Keywords

Introduction

In recent years, trace element contamination in agriculture has become a serious issue as a result of anthropogenic activities, such as intensive use of element-enriched agrochemicals, wastewater irrigation, and industrial or mining activities (Ding et al. 2018). According to the results of Alexakis et al. (2019), the most bioavailable element in soil was Cd, while Cu, Co, and Zn presented average percentages. Nickel, chromium, and manganese are somewhat immobile and have the highest abundance in the residual fraction. This illustration could pose a limited threat to the quality of crops. Cadmium is the chief with moderate potential ecological risk (Alexakis et al. 2019). Sensitivity to metals varies no longer only among plant species but additionally among varieties, clones, and populations, in nontoxic levels of metals (Österås et al. 2000; Witters et al. 2009). Phytoremediation of heavy metals by plants is a promising new technology for remediation of heavy metal-contaminated sites (Gómez et al. 2019). The success of the phytoremediation depends upon the identification of suitable plant species that hyperaccumulate heavy metals and produce large amounts of biomass (Tangahu et al. 2011). This review discusses the factors influencing the performance of phytoremediation and provides some improvement to enhance the phytoremediation efficiency in order to provide a scientific base for a wide commercial application of this technology.

Potentially Toxic Elements

There are two major classes of contaminants: organic and inorganic (Fig. 15.1). Unlike inorganic contaminants, the organic pollutants are relatively less toxic to plants because of being less reactive and accumulative (Dietz and Schnoor 2001). Elevated concentrations of the heavy metals that are essential for the life of plants cause toxicity of plants, animals, and humans and induce inhibition of various processes in plant metabolism (Hendrik et al. 2007). Potentially toxic elements, especially heavy metals, can also be emitted from terrestrial or aquatic ecosystems into the atmosphere (Göhre and Paszkowski 2006). They are grouped into one category of 53 elements with a specific weight higher than 5 g cm−3, and they can enter the cell via nonspecific transporters at high concentrations. Nonessential elements can enter the root via passive diffusion, but also using low-affinity metal transporter with broad specificity (Göhre and Paszkowski 2006). To survive with all, plants develop diverse detoxification mechanisms within their system (Chatterjee et al. 2013). Partitioning throughout the plant organism and cellular homeostasis of essential heavy metals must be well controlled to avoid deficiency as well as excess (Göhre and Paszkowski 2006).

Fig. 15.1
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Two classes of contaminants

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The available concentration of metals is important regarding their uptake and accumulation in the plant rather than a total metal concentration in soil. The metal concentration and availability of metals for plants that can be affected by several factors are provided in Fig. 15.2. Agronomical practices are advanced to improve remediation, e.g., redox potential, conductivity, fertilizers, organic carbon content, addition of chelators, pH, and granulometric composition (Tangahu et al. 2011). For example, high pH of soil due to sludge application causes suboptimal conditions for the uptake of Cu, Zn, and Pb, so metal burdens are not extreme and present no significant association to soil metal concentrations (Pulford and Watson 2003). Chelators consisting of organic acids, siderophores, and phenolics may increase the bioavailability of metal cations from soil particles, and then help to translocate them through the xylem. The chelated metal can be translocated upwards in the xylem without a high cation-exchange capacity (Stanley Rungwa et al. 2013). By decreasing the pH around the root, organic acids such as malate and citrate increase the bioavailability of metal cations as metal chelators (Cherian and Oliveira 2005). However, organic acids can hinder metal uptake from a complex with the heavy metal outside of root. For example, citrate inhibits the aluminum uptake and resulting Al tolerance in some plant species (Papernik et al. 2001). Moreover, different elements, as soil fertility, may progress the resistance to the metal (Vervaeke et al. 2003).

