, Volume 25, Issue 6, pp 1155–1165 | Cite as

The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants

  • Guillermo Noriega
  • Ethel Caggiano
  • Manuel López Lecube
  • Diego Santa Cruz
  • Alcira Batlle
  • María Tomaro
  • Karina Beatriz BalestrasseEmail author


The protective action of salicylic acid (SA) pre-treatment on soybean plants before cadmium (Cd) addition was tested. Oxidative stress parameters, such as TBARS formation, glutathione and chlorophyll content, were altered by Cd, instead no differences were observed in plants only pre-treated with SA. Antioxidant enzymes were affected by Cd treatment, while SA protected against these effects. These findings indicated that SA could act as a protector against oxidative stress induced by Cd. Taking into account the fact that heme-oxygenase-1 (HO-1) has been previously described as a novel antioxidant enzyme, experiments were carried out to determine whether it was involved in the protection exerted by SA. As expected, Cd brought about an enhancement of 57 % in HO-1 activity and 150 % in protein content (150 %), SA also increased both the enzyme activity and its protein content (28 and 75 %, respectively). Surprisingly, the observed rise of HO activity and protein content under SA treatment was lower than that produced by Cd alone. These lower values indicated, that HO-1 could not be directly involved in the protection of SA against Cd effects. In order to shed light in the mechanisms involved in SA effects, Cd content was determined in the tissues of Cd treated plants with and without SA pre-treatment. Results indicated that, in the presence of SA, Cd uptake was inhibited, thus avoiding its deleterious effects. Moreover, the observed HO-1 activity enhancement by SA indicates that this phytohormone could be engaged in the signalling pathway of heme degradation.


