Phytoremediation technologies and their mechanism for removal of heavy metal from contaminated soil: An approach for a sustainable environment (2024)

Table1

List of some plants used in the phytoremediation of different soil contaminants.

Phytoextraction

Plants uptake pollutants from soil, water, or sediments by their roots and transfer them to the aboveground biomass where they accumulate, such as in shoots or other harvestable parts of the plant. This is known as phytoextraction (Singh and Santal, 2015; Sarwar etal., 2017; Yanitch etal., 2020). Plants that can accumulate heavy metals are cultivated on polluted sites for this reason, and the metal-enriched biomass above the ground is collected, resulting in the elimination of some portions of the soil pollutant. Since it is considerably easier to collect shoots than roots, metal transfer to shoots is an important physiological process. The most effective phytoremediation approach for heavy metal and metalloid removal from disturbed soils is phytoextraction. It is also the most commercially viable option. The efficacy of phytoextraction as a possible environmental cleaning solution is dependent on a variety of parameters, including heavy metal bioavailability, soil characteristics, heavy metal speciation, and the plant’s capacity to absorb metals and accumulate aboveground components (Yan etal., 2020). Approximately 450–500 different plants have been recognized as hyperaccumulators (Chaudhary etal., 2018). Plant species must have the following characteristics to be suitable for phytoextraction: (i) metal tolerance to harmful metals, (ii) the production of high biomass, and (iii) active accumulators of heavy metals in easily harvestable parts (Vangronsveld etal., 2009; Suman etal., 2018). The basic idea behind phytoextraction for polluted areas is to cultivate suitable plant species in situ, collect the heavy metal–containing biomass, and treat it to minimize its mass and size, which can be achieved through composting, compressing, dehydrating, and thermal decomposition. The resultant heavy metal–enriched biomass contains high levels of metal contaminants and, if economically feasible, is utilized for trace element reextraction or disposed of as carefully hazardous waste (McGrath etal., 2002; Sheoran etal., 2009; Suman etal., 2018). Lemna valdiviana, an American minute flowering plant, exhibits promising arsenic-bioaccumulating characteristics and can extract up to 82% of arsenic from contaminated water (Souza etal., 2019). Bixa orellana, used as an accumulator of the As(III) of Cr(VI), can accumulate 82.8% of Cr(VI) and 40.4% of As(III) of the initial amount of 3 and 6 ppm, respectively (Kumar etal., 2022b). Suthar etal. (2014) reported a significant phytoextraction potential of the maize (Zea mays L.). This potential was also increased with the addition of the metal chelating agent EDTA, which enhances more than 13-fold extraction of Pb and more than 3-fold extraction of Cd. Phytoaccumulation capacity for Cu contamination by three different lettuces (Romaine lettuce, Redina lettuce, and iceberg lettuce) was investigated by Shiyab (2018) who reported that Redina lettuce is a high accumulator of Cu. Accumulation in root tissue was 1.89 mg kg⁻¹, while, in shoot tissue, it was 0.71 mg kg⁻¹, which is relatively high among these three lettuces.