Fig. 15.2
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The metal concentration and availability of metals for plants

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Identification of Phytoremediation

Various physical, chemical, and biological techniques are being used to remove heavy metals and metalloids from soils (Sarwar et al. 2017). Remediation technologies of soil contaminated by heavy metals are shown in Fig. 15.3. The research of remediation technologies is still in the individual and experimental stage. However, nonbiological difficult and expensive techniques are not fully accepted as they destroy the biotic components of soil and are technically difficult and expensive to implement (Parmar et al. 2013). Then the future remediation technologies should be green and environmental friendly biological remediation, combining remediation and in situ remediation, based on equipped completely quick remediation, and supplying technicality (Yao et al. 2012), in which the plant root system is capable of removing, transferring, stabilizing, and destroying contaminants in soil and sediment (Fig. 15.4) (Capuana 2011; Chatterjee et al. 2013). Different phytotechnologies have already been put into practice, and each one uses different plants or plant properties (Ellis et al. 2006).

Fig. 15.3
figure 3

Different remediation technologies for heavy metal-contaminated soil. Biological remediation: changing physical and chemical characterizations of heavy metals by microorganisms; phytostabilization: establishing a plant cover on the contaminated soil surface; rhizo-filtration: adsorb or uptake pollutants in roots of plants; phytoaccumulation: uptake and accumulation of metal contaminants in stems and leaves; phytovolatilization: absorbing contaminants and volatilizing into the atmosphere; animal remediation: inhibiting heavy metal toxicity by degrading and migrating some lower animals adsorbing heavy metals

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Fig. 15.4
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Processes of phytoremediation technique

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Plant Species in Different Polluted Sites

As mentioned previously (Fig. 15.2), the element concentrations in plants and substrate were different for plant species. On the other hand, plant species that grow in the same site accumulate different concentrations of heavy metals in the same plant organ (Milić et al. 2012), which is governed by their growth rate and ability to translocate metals to the aboveground tissue. The phytoremediation technique’s capacities for various metals have been tested in different plant species. Hyperaccumulators are considered to be herbaceous or woody plants that are able to accumulate potentially phytotoxic elements to concentrations of 50–500 times higher than nonhyperaccumulator plants without obvious symptoms (Cherian and Oliveira 2005; Liu et al. 2019).

Woody Plants for Remediation

Wood is an important sink for biologically available metals, with additional sink tissue being formed in each growing season. These tissues are slow to enter the decomposition cycle, and also will be immobilized in a metabolically inactive compartment for a duration of time (Pulford and Watson 2003). Trees appear as potentially interesting candidates since they can stay on the site for several years without new plantings with a more developed root system (Saladin 2015). The 140 woody species included approximately 20% of hyperaccumulators. Furthermore, woody species known as hyperaccumulators are mainly localized in tropical areas, but it is not optimal for heavy metal extraction. Using rapid-growing tree species (willow or poplar) (Konlechner et al. 2013), large biomass, more extensive root systems, woody metal-accumulating species, plant enzymes exuded from the roots, and the ability to accumulate microelements and stabilize soil surface would increase the efficiency of the phytoextraction method, making it economically possible (Gómez et al. 2019; Konlechner et al. 2013; Marmiroli et al. 2011). Resistant woody plants with exclusion strategy relate to decreasing metal uptake, superior storage in root vacuoles, and constrained translocation into shoots (Marmiroli et al. 2011). However, the information about the responses of plants to metal toxicity in trees is scarce (Sebastiani et al. 2004; Dadea et al. 2017).

The genetically incredible variable Salicaceae family with its genera Populus (poplars) and Salix (willows) includes a vast majority species and hybrids of exotic woody trees and shrubs (Table 15.1). Although poplars are identified to absorb numerous inorganic pollutants such as Se, Cd, and Zn, their heavy metal tolerance is limited (Bañuelos et al. 1999; Dietz and Schnoor 2001). Some poplar or willow varieties transfer As, Cd, Pb, and Zn to aboveground plant tissues (Fischerová et al. 2006), and had been affected greater through the properties of clones than with the aid of the soil properties (Kacálková et al. 2015). Cadmium, zinc, and copper removal positively correlated with biomass production. Poplars allow several cycles of decontamination, and the contaminated biomass appreciably decreased through incineration (Bittsánszky et al. 2005). Removal of zinc, cadmium, and copper by Salix smithiana is the highest regardless of the site (Kacálková et al. 2015).

