Suitability of aromatic plants for phytoremediation of heavy metal contaminated areas: a review

Abstract

This review briefly elucidates the research undertaken and benefits of using aromatic plants for remediation of heavy metal polluted sites. A sustainable approach to mitigate heavy metal contamination of environment is need of the hour. Phytoremediation has emerged to be one of the most preferable choices for combating the metal pollution problem. Aromatic plants can be used for remediation of contaminated sites as they are non-food crops thus minimizing the risk of food chain contamination. Most promising aromatic plants for phytoremediation of heavy metal contaminated sites have been identified from families – Poaceae, Lamiaceae, Asteraceae, and Geraniaceae. They act as potential phytostabilisers, hyper accumulators, bio-monitors, and facultative metallophytes. Being high value economic crops, monetary benefits can be obtained by growing them in tainted areas instead of food crops. It has been observed that heavy metal stress enhances the essential oil percentage of certain aromatic crops. Research conducted on some major aromatic plants in this context has been highlighted in the present review which suggests that aromatic plants hold a great potential for phytoremediation. It has been reported that essential oil from aromatic crops is not contaminated by heavy metals significantly. Thus, aromatic plants are emerging as an ideal candidate for phytoremediation.

Highlights

? Aromatic plants hold a great potential for phytoremediation of heavy metal contaminated sites.

? Being high value economic crops, monetary benefits can be obtained by growing them in contaminated areas instead of food crops.

? Research done on some major aromatic plants in this context has been highlighted in the present review.     

Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution

Phytoremediation to clean up metal- and metalloid-contaminated soil or sediments has gained increasing attention as environmental friendly and cost effective. Achievements of the last decade suggest that genetic engineering of plants can be instrumental in improving phytoremediation. Transgenic approaches successfully employed to promote phytoextraction of metals (mainly Cd, Pb, Cu) and metalloids (As, Se) from soil by their accumulation in the aboveground biomass involved mainly implementation of metal transporters, improved production of enzymes of sulphur metabolism and production of metal-detoxifying chelators — metallothioneins and phytochelatins. Plants producing bacterial mercuric reductase and organomercurial lyase can covert the toxic ion or organomercury to metallic Hg volatized from the leaf surface. Phytovolatization of selenium compounds was promoted in plants overexpressing genes encoding enzymes involved in production of gas methylselenide species. This paper provides a broad overview of the evidence supporting suitability and prospects of transgenic research in phytoremediation of heavy metals and metalloids.     

Perspectives of plant-associated microbes in heavy metal phytoremediation

"Phytoremediation" know-how to do-how is rapidly expanding and is being commercialized by harnessing the phyto-microbial diversity. This technology employs biodiversity to remove/contain pollutants from the air, soil and water. In recent years, there has been a considerable knowledge explosion in understanding plant-microbes-heavy metals interactions. Novel applications of plant-associated microbes have opened up promising areas of research in the field of phytoremediation technology. Various metabolites (e.g., 1-aminocyclopropane-1-carboxylic acid deaminase, indole-3-acetic acid, siderophores, organic acids, etc.) produced by plant-associated microbes (e.g., plant growth promoting bacteria, mycorrhizae) have been proposed to be involved in many biogeochemical processes operating in the rhizosphere. The salient functions include nutrient acquisition, cell elongation, metal detoxification and alleviation of biotic/abiotic stress in plants. Rhizosphere microbes accelerate metal mobility, or immobilization. Plants and associated microbes release inorganic and organic compounds possessing acidifying, chelating and/or reductive power. These functions are implicated to play an essential role in plant metal uptake. Overall the plant-associated beneficial microbes enhance the efficiency of phytoremediation process directly by altering the metal accumulation in plant tissues and indirectly by promoting the shoot and root biomass production. The present work aims to provide a comprehensive review of some of the promising processes mediated by plant-associated microbes and to illustrate how such processes influence heavy metal uptake through various biogeochemical processes including translocation, transformation, chelation, immobilization, solubilization, precipitation, volatilization and complexation of heavy metals ultimately facilitating phytoremediation.     

