Skip to main content
SpringerLink
Log in

Phenolic content and antioxidant activity in two contrasting Medicago ciliaris lines cultivated under salt stress

  • Section Cellular and Molecular Biology
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

The objective of this study was to determine more indepth physiological and antioxidant responses in two Medicago ciliaris lines (a salt-tolerant line TNC 1.8 and a salt-sensitive line TNC 11.9) with contrasting responses to 100 mM NaCl. Under salt stress, both lines showed a decrease in total biomass and in the growth rate for roots, but TNC 1.8 was less affected by salt than TNC 11.9 in that it maintained leaf growth even in the presence of added salt. In both lines, salt stress mainly affected micronutrient status (Fe, Mn, Cu and Zn) rather than K nutrition, but the tolerant line TNC 1.8 accumulated more Na in leaves and less in roots compared with TNC 11.9. Salt stress decreased total soluble sugars (TSS) in all organs of the sensitive line TNC 11.9, whereas TSS was only reduced in roots of the tolerant line. The salt-induced drop in growth was linked to an increase in lipid peroxidation in roots of both lines and in leaves of the sensitive line. The salt-tolerant line TNC 1.8 was more efficient at managing salt-induced oxidative damage in leaves and to a lesser extent in roots than the salt-sensitive line TNC 11.9, by preserving higher phenolic compound and superoxide dismutase levels in both organs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CE:

catechin equivalent

DM:

dry matter

GAE:

gallic acid equivalents

MDA:

malondialdehyde

RGR:

relative growth rate

ROS:

reactive oxygen species

SOD:

superoxide dismutase

TBA:

thiobarbituric acid

TCA:

trichloroacetic acid

TSS:

total soluble sugars

References

  • Abdelly C., Debez A., Smaoui A. & Grignon C. 2011. Halophytefodder species association may improve nutrient availability and biomass production of the sabkha ecosystem, pp. 85–94. In: Öztürk M., Böer B., Barth J.H., Breckle S.W., Clüsener-Godt M. & Khan M.A. (eds), Sabkha Ecosystems, Volume 3: Africa and Southern Europe. Springer, Drodrecht, Heidelberg, London, New York.

    Google Scholar 

  • Abdul Jaleel C., Gopi R., Sankar B., Manivannan P., Kishorekumar A., Sridharan R. & Panneerselvam R. 2007. Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. South Afr. J. Bot. 73: 190–195.

    Article  CAS  Google Scholar 

  • Ballesteros E., Blumwold E., Donnaire J.P. & Belver A. 1997. Na+/H+ antiport activity in tonoplast vesicles isolated from sunflower roots induced by NaCl stress. Physiol. Plant. 9: 328–334.

    Article  Google Scholar 

  • Bates L.S., Waldren R.P. & Teare I.D. 1973. Rapid determination of the free proline in water stress studies. Plant Soil 39: 205–208.

    Article  CAS  Google Scholar 

  • Ben Salah I., Albacete A., Martínez Andújar C., Haouala R., Labidi N., Zribi F., Martinez V., Pérez-Alfocea F. & Abdelly C. 2009. Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress. J. Plant Physiol. 166: 477–488.

    Article  PubMed  CAS  Google Scholar 

  • Ben Salah I., Slatim T., Gruber M., Mesedi D., Gandour M., Benzarti M., Maouala R., Zribi K., Ben Hamed K., Perez-Alfocea F. & Abdelly C. 2011. Relationship between symbiotic nitrogen fixation, sucrose synthesis, and antioxidant activities in source leaves of two Medicago ciliaris lines cultivated under salt stress. Environ. Exp. Bot. 70: 166–173.

    Article  CAS  Google Scholar 

  • Bhattacharjee S. & Mukherjee A.K. 1996. Ethylene evolution and membrane lipid peroxidation as indicators of salt injury in leaf tissues of Amaranthus lividus seedlings. Ind. J. Exp. Biol. 34: 279–281.

    CAS  Google Scholar 

  • Bradford M. 1976. A rapid and sensitive method for the quantification of microgram quantities of proteins utilising the principal of protein-dye binding. Anal. Biochem. 72: 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Cavalcanti F.R., Lima J.P.M.S., Ferreira-Silva S.L., Viégas R.A. & Silveira J.A.G. 2007. Roots and leaves display contrasting oxidative response during salt stress and recovery in cowpea. J. Plant Physiol. 164: 591–600.

    Article  PubMed  CAS  Google Scholar 

  • Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70: 1–9.

