ABB  Vol.5 No.9 , August 2014
Salicylic Acid Alleviates Aluminum Toxicity in Tomato Seedlings (Lycopersicum esculentum Mill.) through Activation of Antioxidant Defense System and Proline Biosynthesis
ABSTRACT

The aim of this work was to evaluate the alleviating efficacy of salicylic acid (100, 250 and 500 μM) against the toxic effects of aluminum (Al) on two tomato cultivars (GOWRI and SIRI) differing in their sensitivity to Al stress. Al treatment (500 μM) caused 40% - 80% drop in plant growth, relative water content (RWC) and cell viability and a reduction of 1 - 2.5 fold and 0.5 - 2 fold in glutathione and proline content respectively, when compared to their control plants grown in Al free medium. Al treatment also resulted in 2 - 5 fold raise in malondialdehyde (MDA) levels, 2 - 3 fold higher Al uptake and 55% - 80% more electrolyte leakage and caused severe DNA damage. Al stress enhanced (1 - 2 fold) the activities of superoxide dismutase (SOD) and peroxidase (POD), but decreased catalase (CAT) activity over their respective controls. Exogenously-applied Salicylic acid (SA) significantly (p < 0.05) and dose-dependently alleviated Al-induced toxicity in tomato seedlings as marked by much improved plant growth, retention of higher RWC, cell viability, glutathione and proline content. SA also caused 0.6 - 1.5 fold reduction in Al uptake, 50% - 80% less electrolyte leakage, 40% - 80% drop in lipid peroxidation and considerable protection against DNA damage. Also, supplementation of SA could considerably reverse the Al-induced changes in the activities of SOD, POD and CAT. Together, our findings demonstrate that, SA is an efficient growth regulator with diversified roles that contribute to its potential alleviating effect against Al induced toxicity and SIRI is a relatively Al-resistant cultivar compared to GOWRI.


Cite this paper
Surapu, V. , Ediga, A. and Meriga, B. (2014) Salicylic Acid Alleviates Aluminum Toxicity in Tomato Seedlings (Lycopersicum esculentum Mill.) through Activation of Antioxidant Defense System and Proline Biosynthesis. Advances in Bioscience and Biotechnology, 5, 777-789. doi: 10.4236/abb.2014.59091.
References
[1]   Kochian, L.V., Pineros, M.S. and Hoekenga, O.A. (2005) The Physiology, Genetics and Molecular Biology of Plant Aluminum Resistance and Toxicity. Plant and Soil, 274, 175-195.
http://dx.doi.org/10.1007/s11104-004-1158-7

[2]   Barcelo, J. and Poschenrieder, C. (2002) Fast Root Growth Responses, Root Exudates and Internal Detoxification as Clues to the Mechanisms of Aluminum Toxicity and Resistance. Environmental and Experimental Botany, 48, 75-92.
http://dx.doi.org/10.1016/S0098-8472(02)00013-8

[3]   Ma, J.F. (2007) Syndrome of Aluminum Toxicity and Diversity of Aluminum Resistance in Higher Plants. International Review of Cytology, 264, 225-252.
http://dx.doi.org/10.1016/S0074-7696(07)64005-4

[4]   Jain, L.Y., Ya, Y.L., Yue, J.Z., Shan, Z., Yun, R.W., Ping, W. and Shao, J.Z. (2008) Cell Wall Polysaccharides Are Specifically Involved in the Exclusion of Aluminum Form the Rice Root Apex. Plant Physiology, 146, 602-611.