Phytostabilization

Phytostabilization means establishing a plant covering the surface of polluted sites to limit the movement of contaminants within the vadose zone by root accumulation or immobilization inside the rhizosphere, therefore lessening off-site pollution. Transpiration and root development immobilize pollutants by a decrease in leaching, establishing aerobic conditions in the root zone, and the addition of organic substances to the substrate, which binds the pollutants (Bolan etal., 2011). The use of organic acid-producing metal-tolerant plant beneficial rhizobacteria, either alone or in combination with biogas residues, reduces Cd pollution in soil by stabilizing maize roots and limiting translocation to shoots. It also helps in improving maize biomass output, quality, and physiology. Furthermore, using poultry manure alone or in combination with biogas residues enhances Cd translocation to the shoot. Organic acid synthesis in maize root exudates is important for Cd stabilization in roots and shoots. Organic acid synthesis was raised in reaction to metal-tolerant plant-beneficial rhizobacteria and biogas residues, but poor production in response to poultry manure lowered Cd content in the root (Tahir etal., 2022). Mahdavian etal. (2022) reported that Scariola orientalis can be used as an efficient plant species in the phytoremediation (phytostabilization) of soils polluted with Zn and Fe. The level of heavy metal Cd in the rice grain can be reduced to improve the food quality. Cd levels in harvested rice (Oryza sativa L.) grains dramatically decreased in the Cd-contaminated fields when rice was intercropped with the alligator flag (Thalia dealbata). This reduction was accomplished because the fine roots of the alligator flag absorb a high quantity of Cd from the rice’s rhizosphere soil, lowering the rice’s Cd intake (Wang etal., 2020a). The alligator flag is most likely the best phytostabilization plant for Cd cleanup. Although soil nutrients varied significantly in the alligator flag cropping systems, Cd concentration was the dominant factor limiting microbial biomass and community structure. Intercropping T. dealbata with rice can be successfully used in the remediation of mild Cd contamination while simultaneously securely producing rice (Wang etal., 2020a). Naturally growing Tetraena qataranse plants in Qatar can accumulate heavy metal contaminants such as Cd, Cr, Cu, and Ni from the soil. This plant is suitable for animal fodder in arid areas (Usman etal., 2019). Two ecotypes of Athyrium wardii, one from a mining site and the other from a non-mining site, demonstrated different phytostabilization potentials for Cd from contaminated soils. The mining ecotype accumulated more Cd in roots, while the translocation of Cd to aerial parts was lower than in the non-mining ecotype. Furthermore, the use of humic compounds promotes the phytoremediation capacity of A. wardii root, particularly in the mining ecotype (Zhan etal., 2016).

Phytovolatilization

Phytovolatilization refers to the use of plants to absorb heavy metal pollutants and transform them into volatile, less hazardous chemical species via transpiration. Some of the heavy metals, such as, Hg, and Se, may exist in the environment as gaseous species (Chandra etal., 2015). A small number of naturally occurring or genetically engineered plants, such as muskgrass (Chara canescens), Indian mustard (Brassica juncea), and Arabidopsis thaliana, have been shown to absorb heavy metals and transform them to gaseous forms within the plant before releasing them into the environment (Ghosh and Singh, 2005). Arundo donax, in association with the plant growth-promoting bacteria Stenotrophom*onas maltophilia and Agrobacterium, can volatize approximately 75% of the initial amount of As (20 mgL⁻¹). Approximately 25% remained in the sand, and only approximately 0.15% accumulated in the plant (Guarino etal., 2020). Arsenic exists in four different oxidative forms (−3, 0, + 3, and +5), but two commonly found species are arsenite (As⁺³) and arsenate (As⁺⁵). Formerly, it was believed that the microorganisms and enzymes reduced and methylated the arsenite and arsenate within the plants. Two As species, trimethylated and dimethylated As, were easily evaporated from the plants’ aerial parts (Zhao etal., 2010). However, recent reports proved that there is no involvement of the plant in the methylation of As from mono- and dimethylated or inorganic form to volatile trimethylated As species, although these volatile species are taken up by the plants’ roots from the soil itself (Jia etal., 2012). Selenium contamination in soil is also a great threat to the environment because of its long half-life period of approximately 327,000 years. It can be removed by the process of phytovolatilization (Sharma etal., 2015). Like As, Se also exists in nature in five different oxidative states (−2, 0, + 2, +4, and +6). The common species of selenium that is found in nature is in the selenate form (+6), and soil plants take it by sulfate transporters. In the plant, various biochemical processes and enzymes are involved in the conversion of inorganic Se to volatile (CH₃)₂Se (Sharma etal., 2015). Dimethyl diselenide [(CH₃)₂Se], dimethyl selenone [(CH₃)₂SeO₂], dimethyl selenylsulfide [(CH₃)₂SeS], and methaneselenol (CH₃Se) are also released by plants from the soil (Terry etal., 2000; Sharma etal., 2015; Chen etal., 2019). The phytovolatilization process also removes the neurodegenerative heavy metal Hg. The methylated form of Hg is a severe threat to humankind because of its biological magnification in the food chain (Kumar etal., 2017). Plants involved in the phytoremediation of Hg take it from the soil via their roots and translocate it to the aerial part of the plant via their vascular system, where it is then transpired. The enzymes of the plant transform Hg into a volatile form (Sharma etal., 2015).

