Abstract
Spinach extracts contain powerful natural antioxidants and have been used to improve the response of animal cells to various stress factors. The aim of the present study was to assess the effects of a methanolic extract of spinach (SE) used at two concentrations (21.7 and 217 ppm) on the growth, certain enzymes and antioxidant systems in wheat seedlings under lead stress. When wheat seedlings were grown for 7 days in a solution containing Pb(NO3)2 (3 mM), germination and growth were impaired, while signs of oxidative stress were observed. SE (217 ppm) pretreatment was able to protect seedlings from Pb toxicity by both reducing Pb uptake and Pb-induced oxidative stress. As a consequence, almost normal germination, elongation, biomass and α-amylase activity were restored by SE (217 ppm) pretreatment of wheat seedlings, in spite of the presence of Pb. Our results support the protective role and the antioxidant effect of SE against Pb. These results show an amazing similarity to the effects of SE in animals, which suggests that providing “nutraceuticals” to plants could improve their “health” status.
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Al-Dosari MS (2010) Antioxidant and protective effects of spinach (Spinacia oleracea L.) leaves against carbon tetrachloride-induced liver injury. Clin Exp Med J 4:129–140
Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khand NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396
Bajguz A, Godlewska-Zylkiewicz B (2004) Protective role of 20-hydroxyecdysone against lead stress in Chlorella vulgaris cultures. Phytochem 65:711–720
Bakrim A, Maria A, Sayah F, Lafont R, Takvorian N (2008) Ecdysteroids in spinach (Spinacia oleracea L.): biosynthesis, transport and regulation of levels. Plant Physiol Biochem 46:844–854
Bates DH, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Beer RFJ, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140
Ben Shaul V, Lomnitski L, Nyska A, Zurovsky Y, Bergman M, Grossman S (2001) The effects of natural antioxidants, NAO and apocynin, on oxidative stress in the rat heart following LPS challenge. Toxicol Lett 123:1–10
Bergman M, Varshavsky L, Gottlieb HE, Grossman S (2001) The antioxidant activity of aqueous spinach extract: chemical identification of active fractions. Phytochem 58:143–152
Bhatia AL, Jain M (2004) Spinacia oleracea L. protects against gamma radiations: a study on glutathione and lipid peroxidation in mouse liver. Phytomedicine 11:607–615
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
Cai YJ, Dai JQ, Fang JG, Ma LP, Hou LF, Yang L, Liu ZL (2002) Antioxidative and free radical scavenging effects of ecdysteroids from Serratula strangulata. Can J Physiol Pharmacol 80:1187–1194
Coleman J, Mechteld BK, Davies E (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci 4:144–151
Edenharder R, Keller G, Platt KL, Unger KK (2001) Isolation and characterization of structurally novel antimutagenic flavonoids from spinach (Spinacia oleracea). J Agric Food Chem 49:2767–2773
Eick MJ, Peak JD, Brady PV, Pesek JD (1999) Kinetics of lead adsorption/desorption on goethite: residence time effect. Soil Sci 164:28–39
Eskling M, Åkerlund HE (1998) Changes in the quantities of violaxanthin de-epoxidase, xanthophylls and ascorbate in spinach upon shift from low to high light. Photosynth Res 57:41–50
Gil MI, Ferreres F, Tomás–Barberán FA (1999) Effect of postharvest storage and processing on the antioxidant constituents (flavonoids and vitamin C) of fresh-cut spinach. J Agric Food Chem 47:2213–2217
Gomathi V, Kodai R, Jayakar B, Poola SB (2010) Phytochemical and pharmacological evaluation of leaves of Spinacia oleracea Linn. J Chem Pharmacol Res 2:266–283
Gorelick-Feldman J, MacLean D, Ilic N, Poulev A, Lila MA, Cheng D, Raskin I (2008) Phytoecdysteroids increase protein synthesis in skeletal muscle cells. J Agric Food Chem 56:3532–3537
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. J Biol Chem 249:7130–7139
Herrmann K (1995) Inhaltsstoffe des Spinats. Industrielle Obst - und Gemüseverwertung 80:424–430
Hong FS (2003) Study of the effect of Pb2+ on alpha-amylase activity by spectroscopy. Guang Pu Xue Yu Guang Pu Fen Xi 23:583–586