[5]   Ribeiro, C., Cambraia, J., Peixoto, P.H.P. and Junior, E.M.F. (2012) Antioxidant System Response Induced by Aluminum in Two Rice Cultivars. Brazilian Journal of Plant Physiology, 24, 2.
http://dx.doi.org/10.1590/S1677-04202012000200004

[6]   Sharma, P., Bhushanm, A., Dubey, R.S. and Pessarakli, M. (2012) Reactive Oxygen Species, Oxidative Damage and Antioxidant Defense Mechanism in Plants under Stressful Conditions. Journal of Botany, 26, Article ID: 217037.
http://dx.doi.org/10.1155/2012/217037

[7]   Zhu, X.F., Lei, G., Wang, Z.W., Shi, Y.Z., Braam, J., Li, G.X. and Zheng, S.J. (2013) Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance. Plant Physiology, 162, 1947-1955.
http://dx.doi.org/10.1104/pp.113.219147

[8]   Pandey. P., Srivastava, R.K. and Dubey, R.S. (2013) Salicylic 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.
http://dx.doi.org/10.1007/s10646-013-1058-9

[9]   Hoagland, D.R. and Arnon, D.I. (1950) The Water Culture Method for Growing Plants Without Soil. California Agriculture Experimental Station, 347.

[10]   Ownby, J.D. (1993) Mechanism of Reaction of Hematoxylin with Aluminum-Treated Wheat Roots. Physiologia Plantarum, 87, 371-380.
http://dx.doi.org/10.1111/j.1399-3054.1993.tb01744.x

[11]   Lin, C.Y., Chen, Y.M. and Key, J.L. (1985) Solute Leakage in Soybean Seedlings under Various Heat Shock Regimes. Plant and Cell Physiology, 26, 1493-1498.

[12]   Heath, R.L. and Packer, L. (1986) Photoperoxidation in Isolated Chloroplasts. I. Kinetics and Stoichiometry of Fatty Acid Peroxidation. Archives of Biochemistry and Biophysics, 125, 189-198.
http://dx.doi.org/10.1016/0003-9861(68)90654-1

[13]   Baker, C.J. and Mock, N.M. (1994) An Improved Method for Monitoring Cell Death in Cell Suspension and Leaf Disc Assays Using Evans Blue. Plant Cell, Tissue and Organ Culture, 39, 7-12.
http://dx.doi.org/10.1007/BF00037585

[14]   Anderson, M.E. (1985) Determination of Glutathione and Glutathione Disulfide in Biological Samples. Methods in Enzymology, 113, 548-555.
http://dx.doi.org/10.1016/S0076-6879(85)13073-9

[15]   Bates, L.S., Waldren, R.P. and Teari, I.D. (1973) Rapid Determination of Free Proline for Water Stress Studies. Plant and Soil, 39, 205-207.
http://dx.doi.org/10.1007/BF00018060

[16]   Bayer, C. and Fridovich, I. (1987) Superoxide Dismutase: Improved Assays and Applicable to Acrylamide Gels. Analytical Biochemistry, 44, 276-287.

[17]   Nakano, Y. and Asada, K. (1981) Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology, 22, 867-880.

[18]   Aebi, H. (1984) Catalase in Vitro. Methods in Enzymology, 105, 121-126.
http://dx.doi.org/10.1016/S0076-6879(84)05016-3

[19]   Jena, K.K. and Kochert, G. (1991) Restriction Fragment Length Polymorphism Analysis of CCDD Genome Species of the Genus Oryza sativa L. Plant Molecular Biology, 16, 831-839.
http://dx.doi.org/10.1007/BF00015075

[20]   Riberio, M.A.Q., Almeda, A.A.F., Mielke, M.S., Gomes, F.P., Pires, M.V. and Baligar, V.C. (2013) Aluminum Effects on Growth, Photosynthesis, and Mineral Nutrition of CACAO Genotypes. Journal of Plant Nutrition, 36, 1161-1179.
http://dx.doi.org/10.1080/01904167.2013.766889

[21]   Panda, S.K., Baluska, F. and Matsumoto, H. (2009) Aluminum Signaling in Plants. Plant Signaling and Behavior, 4, 529-597.
http://dx.doi.org/10.4161/psb.4.7.8903

[22]   Alvim, M.N., Ramos, F.T., Olivera, D., Isaias, R.M.S. and Franca, M.G.C. (2012) Aluminum Localization and Toxicity Symptoms Related to Root Growth Inhibition in Rice (Oryza sativa L.) Seedlings. Journal of Biosciences, 37, 1079-1088.
http://dx.doi.org/10.1007/s12038-012-9275-6

