Phytoremediation strategies for soils contaminated

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Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives Article in Chemosphere · January 2017 DOI: 10.1016/j.chemosphere.2016.12.116

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Nuclear Institute for Agriculture and Biology

University of Agriculture Faisalabad



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Chemosphere 171 (2017) 710e721

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Review

Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives Nadeem Sarwar a, Muhammad Imran b, *, Muhammad Rashid Shaheen c, Wajid Ishaque a, Muhammad Asif Kamran a, Amar Matloob d, Abdur Rehim b, Saddam Hussain e, f, ** a

Nuclear Institute for Agriculture and Biology (NIAB), Faisalabad, Pakistan Department of Soil Science, Bahauddin Zakariya University, Multan, Pakistan Department of Horticultural Sciences, University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur, Pakistan d Department of Agronomy, Muhammad Nawaz Shareef University of Agriculture, Multan, Pakistan e College of Resources and Environment, Huazhong Agricultural University, Wuhan, Hubei, China f Department of Agronomy, University of Agriculture, Faisalabad, Pakistan b c

h i g h l i g h t s We We We We

discussed various sources and harmful effects of some important heavy metals and metalloids. summarized the traditional phytoremediation strategies, and mechanisms involved in phytoremediation of metals. highlighted the limitations and some recent advances in phytoremediation approach. compared the traditional and advanced phytoremediation techniques for effective implications.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 August 2016 Received in revised form 27 November 2016 Accepted 22 December 2016 Available online 23 December 2016

Presence of heavy metals in agricultural soils is of major environmental concern and a great threat to life on the earth. A number of human health risks are associated with heavy metals regarding their entry into food chain. Various physical, chemical and biological techniques are being used to remove heavy metals and metalloids from soils. Among them, phytoremediation is a good strategy to harvest heavy metals from soils and have been proven as an effective and economical technique. In present review, we discussed various sources and harmful effects of some important heavy metals and metalloids, traditional phytoremediation strategies, mechanisms involved in phytoremediation of these metals, limitations and some recent advances in phytoremediation approaches. Since traditional phytoremediation approach poses some limitations regarding their applications at large scale, so there is a dire need to modify this strategy using modern chemical, biological and genetic engineering tools. In view of above, the present manuscript brings both traditional and advanced phytoremediation techniques together in order to compare, understand and apply these strategies effectively to exclude heavy metals from soil keeping in view the economics and effectiveness of phytoremediation strategies. © 2016 Elsevier Ltd. All rights reserved.

Handling Editor: T Cutright Keywords: Agricultural soils Environmental pollution Heavy metals Microbes Phytoremediation

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Heavy metals in agroeecosystem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Natural sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Anthropogenic sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

* Corresponding author. ** Corresponding author. Department of Agronomy, University of Agriculture, Faisalabad, Pakistan. E-mail addresses: [email protected] (M. Imran), [email protected]. edu.cn (S. Hussain). http://dx.doi.org/10.1016/j.chemosphere.2016.12.116 0045-6535/© 2016 Elsevier Ltd. All rights reserved.

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3. 4. 5.

6. 7.

8.

9. 10.

Harmful effects of heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors affecting metal bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytoremediation of heavy metals: traditional concept . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Phytostabilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Phytovolatalization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Phytoextraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanism of heavy metals phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phytoremediation of heavy metals: new concept . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Chemicaleassisted phytoremediation using nonehyperaccumulator plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Biochareassisted phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3. Microbialeassisted phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4. Use of transgenic plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Molecular mechanisms of heavy metals tolerance in higher plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1. Heavy metal uptake and translocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2. Heavy metal sequestration/detoxification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3. Organic acids and heavy metal tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Economic evaluation of phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest and assurance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction In the modern age of rapid industrialization, it is not possible to avoid the toxic chemicals and metals in the environment. Especially heavy metals pollution has become a serious threat to the environment and food security because of rapid growth in industries and agriculture and disturbance of natural ecosystem due to enormous increase in world population. Unlike organic pollutants, biodegradation of heavy metals is just out of question and hence are continuously accumulating in the environment (Sarwar et al., 2010). Accumulation of these heavy metals in agricultural soils and water resources poses a great threat to human health due to potential risk of their entry into food chain (Sarwar et al., 2010). Heavy metals enter into the agroeecosystem by natural as well as anthropogenic processes. Some soils inherit these metals from parent material from which they are being originated. Soils having a high background of these toxic metals are harmful to plants as well as animals, as the parent material naturally having high concentrations of these metals. For example, selenium (Se) toxicity problem in the Kesterson reservoirs in the Westecentral San Joaquin Valley was due to high Se concentration in parent material (Presser, 1994). Anthropogenic sources include application of phosphate fertilizers, sewage sludge and anthropogenic emissions from power stations, metal industries, urban traffic and cement industries (Wu et al., 2004). These processes contribute to higher concentrations of heavy metals to the agricultural soileenvironment. From soil, heavy metals are taken up by plants through the cortical tissues of roots due to their similarity with some essential micronutrients (like zinc) and adopt symplastic and/or apoplastic pathway to reach xylem transport system (Salt and Rauser, 1995). Heavy metals can cause plant growth reduction by decreasing photosynthetic rates and chlorophyll contents (Sarwar et al., 2015). Metals can cause water stress in some plants by decreasing stomatal conductance, transpiration rate and leaf relative water contents due to decrease in size and number of xylem vessels, chloroplasts and cell enlargement (Saifullah et al., 2014). These metals can accumulate in edible plant parts and thus enter into food chain. So, it is a matter of great importance to exclude these metals from the agroeecosystem in order to maintain a safe food chain and healthy environment. Heavy metals are categorized as essential and noneessential

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metals. Essential metals including; copper (Cu), zinc (Zn), manganese (Mn), nickel (Ni) and iron (Fe), have important regulatory roles in a number of biological processes such as in electron transferring proteins and as coefactors of numerous enzymes (Fageria et al., 2009; Chaffai and Koyama, 2011). While, noneessential metals are those having no known biological functions such as cadmium (Cd), mercury (Hg) and lead (Pb). Plants exposed to heavy metals stress respond by altering cellular mechanisms (Choppala et al., 2014) and gene expression (Hussain et al., 2004; Chaffai and Koyama, 2011). All heavy metals may cause the production of reactive oxygen species (ROS) beyond their toxic limits. However, noneessential metals inhibit various biological processes either by replacing essential metals or by altering the structure of biomolecules and important stress regulatory proteins (Sarwar et al., 2010). Heavy metals may cause severe toxicity in plants by; disturbing essential groups of enzymes, destructing the integrity of important biomolecules, modifying some macromolecules, replacing essential metal ions from structural formulae of biomolecules, and altering antioxidant defense mechanisms as a result of ROS production (Sarwar et al., 2010; Chaffai and Koyama, 2011; Choppala et al., 2014). Plants adopt different strategies to cope with metals toxicity which contribute to certain tolerance mechanisms such as metal sequestration, compartmentalization in certain cell organelles, exclusion and inactivation by exudation of organic ligands (Choppala et al., 2014). A number of physical, chemical and biological techniques can be used to remediate metal contaminated soils. However, phytoremediation has been recognized as cost effective method for remediation of metal contaminated soils. This approach of decontamination of soils has great importance especially in case of metal contamination as contaminated soil has entirely different substrate then air or water. The reason behind this might be the longer persistence of heavy metals in soil than any other component of biosphere. Since plants are the primary recipients of heavy metals, so remediation of xenobiotic metals using plants (phytoremediation) seems an effective and attractive approach in the present scenario. In current review, we briefly discuss the sources and impacts of heavy metals in agroeecosystem, factors affecting metals bioavailability, recent phytoremediation techniques with special reference to their advantages, disadvantages, mechanisms and future perspectives, and how these techniques are useful and

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economical for reclamation of heavy metal contaminated soils, and the scope of genetic engineering tools to develop effective transgenic hyperaccumulator plants producing large aboveground biomass for phytoremediation of deleterious metals. 2. Heavy metals in agroeecosystem From plant health point of view, heavy metals are well known to be divided into two categories. Some metals are required by plants as essential micronutrients for proper plant growth such as Zn, Cu, Fe, Mn and Ni at very low concentration (Fageria et al., 2009). But excessive levels of these metals are toxic to plants and can cause growth inhibition, soil quality deterioration, yield reduction and poor quality of food with a potential health risk to human and animals (Seth et al., 2007; Seth, 2012). While some metals and metalloids are essentially heavy metals with no known biological functions in plants such as arsenic (As), chromium (Cr), silver (Ag), Cd, Pb, Se and Hg (Seth, 2012). As discussed earlier, heavy metal enters into agroeecosystem through both natural as well as anthropogenic sources briefly discussed as under.

fertilizers, some organic compounds such as farm yard manures, composts and biosolids containing higher concentrations of heavy metals than in most of agricultural soils are also applied to soils for improving soil fertility status or reclamation of problem soils (see Table 1). The extent of contamination of soils with heavy metals through irrigation varies from location to location depending upon the level of contamination in irrigation water. Fresh water nonecontaminated sources contribute extremely very low level of contamination while application of sewage and industrial waste waters often contain high concentrations of heavy metals. Repeated use of untreated waste waters for irrigation purpose may be a considerable input source of some metals. Dry and wet deposits of emissions from different point sources including steel industry, metal smelters, metal refineries, foundries and cement industries have also a great contribution to metal accumulation in soils (Freedman and Hutchinson, 1981). Moreover, emissions from automobiles using lead enriched fuel are responsible for significant Pb accumulation in soils near highways. Mining activities have also been reported to contaminate the soils with heavy metals in localized areas (Webber, 1981).