Factors affecting heavy metal uptake in plant selection for phytoremediation

The heavy metal uptake of ten plant species was studied under different soil and climatic conditions. Effects of soil pH, temperature, plant species and phenophase on the heavy metal content of stems and leaves were determined in pot experiments. Plants and soil samples were collected from a lead/zinc mine ore (Gy?ngy?soroszi, Hungary) and characterised by high contents of Pb, Zn, As, Cd, Cu. The possibility of an adapted phytoremediation technology was indicated by different bioconcentration factors (BCF). The BCF depended markedly (10- to 100-fold) on plant species and environmental conditions. Based on our results a "season-adapted" phytoextraction technology with different plant species (utilising their different temperature requirements and/or harvest time) is suggested.     

Heavy metal pollution in aquatic ecosystems and its phytoremediation using wetland plants: an ecosustainable approach

This review addresses the global problem of heavymetal pollution originating from increased industrialization and urbanization and its amelioration by using wetland plants both in a microcosm as well as natural/field condition. Heavymetal contamination in aquatic ecosystems due to discharge of industrial effluents may pose a serious threat to human health. Alkaline precipitation, ion exchange columns, electrochemical removal, filtration, and membrane technologies are the currently available technologies for heavy metal removal. These conventional technologies are not economical and may produce adverse impacts on aquatic ecosystems. Phytoremediation of metals is a cost-effective "green" technology based on the use of specially selected metal-accumulating plants to remove toxic metals from soils and water. Wetland plants are important tools for heavy metal removal. The Ramsar convention, one of the earlier modern global conservation treaties, was adopted at Ramsar, Iran, in 1971 and became effective in 1975. This convention emphasized the wise use of wetlands and their resources. This review mentions salient features of wetland ecosystems, their vegetation component, and the pros and cons involved in heavy metal removal. Wetland plants are preferred over other bio-agents due to their low cost, frequent abundance in aquatic ecosystems, and easy handling. The extensive rhizosphere of wetland plants provides an enriched culture zone for the microbes involved in degradation. The wetland sediment zone provides reducing conditions that are conducive to the metal removal pathway. Constructed wetlands proved to be effective for the abatement of heavymetal pollution from acid mine drainage; landfill leachate; thermal power; and municipal, agricultural, refinery, and chlor-alkali effluent. the physicochemical properties of wetlands provide many positive attributes for remediating heavy metals. Typha, Phragmites, Eichhornia, Azolla, Lemna, and other aquatic macrophytes are some of the potent wetland plants for heavy metal removal. Biomass disposal problem and seasonal growth of aquatic macrophytes are some limitations in the transfer of phytoremediation technology from the laboratory to the field. However, the disposed biomass of macrophytes may be used for various fruitful applications. An ecosustainable model has been developed through the author's various works, which may ameliorate some of the limitations. The creation of more areas for phytoremediation may also aid in wetlands conservation. Genetic engineering and biodiversity prospecting of endangered wetland plants are important future prospects in this regard.     

Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation

A relatively small group of hyperaccumulator plants is capable of sequestering heavy metals in their shoot tissues at high concentrations. In recent years, major scientific progress has been made in understanding the physiological mechanisms of metal uptake and transport in these plants. However, relatively little is known about the molecular bases of hyperaccumulation. In this paper, current progresses on understanding cellular/molecular mechanisms of metal tolerance/hyperaccumulation by plants are reviewed. The major processes involved in hyperaccumulation of trace metals from the soil to the shoots by hyperaccumulators include: (a) bioactivation of metals in the rhizosphere through root–microbe interaction; (b) enhanced uptake by metal transporters in the plasma membranes; (c) detoxification of metals by distributing to the apoplasts like binding to cell walls and chelation of metals in the cytoplasm with various ligands, such as phytochelatins, metallothioneins, metal-binding proteins; (d) sequestration of metals into the vacuole by tonoplast-located transporters. The growing application of molecular-genetic technologies led to the well understanding of mechanisms of heavy metal tolerance/accumulation in plants, and subsequently many transgenic plants with increased resistance and uptake of heavy metals were developed for the purpose of phytoremediation. Once the rate-limiting steps for uptake, translocation, and detoxification of metals in hyperaccumulating plants are identified, more informed construction of transgenic plants would result in improved applicability of the phytoremediation technology.     

