To avoid treatment contamination, treatments were sprayed independently outside the climate chamber and plants were left there until complete evaporation of the sprayed solution (about 1 h). Nine treatments were analyzed (0, 40, and 120 mM NaCl, non-sprayed or sprayed with foliar urea or Me-JA). At harvest (60 DAT), 45 plants (5 plants per treatment) were analyzed, and the aerial parts weighed and separated into leaves and stems (including petioles). Dry weight samples were determined after a minimum of 96 h at 65°C.

Ion concentration

Leaf Cl, NO3 , and Na+ concentrations were determined in dry matter, Cl and N-NO3 by Capillary Electrophoresis (Waters, Capillary Ion Analyzer) and Na+ by inductively coupled plasma–optical emission spectrometer (ICP-OES, Varian Vista MPX).

Gas exchange

At the end of the experimental period, net CO2 assimilation was measured in the youngest fully-expanded leaf of each plant, using a CIRAS-2 (PP system) with a PLC6 (U) Automatic Universal Leaf Cuvette. The cuvette provided light (LED) with a photon flux of 800 μmol m−2 s−1, 380 ppm CO2, and a leaf temperature of 22°C. Soil (root) respiration was measured for each plant with the CIRAS-2 and the SRC-1 Soil Respiration Chamber.

Isotope discrimination

Dry, powdered leaf samples were packed in tin capsules and analyzed by isotope ratio mass spectrometry (Continuous Flow Isotope Ratio Mass Spectrometer-CF-IRMS, Micromass Isoprime, Eurovector). The N content was expressed as a percentage of dry matter. The 13C/12C ratios were expressed in δ notation determined by: δ13C (‰) = [(13C/12Csample) − (13C/12Cstandard)]/(13C/12Cstandard) × 1,000 (Farquhar et al. 1989), where ‘sample’ refers to plant material and ‘standard’ refers to Pee Dee Belemnite (PDB) calcium carbonate. The same δ notation was used for the 15N/14N ratio expression (δ15N) but with ‘standard’ referring to air. Isotope secondary standards of known 13C/12C and 15N/14N ratios were used for calibration (USGS-24 and urea, respectively).

Statistical analysis

Data were tested first for homogeneity of variance and normality of distribution, and were analyzed through an analysis of variance using the Generalized Linear Model (GLM) procedure of SPSS (version 13.0). Additionally, Duncan′s multiple range test was used to determine the significance of differences (P ≤ 0.05). The number of replicates for each treatment was five.

Results and discussion

Plant growth, mineral content, and gas exchange

Broccoli is known to be moderately sensitive to salinity (Grattan et al. 2006); consequently, plant dry weight was modified by salinity (Fig. 1). When 40 mM NaCl was added to the nutrient solution, the aerial biomass of non-sprayed plants was reduced by 27.7%; however, no further decrease in biomass was found at higher NaCl concentrations. In contrast, applications of either urea or MeJA maintained growth at 40 mM, but not at 120 mM NaCl, close to that of the non-salinized treatments. A similar response was found when analyzing leaves or stem independently (data not shown). It is well known that the response of plant growth to salinity is the result of various salt effects, including reduced carbon fixation due to specific ion toxicity (Niu et al. 1995), restriction of photosynthesis due to partial stomatal closure (Yeo et al. 1985), waste of energy in the processes of osmotic adaptation and ion exclusion (Yeo 1983), and growth limitations originating from nutritional imbalances (Grattan et al. 2006).
Fig. 1

Effect of NaCl concentration in the substrate and urea or MeJA spray on plant dry weight. Data are means ± SE of 5 different plant samples. *, **, and *** represent P < 0.05, 0.01, and 0.001, respectively. ns not significant. For each column, different letters indicate significant differences (P < 0.05) according to Duncan’s multiple range test

Our data show that supplemental foliar spray of urea to the salinized plants appeared to partially counteract the deleterious effects of salinity. Hasaneen et al. (2008) found a similar effect in lettuce but the magnitude of response was most pronounced with higher urea concentrations. Additionally, Sultana et al. (2001) found that foliar spray of fertilizers partially minimized the salt-induced nutrient deficiency and increased photosynthesis, photosynthesis-related parameters, yield and yield components. Tsonev et al. (1998) reported that pre-treatment of barley plants with JA before salinisation ameliorated the inhibitory effects of salinity on growth when compared to a direct salt stress. However our data show that this nullification of the harmful effects of salinity in broccoli plants by urea or MeJA was only effective at low salt concentration.