2.1. Natural sources The most important and primary source of heavy metals is the parent material from which a soil has been originated. Of the total earth crust, 95% is made up of ingenious rocks and about 5% sedimentary rocks (Thornton, 1981). Among the former, basaltic ingenious rocks contains heavy metals like cobalt (Co), Cd, Zn, Cu and Ni generally in higher concentrations while among the latter, shales derived from fine sediments of organic and inorganic origin have larger amounts of metal elements i.e. Zn, Cu, Mn, Cd and Pb. Generally these heavy metals exist in most of the soils as carbonates, sulfides, oxides or salts. The dominant mineral of every metal may vary from soil to soil. 2.2. Anthropogenic sources Recent advancements in industry and agriculture sector contributed a lot in elevated heavy metal contamination in soils and water resources. Mining and smelting activities are important point sources of heavy metals in agroeecosystem. Use of metal containing substances and contaminated biosolids and fertilizers also play their role in this scenario (He et al., 2005; Sarwar et al., 2010; Czarnecki and Düring, 2015). For sustainable crop production, some metals especially Zn with other phosphatic fertilizers have to be applied in soil (Imran et al., 2016a) or foliar spray on plant leaves as essential micronutrient (Rehim et al., 2014; Imran et al., 2015; Imran and Rehim, 2016). For insect pest and disease management, different chemicals like insecticides, fungicides, and herbicides have to be applied on large scale, also an important source of some elements like Cu, As, Zn and Fe etc. (Fageria et al., 2002). Some important anthropogenic inputs of heavy metals are discussed in this section. Fertilizer especially phosphorous (P) fertilizers such as triple super-phosphate and calcium phosphate contain heavy metals (mostly Zn and Cd) in varying concentrations depending on rock phosphate source. Some rock phosphate sources have Cd concentration even more than 50 mg kg1 of soil and are banned in many countries for agricultural use (Mortvedt and Beaton, 1995). Likewise, Zn, Fe, Cu, Mn and boron (B) containing compounds are also being used for proper plant growth and yields. Czarnecki and Düring (2015) found that longeterm use of mineral fertilizer increased the soil metal content, however, eight years termination of the fertilization reduced the soil Cd, Cu, Mn, Pb, and Zn contents by 82.6, 54.2, 48.5, 74.4, and 56.9%, respectively. Other than

3. Harmful effects of heavy metals Heavy metals once enter into agroeecosystem become very hazardous for life especially human life. Certain heavy metals show duality in plant tolerance like Fe, Cu, Zn and Mn are beneficial at low concentrations by improving plant growth and yield or/and biofortification and hence beneficial for the whole food chain linkages (Verkleij et al., 2009; Imran et al., 2016b). But higher concentrations of these metals and other nonessential elements (mentioned above) not only exert damaging effects on plant health but could have deleterious potential to other organisms including man (Roy and McDonald, 2013). Heavy metals affect various physiological and biochemical processes in plant and could inhibit plant growth and cell death to critical level (Popova et al., 2009; Xu et al., 2009). This growth reduction might be explained on the basis of decreased photosynthetic rate and chlorophyll content. Heavy metal toxicity could cause cell membrane damage and destruction of biomolecules and cellular organelles due to increase in the production of ROS in plants under stress (Ekmekci et al., 2008). The entry of heavy metals in the food chain is of special concern due to a number of associated health risks in animals and human. These elements are very toxic and have potential to cause severe damages even at very low concentrations (Sarwar et al., 2010). Roy and McDonald (2013) conducted a study in a soil contaminated with a variety of heavy metals including Pb, Zn, Cd and Cu, using six household garden plant species and carried out risk assessment for residents of Spelter on the basis of heavy metals concentration in edible tissues of plants. It was observed that carrot accumulated Cd (40 mg kg1) that was five times, eight times and twelve times greater concentration than the maximum permissible limits of male, female and children, respectively. On the basis of results, they concluded that carrot and lettuce grown in soils of Spelter are potential risk of Zn and Cd toxicity in male, female and young ones. A number of health problems are linked to heavy metal toxicity in man depending on concerned metal, concentration and its oxidation state etc. A brief image of these health risks is given as under; Cadmium is well known as mutagenic and carcinogenic; disturb calcium (Ca) metabolism in the body, a problem called hypercalciuria, kidney failure and severe anemia (Awofolu 2005). Zinc at high concentration can cause fatigue and dizziness (Hess and Schmid, 2002).


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Table 1 Information regarding sources, harmful effects and some important hyper accumulator plants of heavy metals. Heavy metal

Sources

Cd

Rock phosphate, plastic stabilizers, paints and pigments, cement industry, power stations, metal industries

Harmful effects

Hypereaccumulator plant species

Carcinogenic, mutagenic, hypercalciuria resulting in Azollapinnata, bone damage and kidney stone and failure Eleocharisacicularis,Rorippaglobosa, solanumphotenocarpum Cr Steel industry, leather industry, contaminated biosolids and Rapid hair loss Pterisvittata manures, fly ash Euphorbia cheiradenia Pb Urban traffic using leaded fuels, electric batteries, Renal failure, cardiovascular disease, reduced weedicides and pesticides intelligence, short term memory loss, coordination problem, decreased learning ability in children Ni Metal industry, kitchen appliances, surgical instruments, Immunotoxic, neurotoxic, genotoxic, hepatotoxic, Alyssum bertolonii, Alyssum caricum, batteries and steel alloys lungs, throat and stomach cancers, rapid hair fall Alyssum corsicum, Alyssum murale As Pesticides, wood preservatives Interferes with cellular processes such as oxidative Corrigiolatelephiifolia phosphorylation and ATP synthesis Hg Mining, coal combustion, surgical instruments, medical Depression, anxiety, fatigue, restlessness, hair loss, _ waste vision disturbances, ulcers, kidney damage Zn Pesticides and fertilizers Dizziness and fatigue in case of over dose Eleocharisacicularis Cu Rock phosphate, zinc fertilizers brain and kidney damage, severe anemia, intestinal Eleocharisacicularis irritation Salem et al. (2000), Hess and Schmid (2002), Li et al. (2003), Rai (2008), Bani et al. References Memon et al. (2001), Salem et al. (2000), He et al. (2010), Kalve et al. (2011), GarciaeSalgado (2005),Tariq et al. (2006), Khan et al. (2007), Saifullah et al. Awofolu (2005), Tripathi et al. (2007) et al. (2012), Ali et al. (2013) (2009), Sarwar et al. (2010), Ali et al. (2013)

Lead toxicity could result in renal failure, cardiovascular disease, and cause reduced intelligence, short term memory loss, coordination problem and decreased learning ability in children (Salem et al., 2000). Chromium can cause rapid hair fall (Salem et al., 2000). Higher levels of Cu have been reported to cause brain and kidney damage, severe anemia and intestinal irritation (Salem et al., 2000). Arsenic in arsenate form being analogous to phosphate interferes with cellular processes such as oxidative phosphorylation and ATP synthesis (Tripathi et al., 2007). Inhalation of Ni can cause lungs cancer. Throat and stomach cancers have also been reported due to Ni toxicity. It is immunotoxic, neurotoxic, genotoxic and hepatotoxic and causes rapid hair fall (Khan et al., 2007).

approach as compared to engineering techniques like excavation, soil incineration, soil washing, flushing, solidification etc. (Ali et al., 2013; Wang et al., 2015). The idea of phytoremediation was suggested for the first time by Chaney (1983). The concept seems pleasant esthetically and gains good public acceptance and can be applied over a large scale field sites where other physical remedial measures may not be so efficient and cost effective. The establishment of green plants on contaminated soil proves more economical in many ways: (i) phytostabilization; (ii) phytoextraction of precious metals like Hg, Ag and Ni; (iii) sustainable land management (Ali et al., 2013). The concept of using green plants for heavy metal remediation gains the popularity as green remediation of deleterious metals and metalloids a good alternate of physical and chemical remedial measures (Ali et al., 2013). Following phytoremediation techniques (Fig. 2) are important to discuss here for remediation of heavy metals from soil.

4. Factors affecting metal bioavailability

5.1. Phytostabilization

From plant uptake point of view, the bioavailable concentration of a metal is of great concern. The term bio availability can be defined as “a part of total concentration of a metal that is available to plants, microbes etc.” and this bioavailable concentration of a metal is important regarding its uptake and accumulation in plant rather than total metal concentration in soil. A number of factors control bioavailability of a metal in the soil including soil organic matter, soil pH, competitive ions concentration, root exudates and species of plants present in the soil and plant age (Harter and Naidu, 2001; Jung, 2008). These factors either influence the release of metal ion into soil solution or affect plant uptake ability in soil.

