Advertisement

Ecotoxicology

, Volume 22, Issue 4, pp 656–670 | Cite as

Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense

  • Poonam Pandey
  • Rajneesh Kumar Srivastava
  • R. S. DubeyEmail author
Article

Abstract

Aluminum toxicity is a major constraint to crop production in acid soils. The present study was undertaken to examine the comparative ameliorating effects of salicylic acid, Ca and Mg on Al toxicity in rice (Oryza sativa L.) seedlings grown in hydroponics. Al treatment (0.5 mM AlCl3) caused decrease in plant vigour, loss of root plasma membrane integrity, increased contents of O 2 ∙− , H2O2, lipid peroxidation, protein carbonyls and decline in the level of protein thiol. Al treatment caused significant changes in activity of antioxidative enzymes in rice seedlings. Exogenously added salicylic acid (60 μM), Ca (1 mM) and Mg (0.25 mM) significantly alleviated Al toxicity effects in the seedlings marked by restoration of growth, suppression of Al uptake, restoration of root plasma membrane integrity and decline in O 2 ∙− , H2O2, lipid peroxidation and protein carbonyl contents. Salicylic acid, Ca and Mg suppressed Al-induced increase in SOD, GPX and APX activities while it elevated Al-induced decline in CAT activity. By histochemical staining of O 2 ∙− using NBT and H2O2 using DAB, it was further confirmed that added salicylic acid, Ca or Mg decreased Al-induced accumulation of O 2 ∙− and H2O2 in the leaf tissues. Results indicate that exogenously added salicylic acid, Ca or Mg alleviates Al toxicity in rice seedlings by suppressing Al uptake, restoring root membrane integrity, reducing ROS level and ROS induced oxidative damage and regulating the level of antioxidative enzyme activities. Further salicylic appears to be superior to Mg and Ca in alleviating Al toxicity effects in rice plants.