[23]   Panda, S.K. and Patra, H.K. (2007) Effect of Salicylic Acid Potentiates Cadmium-Induced Oxidative Damage in Oryza sativa L. Leaves. Acta Physiologiae Plantarum, 29, 567-575.
http://dx.doi.org/10.1007/s11738-007-0069-7

[24]   Krantev, A., Yordanova, R., Janda, T., Szalai, G. and Popova, L. (2008) Treatment with Salicylic Acid Decreases the Effect of Cadmium on Photosynthesis in Maize Plants. Journal of Plant Physiology, 165, 920-931.
http://dx.doi.org/10.1016/j.jplph.2006.11.014

[25]   Nagasubramaniam, A., Pathmanabhan, G. and Mallika, V. (2007) Studies on Improving Production Potential of Baby corn with Foliar Spray of Plant Growth Regulators. Annual Review of Plant Physiology and Plant Molecular Biology, 21, 154-157.

[26]   Farooq, M., Aziz, T., Wahid, A., Lee, D.J. and Siddique, K.H.M. (2009) Chilling Tolerance in Maize: Agronomic and Physiological Approaches. Crop & Pasture Science, 60, 501-516.
http://dx.doi.org/10.1071/CP08427

[27]   Kovacik, J., Klejdus, B., Hedbavny, J. and Backor, M. (2009) Salicylic Acid Alleviates NaCl-Induced Changes in the Metabolism of Matricaria chamomilla Plants. Ecotoxicology, 18, 544-554.
http://dx.doi.org/10.1007/s10646-009-0312-7

[28]   Jayakannan, M., Bose, J., Babourina, O., Rengel, Z. and Shabala, S. (2013) Salicylic Acid Improves Salinity Tolerance in Arabidopsis by Restoring Membrane Potential and Preventing Salt-Induced K+ Loss via a GORK Channel. Journal of Experimental Botany, 64, 2255-2268.
http://dx.doi.org/10.1093/jxb/ert085

[29]   Tamas, L., Budikova, S., Simonovicova, M., Huttova, J., Siroka, B. and Mistrick, I. (2006) Rapid and Simple Method for Al-Toxicity Analysis in Emerging Barley Roots during Germination. Biologia Plantarum, 50, 87-93.
http://dx.doi.org/10.1007/s10535-005-0079-5

[30]   Yamamoto, Y., Kobayashi, Y. and Matsumoto, H. (2001) Lipid Peroxidation Is an Early Symptom Triggered by Aluminum but Not the Primary Cause of Elongation Inhibition in Pea Roots. Plant Physiology, 125, 199-208.
http://dx.doi.org/10.1104/pp.125.1.199

[31]   Xiong, Z.T. and Wang, H. (2005) Copper Toxicity and Bioaccumulation in Chinese Cabbage (Brassica pekinensis Rupr.). Environmental Toxicology, 20, 188-194.
http://dx.doi.org/10.1002/tox.20094

[32]   Shen, R., Ma, J., Kyo, M. and Iwashita, T. (2002) Compartmentalization of Aluminum in Leaves of an Al Accumulator, Fagopyrum esulentum Moench. Planta, 215, 394-398.
http://dx.doi.org/10.1007/s00425-002-0763-z

[33]   Shao, H.B. and Chu, L.Y. (2005) Plant Molecular Biology in China: Opportunities and Challenges. Plant Molecular Biology Reporter, 23, 345-358.

[34]   Liu, J.P., Piñeros, M.A. and Kochian, L.V. (2014) The Role of Aluminum Sensing and Signaling in Plant Aluminum Resistance. Journal of Integrative Plant Biology, 56, 221-230.
http://dx.doi.org/10.1111/jipb.12162

[35]   Noctor, G., Veljovic-Jovanovic, S., Driscoll, S., Novitskaya, L. and Foyer, C.H. (2002) Drought and Oxidative Load in the Leaves of C3 Plants: A Predominant Role for Photorespiration. Annals of Botany, 89, 841-850.
http://dx.doi.org/10.1093/aob/mcf096

[36]   Hayat, S., Hasan, S.A., Fariduddin, Q. and Ahmad, A. (2008) Growth of Tomato (Lycopersicon esculentum) in Response to Salicylic Acid under Water Stress. Journal of Plant Science, 3, 297-304.