Phytostabilization or phytoimmobilization refers to the use of plants having ability to decrease the mobility or/and bioavailability of a metal either to prevent its leaching to ground water or its entry into food chain by certain mechanisms including adsorption by roots, precipitation, complexation in the root zone (Erakhrumen, 2007). Recently, Mahmoud and Abd El-Kader (2014) conducted a pot experiment to study the heavy metal immobilization potential of phosphogypsum (PG) and rice straw compost (CP) in soil and their effect on canola growth. They showed that application of PG alone caused more immobilization of heavy metals (Zn, Ni, Pb and Cd) as compared to CP þ PG combined treatment. However, CP þ PG treatment significantly improved biomass production and gave 67% more canola dry weight as compared to PG alone. It can be inferred that application of PG may effectively immobilize HMs in soil. But phytostabilization is not a permanent solution as heavy metals remains in the soil as it is; only with restricted movement and needs to monitor regularly.

5. Phytoremediation of heavy metals: traditional concept The term phytoremediation refers to the use of green plants and associated microorganisms to minimize the toxic effects of potential contaminant in the environment (Greipsson, 2011). The word “phytoremediation” is derived from Greek word phyto (mean plant) and Latin word Remedium (to correct or remove an evil). This technique can be used for remediation of heavy metals and metalloids from soil and found economically feasible and efficient

5.2. Phytovolatalization Phytovolatalization is another approach which involves the conversion of metal into volatile form and its release into the

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atmosphere through stomata (Ghosh and Singh, 2005). This technique is primarily useful for Hg as mercuric ion is transformed into relatively less toxic elemental form. As the volatile form of Hg released into the atmosphere may be recycled back to the soil by precipitation, so this technique presents a temporary solution of the problem. 5.3. Phytoextraction Phytoextraction is the most important phytoremediation approach for removal of metals and metalloids from contaminated soils water, biosolids and sediments (He et al., 2005; Seth, 2012; Ali et al., 2013). It is more suitable for commercial application as compared to other phytoremediation techniques (Sun et al., 2011). A number of factors affect the efficiency of Phytoextraction including soil properties, metal availability to plant, metal speciation and concerned plant’s characteristics. Plants selected for phytoextraction should possess the characteristics of; (i) rapid growth rate, (ii) more biomass production, (iii) hyperaccumulator of heavy metal, (iv) widely distributed, (v) translocate metal from root to shoot, (vi) tolerate the toxic effects of heavy metal, (vii) resistant to pathogens and pests, (viii) well adopted to prevailing climatic conditions, (ix) easy to cultivate and harvest, and (x) have no attraction to herbivores to avoid its entry into food chain (Tong et al., 2004; Shabani and Sayadi, 2012; Ali et al., 2013). Generally shoot metal concentration and shoot biomass mainly determine a suitable plant species for phytoextraction of metals. Depending upon these parameters, two different phytoextraction approaches have been used i.e. use of hyperaccumulator plants with relatively low biomass production and use of plants with relatively higher aboveground biomass production but lesser metal accumulation such as Brassica juncea (Robinson et al., 1998; Ali et al., 2013). While some researchers preferred hyperaccumulation and metal tolerance as characters of vital importance. Because plants with low biomass and high metal accumulation are easy to dispose after harvesting an economical concentration of heavy metals (Chaney et al., 1997). Ali et al. (2012) proposed that multiecut plant species (Trifolium spp.) were more effective because of their great potential to extract more concentration of a metal than mono-harvest plant species. Grasses having short life cycle, high growth rate, tolerance against abiotic stresses and more biomass production can be preferred over shrubs and trees (Malik et al., 2010). While, use of nonehyperaccumulator plants species such as maize, barley etc. for traditional phytoextraction requires several cropping seasons to remove heavy metals to an acceptable levels and potential risk for food chain contamination.

phytoremediation process as more the plant is tolerant to metal stress more will be the metal accumulation in plant tissues with minimum adverse effects on plant health. Metal tolerance potential of a plant depends on mechanisms like cell wall metal binding, active transport of metal ion into the vacuoles, chelation of metal ions with proteins and peptides and complex formation (Memon €der, 2009). A brief sketch of mechanisms involved in and Schro phytoremediation of heavy metals and metalloids is given in Fig. 1. Besides these physiological mechanisms governing plant tolerance, the annual biomass production i.e. shoots dry weight and net metal content harvested per year are also critical to estimate plant’s phytoextraction potential. T. caerulescens, a Zn/Cd hyperaccumulator species produces about 2 tons ha1 of shoot dry matter (Chaney et al., 1997) and can be increased upto 5 tons ha1 by using breeding tools (Brown et al., 1995). T. caerulescens grown on Zn/Cd contaminated soil has ability to harvest about 60 kg Zn ha1 and 8.4 kg Cd ha1 (Robinson et al., 1998). However, some species of Thalspi have potential to hyperaccumulate more than one metals. These species grown on Ni contaminated soils can accumulate about 30,000 ppm Ni of its total dry weight (Robinson et al., 1998). 7. Phytoremediation of heavy metals: new concept The use of green plants to remediate a contaminated soil seems an attractive approach to tackle the heavy metal problems and having vast research background. Still the traditional phytoremediation techniques lack large scale applications because of a number of limitations. Naturally accruing hyperaccumulator plant species are either slow growing producing low above ground plant biomass or not well adapted to variety of environmental conditions (Saifullah et al., 2009). Traditional phytoremediation approaches face certain limitations such as, i) these require long time to remediate the contaminated soil, ii) phytoextraction ability of

6. Mechanism of heavy metals phytoremediation Generally, plant uptake metals from soil solution which act as bioavailable pool of heavy metals and plant nutrients as well. Factors like soil pH, organic matter, root exudates, microbial biomass, and competitive cations affect the availability of heavy metals in soil (Sarwar et al., 2010). A specific heavy metal once taken up by plant roots may either accumulate in root tissues (phytoimmobilization) or translocate to the aerial parts of plant through xylem vessels via symplastic and/or apoplastic pathways. In shoot, metals are generally accumulated in vacuoles (cellular organelles with low metabolic activity). It might be an important tolerance mechanism in hyperaccumulator plants to keep deleterious metal away from important cellular metabolic processes. Phytoextraction mechanism has five major steps; metal mobilization in rhizosphere, metal ion uptake by plant roots, translocation towards aerial plant parts, metal sequestration in plant tissues and heavy metal tolerance (Ali et al., 2013). Heavy metal tolerance is a prerequisite for

Fig. 1. Mechanisms involved in phytoremediation of heavy metals/metalloids in soils.


Fig. 2. Approaches for heavy metals phytoremediation.

hyperaccumulator plants is limited due to low aboveground biomass production, iii) a very small fraction of metals is bioavailable and this bioavailable concentration varies with soil pH, organic matter, competitive cations, calcareousness etc., iv) applicable to sites with low or moderate contamination, v) lack of knowledge about the agronomy, breeding potential, insect pest and disease spectrum, and vi) any mismanagement or carelessness may result in food chain contamination (Ali et al., 2013). These unavoidable limitations compel the researchers to modify the traditional approaches of phytoremediation to minimize these limitations and to ensure large scale application of phytoremediation. In recent past, a lot of research was conducted in this field and result in recent advancements in phytoremediation (Fig. 2) as reviewed in this section. 7.1. Chemicaleassisted phytoremediation using nonehyperaccumulator plants Selection of suitable species for phytoremediation of heavy metals is the most critical decision. Generally those species which can accumulate high concentration of heavy metal in aerial parts are supposed to be better and called hyperaccumulator plants. Baker et al. (1994) proposed shoot to root metal concentration ratio as criteria to decide whether plant is hyperaccumulator or not. According to them the ratio is above 1.0 for a plant species indicates that metal tend to accumulate more in shoot then roots. Such plant can be taken as hyperaccumulator and might be suitable for €mer (2010), heavy metal conphyroextraction. According to Kra centration in aerial parts of a hyperaccumulator plant varies from 1000 to 10,000 mg kg1 depending upon toxic level of heavy metal and even as low as 100 mg kg1 in case of Cd as it is highly toxic metal. So far, majority of plants classified as hyperaccumulators meet the said criteria. The main disadvantage of using these plants is that these are very slow growing and produce little aboveground biomass (Saifullah et al., 2009). These limitations make such plants unfeasible for phytoremediation at large scale. However these plants can be used as reference to develop genetically modified plants having ability to accumulate high metal concentrations and more biomass production. Therefore nonehyperaccumulator plants producing more aboveground biomass should be studied for