Salinity increased Cl concentration in leaves of non-sprayed plants from 89 (control) to 347 (40 mM NaCl) and 517 (120 mM NaCl) mmol kg−1 DW, and no significant response to urea or MeJA applications was found for this ion (Fig. 2). By contrast, the Na+ concentration in non-sprayed plants had a more pronounced increase than Cl, showing an increase from 39 (control) to 795 mmol kg−1 (40 mM NaCl) whilst for 120 mM NaCl, 880 mmol kg−1 Na+ was found in leaves. At 40 mM NaCl, the concentration of Na+ was significantly lower when urea or MeJA was applied, but at 120 mM NaCl no significant difference was found with respect to the non-sprayed plants. In response to salinity stress, endogenous Na+ concentration increased in the various Brassica genotypes (Purty et al. 2008). Walia et al. (2007) showed that salinized barley plants treated with JA accumulated low levels of Na+ in the shoot tissue compared with untreated salt-stressed plants, after several days of exposure to stress, which agrees with our results under moderate stress. Salt tolerance is not associated exclusively with cellular Na+ homeostasis, but also involves adaptations to secondary effects of salinity such as oxidative damage and changes in the levels and composition of the fatty acids of the major glycerolipids, in roots and leaves of a wide range of plants (Purty et al. 2008). Plants can use three strategies for the maintenance of a low cytosolic sodium concentration: sodium exclusion, compartmentation, and secretion. Thus, MeJA may act as a stress modulator, by changing the stress responses of plants by different and complex mechanisms. The reported increase of MeJA with salinity helped plants to reduce ion accumulations (Fedina and Tsonev 1997), and assisted their osmotic adjustment or synthesis of stress proteins (Ali et al. 1999). It is remarkable that, in addition to Na+ exclusion resulting from both foliar treatments, the N–NO3 concentration in the leaves was not impaired by salinity (40 mM) and was maintained at control values (Fig. 3).
Fig. 2

Effect of NaCl concentration in the substrate and urea or MeJA spray on leaf Cl and Na+ concentrations. Data are means ± SE of 5 different plant samples. *, **, and *** represent P < 0.05, 0.01, and 0.001, respectively. ns not significant. For each column, different letters indicate significant differences (P < 0.05) according to Duncan’s multiple range test

Fig. 3

Effect of NaCl concentration in the substrate and urea or MeJA spray on leaf N-NO3 concentration. Data are means ± SE of 5 different plant samples. *, **, and *** represent P < 0.05, 0.01, and 0.001, respectively. ns not significant. For each column, different letters indicate significant differences (P < 0.05) according to Duncan’s multiple range test

Therefore, the inhibition of nitrogen uptake observed in treatments not involving foliar application, due to salinity-imposed competition with Cl (Papadopoulos and Rending 1983), was successfully overcome at moderate salinity, but not at high salinity. López-Berenguer et al. (2007) found that a NaCl concentration higher than 60 mM exceeded the threshold of resistance in broccoli plants. But the reduced N–NO3 concentration in the leaves at higher salinity could be strongly affected by the higher osmotic effect of the nutrient solution, reducing N uptake.

Salinity significantly reduced the leaf CO2 assimilation, by 28.5 and 41.7% when 40 or 120 mM NaCl was applied, respectively, for non-sprayed plants (Fig. 4). However, when MeJA or foliar urea was applied, combined with 40 mM NaCl, photosynthesis was not impaired significantly. In contrast, with 120 mM NaCl, a dramatic reduction was found despite foliar applications. Boari et al. (1997) also found a significant reduction of photosynthesis when broccoli was grown under high salinity. Previous data about leaf mineral balance support the response of photosynthesis at differing degrees of salinity stress. Thus, the N status of leaf must be closely linked to photosynthetic activity and the expression of some transporters depends on the amount of available carbon (Lejay et al. 2003).
Fig. 4

Effect of NaCl concentration in the substrate and urea or MeJA spray on leaf CO2 assimilation and soil respiration. Data are means ± SE of 5 different plant samples. *, **, and *** represent P < 0.05, 0.01, and 0.001, respectively. ns not significant. For each column, different letters indicate significant differences (P < 0.05) according to Duncan’s multiple range test