[37]   Kavi Kishor, P.B., Sangam, S., Amrutha, R.N., Sri Laxmi, P., Naidu, K.R., Rao, K.R.S.S., Rao, S., Reddy, K.J., Theriappan, P. and Sreenivasulu, N. (2005) Regulation of Proline Biosynthesis, Degradation, Uptake and Transport in Higher Plants: Its Implications in Plant Growth and Abiotic Stress Tolerance. Current Science, 88, 424-438.

[38]   Demiral, T. and Türkan, I. (2005) Comparative Lipid Peroxidation, Antioxidant Defense Systems and Proline Content in Roots of Two Rice Cultivars Differing in Salt Tolerance. Environmental and Experimental Botany, 53, 247-257. http://dx.doi.org/10.1016/j.envexpbot.2004.03.017

[39]   Boscolo, P.R.S., Menossi, M. and Jorge, R.A. (2003) Aluminum Induced Oxidative Stress in Maize. Phytochemistry, 62, 181-189.
http://dx.doi.org/10.1016/S0031-9422(02)00491-0

[40]   Liu, D.H., Zou, J., Meng, Q.M., Zou, J.H. and Jiang, W.S. (2009) Uptake and Accumulation and Oxidative Stress in Garlic (Allium sativam L.) under Lead Phytotoxicity. Ecotoxicology, 18, 134-143.
http://dx.doi.org/10.1007/s10646-008-0266-1

[41]   Breusegem, F.V., Vranova, E., Dat, J.F. and Inze, D. (2001) The Role of Active Oxygen Species in Plant Signal Transduction. Plant Science, 161, 405-414.
http://dx.doi.org/10.1016/S0168-9452(01)00452-6

[42]   Sharma, P. and Dubey, R.S. (2007) Involvement of Oxidative Stress and Role of Antioxidative Defense System in Growing Rice Seedlings Exposed to Toxic Concentrations of Aluminum. Plant Cell Reports, 26, 2027-2038.
http://dx.doi.org/10.1007/s00299-007-0416-6

[43]   Zhou, Z.S., Guo, K., Elbaz, A.A. and Yang, Z.M. (2009) Salicylic Acid Alleviates Mercury Toxicity by Preventing Oxidative Stress in Roots of Medicago sativa. Environmental and Experimental Botany, 65, 27-34.
http://dx.doi.org/10.1016/j.envexpbot.2008.06.001

[44]   Foy, C.D., Chaney, R.L. and White, M.C. (1978) The Physiology of Metal Toxicity in Plants. Annual Review of Plant Physiology, 29, 511-566.
http://dx.doi.org/10.1146/annurev.pp.29.060178.002455

[45]   Wallace, S.U. and Anderson, I.C. (1984) Aluminum Toxicity and DNA Synthesis in Wheat Roots. Agronomy Journal, 76, 5-8.
http://dx.doi.org/10.2134/agronj1984.00021962007600010002x

[46]   Ezaki, B., Gadner, R.C., Ezaki, Y. and Matsumoto, H. (2000) Expression of Aluminum-Induced Genes in Transgenic Arabidopsis Plants Can Ameliorate Al Stress and/or Oxidative Stress. Plant Physiology, 122, 657-666.
http://dx.doi.org/10.1104/pp.122.3.657

[47]   Katsuhara, M. and Kawasaki, T. (1996) Salt Stress Induced Nuclear and DNA Degradation in Meristematic Cells of Barley Roots. Plant and Cell Physiology, 79, 283-288.

[48]   Peitsch, M.C., Muller, C. and Tschopp, J. (1993) DNA Fragmentation during Apoptosis Is Caused by Frequent Single-Strand Cuts. Nucleic Acids Research, 21, 4206-4209.
http://dx.doi.org/10.1093/nar/21.18.4206

 
 
Top