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their phytoremediation potential. Since, these plants extract relatively less amount of heavy metals; it will be more beneficial to enhance their extraction ability using synthetic or organic chelating agents using a process known as chelateeassisted phytoextraction or induced phytoextraction (Salt and Rauser, 1995; Saifullah et al., 2009). Synthetic chelating agents including ethylene diamine tetraeacetic acid (EDTA), diethylene triamine pentaeacetic acid (DTPA), and ethylene glycol tetraeacitic acid (AGTA) can be successfully used to enhance metal bioavailability and thus uptake by plants (Saifullah et al., 2009; Pereira et al., 2010). However there are certain limitations in this technique as there is a risk of environmental contamination due to high mobility of heavy metals. Moreover high uptake of chelated heavy metal may cause toxicity for the plants. Further research is needed to study induced phytoextraction keeping in view some important factors like temperature, soil pH, organic matter, redox potential, soil fertility status, plant morphology, and inter species competition which may also affect metal availability (Souza et al., 2013). Although, metal chelators have great potential to lead even low accumulator plants towards excessive metal uptake by improving metal bioavailability in soil, but such high biomass producing low accumulators are genetically less tolerant to metal toxicity. As described in previous sessions, heavy metal toxicity may result in stunted growth and low biomass production. Alleviation of toxicity is mandatory in order to adopt such innovative phytoremediation techniques to ensure economic benefits and maximum metal harvest from contaminated site. Many researchers in recent past explored a number of strategies to cope with HM stress in metal sensitive plants (Saifullah et al., 2009; Sarwar et al., 2010, 2015; Popova et al., 2012). Use of salicylic acid (SA), a widespread phenolic compound, in stress alleviation is also an effective and emerging field of study. It is well known signaling molecule in plants under biotic and abiotic stress conditions (Shaheen et al., 2015). Convincing results of many scientific investigations have been obtained on the role of SA in plant protection against HM stress. He et al. (2010) inferred that SA pretreatment of rice seeds at 0.1 mM for 24 h significantly improved seed germination parameters and seedling growth in Cd containing growth medium. Popova et al. (2012) showed that exogenous application of SA significantly alleviated negative effects of Cd on chlorophyll contents, proline levels and leaf relative water content of maize. Hence, pretreatment of SA along with chemical assisted phytoremediation program may alleviate toxic effects of heavy metals on metal extractor plants resulting in increased biomass production and heavy metaleharvest potential of plants. Except all these limitations discussed above, the most critical is high prices of these synthetic chelating agents, because phytoextraction at large scale may involve heavy expenses. Instead of these expensive synthetic chemicals, some low molecular weight organic acids such as acetic acid, citric acid, malic acid and oxalic acid can be effectively used as chelating agents of heavy metals. These organic acids can form metal complexes of low to moderate stability. Another advantage is that organic acids are easily biodegradable in soil than synthetic chelating agents with minimum environmental contamination risks (Souza et al., 2013). 7.2. Biochareassisted phytoremediation Biochar is a carbonaceous porous substance synthesized in result of pyrolysis of organic feedstocks such as plant materials, organic manures and sludges (PazeFerreiro et al., 2014). Charcoal, a wood biochar, is the most common biochar that is being used since preterit times. Biochar own some specific physicechemical properties, i.e. high pH, large surface area for sorption of metals, alkaline nature, ash, carbon contents and ability to immobilize toxic heavy

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metals, which place it among good heavy metals remediators. Large surface area available for sorption helps to form heavy metalsebiochar complexes either by exchange of heavy metal cations with other metal cations (i.e., Naþ, Kþ, Ca2þ, Mg2þ) at functional groups present in biochar or by physical adsorption (Lu et al., 2012). High pH and alkalinity of biochar may decrease the bioavailability of metals and increase their precipitation in soil amended with biochar. It has been reported that pH of biochar increases with pyrolysis temperature possibly due to increase in biochar ash content (Wu et al., 2012; Cantrell et al., 2012). Biochar can also be used in combination with traditional phytoremediation techniques to enhance their effectiveness against heavy metals as biochar is widely reported in literature to enhance plant growth and biomass production up to 10% (Jeffery et al., 2011; Liu et al., 2013). This increase in plant biomass is attributed to high nutrient and water holding capacity, cation exchange capacity (CEC), and High pH of biochar which effect nutrient cycling and improve nutrient turnover of plants (Liu et al., 2013; Fellet et al., 2014; Ahmad et al., 2016). Biochar is also reported to influence the soil microbial community possibly by favoring useful microbes and suppressing pathogens as some chemical compounds present in biochar suppress pathogens in soil (Elad et al., 2012). In the nutshell, biochar may improve the growth and yield of plants and can be successfully used in combination with hyperaccumulators and noneaccumulators þ EDTA for remediation of toxic heavy metals. However, further research is needed to test the combined effect of these two approaches on metals phytoextraction. 7.3. Microbialeassisted phytoremediation Soil microorganisms associated with plants may influence heavy metal availability and uptake by plants in the rhizosphere. Some microorganisms live in association with plant roots while others free living. Mycorrhizal fungi are major component of living organisms in the root zone and live in associations with most of the higher plants in different forms i.e. ectomycorrhizas, arbuscular mycorrhizas, orchid mycorrhizas and ericaceous mycorrhizas, with arbuscular mycorrhizal fungi associations with the roots of terrestrial plants being the most widespread (Sheng and Xia, 2006). These associations between fungi and plant roots are beneficial for plants in many ways including more plant nutrients such as N, P, K, Ca, S, Zn, Co, Ni and Cu availability through extensive hyphal network (Zaidi et al., 2006; Sheng and Xia, 2006). These fungal associations can also modify the chemical composition of root exudates and soil pH and hence heavy metal bioavailability in the soil. Chen et al. (2003) observed an enhanced Pb uptake and accumulation in Kummerowia striata, lxeris denticulate and Echinochloa crusgalli when mixed arbuscular mycorrhizal fungi (AMF) inoculums were applied. Plant growth promoting bacteria (PGPR) is another important microbial community helpful for plants to remediate heavy metal contaminated soils (Seth, 2012). These microbes can be dived as symbiotic bacteria and free living rhizobacteria (Liao et al., 2003). These bacteria may increase plant growth by various mechanisms like reduction in ethylene production under stress, nitrogen fixation and specific enzyme activity (Glick et al., 1998). These microbes have shown to alleviate the heavy metals stress/toxicity in plants. Farwell et al. (2007) observed that inoculation of Pseudomonas puteda applied to Brassica napus alleviated Cu toxicity. The use of suitable microbial inoculum may assist plant species to remediate heavy metals from soil effectively. 7.4. Use of transgenic plants Genetic engineering has played a vital role to enhance the

phytoremediation abilities of plants towards the removal or detoxification of hazardous inorganic and organic pollutants in the environment. This technique based on the over expression of specific genes involved in uptake, translocation, sequestration and plant tolerance of xenobiotic compounds in transgenic plants (Aken, 2008). The introduction of specific genes from microbes, plants and animals can be achieved using either direct DNA methods of gene transfer or Agrobacterium tumefaciensemediated transformation to develop transgenic plants (Seth, 2012). Transgenic plants for example Arabidopsis thaliana having overeexpression of gene responsible for expressing mercuric ion reductase to increase Hg tolerance and Nicotiana tabaccum having a yeast metallothionein expressing gene for tolerance against Cd were first developed for remediation of metals from soil (Rugh et al., 1998). Generally, transgenic plants are developed either to enhance immobilization or to increase plant tolerance against heavy metals to facilitate more translocation and accumulation in aboveground plant parts. Metal uptake and transport across the plasma membrane is the function of transport proteins and high affinity binding sites. Transgenic plants can be developed with better transport mechanism with higher metal tolerance to sequester more and more metals in cellular organelles with low metabolic activities like vacuoles. For example, As forms complexes with phytochelatins (PCs) and glutathione (eGSH) in vacuoles (Dhankher et al., 2002). Assuncao et al. (2010) proposed that in transgenic species Thlaspi caerulescens developed by using bacterial gene ArsC from E. Coli reduction of arsenate takes place which is an important detoxification mechanism for As. Seth, 2012 reviewed that bacterial gene merA is responsible for encoding mercuric ion reductase and merB encoding organoemercuial lyase in transgenic plants improved plant tolerance against Hg. So, it can be inferred that transgenic plants with better plant tolerance and metal sequestration ability can be successfully used for phytoremediation of metal contaminated soils. However, a better understanding of plants metal tolerance and detoxification mechanisms is very important in order to develop transgenic hyperaccumulator plants suitable for phytoextraction. Choppala et al. (2014) recently reviewed some important cellular mechanisms in higher plants governing tolerance against Cd toxicity with main objective to identify suitable strategies for Cd toxicity mitigation in higher plants. These authors beautifully presented the physiological basis of cellular mechanism like synthesis of phytochelatins (PCs), metallothiones (MTs) and other complex biomolecules in plants under Cd stress and their role to mitigate its toxic effects. But the said review has focused on the physiological basis of a single metal (Cd) and the information provided is not sufficient to fully understand metal tolerance mechanisms in order to pave way towards the development transgenic plants with improved phytoextraction of metalliferous soils. In this section, we will briefly discuss the genetic/molecular basis of plant tolerance and feasibility to transfer hyperaccumulation traits to rapidly grown high biomass producing plant species. 8. Molecular mechanisms of heavy metals tolerance in higher plants To understand molecular mechanisms of heavy metal tolerance in plants, it is necessary to have a brief background about toxic effects of these metals. Many heavy metals (e.g. Cd, Cu. Fe etc.) are transition metals and have capacity to oxidize as well as to reduce different biomolecules (e.g. GSH) and thus can disturb the harmony of redox status of plant cell (Chaffai and Koyama, 2011). These effects on redox status of cell may be further enhanced due to coupling reaction of these metals with biomolecules or other