Table 15.1 Tree species potential in phytoremediation technique under different polluted sites
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Because of easy development from cuttings and excessive growth rates of willows, they may be well proper both for checking out metallic bioavailability and for accumulation, which may be mixed with energy production from biomass (Bedell et al. 2009). Moreover, besides leaves, willow stem also appeared to be successful cadmium accumulators. Accumulation rates of zinc and cadmium had been excessive until 36 months, which means that willows are successful accumulators of these metals in any such timescale (Tőzsér et al. 2017). Willows have a better Cd tolerance than poplars. Six different willows (S. smithiana, S. babylonica, S. matsudana x alba, S. caprea, S. dasyclados, S. purpurea) in comparison with two poplar species (P. tremula, P. nigra) showed that S. smithiana leaves accumulate the highest cadmium concentration (Vaculík et al. 2012). At the opposing level, poplar species have been capable of removing a more significant part of Pb as different from the other species. However, the removed part was a small volume. Different accumulation of observed elements in plant biomass depends appreciably on the accessibility of those factors inside the soil. Particular detail concentrations have been determined with the aid of inorganic salt solution extraction in natural soil solution (Fischerová et al. 2006).

Distinct willow species have adopted one of the primary techniques for growing metal tolerance: metal accumulation and metal exclusion. Metal exclusion, which includes avoiding metal uptake and limiting metallic transport to leaves, is commonly utilized by pseudometallophytes. True metallophytes merely grow on naturally metal-rich and/or metal-contaminated soils (Bedell et al. 2009). Metal uptake and accumulation have been no longer related to tolerance, and there is evidence of each general tolerance to some of the exclusive metals and particular tolerance to at least one heavy metal (Pulford and Watson 2003). For example, Salix viminalis can grow in soil contaminated with 500 Pb, 3300 Zn, and 1400 Cu mg kg−1 (Jensen et al. 2009), and with 555 Cu, 1.8 Cd, and 620 Zn mg kg−1 (Rosselli et al. 2003). The genera Betula and Acer are intensively recognized to have heavy metallic resistance. Betula has been found to increase a constitutive, genetically determined resistance, whereas the best phenotypic plasticity has been determined in Acer (Kirkey et al. 2012).

Nonwoody Plants for Remediation

Hyperaccumulation

Hyperaccumulators can take up hundreds or even thousands of times higher concentrations of particular heavy metals than most plants (Moray et al. 2015; Ali et al. 2013) and are the optimal choice for the development of environmental technologies for the remediation of metal-contaminated soils. Hyperaccumulators display four main features: (a) accumulation, (b) enrichment, (c) translocation, and (d) tolerance. They cannot be managed as a conventional crop; they often have low biomass and can have a short life cycle (Gisbert et al. 2014).

Several species of hyperaccumulator plants are actually used for phytoextraction of Ni, Co, Mn, Cu, and Cd (Table 15.2). Most reported plants hyperaccumulate nickel, cobalt, and in some cases manganese (Reeves et al. 2018). Nominal threshold values for “hyperaccumulation status” have been established for various elements, including 1000 μg g−1 for Ni, 300 μg g−1 for Co, 10,000 μg g−1 for Mn, and 100 μg g−1 for Cd (van der Ent et al. 2019; Saladin 2015). More than 400 Ni hyperaccumulator plants have been identified (Houzelot et al. 2018). Global centers of distribution for nickel hyperaccumulator plants include the Mediterranean Region, mainly with species in the Brassicaceae family (Reeves et al. 2018), and the Phyllanthaceae family emerged as the primary cobalt and manganese hyperaccumulator group in the tropical ultramafic outcrops and Southeast Asia (van der Ent et al. 2019; Reeves et al. 2018). After nickel hyperaccumulators, the largest group of hyperaccumulator plants are those of the copper/cobalt-enriched soils from Central Africa (Faucon et al. 2007). Table 15.2 shows the heavy metal hyperaccumulation by plant species.