    Article  CAS  Google Scholar 

  • Chanwitheesuk A., Teerawutgulrag A. & Rakariyatham N. 2005. Screening of antioxidant activity and antioxidant compounds of some edible plants of Thailand. Food Chem. 92: 491–497.

    Article  CAS  Google Scholar 

  • Chinnusamy V., Jagendorf A. & Zhu J.K. 2005. Understanding and improving salt tolerance in plants. Crop Sci. 45: 437–448.

    Article  CAS  Google Scholar 

  • Debez A., Saadaoui D., Ramanib B., Ouerghi Z., Koyro H.W., Huchzermeyer B. & Abdelly C. 2006. Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ. Exp. Bot. 57: 285–295.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Di Baccio D., Navari-Izzo F. & Izzo R. 2004. Seawater irrigation: antioxidant defence responses in leaves and roots of a sunflower (Helianthus annuus L.) ecotype. J. Plant Physiol. 161: 1359–1366.

    Article  PubMed  Google Scholar 

  • Dixon R.A. & Paiva N. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085–1097.

    Article  PubMed  CAS  Google Scholar 

  • Gómez J.M., Hernandez J.A., Jimenez A., del Rio L.A. & Sevilla F. 1999. Differential response of antioxidative system of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radic. Res. 31: 11–18.

    Article  Google Scholar 

  • Gossett D.R., Millhollon E.P. & Lucas M.C. 1994. Antioxidant responses to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci. 34: 706–714.

    Article  CAS  Google Scholar 

  • Gould K.S., Markham K.R., Smith R.H. & Goris J.J. 2000. Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. J. Exp. Bot. 51: 1107–1115.

    Article  CAS  Google Scholar 

  • Grassmann J., Hippeli S. & Elstner E.F. 2002. Plant’s defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol. Biochem. 40: 471–478.

    Article  CAS  Google Scholar 

  • Hernandez J.A. & Almansa M.S. 2002. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol. Plant. 115: 251–257.

    Article  PubMed  CAS  Google Scholar 

  • Hewitt E.J. 1966. Sand and Water Culture Methods Used in the Study of Plant Nutrition; 2nd Ed. Commonwealth Agricultural Bureau, Farnham Royal, 547 pp.

    Google Scholar 

  • Kholová J., Sairam R.K., Meena R.C. & Srivastava G.C. 2009. Response of maize genotypes to salinity stress in relation to osmolytes and metal ions contents, oxidative stress and antioxidant enzymes activity. Biol. Plant. 53: 249–256.

    Article  Google Scholar 

  • Kjeldahl J.Z. 1983. New methode zyr Besimming des stickstoffs in organischen Körpen. Anal. Chem. 22: 366–382.

    Google Scholar 

  • Koca H., Ozdemir F. & Turkan I. 2006. Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii. Biol. Plant. 50: 745–748.

    Article  CAS  Google Scholar 

  • Ksouri R., Megdiche W., Debez A., Falleh H., Grignon C. & Abdelly C. 2007. Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol. Biochem. 45: 244–249.

    Article  PubMed  CAS  Google Scholar 

  • Lisiewska Z., Kmiecik W. & Korus A. 2006. Content of vitamin C, carotenoids, chlorophylls and polyphenols in green parts of dill (Anethum graveolens L.) depending on plant height. J. Food Compos. Anal. 19: 134–140.

    Article  CAS  Google Scholar 

  • Mäeser P., Gierth M. & Schroeder J.I. 2002. Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247: 43–54.

    Article  Google Scholar 

  • Mengel K. & Kirkby E.A. 2001. Plant nutrients, pp. 1–14. In: Mengel K., Kirkby E.A., Kosegarten H. & Appel T. (eds) Principles of Plant Nutrition. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Mittova V., Tal M., Volokita M. & Guy M. 2003. Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in responses to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ. 26: 845–856.

    Article  PubMed  CAS  Google Scholar 

  • Munns R. & Tester M. 2008. Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59: 651–681.

    Article  CAS  Google Scholar 

  • Naczk M. & Shahidi F. 2004. Extraction and analysis of phenolics in food. J. Chromatogr. 1054: 95–111.

    CAS  Google Scholar 

  • Navarro J.M., Flores P., Garrido C. & Martinez V. 2006. Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity. Food Chem. 96: 66–73.

    Article  CAS  Google Scholar 

  • Noctor G. & Foyer C.H. 1998. Ascorbate and glutathione: keeping active oxygen under control. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–279.

    Article  CAS  Google Scholar 

  • Oliva S.R., Raitio H. & Mingorance M.D. 2003. Comparison of two wet digestion procedures for multi-element analysis of plant samples. Commun. Soil Sci. Plant Anal. 34: 2913–2923.

