Abstract
This study was performed to determine the possible ameliorative effect of alpha-lipoic acid (LA) against oxidative stress evoked by lead (Pb) toxicity on 5-d wheat seedlings and elucidate how this ameliorative process was mediated. Pb toxicity caused a significant reduction in early seedling growth as evidenced by stunted root and coleoptile growth. To cope with the Pb toxicity, the activities of antioxidant enzymes were significantly stimulated compared to the control. However, in spite of high activities of these enzymes, contents of reactive oxygen species (ROS), superoxide anion and hydrogen peroxide and lipid peroxidation level were significantly high compared with the control. Similarly, Pb toxicity caused a marked decrease in the level of reduced forms of ascorbate and glutathione and thus it changed their reduced/oxidized ratio in favor of oxidized forms. On the other hand, LA supplementation further promoted uptake, accumulation, and transportation of Pb by stimulating tolerance mechanism involving ion uptake/accumulation at a high level. Moreover, ROS content and lipid peroxidation level were recorded as lower than that of the stressed-ones alone. In addition, while Pb toxicity markedly reduced amylase activity by decreasing Ca2+ content in endosperms, LA supplementation mitigated the reduction in amylase activity by increasing Ca2+ content. The changes in amylase activity were supported by isozymes patterns. Taken together, LA carried out its ameliorative effect against Pb toxicity via stimulation of tolerance mechanism, and this mechanism was linked to regeneration of the other main antioxidant compounds due to its own antioxidant property instead of activation of antioxidant enzymes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Agarwal, S., Pandey, V. 2004. Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biol. Plantarum. 48:555–560.
Bush, D.S., Sticher, L., van Huystee, R., Wagner, D., Jones, R.L. 1989. The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone alpha-amylase. J. Biol. Chem. 264:19392–19398.
Cakatay, U. 2006. Pro-oxidant actions of alpha-lipoic acid and dihydrolipoic acid. Med. Hypotheses. 66:110–117.
Chen, J., Zhu, C., Li, L.P., Sun, Z.Y., Pan, X.B. 2007. Effects of exogenous salicylic acid on growth and H2O2-metabolizing enzymes in rice seedlings under lead stress. J. Environ. Sci. 19:44–49.
Du, Z.Y., Bramlage, W.J. 1995. Peroxidative activity of apple peel in relation to development of poststorage disorders. Hortscience. 30:205–209.
Elstner, E.F., Heupel, A. 1976. Inhibition of nitrite formation from hydroxylammonium-chloride: a simple assay for superoxide dismutase. Anal. Biochem. 70:616–620.
Erdal, S. 2012. Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiol. Bioch. 57:1–7.
Foyer, C.H., Halliwell, B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta. 133:21–25.
Genisel, M., Turk, H., Erdal, S., Demir, Y., Genc, E., Terzi, I. 2015. Ameliorative role of beta-estradiol against lead-induced oxidative stress and genotoxic damage in germinating wheat seedlings. Turk. J. Bot. 39:1052–1060.
Gichner, T., Znidar, I., Szakova, J. 2008. Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat. Res-Gen. Tox. En. 652:186–190.
Gorcek, Z., Erdal, S. 2015. Lipoic acid mitigates oxidative stress and recovers metabolic distortions in salt-stressed wheat seedlings by modulating ion homeostasis, the osmo-regulator level and antioxidant system. J. Sci. Food. Agr. 95:2811–2817.
Hodges, D.M., Andrews, C.J., Johnson, D.A., Hamilton, R.I. 1996. Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Physiol. Plantarum. 98:685–692.
Israr, M., Sahi, S.V. 2008. Promising role of plant hormones in translocation of lead in Sesbania drummondii shoots. Environ. Pollut. 153:29–36.
Jiang, W.S., Liu, D.H. 2010. Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant. Biol. 10:40
Juliano, B.O., Varner, J.E. 1969. Enzymic degradiation of starch granules in the cotyledons of germinating peas. Plant Physiol. 44:886–892.
Koller, D., Hadas, A. 1982. Water relations in the germination of seeds, in: Lange, O.L., Nobel, P.S., Osmond, C.B., Zigler, H.E. (eds), In: Encyclopedia of Plant Physiol. Berlin, pp. 401–431.
Kumar, B., Smita, K., Cumbal Flores, L. 2013. Plant mediated detoxification of mercury and lead. Arab. J. Chem. 10:S2335–2342.
Lamhamdi, M., Bakrim, A., Aarab, A., Lafont, R., Sayah, F. 2011. Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. Cr. Biol. 334:118–126.
Mahmood, Q., Ahmad, R., Kwak, S.S., Rashid, A., Anjum, N.A. 2010. Ascorbate and glutathione: Protectors of plants in oxidative stress, in: Anjum, N.A., Umar, S., Chan, M.T. (eds), Ascorbate-Glutathione pathways and stress tolerance in plants. Springer, London.
Nakano, Y., Asada, K. 1981. Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 22:867–880.
