Log in

Assessment of salt tolerance of Nasturtium officinale R. Br. using physiological and biochemical parameters

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Nasturtium officinale R. Br. seedlings were treated with a range of NaCl concentrations (0, 50, 100 and 150 mM) for 21 days after seedling emergence. Physiological analysis based on growth and mineral nutrition, showed a substantial decrease in leaf dry matter with 150 mM NaCl treatment. The growth decrease was correlated with nutritional imbalance and a reduction in potassium accumulation and transport to the leaves. At the same time, we noted an increase in leaf sodium and chloride accumulation and transport. Salt tolerance of N. officinale under 100 mM NaCl was associated with osmotic adjustment via Na+ and Cl and the maintenance of high K+/Na+ selectivity. Salt decreased carotenoid content more than chlorophylls and also disturbed membrane integrity by increasing malondialdehyde content and electrolyte leakage. At 150 mM NaCl, an increase in antioxidant enzyme-specific activities for superoxide dismutase, catalase and guaiacol peroxidase occurred in concert with a decrease in ascorbic acid, polyphenol, tannin and flavonoid content. These results indicate that N. officinale can maintain growth and natural antioxidant defense compounds such as, vitamin C, carotenoids, and polyphenols, when cultivated in 100 mM NaCl, but not at higher salt levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

DW:

Dry weight

FW:

Fresh weight

D:

Day

Chl:

Chlorophylls

CAR:

Carotenoids

EL:

Electrolyte leakage

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

CAT:

Catalase

POD:

Guaiacol peroxidase

References

  • Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5(4):369–374

    Article  CAS  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  Google Scholar 

  • Ashley M, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  CAS  PubMed  Google Scholar 

  • Athar HR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Env Exp Bot 63:224–231

    Article  CAS  Google Scholar 

  • Awika JM, Rooney LW, Wu X, Prior RL, Zevallos LC (2003) Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and Sorghum products. J Agric Food Chem 51:6657–6662

    Article  CAS  PubMed  Google Scholar 

  • Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F et al (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014

    Article  CAS  PubMed  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Bielski BH, Richter HW, Chan PC (1975) Some properties of the ascorbate free radical. Ann NY Acad Sci 258:231–237

    Article  CAS  PubMed  Google Scholar 

  • Boulos L (1983) Medicinal plants of North Africa. Reference Publications, Algonac Michigan

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Brody SS, Chaney SE (1966) Flame photometric detector. J Gas Chromatogr 4:42

    CAS  Google Scholar 

  • Chance B, Maehly SK (1955) Assay of catalase and peroxidases. Method Enzymol 2:764–775

    Article  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163–177

    Article  PubMed  Google Scholar 

  • Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15(10):7313–7352

    Article  CAS  PubMed  Google Scholar 

  • DeFord DD (1960) Electroanalysis and coulometric analysis. Analy Chem 32(5):31–37

    Article  Google Scholar 

  • Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014

    Article  CAS  PubMed  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • El-Ghorab AH, Shibamoto T, Ozcan M (2007) Chemical composition and antioxidant activities of buds and leaves of capers (Capparis ovata Desf. Var. Canesencene) cultivated in Turkey. J Essent Oil Res 19:72–77

    Article  CAS  Google Scholar 

  • Fielding JL, Hall JA (1978) Biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29:969–981

    Article  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  CAS  PubMed  Google Scholar 

  • Frary A, Gol D, Keleş D, Okmen B, Pınar H, Şığva HO, Yemenicioğlu A, Doğanlar S (2010) Salt tolerance in Solanum pennellii: antioxidant response and related QTL. BMC Plant Biol 10:58–74

    Article  PubMed  Google Scholar 

  • Fridovich I (1975) Superoxide dismutase. Ann Rev Biochem 44:507–523

    Article  Google Scholar 

  • Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–882

    Article  CAS  Google Scholar 

  • Gorham J, Wyn Jones RG, Bristol A (1990) Partial characterization of the trait for enhanced K+–Na+ discrimination in the D genome of wheat. Planta 180:590–597

    Article  CAS  PubMed  Google Scholar 

  • GRIN (Germplasm Resources Information Network) (2012) [USDA Online Database]. National Germplasm Resources Laboratory, Beltsville, Maryland. URL: http://www.ars-grin.gov/cgi-bin/npgs/html/taxon.pl?25072 (08 May 2012)

  • Hachicha M (2007) Les sols salés et leur mise en valeur en Tunisie. Secheresse 18:45–50

    Google Scholar 

  • Harinasut P, Srisunak S, Pitukchaisopol S, Charoensataporn R (2000) Mechanisms of adaptation to increasing salinity of mulberry: proline content and ascorbate peroxidase activity in leaves of multiple shoots. Sci Asia 26:207–211

    Article  CAS  Google Scholar 

  • Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938

    Article  PubMed  Google Scholar 

  • Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Env 33:552–565

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Expt Sta Circ 347:1–32

    Google Scholar 

  • Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27:129–138

    Article  CAS  PubMed  Google Scholar 

  • Hussain K, Majeed A, Nawaz K, Hayat KB, Nisar MF (2009) Effect of different levels of salinity on growth and ion contents of black seeds (Nigella sativa L). Curr Res J Biol Sci 1:135–138