Table 15.2 Nonwoody species known as hyperaccumulators of at least one heavy metal
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Halophytes

Successful performance of phytoextraction depends on selecting plant species that are well adapted to specific contaminated sites (high salinity and waterlogged conditions). About 1% of the species of land plants, named as halophytes, can grow and reproduce in coastal or inland saline sites. They can survive and reproduce in environments where the salt concentration is around 200 mM NaCl or more. These above conditions kill 99% of other plant species (Manousaki and Kalogerakis 2011). Halophytes are potentially ideal plants for phytoextraction, phytostabilization, or phytoexcretion applications of heavy metal-polluted soils affected by salinity (Manousaki and Kalogerakis 2011). Although halophytes and hyperaccumulators are rare, they are found in a diverse range of angiosperm families. Specific anatomical adaptations may also allow for some species to tolerate and remove heavy metals and salts (Table 15.3). Although salt tolerance and heavy metal hyperaccumulation often involve multiple physiological or anatomical mechanisms, phylogenetic and taxonomic evidence suggests that there have been many independent evolutionary origins of both salt tolerance (Saslis-Lagoudakis et al. 2014) and heavy metal hyperaccumulation (Cappa and Pilon-Smits 2014). For example, studies have shown that specialized salt glands, which extrude excess salt out of the plant body (Balnokin et al. 2010), are also able to extrude multiple types of heavy metals/metalloids (Moray et al. 2015). Most of them develop vacuoles in the cell where metals are accumulated to be segregated from the cytosol (Balnokin et al. 2010). Salt and heavy metals can both induce osmotic and metabolic stresses; halophytes and hyperaccumulators may use similar mechanisms to combat these stresses. Some halophytes and hyperaccumulators use the same mechanisms for dealing with ROS, including the production of compatible solutes, which act as osmoprotectants (Bose et al. 2014; Nedjimi and Daoud 2009; Sharma and Dietz 2006). In this respect, Ghnaya et al. (2005, 2007) stated that NaCl alleviates the toxicity of Cd2+ and enhances its accumulation in the shoots. Salt may protect the xylem vessel against the toxic effects of Cd2+ and therefore maintains adequate transport of water and other soluble elements toward the shoots. For example, S. portulacastrum, despite the high concentration of Cd2+ in the medium (100 μmol L−1), maintained its halophytic behavior and transported massive quantities of Na+ to the shoots. This species is able to replace K+ by Na+ for specific functions, for example, vacuolar osmotic adjustment with no deleterious effect on growth (Ghnaya et al. 2007). Also, Salicornia europaea showed that this halophyte is tolerant to the high concentration of NaCl up to 0.4 mol L−1 in the nutrient medium and has the great capacity to accumulate Ca2+, K+, Na+, and Mg2+. These metals seem to be sequestered in the well-developed vacuoles, which could be a good reservoir for heavy metals (Ozawa et al. 2007).

Table 15.3 Plant species able to tolerate salinity and hyperaccumulate heavy metals
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Macrophytes

In aquatic ecosystems, water contamination by trace metals is one of the main types of pollution that may stress the biotic community. Macrophytes contribute significantly to primary production in the littoral zone of the lakes and support both the detrital and herbivore food webs (Baldantoni et al. 2004). High concentrations of some macronutrients and trace metals in aquatic plants showed that they might accumulate, remove, and stabilize heavy metals from water or from sediments, indicating aquatic macrophytes as biomonitors (Wang et al. 2014). A wide variety of macrophytes have also shown high As (Falinski et al. 2014; Zhao et al. 2002), Cu (Ashraf et al. 2011; Oustriere et al. 2019), Fe (Xing et al. 2010, 2013), Cd (Mishra and Tripathi 2008; Garg and Chandra 1990), and Ni uptake potential (Khan et al. 2009; Chorom et al. 2012). The accumulation of heavy metals in aquatic systems depends upon the concentration of pollutants in water, as well as the length of time the plants have been exposed to (Table 15.4).

Table 15.4 Macrophyte species able to tolerate hyperaccumulate heavy metals
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Phytoremediation Strategies

Metal resistance in species with exclusion strategy is frequently based on reduced metal uptake into roots, preferential storage of metals in root vacuoles, and restricted translocation into shoots. Hyperaccumulators, in contrast, take up more metals, store a lower proportion of them in root vacuoles, and export higher amounts to shoots (Barcelo and Poschenrieder 2003). Hyperaccumulators require mechanisms of metal detoxification to allow the plants that are genetically independent characters (Hendrik et al. 2007). The pathways of radial root transport of metals and their entrance into the vascular cylinder clarify the basic genetic and molecular mechanisms responsible for metal hyperaccumulation (Baker and Whiting 2002).

