Mechanisms of As, Cd, Pb, and Zn hyperaccumulation by plants and their effects on soil microbiome in the rhizosphere

Abstract

Excess potentially toxic elements (PTEs), including arsenic (As), cadmium (Cd), lead (Pb), and zinc (Zn), above permissible limits in the environment, have detrimental effects on trophic levels. Hence, imperative to devise advertent measures to address this situation, especially in the soil ecosystem: the major reservoir of many PTEs. Using aerial plant parts (shoot) to accumulate As, Cd, Pb, and Zn - hyperaccumulators are considered a permanent approach to PTE removal from soils. This communication expatiated the principles that govern the hyperaccumulation of plants growing on As, Cd, Pb, and Zn-contaminated soils. The contribution of soil microbial communities during hyperaccumulation is well-elaborated to support the preference for this remediation approach. The study confirms a flow direction involving PTE uptake–translocation–tolerance–detoxification by hyperaccumulators. Rhizosphere microbes exhibit a direct preference for specific hyperaccumulators, which is associated with root exudations, while the resultant formation of chelates and solubility of PTEs, with soil physicochemical properties, including pH and redox potential, promote uptake. Different compartments of plants possess specialized transporter proteins and gene expressions capable of influx and efflux of PTEs by hyperaccumulators. After PTE uptake, many hyperaccumulators undergo cellular secretion of chelates supported by enzymatic catalysis and high transport systems with the ability to form complexes as tolerance and detoxification mechanisms. The benefits of combining hyperaccumulators with beneficial microbes such as endophytes and other rhizosphere microbes for PTE removal from soils are vital in enhancing plant survival and growth, minimizing metal toxicity, and supplying nutrients. Inoculation of suitable rhizosphere microbes can promote efficient cleaning of PTEs contaminated sites utilizing hyperaccumulator plants.

1 Introduction

Potentially toxic elements (PTEs), not excluding arsenic (As), cadmium (Cd), zinc (Zn), and lead (Pb), exert antagonistic behavior in the soil ecosystem, associated growing plants, and biomagnifications in animals and humans through ingestion (Knabb et al., 2016; Landrigan et al., 2018). Elements such as copper (Cu) and Zn are ubiquitous and exhibit direct physiological and metabolic relevance in plants as micronutrients, while excess accumulation above threshold limits incurs growth dysfunctions and death (Liu et al., 2018). Arsenic, Pb, and Cd have no benefit to plants and humans with possible health disorders, e.g., cardiovascular disease and diabetes upon accumulation (Fuller et al., 2022), as their environmental exposure increases.

Despite the geogenic occurrence of PTEs, anthropogenic interferences, including mining and smelting (Knabb et al., 2016; Boente et al., 2022), the extended application of untreated organic wastes (e.g., sewage sludge and compost) and mineral fertilizers (e.g., phosphate fertilizers) application to arable lands (Bisht and Chauhan, 2020), and coal ash deposition (Shin et al., 2017) often release enormous contents in soils. Industrialization, war, and intensification of agriculture have left a legacy of soil contamination throughout, with 80,000 sites (in Australia), 1,300 in the United States, 3 million in Europe and the western Balkans, and 16% in China’s soils representing the hot spot of global polluted sites (FAO/UN, 2018). Culminating these data reveals the extent of loss of land resources for agricultural sustainability and calls for more effective, efficient, and affordable removal methods. The vicinity of point sources of potentially toxic elements (PTEs), e.g., As, Cd, Pb, and Zn, become contaminated, affecting the quality of the water table via infiltration and the metabolism of soil microfauna/microflora (Cempel and Nikel, 2006; Ji et al., 2021). For example, mining and metallurgy of the 19th century in the Linares district (Jaén, South Spain) accumulated (mg kg⁻¹) As (42), Cd (140), Pb (4,244—35,899), and up to 768 Zn compared to threshold limits of <20, 2, 100, and 200, respectively (Boente et al., 2022). Environmental exposure to PTEs results in hazardous effects as they are non-degradable (Woldetsadik et al., 2017; Landrigan et al., 2018). These raise significant awareness about the cleaning of affected soils as increases in human population parallel metalliferous activities (Figure 1). Considering climate change in recent decades and the consequences of its impacts (Hardy, 2003; National Academy of Sciences, 2020), removing PTEs in soils by plants offer adequate results over conventional technologies. Conventional strategies for cleaning up contaminated lands, e.g., soil washing (Shen et al., 2019), solidification (Matec industries, 2021), landfilling, soil flushing, and washing, capping, and vitrification (Koul and Taak, 2018; Liu et al., 2018; Khan et al., 2021), are often ex-situ and involve high treatment costs. These approaches often result in losing the fertility of soils and biodiversity, e.g., microfauna (Liu et al., 2022).

