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The alleviating effects of salicylic acid application against aluminium toxicity in barley (Hordeum vulgare) roots

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Aluminium (Al) toxicity is one of the major growth limiting factors that affects large agricultural areas resulting in reduced crop production in acid soils. The present study aims to investigate alleviating effects of salicylic acid (SA) on Al toxicity in barley (Hordeum vulgare L.) roots. The roots were exposed to 20 μ.M AlCl3 with or without SA (5 and 10 μM) for 72 h. In an alternative group, roots were pre-treated with 5 μM and 10 μM SA for 24 h, and then they were exposed to 20 μM AlCl3. To evaluate the ameliorating effects of SA on Al toxicity some cellular stress responses were investigated including root elongation, Al uptake, loss of plasma membrane integrity, mitotic abnormalities, superoxide dismutase activity, peroxidase activity, total protein content and DNA fragmentation. The obtained results suggested that both pre-treatment and co-treatment of 10 μM SA could alleviate Al-induced toxicity in barley roots in relation to inhibition of Al uptake and activation of the antioxidant enzyme system.

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References

  • Aytürk Ö. & Vardar F. 2014. Aluminum-induced caspase-like activities in some Gramineae species. Adv. Food Sci. 37: 71–75

    Google Scholar 

  • Alvarez M.E. 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol. Biol. 44: 429–442.

    Article  CAS  PubMed  Google Scholar 

  • Ananieva E.A., Alexieva V.S. & Popova L.P. 2002. Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J. Plant Physiol. 159: 685–693.

    Article  CAS  Google Scholar 

  • Birecka H., Briber K.A. & Catalfamo J.L. 1973. Comparative studies on tobacco pit and sweet potato root isoperoxidases in relation to injury, indolacetic acid and ethylene effects. Plant Physiol. 52: 43–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borsani O., Valpuesta V. & Botella M.A. 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126: 1024–1030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the princi-pleof protein-dye binding. Anal. Biochem. 72: 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I. & Marschner H. 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismu-tase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 98: 1222–1227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos J.M.S. & Vicini L.F. 2003. Cytotoxicity of aluminum on meristematic cells of Zea mays and Allium cepa. Caryologia 56: 65–73.

    Article  Google Scholar 

  • Ciamporová M. 2002. Morphological and structural responses of plant roots to aluminum at organ, tissue and cellular levels. Biol. Plant. 45: 161–171.

    Article  Google Scholar 

  • Dat J.F., Lopez-Delgado H., Foyer C.H. & Scott I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116: 1351–1357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delhaize E.R.P. 2004. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. PNAS 101: 15249–15254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drazic G. & Mihailovic N. 2005. Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci. 168: 511–517.

    Article  CAS  Google Scholar 

  • Fiskesjö G. 1988. The Allium test as an alternative in environmental studies: The relative toxicity of metal ions. Mutat. Res. 197: 243–260.

    Article  PubMed  Google Scholar 

  • Foy C. 1992. Soil chemical factors limiting plant root growth. Adv. Soil Sci. 19: 97–149.

    Article  CAS  Google Scholar 

  • Guo B., Liang Y. & Zhu Y. 2009. Does salicyclic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J. Plant Physiol. 166: 20–31.

    Article  CAS  PubMed  Google Scholar 

  • Hameed A., Malik S.A., Iqbal N., Arshad R. & Farooq S. 2004. A rapid (100 min) method for isolating high yield and quality DNA from leaves, roots and coleoptile of wheat (Triticum aestivum L.) suitable for apoptotic and other molecular studies. Int. J. Agric. Biol. 2: 383–387.

    Google Scholar 

  • Huang W.J., Oo T.L., He H.Y., Wang A.Q., Zhan J., Li C.Z., Wei S.Q. & He L.F. 2014. Aluminum induced rapidly mitochondria dependent programmed cell death in Al sensitive peanut root tips. Bot. Stud. 55: 67–78.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hue N.V., Craddock G.R. & Adams F. 1986. Effect of organic acids on aluminum toxicity in subsoils. Soil Sci. Soc. Amer. J. 50: 28–34.