In most hyperaccumulators, the metal is sequestered preferentially into compartments, usually the epidermal vacuoles, where it does the least harm to the metabolism (Cosio et al. 2006; Deng et al. 2019). The approximate volume of this storage site multiplied by the metal concentration in it (Hendrik et al. 2007) indicates that 70% of the total accumulated metal in mature leaves is stored in the epidermis. Hyperaccumulation must be mediated by active pumping of the metals into their storage sites. Indeed, starting with Pence et al. (2000), many studies have shown that metal hyperaccumulation is caused by an extremely increased expression of metal transport proteins (Papoyan and Kochian 2004; van der Ent et al. 2013; Hendrik et al. 2007).

The differences of Zn accumulation are caused by altered tonoplast Zn transport in roots and stimulated Zn uptake into leaves (Lasat et al. 1998; Lasat et al. 1996). Stimulation of ZNT1 expression, a gene that encodes a Zn transporter that belongs to the ZIP family of plant micronutrient transporters, was higher in Thlaspi caerulescens (Zn hyperaccumulator) than in Thlaspi arvense (non-hyperaccumulator). Other transporter systems of special interest in hyperaccumulators are the cation diffusion facilitators (CDF type), the ABC transporters for phytochelatins, and the metal chaperones (Barcelo and Poschenrieder 2003). Chelators such as siderophores, organic acids, and phenolics can help release metal cations from soil particles, increasing their bioavailability (Cherian and Oliveira 2005). For example, malate and citrate excreted by plants act as metal chelators. By lowering the pH around the root, organic acids increase the bioavailability of metal cations and may also inhibit metal uptake by forming a complex with the metal outside the root. Citrate inhibition of Al uptake and resulting aluminum tolerance in several plant species is an example of this mechanism (Papernik et al. 2001; Cherian and Oliveira 2005). In Zn-resistant plants, excess Zn is bound to malate in the cytoplasm, and, after transport to the vacuole, a ligand exchange occurs. Zn forms more stable complexes with citrate, oxalate, or other ligands, while malate returns to the cytoplasm (Barcelo and Poschenrieder 2003).

The toxicity of metal cations is mainly due to their tendency to form organic complexes with distinct ligands, which interfere with membrane functions, enzyme reactions, electron transport, etc. (Tolrà et al. 1996). Uptake and transport to shoot of high metal concentrations are only possible by the synthesis of strong chelators to bind the metals in a nontoxic form, thereby allowing the flux to and through the xylem up to the leaves. Organic acids, amino acids, and phytochelatins have been implied in metal detoxification (Barceló and Poschenrieder 2002).

Organic acids and flavonoid-type phenolics form strong complexes with the Al metal (Barceló and Poschenrieder 2002). High concentrations of organic acid anions in leaf tissues help to allow plants to maintain cation-anion homeostasis under conditions of excess ion stress. This ability may be considered a prerequisite, but is not sufficient, for metal tolerance (Tolrà et al. 1996). Oxalate-citrate-oxalate during Al transport from the rhizosphere through roots to leaves is the main way to hyperaccumulate in Fagopyrum esculentum (Ma and Hiradate 2000).

The sulfhydryl-rich phytochelatins (PC) have a high affinity for binding Cd, Hg, Cu, and As (Howden et al. 1995). Nonetheless, treatment of Cd-exposed plants with BSO (L-buthionine sulfoximine), an inhibitor of PC synthesis, increased Cd sensitivity only in plants that lacked Cd hypertolerance, which means that Cd hypertolerance is not based on PC-mediated sequestration (Schat 2002). Furthermore, in the Ni hyperaccumulator Thlaspi goesingense, Ni is bound by several ligands. Cytoplastic Ni seems to be detoxified by binding to histidine, while vacuolar storage of Ni is probably in the form of citrate (Krämer et al. 2000).