FIGURE 1

Some plants demonstrate Cd, Pb, and Zn accumulation in tissues and organs, especially shoots, providing evidence of their suitability in cleaning contaminated soils (Berhongaray et al., 2015; Yan et al., 2020). Hence, plant-based remediation techniques: phytoextraction, phytostabilization, phytodegradation, and phytovolatilization, most recently, have been adopted based on their success in revegetating PTE-polluted soils at an optimized cost and providing a greener ecosystem. Phytoremediation supports large field reclamations, prevents erosion and leaching by stabilizing metals, enhances organic matter (OM) accumulation, and builds up soil fertility (Jacob et al., 2018; Yan et al., 2020). During the reclamation of contaminated lands, a selection of phytoremediation type depends on the contaminants and the intended purpose of the field.

Some plant species extract and accumulate PTEs in aboveground organs (stem, appendages, leaves, lateral buds, flowering stems, and flower buds), with minimal or no signs of toxicity, termed hyperaccumulators (Suman et al., 2018; Ashraf et al., 2019). In recent times, PTE-polluted soils have been well-used to grow high-biomass woody plants, e.g., Salix and Populus spp allowing the reduction of environmental mobility of PTE and producing polluted harvested woody biomass to produce income (Guerra et al., 2011; Mleczek et al., 2018). Extraction of PTEs in contaminated soils to aboveground organs of plants (phytoextraction) prevents surface soils from contaminating other areas via runoff and erosion (Yan et al., 2020). Many hyperaccumulators grow faster, with high-biomass, fast root-to-shoot translocation, PTE-tolerant, and detoxify PTEs (Balafrej et al., 2020). The possibility of other low biomass and slow-growth plant hyperaccumulators, e.g., Solanum nigrum L., exhibit high PTE accumulation under the assistance of microorganisms (Zhang et al., 2021). Plant species from families including Brassicaceae (e.g., Brassica sp. and Noccaea sp.), Pteridaceae (e.g., Pteris vittate L.), Lamiaceae (Lamium maculatum L.), Poaceae (Deschampsia caespitosa L.), and Crassulaceae, are often characterized by high accumulation of PTEs aboveground biomass (Małecka et al., 2019; Castaňares and Lojka, 2020). For example, out of 970 mg kg⁻¹ total Zn content in soils, the leaf, stem, and root of Cratoxylum sumatranum (Jack) accumulated 223, 329, and 210 mg kg⁻¹ of Zn, respectively, in the mountain of Magdiwata, Philippines (Castaňares and Lojka, 2020).

Furthermore, the extension of roots creates a microbe-rhizosphere community with bacteria, fungi, actinomycetes, protozoa, and algae that regulate the mobility and bioavailability of PTE (Jacob et al., 2018; DalCorso et al., 2019). Microbes that tolerate PTEs contribute to plant survival and growth in the rhizosphere. For example, rhizobium represents bacteria that capture groups of plant rhizosphere with symbiotic nitrogen (N) fixation in soils (Visioli et al., 2015) and promote OM decomposition (Geng et al., 2022). Generally, root exudates capture microbes in soils and colonize root surfaces or infiltrate root cortexes (Visioli et al., 2015).

Organic acids, phenolics, and siderophores affect the acidification process, and the dynamics of redox conditions change the potential in rhizospheres (Glick, 2010). Hence, adsorbed, precipitated, and residual fractions of PTEs solubilize by increasing acidity, chelation, and ligand-induced dissolution by microbes to become accessible to plants (Sessitsch et al., 2013). For example, under Cd, Pb, and Zn stress, Enterobacter sp. and Klebsiella sp. cause high accessibility in the root rhizosphere of Brassica napus L. (Jing et al., 2014). It is vital to understand microbial input during hyperaccumulation of PTEs and their extent of effects on hyperaccumulating plants. Such studies enable specific microbes culturing for plants suitable to alleviate PTEs contaminated soils. Although there is individual scattered literature on soil PTEs, hyperaccumulation, and microbial effects on PTE cleaning by plants, a compilation of such studies remains scarce. It is pertinent to treat environmental contamination with urgent concern as the production rate of these metals, e.g., Cd, Pb, and Zn, keep increasing over the years (Figure 1). The end-products, such as litharge, after ore processing, are often disposed of and contribute to high PTE contents, especially in soils.

The current study presents an overview that describes in detail the principles governing the uptake, translocation, accumulation, and detoxification of As, Cd, Pb, and Zn by hyperaccumulating plants. We also answer questions that pertain to the extent of microbial participation in the accessibility of PTEs by hyperaccumulators. The implications of specific rhizosphere microbes in reworking PTEs during phytoextraction by hyperaccumulators deserve critical attention. Knowledge of the intensity of accumulation of exaggerated content of As, Cd, Pb, and Zn by plant hyperaccumulators is essential in avoiding the detrimental effects on soils and living things.