transition metals that can regenerates their ionic state. Some other heavy metals have ability to cleave protein molecules, peptides and nucleic acids (RNAs, and DNAs) directly. So, plants regulate these metals to keep free metal ions at very low concentrations to avoid physiological damages. Such ionic homeostasis is maintained by metal uptake and translocation, metal sequestration and metal binding to proteins and organic ligands (Chaffai and Koyama, 2011). The processes of metal uptake and transport of metals to and from the cell are being regulated by many protein transporter families like ZIP (Zn and Fe regulated transport proteins) and HMA (heavy metal ATPase). Metal binding and sequestration process is controlled by metal binding proteins like Cue chaperone ATX1e like proteins, metallothioneins (MTs), phytochelatins (PCs) and some organic acids (Choppala et al., 2014). The tolerance of a plant species is determined by ion balance and homeostasis capacity which is mainly regulated by transcription and postetranslational processes where many genes are involved. These genes have been identified by molecular approaches in hypersensitive mutants of Arabidopsis thaliana (Buescher et al., 2010). 8.1. Heavy metal uptake and translocation Greater capability of metals uptake, faster and efficient translocation of heavy metals from roots to shoot and pronounced ability to sequester these heavy metals to keep their free ionic state at very low concentration are some salient traits which differentiate hyperaccumulators from heavy metals sensitive plants. Many molecular biological studies strengthen the importance of these attributes. An enhanced Zn uptake in hyperaccumulator species i.e. A. halleri and T. caerulescens roots was observed in comparison to nonehyperaccumulator species due to over expression of genes related to ZIP family encoding plasma membrane located ion ~o et al., 2010). As for as translocation of heavy transporters (Assunça metals is concerned, in comparison to heavy metals sensitive plant species tend to accumulate and sequester heavy metals after detoxification in root cell cytoplasm or vacuoles, the hyperaccumulators efficiently translocate heavy metals via xylem to the shoot (Rascio and NavarieIzzo, 2011). In a typical hyperaccumulator plant T. caerulescens the translocation of Zn was observed twice as faster as in nonehyperaccumulator plants and the root Zn concentration was observed 2e3 fold lower in T. caerulescens (Lasat et al., 2000; Yang et al., 2006). Heavy metals homeostasis is a key function of hyperaccumulators to regulate metals and metalloids within plant tissues. Genome sequencing analysis of A. thaliana has confirmed various families of transporters which are involved in homeostasis i.e. ATPases, cation diffusion facilitators (CDF) ATPebinding cassettes (ABC) copper transporters (COPTs), cation exchangers (CAXs) and ZIPs etc (Williams et al., 2000; Hall and Williams, 2003; Grotz and Guerinot, 2006). which are reported to enhance vacuolar sequestration and ultimately increase metal tolerance. Some noneessential heavy metals such as Cd are transported through noneselective channels or membrane transporters mainly responsible for transport of plant nutrients like Zn (Clemens et al., 1999). One subgroup, P1BeATPase of family HMA transporters plays a vital role in metals detoxification and is involved in transemembrane ATPedependent transport of essential as well as toxic heavy metals (Williams and Mills, 2005). Similarly, two other transporter of the same family i.e. HMA4 and HMA5 are reported to be involved in long distance root to shoot metal translocation (Verret et al., 2004). 8.2. Heavy metal sequestration/detoxification Sequestration and detoxification of heavy metals in above

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ground plant parts is a key characteristic of hyperaccumulators which defines their ability to accumulate huge concentrations of heavy metals without any toxic effect on foliage. The important locations where metal detoxification preferably are cuticle, epidermis and trichomes (Küpper et al., 2000; Robinson et al., 2003; Bidwell et al., 2004; Ma et al., 2005; Asemaneh et al., 2006; Freeman et al., 2006) with least chances of damage. The mechanisms of heavy metal detoxification in above ground plant parts are mainly governed as complexation with organic ligands, removal from metabolic sites and detoxification of ROS due to enhanced activity of antioxidant enzymes (Sarwar et al., 2010). Some important biomolecules having thiol residues such as PCs, GSH and MTs have ability to form complexes with heavy metals and thus are very important for metal detoxification in plants (Choppala et al., 2014). These complexes are thought to be in important component of tolerance mechanism. Complexes of phytochelatins with heavy metals (PCeHM) are compartmentalized in the vacuoles and are transported across the vacuolar membranes by HMT1 transporter (member of family ABC) and are firstly described in yeast (Ortiz et al., 1995). Later on it has been described that plant ABC transporters work in same way as in yeast in detoxification/ compartmentalization of toxic metals. Similarly, GSH also play their role in detoxification of heavy metals and act as strong reducing agents to protect sensitive organelles from ROS synthesized under heavy metal stress (Choppala et al., 2014). GSH are also part of GSHeascorbate pathway of mitigating H2O2 toxicity, flower development detoxification of xenobiotics and production of salicylic acid (Meister, 1995; Reichheld et al., 2007; Parisy et al., 2007; Rouhier et al., 2008). GSH can also detoxify toxic metals by forming GSHeHM complexes and sequestration in vacuoles and these complexes may be excluded to the apoplast (Li et al., 1997). Metallothiones are other low molecular weight chelating protein molecules enriched in cysteine responsible for complex formation with toxic metals (MTeHM complexes). On the basis of cysteine residues arrangement, MTs are classified into four types with distinct tissue specificity and metal element selectivity (Kotrba et al., 2009). All four types of MTs act as metal chelators. MT1 and MT2b are responsible for Cd tolerance partially (Zhou and Goldsbrough, 1994) while typee4 MTs induce Zn tolerance and accumulate higher concentration of Zn as compared to other MTs (Milner et al., 2014).

8.3. Organic acids and heavy metal tolerance Hyperaccumulators and related nonehyperaccumulators, as compared by transcriptome analyses, demonstrated that heavy metal sequestration is a genetic trait of overexpression of genes i.e. Cation diffusion facilitator family (CDF), involved in translocation of metals across the plasma membrane and/or tonoplast and are also named as MTPs (Metal Transporter Proteins). Overexpression of a gene of this family named as MTP1 localized at tonoplast, is responsible for Zn/Ni hyperaccumulation in leaves (Hammond et al., 2006). Moreover, members of MTP family may also mediate heavy metal influx to vacuole in shoot of T. goesingense (Persans et al., 2001). It might be quite interesting that detoxification of heavy metals in hyperaccumulators is not controlled by synthesis of high molecular mass organic ligands i.e. phytochelatins due to involvement of high metabolic cost and excessive amounts of sulphur in their synthesis (Schat et al., 2002). Instead, overexpression of genes related to antioxidant defense system and enhanced production of GSH principally govern the mechanism of heavy metal detoxification as antioxidant enzymes cope with ROS mediated stress caused by toxic effects of heavy metals (Van de Mortel et al., 2008).

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9. Economic evaluation of phytoremediation Unsustainable economic activities use environmental resourceseland, air, water etc.eas input in production process and give rise to negative externalities in the form of pollution and degradation of environmental resources (Champ et al., 2003). Empirical evidence shows that there is inverse relationship between environmental quality and economic growth (suggesting an inverse U relationship) and developing countries tend to use environmentally nonefriendly cheaper technologies that promote environmental degradation. The benefits of polluting activity are reaped by the rich (industrialist, urban developers etc.), while, soil contamination, being a negative externality of economic activities needs specialized tools for valuation of damages and taking remedial measures. The biggest reason for not accounting for such damages is their immediate invisibility. However, the long term consequences can result in irreversible losses to environment, human health, and income. Soil contamination due to heavy metals arises due to negative externalities arising from unsustainable industrial and agricultural practices and policy failures to properly tackle this issue. On the other hand, policy failure to properly subsidize phytoremediation initiatives, discourage positive externalities in the form of improved soil quality and future benefits to groundwater aquifer and higher land productivity. The economic costs of land degradation (and restoration using same analogy) are difficult to measure (Coxhead, 1996). This, in turn, leads to persistence of inactions and heavily damage economic and social development. The soil pollution, is a cost that may be measured by revealed preference technique that takes environment as an input in production process i.e. productivity change and health production function. Environment can also be regarded as a characteristic of market good which is reflected in variation in land prices depending on the soil health (pollution, degradation levels). The issue of land degradation is classical issue of market failure (Randall, 1983), and the political

economy of land degradation shows contribution of political and economic factors on land degradation (Blaikie and Brookfield, 1987). To address issue of market failure, different techniques are used by economists for valuation of nonemarket benefits and costs. Total Economic Value (TEV) strategy is a systematic approach for the assessment of benefits of land restoration (Fig. 3; Pagiola et al., 2004). According to this approach, direct methods of valuation consider productivity differences of a degraded and pristine soil employing market valuation methods. Production function method is the most commonly used approach. Indirect methods take into account environmental quality as an input into the production process that affect quality and price of output. From stakeholder analysis, revealed preference techniques (for example production function and hedonic price methods) estimate environmental values with respect to production and consumption choices. Whereas, stated preference techniques (for example contingent valuation and noneuse valuation methods) takes environmental benefits from hypothetical market scenarios. The noneuse valuation may take form of existence, altruistic, and bequest value (Krutilla, 1967; Krutilla and Fischer, 1975; McConnell, 1983). The value of phytoremediation depends on method of assessment, the crops to be grown on cleaned soil, value of phytoremediation biomass and speed of cleaning (Lewandowski et al., 2006). There are a variety of options available to evaluate returns on investment on phytoremediation and it is important for researchers and policy makers to consider the economic factors and evaluate the phytoremediation crops based on their potential benefits and returns to farmers and society at large. As with other pollutants, it is very difficult to regulate individual behavior. Moreover, soil contamination occurs both due to on-site and offesite practices due to runeoff water from neighboring fields, industry and municipality sewage etc. In this situation, the needed investment to clean soils may be raised through imposing pollution tax on the responsible agency. The contamination can be stopped through proper awareness to farmers about long run

Total Economic Value of PhytoremediaƟon

Non-use Value

Use Value

Potential Benefits of Phytoremediation

Direct Use

Indirect Use

OpƟon Value

For producƟon of goods that can be directly consumed or sold

Contribute to other services that have direct market value

To be used for future and intangible benefits

Crop ProducƟon Forage ProducƟon

Biomass for bio-energy Groundwater quality Soil Quality

Valuation Techniques

ProducƟon FuncƟon Technique to measure change in value of output

Clean Soils Community Integrity Poverty alleviaƟon

Existence

AltruisƟc

Bequest

Knowledge about existence of producƟve resource

Knowledge of consumpƟon of use by current generaƟon

Knowledge of passing resource to future generaƟon

Cultural Value Family Inheritance Sense of land ownership

ProducƟve land for social status Land’s collateral value

Non Market ValuaƟon Methods 1. Revealed Preference Methods (e.g. Hedonic Pricing) 2. Stated Preference Method (e.g. ConƟngent ValuaƟon)

Fig. 3. Economic valuation of phytoremediation (adopted from Pagiola et al., 2004).