Management Practices (Approaches) to Improve Phytoremediation

Phytoremediation technique can be found to be an economically feasible and efficient approach as compared to engineering techniques like excavation, soil incineration, soil washing, flushing, and solidification (Sarwar et al. 2017) through the abilities of transgenic plants, and can be used to understand the mechanisms and effectiveness of phytoremediation techniques (Włóka et al. 2019; Ali et al. 2013).

Biotechnology

Enhanced phytoremediation through transgenics is now considered as the evolution of the concept of “geno-remediation” (Gomes et al. 2016), to enhance the phytoremediation potential for environmental contaminants by improving the antioxidative enzyme systems of plants (Rai et al. 2020). Interestingly, transferred genes in wild plants can boost the homeostasis mechanisms toward metal stress. However, elucidating the stress tolerance mechanisms interlinked with common pathways (i.e., metal cross-homeostasis) can pave the way to address the challenge of engineering metal tolerance (Antosiewicz et al. 2014). This varying geno-remediation potential of hyperaccumulators is attributed to the pace of transmitting stress signals to translate them eventually into physiological/molecular/biochemical responses (Chen et al. 2019).

In woody plants, many species and hybrids of Salix within the genus propose a wide genetic variability. Genetically modified poplar can detoxify the active oxygen species generated by way of the pollutant due to improved glutathione peroxidase activity, and showed accelerated tolerance to Zn (Bittsánszky et al. 2005). Reduction in growth and alterations in photosynthetic parameters have been described for Populus x euramericana clone in high concentrations of Zn (Di Baccio et al. 2003). High tissue cadmium accumulation in transformed poplars with a bacterial glutamylcysteine synthetase had the most effect on cadmium tolerance (Arisi et al. 2000). Lately, poplar plants had been converted to overexpress the bacterial gene encoding g-glutamylcysteine synthetase. GSH (g-l-glutamyl-l-cysteinyl-glycine) can detoxify heavy metals in plants, because of heavy metallic chelating phytochelatins (Cobbett and Goldsbrough 2002). Transformed Liriodendron tulipifera with mer-A gene and Populus deltoides with bacterial mer-A (Hg reductase) and mer-B (organomercury lyase) improved the remediation of ionic mercury and Hg (Hammer et al. 2003). Transgenic trees show tolerance to heavy metals as much as monomethylmercuric chloride and phenylmercuric acetate (PMA- (Lyyra et al. 2007). Transgenic white poplar with PsMTa1 gene from Pisum sativum shows tolerance to high concentrations of CuCl2 (Balestrazzi et al. 2009). Polluted sites and sequester Hg, native macrophytes, can be used to degrade methylmercury for later removal. But this technology is only appropriate for impulsive pollutions, and the application is restricted (Yao et al. 2012).

Rhizo-Engineering

Rhizo-engineering has been confirmed positively by planning approaches that preferred the growth of the target bacteria that influenced the capability to metabolize exotic nutrients from plants (Balestrazzi et al. 2009). One of the first achievements in rhizo-engineering was based on positively partitioning the unique nutrient opines, made by transgenic plants. This brought about the step forward and competitive increase of the microbial metabolism unable to metabolize opines. Research has revealed that such situations are predominant in the plant rhizosphere, which ends up in starvation of root-related bacterial populations (Narasimhan et al. 2003). To achieve environmental remediation and agricultural practices, the establishment of active populations of useful soil microbes is vital (Narasimhan et al. 2003). Moreover, different elements, as soil fertility, may progress the resistance to the metal (Vervaeke et al. 2003).