2 Data acquisition and proceedings

Relevant peer-reviewed publications covering sub-headings of this study were critically elucidated from ScienceDirect, Google Scholar, Web of Science, ResearchGate, and Scopus in the last decades to date to satisfy the flow chart in Figure 2. We used the search engines to elaborate on keywords, including the impacts of PTEs on the environment, processes of PTE uptake and translocation in plants, and effects of plant hyperaccumulators on microbes growing on PTE-contaminated soils.

FIGURE 2

3 Fractionation and speciation of PTEs in soils and their interactions with plants

Different elements are well-categorized by their physicochemical forms in soils, especially in organic complexes, adsorbed in solid phases or constituents of solid/mineral phases, with diverse solubility (Wu et al., 2019; Salman et al., 2021). Plant-accessible forms represent the exchangeable complexes (organic and inorganic components) and soluble forms in soil solution taken predominantly by plants as divalent ions.

In soils with free molecular oxygen, reductive dissolution of Fe/Mn (hydr)oxides releases Zn into the aqueous phase, which repartitions with Zn into sulfide and carbonate solids. In dry oxidized soils, Zn relates with (hydr)oxide phases, and in flooded systems, sulfides and carbonates (Mondillo et al., 2018). In general, the speciation and bioavailability of As, Cd, Pb, and Zn in soils are individually or collectively associated with soil reaction (pH), redox potential (Eh), dissolved organic carbon, clay content, Fe/Mn/Al (hydr)oxides, and microbial processes (Dary et al., 2010; Sungur et al., 2020).

Meanwhile, plants modulate the mobility and accessibility of PTEs by discharging root exudates: oxalic, fumaric, malic, and acetic acids (Lapie et al., 2019), which enhance solubilization. However, root exudates can remove PTEs by chelating and complexation, altering the numbers and activity of rhizosphere microbes (Jing et al., 2014; Lapie et al., 2019). Uptake of PTE is partly possible via diffusion into the root epidermis. However, the primary passage occurs via the apoplast and symplast (Yan et al., 2020). Apoplastic movement involves several transporter proteins for uptake and translocation (Guerinot, 2000). Casparian strips represent an apoplastic restriction of PTE, especially Pb (Wang et al., 2015; Wilkins et al., 2016). The uptake of PTEs through the symplast is well-governed by metal carriers or complexing agents (Asare et al., 2023). Chelation resulting from the production of phytochelatins can result in the immobilization of PTEs in roots (Flores-Cáceres et al., 2015) while remaining PTEs sequester in cellular organelles. Cadmium, As, Pb, and Zn sequestered inside the vacuoles can transport into the stele and enter the xylem via the root symplast (Thakur et al., 2016). In the apoplast, many precipitated forms of compounds, e.g., CO^2-₃, get immobilized. However, the mobile fractions of PTEs at this point are translocated via the apoplast or symplast movement into leaves and sequestered in extracellular parts to stop compartmental cellular accumulation (Tong et al., 2004).

4 PTE hyperaccumulators and their protein transporters

4.1 PTE hyperaccumulators

Several plants can accumulate As, Cd, Pb, and Zn above threshold levels in aboveground organs. At the organ level, leaves are well-considered in establishing the hyperaccumulating statuses of plants (Yan et al., 2020; Lima et al., 2022). Hyperaccumulators of PTEs have distinguished physiological properties capable of sequestering high contents of PTEs at a high rate (Lima et al., 2022).

Due to health and ecotoxicological reasons, PTE contents in plants have assigned global and regional permissible limits. According to WHO (1996), the content of (in mg kg⁻¹) As- 0.1, Cd- 0.02, Pb- 2, and Zn- 0.60 should not exceed the standard reference in plants. The use of translocation (root-to-shoot quotient, TF) and bioaccumulation (plant-to-soil quotient, BF) factors over 1 are vital parameters when associated with permissible limits of PTEs determining plant hyperaccumulating abilities (Ghori et al., 2016; Souri et al., 2017). Many hyperaccumulating plant species, including Lysimachia deltoids L., Viola baoshanensis (W. S. Shu), Silene gracilicanlis L., and Gentiana sp. exhibit translocation factors >1 for Cd, Zn, and Pb (Reeves and Baker, 2000; Table 1).