Inheritance Sense of IntergeneraƟonal Economic security


impacts of contamination and through government regulation on industries and municipalities to take sole responsibility of cleaning their wastes before releasing from factory. The economic solutions to overcome negative externalities include imposing a tax per unit of degradation or pollution (Pigou, 1920), or a mutually beneficial market solution by the involved parties (Coase, 1960). Baumol and Oates (1988) suggested a twoestage approach to understand marginal damages and socially optimal output i.e. setting ambient standards based on research, and as a second step set solution in the form of charges or permits to limit pollution. It is also hard fact that the positive externalities arising from such interventions are not brought into financial calculations. The United Nations Conference on Environment and Development (UNCED, 1992) has emphasized on use of market instruments to overcome environmental problems (Najam, 1995). The policy makers, under UNCED guidelines, should tax the polluters and subsidize the cleaning technologies like phytoremediation to avert pollution problem. The economic viability of the phytoremediation technologies must consider multifunctional and sustainable alternative to conventional alternative technologies. Any technological intervention without considering economic and human dimensions doomed to failure due to lack of acceptance by end users. Therefore, economic viability, social acceptability and environmental suitability are preerequisites for success of any phytoremediation prescription. 10. Conclusions and future perspectives Heavy metal contamination of agricultural soils is a major environmental and health concern of today due to potential risk of food chain contamination and other associated health risks. In this situation, phytoremediation techniques may prove as important tool to tackle the problem as other physical and chemical approaches to decontaminate the polluted soils seems economically unfeasible and time consuming with less effective results. Hyperaccumulator plants can be effectively used to extract and harvest large concentrations of deleterious metals as well as other inorganic and organic pollutants from soil. But traditional phytoremediation approaches are less economical to be applied on large scales as naturally occurring hyperaccumulators are generally slow growing and produce relatively less harvestable aboveground biomass production. So genetic engineering approach to develop transgenic plants with characters of high biomass production, more metal accumulation, tolerance against metal toxicity and well adapted to a variety of climatic conditions, might be more beneficial in this respect. Some other recent phytoremediation approaches like chemical assisted phytoextraction and microbial assisted phytoremediation techniques may also be used to decontaminate polluted soils on large scales. Further research is needed in the field of genetic engineering to improve the phytoremediation abilities of transgenic plants, and to understand the mechanisms and effectiveness of phytoremediation techniques in order to make these technologies more effective, time saving and economically feasible. Conflict of interest and assurance All the authors have no any conflict of interest. We assured that no human being or animal was used for experimental purpose in the study. References Ahmad, N., Imran, M., Marral, M.W.R., Mubashir, M., Butt, B., 2016. Influence of biochar on soil quality and yield related attributes of wheat (Triticum aestivum L.). J. Environ. Agric. Sci. 7, 68e72.

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Aken, B.V., 2008. Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Trend Biotech. 26, 225e237. Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metalseConcepts and applications. Chemosphere 91, 869e881. Ali, H., Naseer, M., Sajad, M.A., 2012. Phytoremediation of heavy metals by Trifolium alexandrinum. Int. J. Environ. Sci. 2, 1459e1469. Asemaneh, T., Ghaderian, S.M., Crawford, S.A., Marshall, A.T., Baker, A.J.M., 2006. Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta 225, 193e202. Assunç~ ao, A.G., Herrero, E., Lin, Y.F., Huettel, B., Talukdar, S., Smaczniak, C., Aarts, M.G., 2010. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc. Nat. Acad. Sci. 107, 10296e10301. Awofolu, O., 2005. A survey of trace metals in vegetation, soil and lower animal along some selected major roads in metropolitan city of Lagos. Environ. Monit. Assess. 105, 431e447. Baker, A.J.M., Reeves, R.D., Hajar, A.S.M., 1994. Heavy metal accumulation and tolerance in british populations of the metallophyte Thlaspicaerulescens J and C Presl (Brassicaceae). New Phytol. 127, 61e68. Bani, A., Pavlova, D., Echevarria, G., Mullaj, A., Reeves, R.D., Morel, J.L., Sulce, S., 2010. Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot. Serb 34, 3e14. Baumol, W., Oates, W.E., 1988. Theory of Environmental Policy. Cambridge University Press. Bidwell, S.D., Crawford, S.A., Woodrow, I.E., Sommer-Knudsen, J., Marshall, A.T., 2004. Subecellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell. Environ. 27, 705e716. Blaikie, P., Brookfield, H., 1987. Land Degradation and Society, p. 299. London and New York: Methuen. Brown, S.L., Chaney, R.L., Angle, J.S., Baker, A.J.M., 1995. Zinc and cadmium uptake of Thlaspi caerulescens grown in nutrient solution. Soil Sci. Soc. Am. J. 59, 125e133. Buescher, E., Achberger, T., Amusan, I., Giannini, A., Ochsenfeld, C., Rus, A., Lahner, B., Hoekenga, O., Yakubova, E., Harper, J.F., Guerinot, M.L., Zhang, M., 2010. Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLOS One 5, 11081e11081. Cantrell, K.B., Hunt, P.G., Uchimiya, M., Novak, J.M., Ro, K.S., 2012. Impact of pyrolysis temperature and manure source on physicochemical characteristics of biochar. Bioresour. Tech. 107, 419e428. Chaffai, R., Koyama, H., 2011. Heavy metal tolerance in Arabidopsis thaliana. Adv. Bot. Res. 60, 1e49. Champ, P.A., Boyle, K.J., Brown, T.C., 2003. A Primer on Nonmarket Valuation. Kluwer Academic Publishers, Boston. Chaney, R.L., 1983. Plant uptake of inorganic waste constituents. In: Parr, J.F.E.A. (Ed.), Land Treatment of Hazardous Wastes. Noyes Data Corp, Park Ridge, NJ, pp. 50e76. Chaney, R.L., Malik, M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S., Baker, A.J.M., 1997. Phytoremediation of soil metals. Curr. Opin. Biotech. 8, 279e284. Chen, B.D., Li, X.L., Tao, H.Q., Christie, P., Wong, M.H., 2003. The role of arbuscular mycorrhizal in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50, 839e846. Choppala, G., Saifullah, Bolan, N., Bibi, S., Iqbal, M., Rengel, Z., Kunhikrishnan, A., Ok, Y.S., 2014. Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit. Rev. Plant Sci. 33, 374e391. Clemens, S., Kim, E.J., Neumann, D., Schroeder, J.L., 1999. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 18, 3325e3333. Coase, R., 1960. The problem of social cost. J. Law Econ. 3, 1e44. Coxhead, I., 1996. Economic Modeling of Land Degradation in Developing Countries. Agricultural and Applied Economics Staff Paper Series. University of WisconsineMadison, USA. Czarnecki, S., Düring, R.A., 2015. Influence of longeterm mineral fertilization on metal contents and properties of soil samples taken from different locations in Hesse, Germany. Soil 1, 23e33. Dhankher, O.P., Li, Y.J., Rosen, B.P., Shi, J., Salt, D., Senecoff, J.F., Sashti, N.A., Meagher, R.B., 2002. Engineering tolerance and hyperaccumulation of arsenic in plants bycombining arsenate reductase and geglutamylcysteine synthase expression. Nat. Biotech. 20, 1140e1150. Ekmekci, Y., Tanyolac, D., Ayhan, B., 2008. Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J. Plant Physiol. 165, 600e611. Elad, Y., Cytryn, E., Harel, Y.M., Lew, B., Graber, E.R., 2012. The biochar effect: plant resistance to biotic stresses. Phytopathol. Mediterr. 50, 335e349. Erakhrumen, A.A., 2007. Phytoremediation: an environmentally sound technology for pollution prevention, control and remediation in developing countries. Educ. Res. Rev. 2, 151e156. Fageria, N.K., Baligar, V.C., Clark, R.B., 2002. Micronutrients in crop production. Adv. Agron. 77, 185e268. Fageria, N.K., Filho, M.P.B., Moreira, A., Guimaraes, C.M., 2009. Foliar fertilization of crop plants. J. Plant Nut 32, 1044e1064. Farwell, A.J., Vesely, S., Nero, V., Rodriguez, H., McCormack, K., Shah, S., Dixon, D.G., Glick, B.R., 2007. Tolerance of transgenic canola plants (Brassica napus) amended with plant growth promoting bacteria to flooding stress at a metal contaminated field site. Environ. Poll. 147, 540e545. Fellet, G., Marmiroli, M., Marchiol, L., 2014. Elements uptake by metal accumulator