Cadmium Heme oxygenase Oxidative stress Salicylic acid Soybean plants 


  1. Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–554PubMedCrossRefGoogle Scholar
  2. Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxygenase as antioxidant defense in soybean nodules. Free Radic Res 39:145–151PubMedCrossRefGoogle Scholar
  3. Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxigenase activity and stress signaling in soybean leaves. Plant Sci 170(2):339–346CrossRefGoogle Scholar
  4. Balestrasse KB, Yannarelli GG, Noriega GO, Batlle A, Tomaro M (2008) Heme oxygenase and catalase gene expression in nodules and roots of soybean plants subjected to cadmium stress. Biometals 21(4):433–441PubMedCrossRefGoogle Scholar
  5. Becana M, Aparicio-Tejo P, Irigoyen J, Sánchez-Díaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol 82:1169–1171PubMedCrossRefGoogle Scholar
  6. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  7. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: role of heavy metal detoxication and homeostasis. Annu Rev Plant Biol 53:159–182PubMedCrossRefGoogle Scholar
  8. Dat J, Foyer C, Scott M (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461PubMedCrossRefGoogle Scholar
  9. Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168(2):511–517CrossRefGoogle Scholar
  10. Durner J, Klessig DF, Shah J (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274CrossRefGoogle Scholar
  11. Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523CrossRefGoogle Scholar
  12. Gunes A, Inal A, Alpaslam M, Erslan F, Bagsi E, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736PubMedCrossRefGoogle Scholar
  13. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11PubMedCrossRefGoogle Scholar
  14. Hayat S, Ali B, Ahmad A (2007) Salicylic acid: biosynthesis, metabolism and physiological role in plants. In: Hayat S, Ahmad A (eds) Salicylic acid: a plant hormone. Springer, Drodrecht, pp 1–14CrossRefGoogle Scholar
  15. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198PubMedCrossRefGoogle Scholar
  16. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. University of California, the Agricultural Experiment Station. Berkley Circ 347:1–39Google Scholar
  17. Horváth E, Szalai G, Janda T (2007) Induction of a biotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  18. Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208PubMedCrossRefGoogle Scholar
  19. Kang H, Saltveit M (2002) Chilling tolerance of maize, cucumber, and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576PubMedCrossRefGoogle Scholar
  20. Kikuchi G, Yoshida T, Noguchi M (2005) Heme oxygenase and heme degradation. Biochem Biophys Res Commun 338:558–567PubMedCrossRefGoogle Scholar
  21. Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931PubMedCrossRefGoogle Scholar
  22. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  23. Ling T, Zhang B, Cui W, Wu M, Lin J, Zhou W, Huang J, Shen W (2009) Carbon monoxide mitigates salt-induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci 177:331–340CrossRefGoogle Scholar
  24. Malamy J, Carr J, Klessig D, Raskin I (1990) Salicylic acid a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002PubMedCrossRefGoogle Scholar
  25. Mc Laughlin M, Parker D, Clarke J (1999) Metal and micronutrients––food safety issues. Field Crop Res 60:143–163CrossRefGoogle Scholar
  26. Metwally A, Finkermeier I, Georg M, Dietz J (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281PubMedCrossRefGoogle Scholar
  27. Mishra A, Chudhuri M (1999) Effect of salicylic acid on heavy metal-induced membrane deterioration in rice. Biol Plant 42:409–415CrossRefGoogle Scholar
  28. Muramoto T, Kohchi T, Yokota A, Hwang T, Goodman H (1999) The Arabidopsis photomorphogenic mutant hyl is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11:335–348PubMedGoogle Scholar
  29. Muramoto T, Tsurui N, Terry M, Yokota A, Kohchi T (2002) Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 130:1958–1966PubMedCrossRefGoogle Scholar
  30. Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun 323:1003–1008PubMedCrossRefGoogle Scholar
  31. Noriega GO, Santa Cruz DM, Batlle A, Tomaro ML, Balestrasse KB (2012) Heme oxygenase is involved in the protection exerted by jasmonic acid against cadmium stress in soybean roots. J Plant Growth Regul 31(1):79–89CrossRefGoogle Scholar
  32. Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231PubMedCrossRefGoogle Scholar
  33. Ray S (1986) GA, ABA, phenol interaction in the control of growth: phenolic compounds as effective modulators of GA–ABA interaction in radish seedlings. Biol Plant 28:361–369CrossRefGoogle Scholar
  34. Rodriguez-Serrano M, Romero-Puertas M, Zabalza A, Corpas F, Gomez M, Del Rio L, Sandalio L (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544PubMedCrossRefGoogle Scholar
  35. Schutzendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen per oxide content, and differentiation in scot pine roots. Plant Physiol 127:887–889PubMedCrossRefGoogle Scholar
  36. Shah J (2003) The salicylic acid loop in plant defence. Curr Opin Plant Bio l6:365–371CrossRefGoogle Scholar
  37. Vázquez S, Goldsbrough P, Carpena R (2006) Assessing the relative contributions of phytochelatins and the cell wall to cadmium resistance in white lupin. Physiol Plantarum 128:487–495CrossRefGoogle Scholar
  38. Wagner G (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212CrossRefGoogle Scholar
  39. Wang C, Zhang Songhe, PeiFang W, Jun H, Jin Q, Yanhui A, Jie L, Li L (2011) Salicylic acid involved in the regulation of nutrient elements uptake and oxidative stress in Vallisneria natans (Lour.) Hara under Pb stress. Chemosphere 84:136–142PubMedCrossRefGoogle Scholar
  40. Wintermans J, de Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta 109:448–453PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2012

Authors and Affiliations

  • Guillermo Noriega
    • 1
  • Ethel Caggiano
    • 2
  • Manuel López Lecube
    • 2
  • Diego Santa Cruz
    • 2
    • 3
  • Alcira Batlle
    • 1
  • María Tomaro
    • 1
  • Karina Beatriz Balestrasse
    • 2
    • 3
    Email author
  1. 1.Centro de Investigaciones sobre Porfirinas y Porfirias (CIPYP)CONICETBuenos AiresArgentina
  2. 2.Departamento de Química Biológica, Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina
  3. 3.Instituto de Investigaciones en Biociencias Agrícolas y Ambientales (INBA)CONICETBuenos AiresArgentina

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