Hossain MA, Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295
Karoly DE, Rose LR, Thompson DM, Hodgson E, Rock GC, Roe MR (1996) Monooxygenase, esterase, and glutathione transferase activity associated with azinphosmethyl resistance in the tufted apple bud moth, Platynota idaeusalis. Pestic Biochem Physiol 55:109–121
Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915–920
Kumar A, Prasad MN, Mohan Murali Achary V, Panda BB (2012) Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environ Sci Pollut Res. doi:10.1007/s11356-012-1354-6
Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2010) A comparison of lead toxicity using physiological and enzymatic parameters on spinach (Spinacia oleracea) and wheat (Triticum aestivum) growth. Moroccan J Biol 6–7:64–73
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
Lamhamdi M, El Galiou O, Bakrim A, Nóvoa–Muñoz JC, Arias–Estévez M, Aarab A, Lafont R (2013) Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi J Biol Sci 20:29–36
Lomnitski L, Carbonatto M, Ben-Shaul V, Peano S, Conz A, Corradin L, Maronpot RR, Grossman S, Nyska A (2000) The prophylactic effects of natural water-soluble antioxidant from spinach and apocynin in a rabbit model of lipopolysaccharide-induced endotoxemia. Toxicol Pathol 28:588–600
Lomnitski L, Padilla-Banks E, Jefferson WN, Nyska A, Grossman S, Newbold RR (2003) A natural antioxidant mixture from spinach does not have estrogenic or antiestrogenic activity in immature CD-1 mice. J Nutr 3:3584–3587
Maeda N, Yoshida H, Mizushina Y (2010) Spinach and health: anticancer effect. In: Watson RR, Preedy VR (eds) Bioactive foods in promoting health: fruit and vegetables. Elsevier, Amsterdam, pp 393–405
Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223
Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Env Contam Toxicol 213:113–136
Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012
Sengar RS, Gautam M, Sengar RS, Garg SK, Sengar K, Chaudhary R (2008) Lead stress effects on physiobiochemical activities of higher plants. Rev Environ Contam Toxicol 196:73–93
Seregin IV, Kosevnikova AD (2008) Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russ J Plant Physiol 55:1–22
Shahida M, Pinelli E, Dumata C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J Hazard Mater 219–220:1–12
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Slooten L, Capiau K, Van Camp W, Van Montagu M, Sybesma C, Inze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in chloroplasts. Plant Physiol 107:737–750
Supalkova V, Petrek J, Baloun J, Adam V, Bartusek K, Trnkova L, Beklova M, Diopan V, Havel L, Kizek R (2007) Multi-instrumental investigation of affecting of early somatic embryos of spruce by cadmium(II) and lead(II) ions. Sensors 7:743––759
Umar BU (2007) Effect of hexane extract of spinach in the removal of arsenic from rat. Bangladesh J Pharmacol 2:27–34
Valencia A, Bustillo AE, Ossa GE, Chrispeels MJ (2000) Α-Amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Ins Biochem Mol Biol 30:207–213
Watanabe MA (1997) Phytoremediation on the brink of commercialization. Environ Sci Technol 31:182–186
Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124:1019–1026
Zhang J, Cui S, Li J, Kirkham MB (1995) Protoplasmic factors, antioxidant responses, and chilling resistance in maize. Plant Physiol Biochem 33:567–575
Zheng Y, Yang C, Pu W, Zhang J (2009) Determination of oxalic acid in spinach with carbon nanotubes-modified electrode. Food Chem 114:1523–1528
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The authors are grateful to Dr. Laurence Neil Dinan (University Paris 6, France) and Pr. Mohamed Benouham (University Mohamed 1st, Oujda) for critical reading of the manuscript and language improvement.
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Lamhamdi, M., Bakrim, A., Bouayad, N. et al. Protective role of a methanolic extract of spinach (Spinacia oleracea L.) against Pb toxicity in wheat (Triticum aestivum L.) seedlings: beneficial effects for a plant of a nutraceutical used with animals. Environ Sci Pollut Res 20, 7377–7385 (2013). https://doi.org/10.1007/s11356-013-1755-1
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DOI: https://doi.org/10.1007/s11356-013-1755-1