Rhizofiltration/hydraulic control

Rhizofiltration, or hydraulic control, is the method based on plant roots’ capacity to absorb and sequester metal pollutants from the water. Using this mechanism of phytoremediation, cleaning out metals such as Cd, Cr, Cu, Ni, Pb, and V and radionuclides (U, Cs, Sr) is possible (Jabeen etal., 2009; Singh and Santal, 2015). Long-rooted trees can absorb a large quantity of water, which was employed as a primary component in this procedure (Ahlfeld and Heidari, 1994). Long-rooted trees operate as pumps, drawing vast amounts of water from the subsurface water table (Muthusaravanan etal., 2018). As a consequence, contaminants in the water table are absorbed along with the water throughout this process. Root exudates such as citric acid and malic acid can scavenge or enhance the absorption, adsorption, or sedimentation of pollutants (Banerjee and Roychoudhury, 2022). Z. mays L. was evaluated (Benavides etal., 2018) and reported a 12% decrease in Hg, a 32% decrease in Pb, and a 30% decrease in Cr. The high potential of rhizofiltration is exhibited by the aquatic plant Typha angustifolia. It can uptake Cd and Zn 4,941.1–14,109.4 mg per plant and 14,039.3–59,360.8 mg per plant, respectively. T. angustifolia having a BCF value greater than 100 and a TF value less make it an excellent candidate for phytoremediation (Woraharn etal., 2021). Three very common aquatic plants Azolla (water fern), Pistia (water lettuce), and Eichhornia (water hyacinth) have different phytoremediation properties. Pistia has a good capacity for the phytoextraction and phytostabilization of As, Pb, and F, while, Eichhornia and Azolla effectively absorb Ni and Cu from the contaminated water. The TF of Pistia for fluoride is 5.0, making it an excellent hyperaccumulator of fluoride (Banerjee and Roychoudhury, 2022).

Table2

Plant proteins and respective genes in the phytoremediation of heavy metals.

Phytochelatins

Plant PCs are cysteine-rich low-molecular-weight polypeptides that are synthesized enzymatically, and their formation is stimulated by the presence of heavy metals (Chia, 2021). The PCs are structurally associated with glutathione synthetase (GSH), and the common structural formula of the PCs is “(γ-Glu-Cys)n-Aa,” where n ranges between 2 and 11 and Aa is an amino acid at the C-terminal. Due to the high range of “n,” the structural species of the PCs are also high (Grill etal., 2007; Vershinina etal., 2022). The C-terminal ‘Aa’ is generally represented by Gly. However, in several plant families, C-terminal ‘Ala,’ ‘Glu,’ and ‘Ser’ isophytochelatins have been reported (Vershinina etal., 2022). PCs chelate heavy metals by using their thiol groups. The complexes of metals and PCs that are produced as a consequence are stored in vacuoles (Ovečka and Takáč, 2014). The phytoremediation capacity of the PCs is largely dependent on their polymerization. An aquatic plant, L. minor, was evaluated for its phytoremediation capacity. PC species with a higher degree of polymerization (PC4, PC6, and PC7) accumulated more Cd than PC species with a lower degree of polymerization (PC2 and PC3) (Török etal., 2015).

Metallothionein

Plants have developed some adaptations to tackle metal ion concentrations’ increase in soil. An excessive amount of essential metal ions also causes toxicity similar to the non-essential metal ions; the foresaid mechanism provides metal tolerance as well as plays a significant role in the detoxification of excessive metal ions. MT was first discovered in animals than in plants; plant MTs have been discovered only approximately 30 years ago (Joshi etal., 2016). The superfamily of MT protein includes 15 families combined from animals, plants, fungi, and cyanobacteria (Joshi etal., 2016). The plant MTs are grouped into four distinct subfamilies: p1 (class 1), p2 (class 2), p3 (class 3), and pec (class 4). The MT1 gene from Cicer arietinum is part of the P1 subfamily, together with MT1a and MT1c from A. thaliana. On the other hand, the MT2 gene from C. arietinum is part of the P2 subfamily, along with MT2a and MT2b from A. thaliana. Musa acuminate and A. thaliana MT3 are both members of the P3 subfamily. Members of the ‘pec’ subfamily include A. thaliana MT4a (Ec-2) and MT4b (Ec-1), in addition to Ec-1 from T. aestivum. There are four different kinds of MT-encoding genes, and these genes may be found in Arabidopsis, rice, and sugarcane (Joshi etal., 2016).