    CAS  Google Scholar 

  • Imaida K, Fukushima T, Shivai T, Ohtani M, Nakanishi K, Ito N (1983) Promoting activities of butylatedhydroxyanisole and butylatedhydroxytoluene on 2-stage urinary bladder carcinogenesis and inhibition of ç-glutamyltranspeptidase-positive foci development in the liver of rats. Carcinogen 75(4):895–899

    Article  Google Scholar 

  • Iturbe-Ormaetxe I, Escudero PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116:173–181

    Article  CAS  Google Scholar 

  • Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL, Conejero G, Rodriguez-Navarro A, Sentenac H, Guiderdoni E, Abdelly C et al (2009) Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955–1971

    Article  CAS  PubMed  Google Scholar 

  • ** X, Huang Y, Zeng F, Zhou M, Zhang G (2009) Genotypic difference in response of peroxidase and superoxide dismutase isozymes and activities to salt stress in barley. Acta Physiol Plant 31:1103–1109

    Article  CAS  Google Scholar 

  • Kaddour R, Nasri N, M’rah S, Berthomieu P, Lachaâl M (2009) Comparative effect of potassium on K and Na uptake and transport in two accessions of Arabidopsis thaliana during salinity stress. C R Biol 332:784–794

    Article  CAS  PubMed  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  PubMed  Google Scholar 

  • Katsuhara M, Otsuka T, Ezaki B (2005) Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci 169:369–373

    Article  CAS  Google Scholar 

  • Lebaudy A, Very AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366

    Article  CAS  PubMed  Google Scholar 

  • Lemordant D (1977) Plantes utiles et toxiques de Tunisie. Fitoterapia 18:191–214

    Google Scholar 

  • Lichtenthaler HK (1988) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–383

    Article  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N et al (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161

    Article  PubMed  Google Scholar 

  • Míková K (2002) The regulation of antioxidants in food. In: Watson DH (ed) Food Chemical Safety, Additives, vol 2, 1st edn. Woodhead Publishing Limited, Boca Raton

  • Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    Article  CAS  PubMed  Google Scholar 

  • M’rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaal M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384

    Article  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Namiki M (1990) Antioxidants/antimutagens in food. CRC Crit Rev Food Sci Nutr 29:273–300

    Article  CAS  Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    CAS  PubMed  Google Scholar 

  • Patel AD, Bhensdadia H, Nath PA (2009) Effect of salinisation of soil growth, water status and general nutrient accumulation in seedlings of Delonixregia (Fabaceae). Acta Ecol Sin 29(2):109–115

    Article  Google Scholar 

  • Pitman MG (1988) Whole plants. In: Baker A, Hall JL (eds) Solute transport in plant cells and tissues. Longman Scientific and Technical, Essex, pp 346–385

  • Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive 1 Na+–H+ antiporter during salinity stress. Plant Physiol 136:2548–2555

    Article  CAS  PubMed  Google Scholar 

  • Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    Article  CAS  PubMed  Google Scholar 

  • Romero-Aranda R, Moya JL, Tadeo FR, Legaz F, Primo-Millo E, Talon M (1998) Physiological and anatomical disturbances induced by chloride salts in sensitive and tolerant citrus: beneficial and detrimental effects of cations. Plant Cell Environ 21:1243–1253

    Article  CAS  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Sun J, Chu YF, Wu XZ, Liu RH (2002) Antioxidant and antiproliferative activities of common fruits. J Agric Food Chem 50(25):7449–7454

    Article  CAS  PubMed  Google Scholar 

  • Tavakkoli E, Rengasamy P, Mcdonald GK (2010) High concentrations of Na+ and Cl ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61(15):4449–4459

    Article  CAS  PubMed  Google Scholar 

  • Teakle NL, Flowers TJ, Real D, Colmer TD (2007) Lotus tenuis tolerates the interactive effects of salinity and waterlogging by ‘excluding’ Na+ and Cl from the xylem. J Exp Bot 58:2169–2180

    Article  CAS  PubMed  Google Scholar 

  • Turhan E, GulenErics A (2008) The activity of antioxidative enzymes in three strawberry cultivars related to salt-stress tolerance. Acta Physiol Plant 30:201–208

    Article  CAS  Google Scholar 

  • Yang F, **ao X, Zhang S, Korpelainen H, Li C (2009) Salt stress responses in Populus cathayana Rehder. Plant Sci 176(5):669–677

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zörb C, Schmitt S, Neeba A, Karl A, Linder M, Schubert S (2004) The biochemical reaction of maize (Zea mays L.) to salt stress is characterized by a mitigation of symptoms and not by a specific adaptation. Plant Physiol 167:91–100

    Google Scholar 

Download references

Acknowledgments

Authors would like to thank all who participated in the elaboration of this work, with chemicals, instruments or critical reading.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rym Kaddour.

Additional information

Communicated by J. Kovacik.

R. Kaddour and E. Draoui have equally participated in the elaboration of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaddour, R., Draoui, E., Baâtour, O. et al. Assessment of salt tolerance of Nasturtium officinale R. Br. using physiological and biochemical parameters. Acta Physiol Plant 35, 3427–3436 (2013). https://doi.org/10.1007/s11738-013-1377-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-013-1377-8

Keywords

Navigation