Metal hyperaccumulation is related to plant genetic traits that have been revised, and it has become more and more clear that also the plant-associated microorganisms and their genes are very likely to explain together the observed hyperaccumulator plant phenotype. The high bacterial and fungal diversity in the rhizosphere is due to the high level of nutrients such as amino acids, organic acids, and sugars exuded from the plant roots and capable of supporting microbial growth (López-Guerrero et al. 2013). However, environmental changes do not appear to be a relevant mechanism for metal mobilization by this kind of plant (Barcelo and Poschenrieder 2003). Bacterial production of siderophores may be responsible for enhanced bioavailability of Zn mobilization in the rhizosphere of Thlaspi caerulescens (Whiting et al. 2001). Since the bioavailability of heavy metals in soils decreases above pH 5.5–6, the use of a chelating agent is required, in alkaline soils (Tangahu et al. 2011). Exposing plants to EDTA for a 2-week period could improve metal translocation in plant tissue as well as overall phytoextraction performance. This faster uptake of heavy metals will result in shorter and, therefore, less expensive remediation periods. With the use of synthetic chelating agents, the risk of increased leaching must be taken into account (Van Ginneken et al. 2007).

Genetic engineering of plants for enhanced synthesis and exudation of natural chelators into the rhizosphere would emerge as a promising area for the success of phytoremediation in the field, especially with the help of plant growth-promoting rhizobacteria (PGPR) (Prasad 2003).

PGPR, a diverse group of rhizospheric microorganisms, may increase plant growth and development in potentially toxic element-polluted soils (Karimi et al. 2018) via generating several plant growth regulators and increasing metal bioavailability. Metabolite release and oxidation/reduction reactions are the main mechanisms of bioavailability, mobility, and uptake of nutrients (Thijs et al. 2017). In addition, ectomycorrhizal fungi may cause to accumulate heavy metals in their vacuoles and their cell walls. The hyphae of mycorrhizal fungi bind heavy metals to polyphosphate granules and cell walls by “polyphosphate granules” accumulating over time up to saturation (Brunner et al. 2008). Mineral solubilization, N fixation, siderophores, hormone production, and nutrient transformation are the mechanisms through which rhizobacteria stimulate the host plant growth in contaminated toxic sites (Rajkumar et al. 2009).

Deep Planting

For efficient phytoextraction, the roots should be in direct contact with the contaminants in deeper layers. Limitation of the phytoremediation method of contaminants released from carcass burial sites is located principally in the deep layers (Seo et al. 2017), which differs from the species used, but on average it is less than 50 cm (Vassilev et al. 2004). Based on ecological managing instruction of carcass burial locations, in Korea, the carcasses would be placed at depth in two meters belowground level (Kim and Pramanik 2016). For this reason, plants should be capable of growing deep roots for the application of phytoremediation to carcass burial sites. One choice is using the deep planting method of long stem nursery stock used formerly by the US Department of Agriculture for revegetation (Dreesen and Fenchel 2010). Deep planting of long stem stock may severely decrease the need to irrigate for the establishment of riparian trees and shrubs because of capillary fringe (Dreesen and Fenchel 2010). In carcass burial sites, the deep planting method has not been used in phytoremediation. The removal efficiency of deep-rooted plants was higher than the surface plants as the roots in deep-rooted techniques easily reached the depth and could transfer a significant amount of metal.

Economic Aspects

The phytoremediation techniques are commonly given as methods recommended for polluted soil treatment due to its cost efficiency, eco-friendliness, and ease of implementation (Xing et al. 2010; Włóka et al. 2019; Ali et al. 2013; Barcelo and Poschenrieder 2003; Chatterjee et al. 2013). Rhizo-filtration is effective and economically attractive for dilute concentrations of contaminants in large volumes of water (Prasad 2003). Trees provide economic return of contaminated land through the production of biomass, despite small amounts of heavy metals (Kacálková et al. 2015). Certain commercial companies are gaining economic benefits from phytoextraction by recovering extracted metals from plant biomass, and using the biomass for energy generation (Prasad 2003). For successful and economically feasible phytoextraction, it is necessary to use plants having a metal bioconcentration factor (BCF, a ratio of the concentration of chemical inside biological tissues to that of the surrounding environment) of 20 and biomass production of 10 tons per hectare (t ha−1) (Kacálková et al. 2015). Fast-growing trees, such as willow and poplar, have shown to be suitable candidates for phytoremediation-polluted soils and to produce wooden biomass for energy production (Giachetti and Sebastiani 2006). Harnessing the abilities of plants and microorganisms is a potential headway for cost-effective cleanup of hydrocarbon-polluted sites and could be very important in countries with great oil-producing records over many years but still developing.