Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii

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Abstract

Sesbania drummondii seedlings were grown in a medium to which lead (Pb), copper (Cu), nickel (Ni) and zinc (Zn) were added singly and in combinations in order to assess the effects of metal interactions on seedling growth, metal accumulation and anti-oxidative system. S. drummondii growth was significantly inhibited with metal treatments. S. drummondii accumulated substantially higher concentrations of metals in the roots than shoots. The uptake of metals followed the order Pb > Cu > Zn > Ni in roots and Pb > Zn > Cu > Ni in shoots. In addition, uptake of a single metal by S. drummondii was affected by the presence of a second metal, suggesting an antagonistic effect or competition between metals at the plant uptake site. A significant increase in both enzymatic [superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR)] and non-enzymatic (glutathione) antioxidant was observed in the S. drummondii seedlings exposed to different metal treatments. The enhancement in enzyme activities followed the order of Cu > Ni > Pb > Zn. However, compared to the effect of individual metal, metals in combination increased the enzyme activities to varying degrees.

Introduction

Compound pollution of trace elements is a common phenomenon in nature where additive, synergistic, and antagonistic effects can occur [1]. It occurs not only in mining and sewage irrigation areas, but also in suburban vegetable plots caused by atmospheric deposition or additives [2]. Heavy metals like copper (Cu), nickel (Ni) and zinc (Zn) are essential micronutrients for plants, but in excess all these metals are harmful to humans, animals and plants; as are the non essential metals Pb, Cd and Hg [3]. The primary sources of these metals are the burning of fossil fuels, the mining and smelting of metalliferous ores, municipal wastes, fertilizers, pesticides and sewage [4].

Heavy metals are known to induce oxidative stress by generating high concentrations of reactive oxygen species (ROS) such as superoxide radical (O2radical dot), singlet oxygen (1O2) and hydrogen peroxide (H2O2). These species react very rapidly with lipids, nucleic acids, pigments and proteins and cause lipid peroxidation, membrane damage and inactivation of enzymes, thus affecting cell viability [5]. Plants cope with oxidative stress by using antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), peroxidase (POX) and glutathione reductase (GR) and the low molecular weight antioxidants like cysteine, non-protein thiols, ascorbic acid and glutathione [6]. The enzyme SOD catalyzes the O2radical dot to H2O2 and oxygen. However, high concentration of H2O2 is also toxic to cells and has to be further detoxified by catalase and peroxidases to water and oxygen. Glutathione, cysteine and ascorbic acid can directly interact with and detoxify oxygen free radicals [7].

Several technologies are available to remediate soils that are contaminated by heavy metals. However, many of these technologies (for example, excavation of contaminated material and chemical/physical treatment) are extremely costly or do not achieve a long term solution [8], [9]. Phytoremediation is defined as the use of plants to remove or sequester hazardous contaminants from various media such as soil, water and air [10]. This technique has become a tangible alternative to traditional methodologies. More than four hundred metal hyperaccumulator plants are known, they can accumulate high concentrations of metals into their aboveground biomass [4]. Hyperaccumulators are defined as plants that can accumulate >1000 mg kg−1 of Cu, Co, Cr, Ni and Pb, and >10,000 mg kg−1 of Mn and Zn [11]. However, many of the hyperaccumulator plants are of small biomass and have a slow growth rate, thus limiting their usefulness for phytoextraction [12]. In addition, very few plants are known that can accumulate more than one metal. Therefore, researchers are searching new plant species that could potentially be used to remediate different metals from contaminated sites. Furthermore, compared to single metal studies, there have been relatively fewer reports on the interactive effects of heavy metals on plants [13], [14], [15], [16], [17]. Sesbania drummondii is a perennial shrub which is distributed in southern coastal areas of the United States. It has been studied extensively in relation to the accumulation of Pb, Hg and Cu [18], [19], [20], [21]. However, the effect of combinations of metals (Pb, Cu, Ni and Zn) on growth, metal accumulation and physiology of S. drummondii has not been studied yet. Therefore, the present study was undertaken to determine the Pb, Cu, Ni and Zn accumulation capability of S. drummondii and to examine the possible interactions between these metals at roots and shoots level. In addition, this study also reports the involvement of various antioxidants (enzymatic and non-enzymatic) in the tolerance against Pb, Cu, Ni and Zn induced stress, individually and in combinations. The results of this study should be helpful to determine the potential application of S. drummondii to remediate different metals from contaminated sites and to elucidate the biochemical detoxification mechanisms against Pb, Cu, Ni and Zn-induced stress.

Section snippets

Plant growth and metal treatment

The seeds of S. drummondii were scarified in 85% H2SO4 for 35 min, rinsed in running water for 1 h and then finally rinsed in deionized (DI) water for 5 min. Scarified seeds were germinated and grown in pro-mix (Premier Horticulture INC., Quakertown, PA, USA). Two-week-old seedlings were first acclimatized in Hoagland's solution (half strength) for 3 days, then seedlings were transferred in the medium containing the following treatments: (1) Pb, (2) Cu, (3) Ni, (4) Zn, (5) Pb + Cu, (6) Pb + Ni, (7) Pb +

Metal concentrations in plant tissues

The concentrations of metals (Pb, Cu, Ni and Zn) in the roots and shoots of S. drummondii seedlings grown at different treatments (Pb, Cu, Ni, Zn, Pb + Cu, Pb + Ni, Pb + Zn, Cu + Ni, Cu + Zn, Zn + Ni and Pb + Cu + Ni + Zn) are shown in Table 1. The results show that the metal contents in the plant tissues varied among metals in different combinations. Accumulation of all the metals was substantially higher in roots than in shoots. S. drummondii accumulated significantly (P < 0.05) higher Pb in its roots as well as

Discussion

There has been a continuing interest in searching for plants that are tolerant to heavy metals and accumulate high amounts of more than one metal. The present study shows that S. drummondii plant can accumulate higher concentrations of metals: Pb, Cu, Ni and Zn. Our results also suggest that the uptake of Pb, Cu, Ni and Zn by S. drummondii was affected not only by the elements in single applications, but also by the combinations of the elements. The accumulation of Pb was increased in roots as

Conclusion

This study was conducted to determine the interactive role of Pb, Cu, Ni and Zn on metal uptake, plant growth and anti-oxidative system of S. drummondii. Results suggest that the uptake of one metal was affected with the presence of other metals. S. drummondii accumulated Pb well above the threshold level for a Pb hyperaccumulator (>1000 mg kg−1), suggesting its usefulness in phytoextraction of Pb. The co-presence of metals resulted in a greater reduction in S. drummondii biomass than exposure to

Acknowledgements

This research was partially supported by the National Science Foundation-Research Experience for Undergraduates (NSF-REU) grant, Dean Ogden College of Science and Engineering and Applied Research and Technology Program, Western Kentucky University. Authors would also like to express sincere thanks to Ms. Jennifer Anderson for reviewing and editing the manuscript.

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