Emerging mechanisms for heavy metal transport in plants

Heavy metal ions such as Cu(2+), Zn(2+), Mn(2+), Fe(2+), Ni(2+) and Co(2+) are essential micronutrients for plant metabolism but when present in excess, these, and non-essential metals such as Cd(2+), Hg(2+) and Pb(2+), can become extremely toxic. Thus mechanisms must exist to satisfy the requirements of cellular metabolism but also to protect cells from toxic effects. The mechanisms deployed in the acquisition of essential heavy metal micronutrients have not been clearly defined although a number of genes have now been identified which encode potential transporters. This review concentrates on three classes of membrane transporters that have been implicated in the transport of heavy metals in a variety of organisms and could serve such a role in plants: the heavy metal (CPx-type) ATPases, the natural resistance-associated macrophage protein (Nramp) family and members of the cation diffusion facilitator (CDF) family. We aim to give an overview of the main features of these transporters in plants in terms of structure, function and regulation drawing on information from studies in a wide variety of organisms.     

Transgenic plants for phytoremediation

Phytoremediation is a green, sustainable and promising solution to problems of environmental contamination. It entails the use of plants for uptake, sequestration, detoxification or volatilization of inorganic and organic pollutants from soils, water, sediments and possibly air. Phytoremediation was born from the observation that plants possessed physiological properties useful for environmental remediation. This was shortly followed by the application of breeding techniques and artificial selection to genetically improve some of the more promising and interesting species. Now, after nearly 20 years of research, transgenic plants for phytoremediation have been produced, but none have reached commercial existence. Three main approaches have been developed: (1) transformation with genes from other organisms (mammals, bacteria, etc.); (2) transformation with genes from other plant species; and (3) overexpression of genes from the same plant species. Many encouraging results have been reported, even though in some instances results have been contrary to expectations. This review will illustrate the main examples with a critical discussion of what we have learnt from them.     

Laboratory study of heavy metal phytoremediation by three wetland macrophytes

Detention ponds and constructed wetlands have proven to be effective in reducing peak stormwater runoff volume and flow, and recent interest has extended to utilizing them to improve stormwater runoff quality. A review of stormwater runoff studies indicated that lead, zinc, copper, cadmium, phosphorus, and chloride are contaminants of primary concern. In laboratory settings, the uptake of contaminants by three wetland plant species, Glyceria grandis, Scirpus validus, and Spartina pectinata, was examined and removal rates from nutrient solutions inflow and nonflow reactors were measured. The removal rates varied by plant species and target contaminant, and no one species was the best accumulator of all six contaminants. Belowground tissues of all three species accumulated higher concentrations of the four heavy metals and aboveground tissues accumulated higher concentrations of phosphorus and chloride. Plants grown in flow reactors showed significantly higher accumulation rates than those grown in nonflow reactors. Also, plants grown hydroponically accumulated higher concentrations of the six target contaminants than those grown in sand reactors. However, those grown in sand had a much greater increase of biomass and removed a greater mass of the six target contaminants. Removal rates measured in these experiments can be used to design detention ponds to maximize stormwater remediation.     

Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.     

重金属污染土壤植物修复的研究进展和应用前景

土壤污染是当今面临的一个严峻的问题。其中重金属污染尤为严重。因此重金属污染土壤的修复日益受到各国政府和学者的重视。植物修复技术作为一种绿色安全的技术以其潜在的高效、经济及生态协调性成为当前国际学术界研究的热点领域。就植物修复技术的概念、方法原理、植物修复技术的研究历史和现状以及优点、应用前景作了系统阐述,并介绍了国内外开展的一些应用性实例。指出了植物修复技术当前还存在的问题。对今后发展的方向。作出了几点展望。     