    Article  CAS  Google Scholar 

  • Polle A. & Rennenberg H. 1993. Significance of antioxidants in plant adaptation to environmental stress, pp. 263–273. In: Fowden L., Mansfield T. & Stoddart J. (eds), Plant Adaptation to Environmental Stress. Chapman & Hall, London.

    Google Scholar 

  • Poustini K., Siosemardeh A. & Ranjbar M. 2007. Proline accumulation as a response to salt stress in 30 wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Gen. Resour. Crop Evol. 54: 925–934.

    Article  CAS  Google Scholar 

  • Scebba F., Sebastiani L. & Vitagliano C. 1999. Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: responses to cold acclimation. J. Plant Physiol. 55: 762–768.

    Google Scholar 

  • Sgherri C., Stevanovic B. & Navari-Izzo F. 2004. Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol. Plant. 122: 478–488.

    Article  CAS  Google Scholar 

  • Shevyakova N.I., Bakulina E.A. & Kuznetsov V.I.V. 2009. Proline antioxidant role in the common ice plant subjected to salinity and paraquat treatment inducing oxidative stress. Russ. J. Plant Physiol. 56: 663–669.

    Article  CAS  Google Scholar 

  • Smirnoff N., Conklin P.L. & Loewus F.A. 2001. Biosynthesis of ascorbic acid in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 52: 437–467.

    Article  CAS  Google Scholar 

  • Srinivas N.D., Rshami K.R. & Raghavarao K.S.M.S. 1999. Extraction and purification of a plant peroxidase by aqueous two-phase extraction coupled with gel filtration. Process Biochem. 35: 43–48.

    Article  CAS  Google Scholar 

  • Sun B., Ricardo-da-Silva J.M. & Spranger I. 1998. Critical factors of vanillin assay for catechins and proanthocyanidins. J. Agric. Food Chem. 46: 4267–4274.

    Article  CAS  Google Scholar 

  • Tester M. & Davenport R. 2003. Na+ tolerance and Na+ transport in higher plants. Annals Bot. 91: 503–527.

    Article  CAS  Google Scholar 

  • Tounekti T., Vadel A.M., Onate M., Khemira H., Munné-Bosch S. 2011. Salt-induced oxidative stress in rosemary plants: damage or protection? Environ. Exp. Bot. 71: 298–305.

    Article  CAS  Google Scholar 

  • Türkan I. & Demiral T. 2009. Recent developments in understanding salinity tolerance. Environ. Exp. Bot. 67: 2–6.

    Article  Google Scholar 

  • Verbruggen N. & Hermans C. 2008. Proline accumulation in plants: a review. Amino Acids 35: 753–759.

    Article  PubMed  CAS  Google Scholar 

  • Wang X.S. & Han J.G. 2009. Changes of proline content, activity, and active isoforms of antioxidative enzymes in two alfalfa cultivars under salt stress. Agric. Sci. China 8: 431–440.

    CAS  Google Scholar 

  • Yasici I., Türkan I., Sekmen A.H. & Demiral T. 2007. Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ. Exp. Bot. 61: 49–57.

    Article  Google Scholar 

  • Yemm E.W. & Willis J. 1954. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57: 508–514.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire des Plantes Extręmophiles, CBBC, BP 901, 2050, Hammam-Lif, Tunisia

    Imène Ben Salah, Tarek Slatni, Mondher Boulaaba, Mhemmed Gandour, Dorsaf Messedi, Karim Ben Hamed, Riadh Ksouri & Chedly Abdelly

  2. Physiologie et Biochimie de la Tolérance au Sel des Plantes, Faculté des Sciences de Tunis, Campus Universitaire, 2092, Tunis El Manar, Tunisia

    Héla Mahmoudi

  3. Saskatoon Research Centre, Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, SK, S7N0X2, Canada

    Margaret Gruber

  4. Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, 1391 Sandford Street, London, ON, N5V 4T3, Canada

    Abdelali Hannoufa

Authors
  1. Imène Ben Salah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Héla Mahmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Margaret Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tarek Slatni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mondher Boulaaba
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mhemmed Gandour
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dorsaf Messedi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Karim Ben Hamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Riadh Ksouri
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Abdelali Hannoufa
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chedly Abdelly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Imène Ben Salah.

Additional information

These authors contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salah, I.B., Mahmoudi, H., Gruber, M. et al. Phenolic content and antioxidant activity in two contrasting Medicago ciliaris lines cultivated under salt stress. Biologia 66, 813–820 (2011). https://doi.org/10.2478/s11756-011-0102-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-011-0102-6

Key words

Search

Navigation