Navari-Izzo, F., Quartacci, M.F., Sgherri, C. 2002. Lipoic acid: a unique antioxidant in the detoxification of activated oxygen species. Plant Physiol. Bioch. 40:463–470.
Ou, P., Tritschler, H.J., Wolff, S.P. 1995. Thioctic (lipoic) acid: a therapeutic metal-chelating antioxidant? Biochem. Pharmacol. 50:123–126.
Ovecka, M., Takac, T., 2014. Managing heavy metal toxicity stress in plants: Biological and biotechnological tools. Biotechnol. Adv. 32:73–86.
Patrick, L. 2002. Mercury toxicity and antioxidants: Part 1: role of glutathione and alpha-lipoic acid in the treatment of mercury toxicity. Altern. Med. Rev. 7:456–471.
Perez-Clemente, R.M., Vives, V., Zandalinas, S.I., Lopez-Climent, M.F., Munoz, V., Gomez-Cadenas, A. 2013. Biotechnological approaches to study plant responses to stress. Biomed. Res. Int. 654120
Pourrut, B., Shahid, M., Douay, F., Dumat, C., Pinelli, E. 2013. Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants, in: Gupta, D.K., Corpas, F.J., Palma, J.M. (eds), Heavy metal stress in plants. Springer-Verlag Berlin Heidelberg.
Ramegowda, V., Senthil-Kumar, M. 2015. The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176:47–54.
Samardakiewicz, S., Wozny, A. 2005. Cell division in Lemna minor roots treated with lead. Aquat. Bot. 83:289–295.
Sears, M.E. 2013. Chelation: harnessing and enhancing heavy metal detoxification – a review. Sci. World J. 219840.
Sengar, R.S., Gautam, M., Sengar, R.S., Garg, S.K., Sengar, K., Chaudhary, R. 2008. Lead stress effects on physiobiochemical activities of higher plants. Rev. Environ. Contam. T. 196:73–93.
Sgherri, C., Quartacci, M.F., Izzo, R., Navari-Izzo, F. 2002. Relation between lipoic acid and cell redox status in wheat grown in excess copper. Plant Physiol. Bioch. 40:591–597.
Sharma, P., Dubey, R.S. 2005. Lead toxicity in plants. Braz. J. Plant. Physiol. 17:35–52.
Sharma, S.S., Dietz, K.J. 2009. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14:43–50.
Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J., Klenk, D.C. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76–85.
Tarchoune, I., Sgherri, C., Baâtour, O., Izzo, R., Lachaâl, M., Navari-Izzo, F., Ouerghi, Z. 2013. Effects of oxidative stress caused by NaCl or Na2SO4 excess on lipoic acid and tocopherols in Genovese and Fine basil (Ocimum basilicum). Ann. Appl. Biol. 163:23–32.
Turk, H., Erdal, S. 2015. Melatonin alleviates cold-induced oxidative damage in maize seedlings by up-regulating mineral elements and enhancing antioxidant activity. J. Plant Nutr. Soil Sci. 178:433–439.
Turk, H., Erdal, S., Genisel, M., Atici, O., Demir, Y., Yanmis, D. 2014. The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul. 74:139–152.
Velikova, V., Yordanov, I., Edreva, A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants – Protective role of exogenous polyamines. Plant Sci. 151:59–66.
Verma, S., Dubey, R.S. 2003. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 164:645–655.
Wang, P.F., Zhang, S.H., Wang, C., Lu, J. 2012. Effects of Pb on the oxidative stress and antioxidant response in a Pb bioaccumulator plant Vallisneria natans. Ecotox. Environ. Safe. 78:28–34.
Yan, D.W., Duermeyer, L., Leoveanu, C., Nambara, E. 2014. The Functions of the Endosperm During Seed Germination. Plant Cell Physiol. 55:1521–1533.
Yasuno, R., Wada, H. 2002. The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. Febs Lett. 517:110–114.
Ye, S.C., Hu, L.Y., Hu, K.D., Li, Y.H., Yan, H., Zhang, X.Q., Zhang, H. 2015. Hydrogen sulfide stimulates wheat grain germination and counteracts the effect of oxidative damage caused by salinity stress. Cereal Res. Commun. 43:213–224.
Ye, Y., Tam, N.F.Y., Wong, Y.S., Lu, C.Y. 2003. Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environ. Exp. Bot. 49:209–221.
Yildiz, M., Akcali, N., Terzi, H. 2015. Proteomic and biochemical responses of canola (Brassica napus L.) exposed to salinity stress and exogenous lipoic acid. J. Plant Physiol. 179:90–99.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Aniol and I. Molnár
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Turk, H., Erdal, S., Karayel, U. et al. Attenuation of Lead Toxicity by Promotion of Tolerance Mechanism in Wheat Roots by Lipoic Acid. CEREAL RESEARCH COMMUNICATIONS 46, 424–435 (2018). https://doi.org/10.1556/0806.46.2018.020
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1556/0806.46.2018.020