A heavy metal biotrap for wastewater remediation using poly-gamma-glutamic acid

Poly-gamma-glutamic acid (gamma-PGA) obtained from Bacillus licheniformis ATCC 9945 was evaluated as a potential biosorbent material for use in the removal of heavy metals from aqueous solution. Copper (Cu(2+)) was chosen as the model heavy metal used in these studies since it is extensively used by electroplating and other industries, has been the model for many other similar studies, and can be easily assayed through a number of convenient methods. Cu(2+)-gamma-PGA binding parameters under varying conditions of pH, temperature, ionic strength, and in the presence of other heavy metal ions were determined for the purified biopolymer using a specially designed dialysis apparatus. Applying the Langmuir adsorption isotherm model showed that gamma-PGA had a copper capacity approaching 77.9 mg/g and a binding constant of 32 mg/L (0.5 mM) at pH 4.0 and 25 degrees C. Cu(2+)-gamma-PGA adsorption was relatively temperature independent between 7 and 40 degrees C, while an increase in ionic strength led to a decrease in metal ion binding. Cd(2+) and Zn(2+) ions compete with Cu(2+) for binding sites on the gamma-PGA biopolymer. Metal uptake by gamma-PGA was further tested using a tangential flow filtration apparatus in a diafiltration mode in which metal was continually processed through a dilute solution of gamma-PGA without allowing for equilibrium to be established. The circulating polymer solution was able to complex metal as well as successfully prevent passage of unbound copper ions present in solution through the membrane. Using 500 mL of a 0.2% gamma-PGA solution, up to 97% of a 50 mg/L copper sulfate solution processed at a flow rate of 115 mL/min was retained by the polymer. For a 10 mg/L solution of Cu(2+) as copper sulfate, filtrate concentrations of Cu(2+) never rose above 0.6 mg/L while processing 2.5 L of dilute copper sulfate.     

Signaling responses in plants to heavy metal stress

Heavy metal toxicity is one of the major abiotic stresses leading to hazardous health effects in animals and plants. Because of their high reactivity they can directly influence growth, senescence and energy synthesis processes. In this review a new indirect mechanism of heavy metal action is proposed. This mechanism is connected with the generation of reactive oxygen species (especially H₂O₂) and jasmonate and ethylene signaling pathways and shows that toxicity symptoms observed in plants may result from direct heavy metal influence as well as the activity of some signaling molecules induced by the stress action.     

H(+)-coupled heavy metal transport in plants

It has been recently well documented that metal transport systems play a crucial role in the uptake, distribution and detoxification of heavy metals throughout the plant. A range of gene families that are likely to be involved in essential and non-essential metal transport has been now identified and their plasma membrane and/or tonoplast localization in plant cells has been recently confirmed. These include the primary metal transporters, using ATP as the source of energy and H(+)-coupling transporters, utilizing the electrochemical gradient previously generated by plasma membrane and tonoplast proton pumps. As the presence of nucleotide binding domains in the protein sequence may indicate its ATP-hydrolytic activity, it is more difficult to determine the H(+)-coupling activity of protein on the base of its structure. Thus, the H(+)-coupling activity of protein may be only proved by functional analysis of the protein. In this work, we briefly review the structure, regulation and function of the metal transporters operating as H(+)/metal cotransporters.     

Predicted metal binding sites for phytoremediation

Metal ion binding domains are found in proteins that mediate transport, buffering or detoxification of metal ions. The objective of the study is to design and analyze metal binding motifs against the genes involved in phytoremediation. This is being done on the basis of certain pre-requisite amino-acid residues known to bind metal ions/metal complexes in medicinal and aromatic plants (MAP''s). Earlier work on MAP''s have shown that heavy metals accumulated by aromatic and medicinal plants do not appear in the essential oil and that some of these species are able to grow in metal contaminated sites. A pattern search against the UniProtKB/Swiss-Prot and UniProtKB/TrEMBL databases yielded true positives in each case showing the high specificity of the motifs designed for the ions of nickel, lead, molybdenum, manganese, cadmium, zinc, iron, cobalt and xenobiotic compounds. Motifs were also studied against PDB structures. Results of the study suggested the presence of binding sites on the surface of protein molecules involved. PDB structures of proteins were finally predicted for the binding sites functionality in their respective phytoremediation usage. This was further validated through CASTp server to study its physico-chemical properties. Bioinformatics implications would help in designing strategy for developing transgenic plants with increased metal binding capacity. These metal binding factors can be used to restrict metal update by plants. This helps in reducing the possibility of metal movement into the food chain.     

