Ameliorative role of β-estradiol against lead-induced oxidative stress and genotoxic damage in germinating wheat seedlings

Ameliorative role of β-estradiol against lead-induced oxidative stress and genotoxic damage in germinating wheat seedlings

In the present study, to determine the effects of β-estradiol on the ability of plants to tolerate lead toxicity, β-estradiol (10 µM) and lead (1.75 mM), singly or in combination, were exogenously applied to wheat seeds. Although lead resulted in a marked increase in the activities of antioxidant enzymes, including superoxide dismutase, guaiacol peroxidase, ascorbate peroxidase, and glutathione reductase (but not catalase), as well as an increase in the level of antioxidant compounds such as ascorbic acid and glutathione, this was insufficient to ameliorate the lead-induced oxidative injury or the superoxide anion, hydrogen peroxide, and malondialdehyde levels. However, β-estradiol was able to reduce the lead-induced oxidative damage and improved the antioxidant system. Similarly, β-estradiol reduced lead-induced α-amylase activity. The effects of lead toxicity on genetic material were also determined using the randomly amplified polymorphic DNA technique. While lead led to DNA damage in wheat seedlings, β-estradiol significantly mitigated this damage. Our element analysis results show that β-estradiol did not prevent lead uptake by roots, even it did stimulate the accumulation there. Taken together, our data demonstrate for the first time that β-estradiol-induced lead tolerance is associated with many biochemical and molecular mechanisms, including the antioxidant system, detoxification of reactive oxygen species, modulation of uptake and accumulation of lead, and protection of genetic material.