    Article  CAS  Google Scholar 

  • Janda T., Szalai G., Tari I. & Páldi E. 1999. Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208: 175–180.

    Article  CAS  Google Scholar 

  • Jones D.L. & Kochian L.V. 1995. Aluminum inhibition of the inositol 1-4-5-trisphosphate signal transduction pathway in wheat roots: A role in aluminum toxicity? Plant Cell 7: 1913–1922.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale J. & Knight M.R. 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128: 682–695.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z. & Xing D. 2010. Mitochondrial pathway leading to programmed cell death induced by aluminum phytotoxicity in Arabidopsis. Plant Signal. Behav. 5: 1660–1662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loake G. & Grant M. 2007. Salicylic acid in plant defence - the players and protagonists. Curr. Opin. Plant Biol. 10: 466–472.

    Article  CAS  Google Scholar 

  • Ma J.F., Chen Z.C. & Shen R.F. 2014. Molecular mechanism of Al tolerance in gramineous plants. Plant Soil. 381: 1–12.

    Article  CAS  Google Scholar 

  • Mahendranath M., Santosh C., Mohan M., Ramesh L. & Radhaiah A. 2012. Protective effect of salicylic acid on aluminium induced stress in Sorghum bicolor varieties. Ind. J. Plant Sci. 2: 99–104.

    Google Scholar 

  • Matsumoto H. 2000. Cell biology of aluminum toxicity and tolerance in higher plants. Int. Rev. Cytol. 200: 1–46.

    Article  CAS  PubMed  Google Scholar 

  • Metwally A., Finkemeier I., Georgi M. & Dietz K.J. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol. 132: 272–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra A. & Choudhuri M.A. 1999. Monitoring of phytotoxicity of lead and mercury from germination and early seedling growth indices in two rice cultivars water, air, and soil pollution. 114: 339–346.

    CAS  Google Scholar 

  • Munoz-Sánchez A., Altúzar-Molina A.R. & Hernández-Soto-mayor S.M.T. 2013. Phospholipase signaling is modified differentially by phytoregulators in Capsicum, chinense cells. Plant Signal. Behav. 79: 1103–1105

    Google Scholar 

  • Ownby J.D. 1993. Mechanism of reaction of hematoxylin with aluminium treated wheat roots. Physiol. Plant 87: 371–381.

    Article  CAS  Google Scholar 

  • Pal M., Szalai G., Horvath E., Janda T. & Paldi E. 2002. Effect of salicylic acid during heavy metal stres. Proc. 7th Hungarian Congress on Plant Physiology. Acta Biolog. Szeged. 46: 119–120.

    Google Scholar 

  • Pandey P., Srivastava R.K. & Dubey R.S. 2013. Salycilic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology 22: 656–670.

    Article  CAS  PubMed  Google Scholar 

  • Petrov V., Hille J., Mueller-Roeber B. & Gechev T.S. 2015. ROS mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6: 69.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy A.K., Sharma A. & Talukder G. 1989. A time course study on effects of aluminium on mitotic cell division in Allium, sativum. Mutat. Res. 227: 221–226.

    Article  CAS  PubMed  Google Scholar 

  • Schildknecht P.H.P.A. & De Campos Vidal B. 2002. A role for the cell wall in Al+3 resistance and toxicity: Crystallinity and availability of negative charges. Int. Arch. Biosci. 2000: 1087–1095.

    Google Scholar 

  • Senaratna T., Touchell D., Bunn E. & Dixon K. 2000. Acetyl salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul. 30: 157–161.

    Article  CAS  Google Scholar 

  • Shakirova F., & Bezrukova M. 1997. Induction of wheat resistance against environmental salinization by salicylic acid. Biol. Bull. 24: 109–112.

    Google Scholar 

  • Sharma Y.K., Leon J., Raskin I. & Davis K.R. 1996. Ozone-induced responses in Arabidopsis thaliana: The role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc. Natl. Acad. Sci. USA. 93: 5099–5104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song H., Xu X., Wang H. & Tao Y. 2011. Protein carbonylation in barley seedling roots caused by aluminum and proton toxicity is suppressed. Russ. J. Plant Physiol. 58: 653–659.