Foliar urea or MeJA did not improve root respiration under non-saline conditions, but irrigation with 40 mM NaCl increased soil respiration by 36.4 and 29.4% when urea or MeJA was applied, compared with the non-sprayed plants under the same growth conditions. However, a non-beneficial effect was found at 120 mM NaCl. At high salinity, salts can build up in leaves to excessive levels, but exactly how the salts exert their toxicity remains unknown. Salts may build up in the apoplast and dehydrate the cell, they may build up in the cytoplasm and inhibit enzymes involved in carbohydrate metabolism, or they may build up in the chloroplast and exert a direct toxic effect on photosynthetic processes (Munns and Tester 2008).

Chloride build up in leaves of plants can produce a progressive decrease in plant growth and a reduction in photosynthesis and transpiration (López-Climent et al. 2008; Zheng et al. 2008). However, as reported by Walia et al. (2007), the treatment with JA partially alleviated photosynthetic inhibition caused by moderate salinity stress, and genes involved in JA biosynthesis show increased abundance (Walia et al. 2006). Additionally, foliar application of urea also appeared to counteract the stress-induced damage, maintaining growth and photosynthesis at moderate stress. Recently, Hasaneen et al. (2008) found a similar effect for NaCl-stressed lettuce, thus indicating that toxic ions, such as Na+ in the leaves, may interfere with phloem loading, restricting the movement of nutrients from roots to shoot (Sultana et al. 2001). Therefore, N applied directly to the leaves decreases the inhibition due to the toxic effects of Na+ and Cl or minimizes the salinity-induced nutrient deficiency, maintaining the NO3 concentration.

Carbon and nitrogen isotope composition

Salinity significantly decreased nitrogen isotope discrimination and increased the carbon isotope discrimination in leaf dry matter (Fig. 5), but a non-specific response was found regarding the application of foliar treatments (urea or MeJA). Clearly, an important reduction from 7.40 to 4.93‰ was observed when 120 mM NaCl was imposed on non-sprayed plants, for N isotopes. Additionally, for C isotopes, an increase from −35.2 to −34.5‰ was obtained for these saline treatments. Natural abundances of 15N and 13C may provide complementary information on how nitrogen fertilizer is used by the plant (Serret et al. 2008), and the different response pattern in δ 13C was reported as a consequence of the variation in stomata in relation to the differences in salinity tolerance (Wei et al. 2008). Our data, considering the conditions of highest saline stress, show that both δ 13C and δ 15N were also highly correlated with broccoli shoot biomass and net photosynthesis.
Fig. 5

Changes in leaf δ15N and δ13C of plants supplied with 0, 40, or 60 mM NaCl and sprayed with methyl-jasmonate or foliar urea. Data are means ± SE of 5 different plant samples. *, **, and *** represent P < 0.05, 0.01, and 0.001, respectively. ns not significant. For each column, different letters indicate significant differences (P < 0.05) according to Duncan’s multiple range test

Foliar δ 15N values also show a strong relationship with water availability (Handley et al. 1999): in our experiment, this may be the result of the osmotic effect of the saline solution, and these values may reflect changes in N allocation within leaves (Stock and Evans 2006).

Values of δ 13C are determined mainly by three processes: diffusion of CO2 through stomata, CO2 assimilation by carboxylase, and metabolism of compounds (Wei et al. 2008). The data showing depression of photosynthesis may be attributed to stomatal closure, increase in water use efficiency, and non-stomatal factors such as damaged cell membranes, reduced mesophyll conductance, and decreased Rubisco activity (Sobrado 1999), but δ 13C could be used as one of the key limiting factors of photosynthesis (Brugnoli and Lauteri 1991). Thus, if stomatal limitation was the main cause of photosynthetic inhibition, leaf δ 13C would increase with increasing salinity, whereas if non-stomatal factors became the key limitation, the values would tend to decrease (Wei et al. 2008). Therefore, our results indicate a stomatal limitation of photosynthesis in broccoli plants due to salinity.