Transporter proteins

The transporter proteins of the plants can uptake, translocate and, sequester the heavy metals to provide tolerance to the plants and eventually remediate the contaminated soil. The transporter protein involved in the uptake of the heavy metals such as Cd is divided into several families based on the sequence similarity between them. The Cd transporter includes ZIP family transporter protein (Zn-regulated transporter protein and Fe-regulated transporter protein), metal tolerance proteins (MTPs), and natural resistance–associated macrophage proteins (NRAMPs) (Luo and Zhang, 2021). The HMA can transport heavy to the distant part of the plants e.g., the transportation of Cd from the root to the shoot (Mills etal., 2003; Wong and Cobbett, 2009). Many ions are stored in the vacuoles, and this storage can minimize the toxic effect of heavy metals. Various transporters are involved in the transportation of the free Cd and PC-Cd complex to the vacuoles. The vacuolar transporters are HMAs, NRAMPs, ATP-binding cassette transporters (ABCCs), and H⁺/cation exchangers (CAXs) (Lanquar etal., 2005; Park etal., 2012; Brunetti etal., 2015).

Metal-binding proteins in rice

The elevated level of the heavy metal in the contaminated soil induced the expression of glutathione S-transferases (GSTs) and GSH in rice, which quenches the reactive molecules that induce the biosynthesis of the PCs. The PCs make a complex with the As, and the complex is sequestered into the vacuoles by ABCC1/ABCC2 transporters. Therefore, GST is involved in arsenic detoxification (Khan etal., 2018; Kumar and Trivedi, 2018; Tiwari etal., 2022). Localized near the root tip, OsNramp5 is a key transporter for Cd absorption in rice and a member of the NRAMP transporter family. In contrast, Cd is sequestered into root vacuoles by OsHMA3, a member of the HMA family. The OsHMA2, which is found in the root’s pericycle cells, has a role in mediating the translocation of Cd from the roots to the shoots (Wang etal., 2019).

Metal-binding proteins in maize

Maize is established as a heavy metal accumulator; however, the detailed molecular mechanism is not amply known. The expression of the ZmMTs gene under heavy metal stresses (Cu, Cd, and Pb) regulated by the hormones and MT synthesis improves the growth and development of the maize plants (Gao etal., 2022). Jin etal. (2022) investigated the role of the PC synthase gene ZmPCS1 of maize in Cd stress. The overexpression of this gene in the shoot and root of the maize plant prevented the toxic effect of the Cd and enhanced phytoremediation capacity. The expression of the PCs, MTs, and GSH in the root of the maize and barley plants increased when Nocardiopsis lucentensis (an actinomycete strain) was inoculated under As stress and enhanced the As-phytoremediation ability of both plants (AbdElgawad etal., 2021).

Metal-binding proteins in wheat

The role of wheat in phytoremediation is sparingly studied; however, few studies reported an increase in the expression of the PC synthase (TaPCS1) gene under Cd stress and Pb stress (Repkina etal., 2019; Rahman etal., 2022). The application of Si to the wheat plants under As stress induces the level of PCs and MTs, which further reduces the translocation of As to the shoot by sequestrating it into the roots of wheat (Hossain etal., 2018).

Metal-binding proteins in barley

Barley is the most abiotic stress-tolerant cereal crop against salinity stress, drought stress, and heat stress. It is also tolerant to some heavy metals like Cr, Zn, Cu, Cd, and Pb (Brunetti etal., 2012). A barley P1B-ATPase transports the important element Zn as well as the harmful pollutant Cd (Mills etal., 2012). The lipid-transfer protein from barley may play an important role in the phytoextraction of heavy metal ions from polluted soil. By using differential pulse polarography, Gorjanovi etal. (2004) evaluated the lipid-transfer protein-binding capacity to various metal ions and found that the protein has an affinity for Co (II) and Pb (II) but no affinity for Cd (II), Cu (II), Zn (II), and Cr (III) (Gorjanović etal., 2004). The expression of the OsMT1e gene for MT protein significantly enhances the Cd tolerance, detoxification, and accumulation of Cd ions (Rono etal., 2021).

Table3

Plant–microbe interaction in various mechanisms of heavy metal phytoremediation.

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