720


species grown on mine tailings amended with three types of biochar. Sci. Total Environ. 468, 598e608. Freedman, B., Hutchinson, T.C., 1981. Sources of metal and elemental contaminants of terrestrial environments. In: Lepp, N.W. (Ed.), Effect of Heavy Metal Pollution on Plants: Metals in the Environment, vol. II. Applied Science Publishers, London and New Jersey, pp. 35e94. Freeman, J.L., Zhang, L.H., Marcus, M.A., Fakra, S., McGrath, S.P., PiloneSmits, E.A., 2006. Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol. 142, 124e134. GarciaeSalgado, S., GarciaeCasillas, D., QuijanoeNieto, M.A., BonillaeSimon, M.M., 2012. Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water Air Soil Pollut. 223, 559e572. Ghosh, M., Singh, S.P., 2005. A review on phytoremediation of heavy metals and utilization of it’s by products. Asian J. Energy Environ. 6, 214e231. Glick, B.R., Penrose, D.M., Li, J., 1998. A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J. Theor. Biol. 190, 63e68. Greipsson, S., 2011. Phytoremediation. Nat. Educ. Knowl. 2, 7. Grotz, N., Guerinot, M.L., 2006. Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica Biophysica Acta. (BBA)eMol. Cell. Res. 1763, 595e608. Hall, J.L., Williams, L.E., 2003. Transition metal transporters in plants. J. Exp. Bot. 54, 2601e2613. Hammond, J.P., Bowen, H.C., White, P.J., Mills, V., Pyke, K.A., Baker, A.J., Broadley, M.R., 2006. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol. 170, 239e260. Harter, R.D., Naidu, R., 2001. An assessment of environmental and solution parameter impact on traceemetal sorption by soil. Soil Sci. Soc. Am. J. 65, 597e612. He, J., Ren, Y., Pan, X., Yan, Y., Zhu, C., Jiang, D., 2010. Salicylic acid alleviates the toxicity effect of cadmium on germination, seedling growth, and amylase activity of rice. J. Plant Nutr. Soil Sci. 173, 300e305. He, Z.L., Yang, X.E., StoVella, P.J., 2005. Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 19, 125e140. Hess, R., Schmid, B., 2002. Zinc supplement overdose can have toxic effects. J. Paediatr. Haematol. Oncol. 24, 582e584. Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F., Cobbett, C.S., 2004. Petype ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell. 16, 1327e1339. Imran, M., Kanwal, S., Hussain, S., Maqsood, M.A., Aziz, T., 2015. Efficacy of zinc application methods for concentration and estimated bioavailability of zinc in grains of rice grown on a calcareous soil. Pak. J. Agric. Sci. 52, 169e175. Imran, M., Rehim, A., 2016. Zinc fertilization approaches for agronomic biofortification and estimated human bioavailability of zinc in maize grain. Arch. Agron. Soil Sci. http://dx.doi.org/10.1080/03650340.2016.1185660. Imran, M., Rehim, A., Hussain, S., Zafar ul Hye, M., Rehman, H.U., 2016a. Efficiency of zinc and phosphorus applied to open-pollinated and hybrid cultivars of maize. Int. J. Agric. Biol. http://dx.doi.org/10.17957/IJAB/15.0239. Imran, M., Rehim, A., Sarwar, N., Hussain, S., 2016b. Zinc bioavailability in maize grains in response of phosphorousezinc interaction. J. Plant Nutr. Soil Sci. 179, 60e66. Jeffery, S., Verheijen, F.G.A., Van DerVelde, M., Bastos, A.C., 2011. A quantitative review of the effects of biochar application to soils on crop productivity using metaeanalysis. Agric. Ecosyst. Environ. 144, 175e187. Jung, M.C., 2008. Heavy metal concentration in soils and factors affecting metal uptake by plants in the vicinity of a Korean CueW mine. Sensors 8, 2413e2423. Kalve, S., Sarangi, B.K., Pandey, R.A., Chakrabarti, T., 2011. Arsenic and chromium hyperaccumulation by an ecotype of Pterisvittataeprospective for phytoextraction from contaminated water and soil. Curr. Sci. 100, 888e894. Khan, M.A., Ahmad, I., Rahman, I., 2007. Effect of environmental pollution on heavy metals content of with aniasomnifera. J. Chin. Chem. Soc. 54, 339e343. Kotrba, P., Najmanova, J., Macek, T., Ruml, T., Mackova, M., 2009. Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotech. Adv. 27, 799e810. Kr€ amer, U., 2010. Metal hyperaccumulation in plants. Ann. Rev. Plant Biol. 61, 517e534. Krutilla, J.V., 1967. Conservation reconsidered. Am. Econ. Rev. 57, 777e786. Krutilla, J.V., Fischer, A.C., 1975. The Economics of Natural Environments. Resources for the Future. The John Hopkins Press, Baltimore. Küpper, H., Lombi, E., Zhao, F.J., McGrath, S.P., 2000. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212, 75e84. Lasat, M.M., Pence, N.S., Garvin, D.F., Ebbs, S.D., Kochian, L.V., 2000. Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J. Exp. Bot. 51, 71e79. Lewandowski, I., Schmidt, U., Londo, M., Faaij, A., 2006. The economic value of the phytoremediation function assessed by the example of cadmium remediation by willow (Salix ssp). Agric. Syst. 89, 68e89. Li, Y.M., Chaney, R., Brewer, E., Roseberg, R., Angle, J.S., Baker, A., Reeves, R., Nelkin, J., 2003. Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249, 107e115. Li, Z.S., Lu, Y.P., Zhen, R.G., Szczypka, M., Thiele, D.J., Rea, P.A., 1997. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1ecatalyzed transport of bis (glutathionato) cadmium. Proc. Natl. Acad. Sci. 94, 42e47. Liao, J.P., Lin, X.G., Cao, Z.H., Shi, Y.Q., Wong, M.H., 2003. Interactions between

arbuscular mycorrhizae and heavy metals under a sand culture experiment. Chemosphere 50, 847e853. Liu, X., Zhang, A., Ji, C., Joseph, S., Bian, R., Li, L., PazeFerreiro, J., 2013. Biochar’s effect on crop productivity and the dependence on experimental conditions a metaeanalysis of literature data. Plant soil 373, 583e594. Lu, H., Zhang, W., Yang, Y., Huang, X., Wang, S., Qiu, R., 2012. Relative distribution of Pb2þ sorption mechanisms by sludgeederived biochar. Water Res. 46, 854e862. Ma, J.F., Ueno, D., Zhao, F.J., McGrath, S.P., 2005. Subcellular localisation of Cd and Zn in the leaves of a Cdehyperaccumulating ecotype of Thlaspi caerulescens. Planta 220, 731e736. Mahmoud, E., Abd El-Kader, N., 2014. Heavy metal immobilization in contaminated soils using phosphogypsum and rice straw compost. Land Degrad. Dev. http:// dx.doi.org/10.1002/ldr.2288. Malik, R.N., Husain, S.Z., Nazir, I., 2010. Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad. Pak. Pak. J. Bot. 42, 291e301. McConnell, K., 1983. Existence and bequest value. In: Rowe, R., Chestnut, L. (Eds.), Managing Air Quality and Scenic Resources at National Parks and Wilderness Areas. Westview Press, Boulder. Meister, A., 1995. Glutathione metabolism. Methods Enzym. 251, 3e7. Memon, A.R., Aktoprakligil, D., Ozdemir, A., Vertii, A., 2001. Heavy metal accumulation and detoxification mechanisms in plants. Tur. J. Bot. 25, 111e121. €der, P., 2009. Implications of metal accumulation mechanisms to Memon, A.R., Schro phytoremediation. Environ. Sci. Poll. Res. 16, 162e175. ~ eros, M., Kochian, L.V., 2014. Molecular and Physiological MechaMilner, M.J., Pin nisms of Plant Tolerance to Toxic Metals. Plant Abiotic Stress, second ed., pp. 179e201 Mortvedt, J.J., Beaton, J.D., 1995. Heavy metal and radionuclide contaminants in phosphate fertilizers. In: Tiessen, H. (Ed.), Phosphorus in the Global Environment: Transfer, Cycles and Management. Wiley, New York, pp. 93e106. Najam, A., 1995. An environmental negotiation strategy for the South. Int. Environ. Aff. 7, 249e287. Ortiz, D.F., Ruscitti, T., McCue, K.F., Ow, D.W., 1995. Transport of metalebinding peptides by HMT1, a fission yeast ABCetype vacuolar membrane protein. J. Biol. Chem. 270, 4721e4728. Pagiola, S., Ritter, K., Bishop, J.T., 2004. How Much Is an Ecosystem Worth? Assessing the Economic Value of Conservation. The International Bank for Reconstruction, Washington, DC. Parisy, V., Poinssot, B., Owsianowski, L., Buchala, A., Glazebrook, J., Mauch, F., 2007. Identification of PAD2 as a g-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 49, 159e172. ndez, A., Gasco , G., 2014. Use of phytoremediation PazeFerreiro, J., Lu, H., Fu, S., Me and biochar to remediate heavy metal polluted soils: a review. Solid Earth. 5, 65e75. Pereira, B.F.F., DeeAbreu, C.A., Herpin, U., DeeAbreu, M.F., Berton, R.S., 2010. Phytoremediation of lead by jack beans on a rhodic hapludox amended with EDTA. Sci. Agric. 67, 308e318. Persans, M.W., Nieman, K., Salt, D.E., 2001. Functional activity and role of cationeefflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc. Nat. Acad. Sci. 98, 9995e10000. Pigou, A.C., 1920. The Economics of Welfare. Macmillan, London. Popova, L.P., Maslenkova, L.T., Ivanova, A., Stoinova, Z., 2012. Role of salicylic acid in alleviating heavy metal stress. In: Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, New York, pp. 447e466. Popova, L.P., Maslenkova, L.T., Yordanova, R.Y., Ivanova, A.P., Krantev, A.P., Szalai, G., 2009. Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem. 47, 224e231. Presser, T.S., 1994. Geologic origin and pathways of selenium from the California coast ranges to the westecentral San Joaquin valley. Selenium Environ. 139e155. Rai, P.K., 2008. Phytoremediation of Hg and Cd from industrial effluents using an aquatic free floating macrophyte Azollapinnata. Int. J. Phytoremediation 10, 430e439. Randall, A., 1983. The problem of market failure. Nat. Resour. J. 23, 131e148. Rascio, N., NavarieIzzo, F., 2011. Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci. 180, 169e181. Rehim, A., ZafareuleHye, M., Imran, M., Ali, M.A., Hussain, M., 2014. Phosphorus and zinc application improves rice productivity. Pak. J. Sci. 66, 134e139. Reichheld, J.P., Khafif, M., Riondet, C., Droux, M., Bonnard, G., Meyer, Y., 2007. Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell. Online 19, 1851e1865. Robinson, B.H., Leblanc, M., Petit, D., Brooks, R.R., Kirkman, J.H., Gregg, P.E.H., 1998. The potential of Thlaspicaerulescens for phytoremediation of contaminated soils. Plant Soil 203, 47e56. Robinson, B.H., Lombi, E., Zhao, F.J., McGrath, S.P., 2003. Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol. 158, 279e285. Rouhier, N., Lemaire, S.D., Jacquot, J.P., 2008. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu. Rev. Plant Biol. 59, 143e166. Roy, M., McDonald, L.M., 2013. Metal uptake in plants and health risk assessments