In conclusion this study shows (1) the feasibility of using both foliar urea or methyl-jasmonate to increase salinity tolerance as growth, photosynthesis, and root respiration were not impaired under moderate saline stress (2) that foliar treatments maintained NO3 and reduced Na+ concentrations in the leaves at moderate salinity, and (3), a significant relationship for δ 13C and δ 15N, with salinity: δ 13C values increased whilst δ 15N decreased–which may be attributable to stomatal adjustment and changes in N allocation within leaves, respectively.

Notes

Acknowledgments

Paula Cuadra-Crespo is the recipient of a pre-doctoral fellowship from the IMIDA. The authors thank G. Ortuño for his technical assistance. This work has been supported by the Instituto Nacional de Investigaciones Agrarias (INIA), through project RTA2008-00089. Part of this work was also funded by the European Social Fund.

References

  1. Ali G, Srivastava PS, Iqbal M (1999) Proline accumulation, protein pattern and photosynthesis in regenerants grown under NaCl stress. Biol Plant 42:89–95CrossRefGoogle Scholar
  2. Bar Y, Apelbaum A, Kafkafi U, Goren R (1997) Relationship between chloride and nitrate and its effect on growth and mineral composition of avocado and citrus plants. J Plant Nutr 20:715–731CrossRefGoogle Scholar
  3. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  4. Boari F, Cantore V, Cucci G (1997) Brackish water and physiological aspects of broccoli. Acta Hort 449:657–664Google Scholar
  5. Borsani O, Valpuesta V, Botella MA (2003) Developing salt tolerant plants in a new century: a molecular biology approach. Plant Cell Tiss Organ Cult 73:101–115CrossRefGoogle Scholar
  6. Brugnoli E, Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism, Advances in photosynthesis, vol 9. Academic Publishers, The Netherlands, pp 399–434Google Scholar
  7. Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium Hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiol 95:628–635CrossRefPubMedGoogle Scholar
  8. Cabrera-Bosquet L, Molero G, Bort J, Nogues S, Araus JL (2007) The combined effect of constant water deficit and nitrogen supply on WUE, NUE and Delta C-13 in durum wheat potted plants. Ann Appl Biol 151:277–289CrossRefGoogle Scholar
  9. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677CrossRefPubMedGoogle Scholar
  10. Choi WJ, Ro HM, Chang SX (2005) Carbon isotope composition of Phragmites australis in a constructed saline wetland. Aquat Bot 82:27–38CrossRefGoogle Scholar
  11. Cram WJ (1983) Chloride accumulation as a homeostatic system: set points and perturbation. J Exp Bot 34:1484–1502CrossRefGoogle Scholar
  12. De Pascale S, Maggio A, Barbieri G (2005) Soil salinization affects growth, yield and mineral composition of cauliflower and broccoli. Eur J Agron 23:254–264CrossRefGoogle Scholar
  13. del Amor FM, Cuadra-Crespo P, Varó P, Gómez MC (2009) Influence of foliar urea on the antioxidant response and fruit color of sweet pepper under limited N supply. J Sci Food Agric 89:504–510CrossRefGoogle Scholar
  14. del Amor FM, Cuadra-Crespo P, Walker DJ, Cámara JM, Madrid R (2010) Effect of foliar application of antitranspirant on photosynthesis and water relations of pepper plants under different levels of CO2 and water stress. J Plant Physiol 167:1232–1238CrossRefPubMedGoogle Scholar
  15. Dong SF, Cheng LL, Scagel CF, Fuchigami LH (2004) Nitrogen mobilization, nitrogen uptake and growth of cuttings obtained from poplar stock plants grown in different N regimes and sprayed with urea in autumn. Tree Physiol 24:355–359PubMedGoogle Scholar
  16. Embleton TW, Stolzy LH, Devitt DA, Jones WW, EI-Motaium R, Summers LL (1986) Citrus nitrogen fertilizer management, groundwater pollution, soil salinity and nitrogen balance. Appl Agr Res 1:57–64Google Scholar
  17. Everaarts AP, De willigen P (1999) The effect of nitrogen and the method of application on yield and quality of broccoli. Nether J Agric Sci 47:123–133Google Scholar