Silicon and heavy metal tolerance of higher plants

The heavy metal tolerant Cardaminopsis halleri, grown on Zn and Cu polluted soil, showed electron dense metal containing precipitates (Zn, Cu, Sn, Fe, Al) on the leaf surface, in the intercellular spaces (Zn, Cu, Sn), the cell walls and the cell wall thickenings of the xylem vessels (Zn, traces of Cu and Fe). Large amounts of Zn were measured in the vacuoles, the main storage compartment for this metal in Cardarminopsis. The cytoplasm and nuclei contained small precipitates, including mainly Zn and Si. As shown by ESI Zn was co-localized with Si in these structures. The EEL-spectra of the cytoplasmic precipitates corresponded with the spectra of Zn-silicate. Besides Zn-silicate, electron translucent structures in the cytoplasm were identified as SiO2 by their EEL spectra. It was concluded that in the cytoplasm of Cardaminopsis Zn is transiently accumulated as silicate, being slowly degraded to SiO2. Zn is translocated into the vacuole and accumulated in an unknown form. A second Si and Zn-uptake mechanism was found, excluding a membrane and cytoplasm passage. Pinocytotic vesicles, formed by the plasmamembrane and the tonoplast, enable a direct translocation of Si and Zn from extracellular compartments into the vacuole. The formation of Zn-silicate is part of the heavy metal tolerance mechanism and may be responsible for the amelioration of the Zn toxicity in Cardaminopsis.     

Development of a fluorescent transgenic zebrafish biosensor for sensing aquatic heavy metal pollution

We report a transgenic zebrafish (Danio rerio) designed to respond to heavy metals using a metal-responsive promoter linked to a fluorescent reporter gene (DsRed2). The metallothionein MT-Ia1 promoter containing metal-responsive elements was derived from the Asian green mussel, Perna viridis. The promoter is known to be induced by a broad spectrum of heavy metals. The promoter-reporter cassette cloned into the Tol2 transposon vector was microinjected into zebrafish embryos that were then reared to maturity. A transgene integration rate of 28 % was observed. The confirmed transgenics were mated with wild-type counterparts, and pools of F₁ embryos were exposed to sub-lethal doses of Cd²⁺, Cu²⁺, Hg²⁺, Pb²⁺ and Zn²⁺. The red fluorescence response of zebrafish embryos was observed 8 h post- exposure to these sub-lethal doses of heavy metals using a fluorescence microscope. Reporter expression estimated by real-time PCR revealed eightfold, sixfold and twofold increase on exposure to highest concentrations of Hg²⁺, Cd²⁺ and Cu²⁺, while Pb²⁺ and Zn²⁺ had no effect. This biosensor could be a first-level screening method for confirming aquatic heavy metal bio-toxicity to eukaryotes.     

Water relations in plants subjected to heavy metal stresses

Concentrations of heavy metals in soil seldom reach a level sufficient to cause osmotic disturbances in plants. It is likely that water entry to the roots is indirectly governed by other factors which are themselves affected by metals. Decreased elongation of the primary root, impaired secondary growth, increased root dieback, or reduced root hair caused by toxic ions all exert a deleterious effect on the root-absorbing area and water uptake. Moreover, metals are able to decelerate short-distance water transfer both in symplast and apoplast, which in turn reduce the movement of water into the vascular system and affect water supply to the shoot. Long-distance transport is limited also due to decreased hydraulic conductivity in the root, stem and leaf midrib caused by a reduction in the size of vessels and tracheids, and partial blockage of xylem elements by cellular debris or gums. Heavy metals influence water delivery to the shoot due to inhibition of transpiration as they decrease the size of the leaves and the thickness of the lamina, reduce intercellular spaces, affect the density of stomata and decrease their aperture. Stomata closure is induced by direct interaction of toxic metals with guard cells and/or as a consequence of the early effects of metal toxicity on roots and stems. In metal-stressed plants, root-derived ABA or ABA-induced signals might play a role in stomatal movement. Disturbances in water relations trigger differential regulation of aquaporin gene expression, which may contribute to further reductions in water loss.     

Phytolacca acinosa Roxb. with Arthrobacter echigonensis MN1405 enhances heavy metal phytoremediation

The growth and metal-extraction efficiency of plants when exposed to toxic metals can be enhanced by inoculating with certain bacteria, but the mechanisms of this process remain unclear. We report results from glasshouse experiments on the effect of Arthrobacter echigonensis MN1405 in promoting Phytolacca acinosa Roxb. growth when exposed to 100 mg/L Mn solution. Mn removal efficiency in solution was significantly enhanced by bacterial inoculation; Mn was accumulated in the root of P. acinosa Roxb. plant. The bacteria oxidized the Mn on root surface, which formed a Mn plaque to serve as a barrier or a containment to prevent metal toxicity. In this process, pH condition was an important factor on the effects of microbial-assisted heavy metal phytoremediation. Our finding suggests that A. echigonensis MN1405 assisted P. acinosa to achieve high remediation efficiency of Mn removal and accumulation in Mn contamination area.