N. Sarwar et al. / Chemosphere 171 (2017) 710e721 in metal-contaminated smelter soils. Land Degrad. Dev. http://dx.doi.org/ 10.1002/ldr.2237. Rugh, C.L., Seueoff, J.F., Meagher, R.B., Merkle, S.A., 1998. Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotech. 16, 925e928. Saifullah, Meers, E., Qadir, M., DeeCaritat, P., Tack, F.M.G., Laing, G.D., Zia, M.H., 2009. Chemosphere 74, 1279e1291. Saifullah, Sarwar, N., Bibi, S., Ahmad, M., Ok, Y.S., 2014. Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L. Environ. Earth Sci. 71, 1663e1672. Salem, H.M., Eweida, E.A., Farag, A., 2000. Heavy Metals in Drinking Water and Their Environmental Impact on Human Health. ICEHM2000. Cairo University, Egypt, pp. 542e556. Salt, D.E., Rauser, W.E., 1995. MgeATP dependent transport of phytochelatins across tonoplast of oat roots. Plant Physiol. 107, 1293e1301. Sarwar, N., Ishaq, W., Farid, G., Shaheen, M.R., Imran, M., Geng, M., Hussain, S., 2015. Zincecadmium interactions: impact on wheat physiology and mineral acquisition. Ecotox. Environ. Saf. 122, 528e536. Sarwar, N., Saifullah, Malhi, S.S., Zia, M.H., Naeem, A., Bibi, S., Farid, G., 2010. Role of plant nutrients in minimizing cadmium accumulation by plant. J. Sci. Food Agric. 90, 925e937. Schat, H., Llugany, M., Vooijs, R., HartleyeWhitaker, J., Bleeker, P.M., 2002. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and nonehyperaccumulator metallophytes. J. Exp. Bot. 53, 2381e2392. Seth, C.S., 2012. A review on mechanisms of plant tolerance and role of transgenic plants in environmental cleaneup. Bot. Rev. 78, 32e62. Seth, C.S., Chaturvedi, P.K., Misra, V., 2007. Toxic effect of arsenic and cadmium alone and in combination on Giant duckweed (Spirodela polyrrhiza L.) in response to its accumulation. Environ. Toxicol. 22, 539e549. Shabani, N., Sayadi, M.H., 2012. Evaluation of heavy metals accumulation by two emergent macrophytes from the polluted soil: an experimental study. Environmentalist 32, 91e98. Shaheen, M.R., Ayyub, C.M., Amjad, M., Waraich, E.A., 2015. Morpho-physiological evaluation of tomato genotypes under high temperature stress conditions. J. Sci. Food Agric. http://dx.doi.org/10.1002/jsfa.7388. Sheng, X.F., Xia, J.J., 2006. Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmiumeresistant bacteria. Chemosphere 64, 1036e1042. Souza, L.A., Piotto, F.A., Nogueirol, R.C., Azevedo, R.A., 2013. Use of nonehyperaccumulator plant species for the phytoextraction of heavy metals using chelating agents. Sci. Agric. 70, 290e295. Sun, Y., Zhou, Q., Xu, Y., Wang, L., Liang, X., 2011. The role of EDTA on cadmium phytoextraction in a cadmiumehyperaccumulator Rorippa globosa. J. Environ. Chem. Ecotoxicol. 3, 45e51. Tariq, M., Ali, M., Shah, Z., 2006. Characteristics of industrial effluents and their possible impacts on quality of underground water. Soil Environ. 25, 64e69. Thornton, I., 1981. Geochemical aspects of the distribution and forms of heavy metals in soils. In: Lepp, N.W. (Ed.), Effect of Heavy Hetal Pollution on Plants: Metals in the Environment, vol. II. Applied Science Publishers, London and New

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Jersey, pp. 1e34. Tong, Y.P., Kneer, R., Zhu, Y.G., 2004. Vacuolar compartmentalization: a second generation approach to engineering plants for phytoremediation. Trends Plant Sci. 9, 7e9. Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., Maathuis, F.J.M., 2007. Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotech. 25, 158e165. UNCED, United Nations Convention on Environment and Development, 1992. Agenda 21. Rio de Janerio, Brazil, 3e14 June, 1992. VanedeeMortel, J.E., Schat, H., Moerland, P.D., Themaat, E.V.L., Ent, S., Blankestijn, H., Aarts, M.G., 2008. Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cdehyperaccumulator Thlaspi caerulescens. Plant Cell. Environ. 31, 301e324. Verkleij, J.A.C., GolaneGoldhirsh, A., Antosiewisz, D.M., Schwitzguebel, J.P., Schroder, P., 2009. Dualities in plant tolerance to pollutants and their uptake and translocation to the upper plant parts. Environ. Exp. Bot. 67, 10e22. Verret, F., Gravot, A., Auroy, P., Leonhardt, N., David, P., Nussaume, L., Richaud, P., 2004. Overexpression of AtHMA4 enhances rootetoeshoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 576, 306e312. Wang, H.Q., Zhao, Q., Zeng, D.H., Hu, Y.L., Yu, Z.Y., 2015. Remediation of a magnesium-contaminated soil by chemical amendments and leaching. Land Degradation and Development. http://dx.doi.org/10.1002/ldr.2362. Webber, J., 1981. Trace metals in agriculture. In: Lepp, N.W. (Ed.), Effect of Heavy Metal Pollution on Plants: Metals in the Environment, vol. II. Applied Science Publishers, London and New Jersey, pp. 159e184. Williams, L.E., Mills, R.F., 2005. P 1BeATPasesean ancient family of transition metal pumps with diverse functions in plants. Trends plant sci 10, 491e502. Williams, L.E., Pittman, J.K., Hall, J.L., 2000. Emerging mechanisms for heavy metal transport in plants. Biochimica Biophysica Acta (BBA)eBiomembranes 1465, 104e126. Wu, F.B., Chen, F., Wei, K.G., Zhang, P., 2004. Effects of Cadmium on free amino acids, glutathione, and ascorbic acid concentration in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57, 447e454. Wu, W., Yang, M., Feng, Q., McGrouther, K., Wang, H., Lu, H., Chen, Y., 2012. Chemical characterization of rice strawederived biochar for soil amendment. Biomass bioenergy 47, 268e276. Xu, J., Yin, H.X., Li, X., 2009. Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell. Rep. 28, 325e333. Yang, X., Li, T., Yang, J., He, Z., Lu, L., Meng, F., 2006. Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance. Planta 224, 185e195. Zaidi, S.S., Usmani, B.R., Singh, M.J., 2006. Significance of Bacillus subtilis strain SJe101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64, 991e997. Zhou, J., Goldsbrough, P.B., 1994. Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell. Online 6, 875e884.