  18. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  19. Fedina IS, Benderliev KM (2000) Response of Scenedesmus Incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43:625–627CrossRefGoogle Scholar
  20. Fedina IS, Tsonev TD (1997) Effect of pretreatment with methyl jasmonate on the response of Pisum sativum to salt stress. J Plant Physiol 151:735–740Google Scholar
  21. Grattan SR, Grieve CM, Smith TE, Lauchli A, Poss JA, Suarez DL (2006) Can broccoli tolerate higher concentrations of boron under saline conditions? 18th World Congress of Soil Science, Philadelphia, p 75Google Scholar
  22. Habib R, Millard P, Proe MF (1993) Modeling the seasonal nitrogen partitioning in young sycamore (Acer-Pseudoplatanus) trees in relation to nitrogen supply. Ann Bot 71:453–459CrossRefGoogle Scholar
  23. Handley LL, Scrimgeour CM (1997) Terrestrial plant ecology and N-15 natural abundance: The present limits to interpretation for uncultivated systems with original data from a Scottish old field. Adv Ecol Res 27:133–212CrossRefGoogle Scholar
  24. Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S, Stewart GR (1999) The N-15 natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Austr J Plant Physiol 26:185–199CrossRefGoogle Scholar
  25. Hasaneen MNA, Younis ME, El-Bialy DMA (2008) Plant growth, metabolism and adaptation in relation to stress conditions: Further studies supporting nullification of harmful effects of salinity in lettuce plants by urea treatment. Plant Soil Environ 54:123–131Google Scholar
  26. Hawkins HJ, Lewis OAM (1993) Effect of NaCl salinity, N form, calcium and potassium concentration on N uptake and kinetics in Triticum aestivum L. cv. Gametos. New Phytol 124:171–177CrossRefGoogle Scholar
  27. Hu Y, Schmidhalter U (1998) Spatial distributions and net deposition rates of mineral elements in the elongating wheat (Triticum aestivum L.) leaf under saline soil conditions. Planta 204:212–219CrossRefGoogle Scholar
  28. Kafkafi U, Yaeesh Siddiqi M, Ritchie RJ, Glass ADM, Ruth TJ (1992) Reduction of nitrate (13NO3) influx and nitrogen (13N) translocation by tomato and melon varieties after short exposure to calcium and potassium chloride salts. J Plant Nutr 15:959–975CrossRefGoogle Scholar
  29. Lejay L, Gansel X, Cerezo M, Tilliard P, Müller C, Krapp A, von Wirén N, Daniel-Vedele F, Gojon A (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15:2218–2232CrossRefPubMedGoogle Scholar
  30. LeStrange M, Mayberry KS, Koike ST, Valencia J (1996) Broccoli production in California. UCANR Publication 7211Google Scholar
  31. López-Berenguer C, Carvajal M, García-Viguera C, Alcaraz CF (2007) Nitrogen, phosphorus, and sulphur nutrition in Broccoli plants grown under salinity. J Plant Nutr 30:1855–1870CrossRefGoogle Scholar
  32. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184CrossRefGoogle Scholar
  33. Maas EV, Grattan SR (1999) Crop yields as affected by salinity. In: Skaggs RW, van Schilfgaarde J (eds) Agricultural drainage. Agron Monogr. Amer Soc Agron, Madison, pp 55–108Google Scholar
  34. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  35. Munns R, Tester M (2008) Mechanisms of Salinity Tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  36. Nicoulaud BAL, Bloom AJ (1996) Absorption and assimilation of foliarly applied urea in tomato. J Amer Soc Hort Sci 121:1117–1121Google Scholar
  37. Niu XM, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in Nacl stress environments. Plant Physiol 109:735–742PubMedGoogle Scholar
  38. Papadopoulos I, Rending VV (1983) Interactive effects of salinity and nitrogen on growth and yields of tomato plants. Plant Soil 73:47–57CrossRefGoogle Scholar
  39. Parra-Lobato MC, Fernández-Garcia N, Olmos E, Alvarez-Tinauta MC, Gómez-Jiméneza MC (2009) Methyl jasmonate-induced antioxidant defence in root apoplast from sunflower seedlings. Environ Exp Bot 66:9–17CrossRefGoogle Scholar