    Article  CAS  Google Scholar 

  • Srivastava S. & Dubey R.S. 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: 1–16.

    Article  CAS  Google Scholar 

  • Srivastava M.K. & Dwivedi U.N. 1998. Salicylic acid modulates glutathione metabolism in pea seedlings. J. Plant Physiol. 153: 409–414.

    Article  CAS  Google Scholar 

  • Strobel N.E. & Kuc J.A. 1995. Chemical and biological inducers of systemic resistance to pathogens protect cucumber and tobacco plants from damage caused by paraquat and cupric chloride. Phytopathology 85: 1306–1310.

    Article  CAS  Google Scholar 

  • Surapu V., Ediga A. & Meriga B. 2014. Salicylic acid alleviates aluminum toxicity in tomato seedlings (Lycopersicum, esculentum Mill.) through activation of antioxidant defense system and proline biosynthesis. Adv. Biosci. Biotechnol. 5: 777–789.

    Article  CAS  Google Scholar 

  • Uysal D., Ozdener Y., Aydin B. & Demir E. 2009. Determination of ameliorating effect of salicylic acid on toxicity of aluminum in wheat roots. Fresen. Environ. Bull. 18: 32–39.

    CAS  Google Scholar 

  • Vardar F., Arican E. & Gözükirmizi N. 2006. Effects of aluminum on in vitro root growth and seed germination of tobacco (Nicotiana tabacum L.). Adv. Food Sci. 28: 85–88.

    CAS  Google Scholar 

  • Vardar F., Akgül N., Aytürk Ö. & Aydin Y. 2015. Assessment of aluminum induced genotoxicity with comet assay in wheat, rye and triticale roots. Fresen. Environ. Bull. 37: 3352–3358.

    Google Scholar 

  • Vardar F., Çabuk E., Aytürk Ö. & Aydin Y. 2016. Determination of aluminum induced programmed cell death characterized by DNA fragmentation in Gramineae species. Caryologia 69: 111–115.

    Article  Google Scholar 

  • Vardar F., Ismailoĝlu I., Inan D. & Ünal M. 2011. Determination of stress responses induced by aluminum in maize (Zea mays). Acta Biol. Hung. 62: 156–170.

    Article  CAS  PubMed  Google Scholar 

  • Vardar F. & Unal M. 2007. Aluminum toxicity and resistance in higher plants. Adv. Mol. Biol. 1: 1–12.

    Google Scholar 

  • Wang Y.S., Wang J., Yang Z.M., Wang Q.Y., Lü B., Li S.Q., Lu Y.P., Wang S.H. & Sun X. 2004. Salicylic acid modulates aluminum-induced oxidative stress in roots of Cassia tora. Acta Bot. Sin. 46: 819–828.

    CAS  Google Scholar 

  • Wang L.J. & Li S.H. 2006. Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci. 170: 685–694.

    Article  CAS  Google Scholar 

  • War A.R., Paulraj G., War M.Y. & Ignacimuthu S. 2011. Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal. Behavior. 6: 1787–1792.

    Article  CAS  Google Scholar 

  • Yamamato Y., Kobayashi Y. & Matsumoto H. 2001. Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea root. Plant Physiol. 125: 199–208.

    Article  Google Scholar 

  • Yang Z.M., Wang J. & Wang S.H. 2003. Salicylic acid-induced aluminium tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217: 74.

    Google Scholar 

  • Zhang L., Xu Q., Xing D., Gao C. & Xiong H. 2009. Real time detection of caspase-3 like protease activation in vivo using fluorescence resonance energy transfer during plant programmed cell death induced by ultraviolet C overexposure. Plant Physiol. 150: 1773–1783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Z.S., Guo K., Elbaz A.A. & Yang Z.M. 2009. Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ. Exp. Bot. 65: 27–34.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Research Foundation of Marmara University (BAPKO) under Grant (no. FEN-CYLP-141014-0349).

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Correspondence to Filiz Vardar.

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Yalcin, G., Vardar, F. The alleviating effects of salicylic acid application against aluminium toxicity in barley (Hordeum vulgare) roots. Biologia 71, 1338–1344 (2016). https://doi.org/10.1515/biolog-2016-0166

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