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  • Agarwal S, Pandey V (2004). Antioxidant enzyme responses to NaCl stress in Cassia angustifoli. Biol Plantarum 48: 555-560.
  • Agati G, Matteini P, Goti A, Tattini M (2007). Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol 174: 77- 89.
  • Ahmad MSA, Ashraf M, Tabassam Q, Hussain M, Firdous H (2011). Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages. Biol Trace Elem Res 144: 1229-1239.
  • Basharat A, Theodore MM, Rafaqat AG, Chong Y, Shafaqat A, Muhammad KD, Yueyan W, Weijun Z (2014). Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74: 261-273.
  • Biteur N, Aoues A, Kharoubi O, Slimani M (2011). Oxidative stress induction by lead in leaves of radish (Raphanus sativus) Seedlings. Not Sci Biol 3: 93-99.
  • Bowler C, Montagu MV, Inze D (1992). Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83-116.
  • Bozari S, Agar G, Aksakal O, Erturk FA, Yanmis D (2013). Determination of chemical composition and genotoxic effects of essential oil obtained from Nepeta nuda on Zea mays seedlings. Toxicol Ind Health 29: 339-348.   
  • Carvalho LC, Vidigal P, Amâncio S (2015). Oxidative stress homeostasis in grapevine (Vitis vinifera L.). Front Environ Sci 3: 1-15.
  • Chaoui A, El Ferjani EE (2013). β-estradiol protects embryo growth from heavy-metal toxicity in germinating lentil seeds. J Plant Growth Regul 32: 636-645.
  • Chaoui A, El Ferjani EE (2014). Heavy metal-induced oxidative damage is reduced by β-estradiol application in lentil seedlings. Plant Growth Regul 74: 1-9.
  • Choudhary SP, Oral HV, Bhardwaj R, Yu JQ, Tran LSP (2012). Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63: 5659-5675.
  • Chrispeels MJ, Varner JE (1967). Gibberellic acid enhanced synthesis and release of α-amylase and ribonuclease by isolated barley aleurone layers. Plant Physiol 42: 398-406.
  • Dogra R, Kaur A (1994). Effect of steroids on some growth and biochemical parameters of Triticum aestivum L. during germination. Crop Res 8: 611-620.
  • Dumlupinar R, Genisel M, Erdal S, Korkut T, Taspinar MS, Taskin M (2011). Effects of progesterone, β-estradiol, and androsterone on the changes of inorganic element content in barley leaves. Biol Trace Elem Res 143: 1740-1745.
  • Elstner E, Heupel A (1976). Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70: 616-620.
  • Erdal S (2012a). Exogenous mammalian sex hormones mitigate inhibition in growth by enhancing antioxidant activity and synthesis reactions in germinating maize seeds under salt stress. J Sci Food Agr 92: 839-843.
  • Erdal S (2012b). Alleviation of salt stress in wheat seedlings by mammalian sex hormones. J Sci Food Agric 92: 1411-1416.
  • Erdal S, Dumlupinar R (2010). Progesterone and β-estradiol stimulate the seed germination in chickpea by causing important changes in biochemical parameters. Z Naturforsch C 65: 239-244.
  • Erdal S, Dumlupinar R (2011). Mammalian sex hormones stimulate antioxidant system and enhance growth of chickpea plants. Acta Physiol Plant 33: 1011-1017.
  • Erdal S, Dumlupinar R, Cakmak T, Genisel M (2010). Mammalian sex hormones influence germination velocity and enzyme activities in germinating maize seeds. Fresen Environ Bull 19: 1458-1465.
  • Fahr M, Laplaze L, Bendaou N, Hocher V, Mzibri ME, Bogusz D, Smouni A (2013). Effect of lead on root growth. Front Plant Sci 4: 175.
  • Foyer CH, 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 (2013). Exogenous progesterone application protects chickpea seedlings against chillinginduced oxidative stress. Acta Physiol Plant 35: 241-251.
  • Havir EA, McHale NA (1987). Biochemical and development characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84: 450-455.
  • Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1996). Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Plant Physiol 98: 685-692.
  • Horwitz W, Latimer GW (2005). Official Methods of Analysis of AOAC International. Gaithersburg, MD, USA: AOAC.
  • Janeczko A, Oklestkova J, Novak O, Sniegowska-Swierk K, Snaczke Z, Pociecha E (2015). Disturbances in production of progesterone and their implications in plant studies. Steroids 96: 153-163.
  • Juliano BO, Varner JE (1969). Enzymatic degradation  of starch granules in the cotyledons of germinating peas. Plant Physiol 44: 886-892.
  • Karmous I, Jaouani K, Chaoui A, Ferjani EE (2012). Proteolytic activities in Phaseolus vulgaris cotyledons under copper stress. Physiol Mol Biol Plants 18: 337-343.
  • Krasensky J, Jonak C (2012). Drought, salt, and temperature stressinduced metabolic rearrangements and regulatory networks. J Exp Bot 3: 1593-1608.
  • Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2011). Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. C R Biol 334: 118-126.
  • Li G, Quiros CF (2001). Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor Appl Genet 103: 455-461.
  • Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880.
  • Nguyen LTH, Vandegehuchte MB, van der Geest HG, Janssen CR (2012). Evaluation of the mayfly Ephoron virgo for European sediment toxicity assessment. J Soils Sediments 12: 749-757.
  • Racchi ML (2013). Antioxidant defenses in plants with attention to Prunus and Citrus spp. Antioxidants 2: 340-369.
  • Shahid M, Dumat C, Pourrut B, Silvestre J, Laplanche C, Pinelli E (2013). Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J Soils Sediment 14: 835- 843.
  • Sheng J, Liu K, Fan B, Yuan Y, Shen L, Ru B (2007). Improving zinc content and antioxidant activity in transgenic tomato plants with expression of mouse metallothionein-I by mt-I gene. J Agr Food Chem 55: 9846-9849.
  • Smith P, Krohn R, Hermanson G, Mallia A, Gartner F, Provenzano M, Fujimoto E, Goeke N, Olson B, Klenk D (1985). Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
  • Su X, Wu S, Yang L, Xue R, Li H, Wang Y, Zhao H (2014). Exogenous progesterone alleviates heat and high light stress-induced inactivation of photosystem II in wheat by enhancing antioxidant defense and D1 protein stability. Plant Growth Regul 74: 311-318.
  • 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 RS (2003). Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164: 645-655.
  • Wang CQ, Song H (2009). Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28: 1341- 1349.
  • Wang P, Zhangn S, Wang C, Lu J (2012). Effects of Pb on the oxidative stress and antioxidant response in a Pb bio accumulator plant Vallisneria natans. Ecotox Environ Safe 78: 28-34.
  • Wu T, Hsu Y, Lee T (2009). Effects of cadmium on the regulation of antioxidant enzyme activity, gene expression, and antioxidant defenses in the marine macroalga Ulva fasciata. Bot Stud 50: 25-34.
  • Yang XH, Xu ZH, Xue HW (2005). Arabidopsis Membrane Steroid Binding Protein 1 is involved in inhibition of cell elongation. Plant Cell 17: 116-131.
  • Yang Y, Wei X, Lu J, You J, Wang W, Shi R (2010). Lead-induced phytotoxicity mechanism involved in seed germination and seedling growth of wheat (Triticum aestivum L.). Ecotox Environ Safe 73: 1982-1987.
  • Yang Y, Zhang Y, Wei X, You J, Wang W, Lu J, Shi R (2011). Comparative antioxidative responses and proline metabolism in two wheat cultivars under short term lead stress. Ecotox Environ Safe 74: 733-740.
  • Yee Y, Tam N, Wong Y, Lu C (2002). Growth and physiological responses of two mangrove species (Bruguira gymnorrhiza and Kandelia candel) to water logging. Environ Exp Bot 49: 209-221.
  • Yu C, Xie F, Ma L (2014). Effects of exogenous application of ascorbic acid on genotoxicity of Pb in Vicia faba roots. Int J Agric Biol 16: 831-835.
  • Zhou F, Wang J, Yang N (2014). Growth responses, antioxidant enzyme activities and lead accumulation of Sophora japonica and Platycladus orientalis seedlings under Pb and water stress. Plant Growth Regul 75: 383-389.
Turkish Journal of Botany-Cover
  • ISSN: 1300-008X
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
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