  40. Pessarakli M (1991) Dry-matter yield, N-15 absorption, and water-uptake by green bean under sodium-chloride stress. Crop Sci 31:1633–1640CrossRefGoogle Scholar
  41. Purty RS, Kumar G, Singla-Pareek SL, Pareek A (2008) Towards salinity tolerance in Brassica: an overview. Physiol Mol Biol Plants 14:39–49CrossRefGoogle Scholar
  42. Robinson D, Handley LL, Scrimgeour CM, Gordon DC, Forster BP, Ellis RP (2000) Using stable isotope natural abundances (delta N-15 and delta C-13) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. J Exp Bot 51:41–50CrossRefPubMedGoogle Scholar
  43. Serret MD, Ortiz-Monasterio I, Pardo A, Araus JL (2008) The effects of urea fertilisation and genotype on yield, nitrogen use efficiency, delta N-15 and delta C-13 in wheat. Ann Appl Biol 153:243–257Google Scholar
  44. Sobrado MA (1999) Leaf photosynthesis of the mangrove Avicennia germinans as affected by NaCl. Photosynthetica 36:547–555CrossRefGoogle Scholar
  45. Stock WD, Evans JR (2006) Effects of water availability, nitrogen supply and atmospheric CO2 concentrations on plant nitrogen natural abundance values. Func Plant Biol 33:219–227CrossRefGoogle Scholar
  46. Suhayda CG, Giannini JL, Briskin DP, Shannon MC (1990) Electrostatic changes in Lycopersicon esculentum root plasma membrane resulting from salt stress. Plant Physiol 93:471–478CrossRefPubMedGoogle Scholar
  47. Sultana N, Ikeda T, Kashem MA (2001) Effect of foliar spray of nutrient solutions on photosynthesis, dry matter accumulation and yield in seawater-stressed rice. Environ Exp Bot 46:129–140CrossRefGoogle Scholar
  48. Tani T, Sobajima H, Okada K, Chujo T, Arimura S, Tsutsumi N, Nishimura M, Seto H, Nojiri H, Yamane H (2008) Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227:517–526CrossRefPubMedGoogle Scholar
  49. Tsonev TD, Lazova GN, Stoinova ZG, Popova LP (1998) A possible role for jasmonic acid in adaptation of barley seedlings to salinity stress. J Plant Growth Regul 17:153–159CrossRefGoogle Scholar
  50. Tuna AL, Kaya C, Dikilitas M, Higgs D (2008a) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62:1–9CrossRefGoogle Scholar
  51. Tuna AL, Kaya C, Higgs D, Murillo-Amador B, Aydemir S, Girgin AR (2008b) Silicon improves salinity tolerance in wheat plants. Environ Exp Bot 62:10–16CrossRefGoogle Scholar
  52. Walia H, Wilson C, Wahid A, Condamine P, Cui X, Close TJ (2006) Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Func Integr Genom 6:143–156CrossRefGoogle Scholar
  53. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30:410–421CrossRefPubMedGoogle Scholar
  54. Wang Y, Mopper S, Hasenstein KH (2001) Effects of salinity on endogenous ABA, IAA, JA and SA in Iris hexagona. J Chem Ecol 27:327–342CrossRefPubMedGoogle Scholar
  55. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697CrossRefPubMedGoogle Scholar
  56. Wei L, Yan C, Guo X, Ye B (2008) Variation in the δ13C of two mangrove plants is correlated with stomatal response to salinity. J Plant Growth Regul 27:263–269CrossRefGoogle Scholar
  57. Witte CP, Tiller SA, Taylor MA, Davies HV (2002) Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of 15 N after foliar urea applications in wild-tipy and urease-antisense transgenics. Plant Physiol 128:1129–1136CrossRefPubMedGoogle Scholar
  58. Yeo AR (1983) Salinity resistance—physiologies and prices. Plant Physiol 58:214–222CrossRefGoogle Scholar
  59. Yeo AR, Caporn SJM, Flowers TJ (1985) The effect of salinity upon photosynthesis in rice (Oryza-Sativa L.): gas-exchange by individual leaves in relation to their salt content. J Exp Bot 36:1240–1248CrossRefGoogle Scholar
  60. Zheng Y, Wang Z, Sun X, Jia A, Jiang G, Li Z (2008) Higher salinity tolerance cultivars of winter wheat relieved senescence at reproductive stage. Environ Exp Bot 62:129–138CrossRefGoogle Scholar
  61. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Departament of Citricultura y Calidad AlimentariaInstituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA)La AlbercaSpain

Personalised recommendations