Keywords

Aluminum Salicylic acid Calcium Magnesium Oryza sativa L. Oxidative stress 

Notes

Acknowledgments

PP and RKS are grateful to Banaras Hindu University for providing Research Fellowships to conduct this work. Financial support for this work was provided by Department of Science and Technology, Govt of India, New Delhi in form of a major research project SP/SO/PS-29/05.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal Biochem 44:176–287CrossRefGoogle Scholar
  2. Beers RF, Sizer IW (1952) Colorimetric method for estimation of catalase. J Biol Chem 195:133–139Google Scholar
  3. Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum- induced oxidative stress in maize. Phytochemistry 62:181–189CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Breusegem FV, Vranova E, Dat JF, Inze D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  6. Chen ZC, Ma JF (2012) Magnesium transporters and their role in Al tolerancein plants. Plant Soil. doi: 10.1007/s11104-012-1433-y Google Scholar
  7. Chen BC, Ho PC, Juang KW (2013) Alleviation effects of magnesium on copper toxicity and accumulation in grapevine roots evaluated with biotic ligand models. Ecotoxicology 22:174–183CrossRefGoogle Scholar
  8. Dat JF, Lopez-Delgado H, Christine H, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermo tolerance in mustard seedlings. Plant Physiol 118:1455–1461CrossRefGoogle Scholar
  9. Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (2000) Effects of salicylic acid on oxidative stress tolerance and thermotolerance in tobacco. J Plant Physiol 156:659–665CrossRefGoogle Scholar
  10. de Kok LJ, Kuiper PJC (1986) Effect of short-term dark incubation with chloride and selenate on the glutathione content of spinach leaf discs. Physiol Plant 68:477–482CrossRefGoogle Scholar
  11. Egley GH, Paul RN, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157:224–232CrossRefGoogle Scholar
  12. Eva D, Helga A, Eva SB, Jozsef F, Ferenc B, Beata B (2004) Aluminum toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 66:583–591Google Scholar
  13. Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plant Anal 19:959–987CrossRefGoogle Scholar
  14. Frahry G, Schopfer P (2001) NADH stimulated, cyanide resistant superoxide production in maize coleoptiles analyzed with tetrazolium based assay. Planta 212:175–183CrossRefGoogle Scholar
  15. Franco CR, Chagas AP, Jorge RA (2002) Ion-exchange equilibria with aluminum pectinates. Colloids Surf A Physicochem Eng Asp 204:183–192CrossRefGoogle Scholar
  16. Grauer UE, Horst WJ (1992) Modeling cation amelioration of aluminum phytotoxicity. Soil Sci Soc Am J 56:166–172CrossRefGoogle Scholar
  17. Guo TR, Chen Y, Zhang YH, Jin YF (2006) Alleviation of Al toxicity in barley by addition of calcium. Agri Sci China 5:828–833CrossRefGoogle Scholar
  18. Hayat S, Hasan SA, Fariduddin Q, Ahmad A (2008) Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. Int J Plant Sci 3:297–304Google Scholar
  19. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  20. Jana S, Choudhuri MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354CrossRefGoogle Scholar
  21. Jones DL, Gilroy S, Larsen PB, Howell SH, Kochian LV (1998) Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206:378–387CrossRefGoogle Scholar
  22. Kinraide TB, Pedler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259:201–208CrossRefGoogle Scholar
  23. Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  24. Kováčik J, Klejdus B, Hedbavny J, Bačkor M (2009) Salicylic acid alleviates NaCl-induced changes in the metabolism of Matricaria chamomilla plants. Ecotoxicology 18:544–554CrossRefGoogle Scholar
  25. Levine RL, Williams J, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357CrossRefGoogle Scholar
  26. Liu K, Luan S (2001) Internal aluminum block of plant inward K+ channels. Plant Cell 13:1453–1466Google Scholar
  27. Liu D, Zou J, Meng Q, Zou J, Jiang W (2009) Uptake and accumulation and oxidative stress in garlic (Allium sativum L.) under lead phytotoxicity. Ecotoxicology 18:134–143CrossRefGoogle Scholar
  28. Ma JF (2005) Physiological mechanisms of Al resistance in higher plants. Soil Sci Plant Nutr 61:609–612CrossRefGoogle Scholar
  29. Ma B, Wan J, Shen Z (2007) H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. Plant Growth Regul 52:91–100CrossRefGoogle Scholar
  30. Meriga B, Attitala IH, Ramgopal M, Ediga A, Kavikishor PB (2010) Differential tolerance to aluminum toxicity in rice cultivars: involvement of antioxidative enzymes and possible role of aluminum resistant locus. Acad J Plant Sci 3:53–63Google Scholar
  31. Misra HP, Fridovich I (1972) The role of superoxide anion in autooxidation of the epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175Google Scholar
  32. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  33. Noble AD, Sumner ME (1988) Calcium and Al interactions and soybean growth in nutrient solutions. Commun Soil Sci Plant Anal 19:1119–1131CrossRefGoogle Scholar
  34. Ownby JD (1993) Mechanism of reaction of hematoxylin with aluminum-treated wheat roots. Physiol Plant 87:371–380CrossRefGoogle Scholar
  35. Panda SK, Patra HK (2007) Effect of salicylic acid potentiates cadmium-induced oxidative damage in Oryza sativa L. leaves. Acta Physiol Plant 29:567–575CrossRefGoogle Scholar
  36. Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4:592–597CrossRefGoogle Scholar
  37. Rengel Z (1990) Competitive Al3+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots: II. Plant age effects. Plant Physiol 93:1261–1267CrossRefGoogle Scholar
  38. Sauvant MP, Pepin D, Bohatier J, Groliere CA (2004) Effect of chelators on the acute toxicity and bioavailability of aluminum to Tetrahymena pyriformis. Aquat Toxicol 47:259–275CrossRefGoogle Scholar
  39. Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content and differentiation in scot pine (Pinus sylvestris) roots. Plant Physiol 127:887–892CrossRefGoogle Scholar
  40. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038CrossRefGoogle Scholar
  41. Silva IR, Smyth TJ, Israel DW, Rufty TW (2001) Altered aluminum inhibition of soybean root elongation in the presence of magnesium. Plant Soil 230:223–230CrossRefGoogle Scholar
  42. Song H, Xu X, Wang H, Tao Y (2011) Protein carbonylation in barley seedling roots caused by aluminum and proton toxicity is suppressed by salicylic acid. Russ J Plant Physiol 58:653–659CrossRefGoogle Scholar
  43. Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  44. Takami C, Takenaka C, Tezuka T (2005) Mitigation of aluminum toxicity by calcium and magnesium in Japanese cedar (Cryptomeria japonica). J Forest Res 10:9–14CrossRefGoogle Scholar
  45. Talukdar D (2012) Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in Lens culinaris Medic. Seedlings through modulation of antioxidant enzyme activities. J Crop Sci Biotech 15:325–334CrossRefGoogle Scholar
  46. Taylor GJ (1988) The physiology of aluminum tolerance metals ions in biological systems. In: Sigel H (ed) Aluminum and its role in biology. Marcel-Dekker, New York, pp 165–198Google Scholar
  47. Thordal-Christensen H, Zhang Z, Wei YD, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  48. Valentine JS (2007) Dioxygen reactivity and toxicity. In: Bertini I, Gray HB, Stiefel EI, Valentine JS (eds) Biological inorganic chemistry: structure and reactivity. University Science Books, California, pp 31–41Google Scholar
  49. Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurement of water deficits in leaves. New Phytolo 49:81–87CrossRefGoogle Scholar
  50. Yang ZM, Wang J, Wang SH, Xu LL (2003) Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217:168–174Google Scholar
  51. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611CrossRefGoogle Scholar
  52. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Philippines, p 83Google Scholar
  53. Zhou ZS, Guo K, Elbaz AA, Yang ZM (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Poonam Pandey
    • 1
  • Rajneesh Kumar Srivastava
    • 1
  • R. S. Dubey
    • 1
    Email author
  1. 1.Department of Biochemistry, Faculty of ScienceBanaras Hindu UniversityVaranasiIndia

Personalised recommendations