Studies show that Cd, Pb, and Zn-hyperaccumulator can accumulate (in mg kg^-1 dry weight) > 100 (Baker et al., 2000), >1,000 (Baker et al., 2000), and 3,000 (Reeves and Baker, 2000), respectively, in any above-ground organ. According to Baker and Whiting (2002), these high contents only provide guidelines in recognition of the extreme behavior of plants during PTE uptake. High consideration is, thus, given to the content of PTEs in contaminated soils and their respective accumulation by the aboveground biomass, especially in the case where BF > 1. Plant species such as Pteris vittata L. (Danh et al., 2014) and Isatis cappadocica Desv (Karimi et al., 2009), hyperaccumulate As. For example, Pteris vittata adopts a mechanism of arsenate and arsenite uptake, translocation, and vacuolar sequestration (Danh et al., 2014), while the stem and shoot remain unaffected by As stress (Sridhar et al., 2011). Many hyperaccumulators possess multiple abilities in accumulating several PTEs. Wu et al. (2010) observed that V. baoshanensis accumulated (in mg kg⁻¹) 1,090 of Cd, 1,902 Pb, and 3,428 Zn in the shoots.

4.2 PTE transporters

Plant uptake and subsequent transport of PTEs are well-mediated by complex sequences. Many specialized protein transporters in different plant parts exhibit diverse abilities for PTE translocation, maintaining homeostasis, and controlling ion movements across cellular channels from roots to shoots (Ricachenevsky et al., 2013; Mishra et al., 2017). These transporters enable the re-mobilization of sugar molecules from photosynthetic tissues in leaves to roots, stems, and seeds through phloem loading. Primary protein transporter families for PTEs include;

Zinc/iron protein transporter (ZIP): Most divalent cationic elements (Cd, Ni, Cu, Co, and Fe), especially Zn, undergo uptake and active translocation in the plant system by ZIP and associated transcription genes (Table 2). Another subfamily, the iron-regulated transporters (IRTs), are implicated mainly in the transport of Fe (Verret et al., 2004). The IRT is also responsible for Cd transport in the Arabidopsis (Lee and An, 2009).

Metal tolerance protein (MTPs): This transporter transports metals at the whole plant level (Desbrosses-Fonrouge et al., 2005) and regulates homeostasis and active Zn translocation (Ricachenevsky et al., 2013). The MTP transporters have different sub-families; Fe/Zn-MTP, Zn-MTP, and Mn-MTP (Shirazi et al., 2019), and can exist in several assessions from MTP1 to MTP12 (Shirazi et al., 2019).

Members of this family and their accessions partly mediate Co, Ni, and Cd transport. Studies have previously shown MTP1 in Hordeum vulgare (HvMTP1), Oryza sativa- (OsMTP1), and Cucumis sativus (CsMTP1), with MTP3 and MTP4 in A. thaliana and Cucumis sativus, respectively, into different compartments (Shahzad et al., 2010; Yuan et al., 2012).

Yellow Strip-like transporter family (YSL): YSL is well-known for the transport of Zn and Cd; described as an essential regulator of excess Zn together with Ferric Reductase Defective3 (FRD3), a MATE (multi-drug and toxin efflux) transporter (Pineau et al., 2012). They mediate the cellular uptake of metals that form complex to non-proteinogenic amino acids (Socha and Guerinot, 2014). According to DiDonato Jr et al. (2004), YSL2 is expressed in many cell types in roots and shoots of Arabidopsis and represents a metal-regulated gene encoding transporter of nicotianamine–metal complexes. In A. thaliana, YSL4 and YSL6 buffer the adverse effects of excess Fe (Divol et al., 2013).

Natural resistance-associated macrophage protein (NRAMP): The functions of the NRAMP were previously related to Fe²⁺ uptake and translocation (Williams and Mills, 2005; Mishra et al., 2017). The NRAMPs are well-identified in varied compartments of Arabidopsis, and other monocot and dicot, governing the transport of divalent PTEs, e.g., Cd, Zn, and Pb (Bastow et al., 2018).

Nodulin 26-like intrinsic proteins (NIP): NIPs are cationic element transporters, including Si, Se, As, and Sb. Various species of As in soils are loaded into plants by NIP (Zhao et al., 2008; Chen et al., 2016). Evidence of As^(V) species transport in P. vittate and I. cappadocica was well-demonstrated by Su et al. (2008) and Karimi and Souri (2015).

FIGURE 3

Plant roots select As species by distinct transporters. For instance, in A. thaliana, As ^(v) uptake is mediated by phosphate (PHT) transporters AtPHT1, 4, 5, 7,8, and 9, while the NIP1-3, 5, and 7 for As ^(III) (Xu et al., 2015). Moreover, NIP has shown evidence in root-to-shoot translocation of As ^(III) (LeBlanc et al., 2013), with ACCC1 and 2 responsible for cellular transport of As ^(III) in the cytosol while in the presence of phytochelatins (Song et al., 2010).

Transporters Nramp, HMA, ZIP, ATP, YSL, and ABC (ATP Binding Cassette) families are involved in Cd distribution. The Nramps are well-identified in different compartments of Arabidopsis, and other monocots and dicots, Cd transport (Bastow et al., 2018). Meanwhile, Nramp1, 3, and 4 are often in charge of Cd above-organ accumulation in A. thaliana. Nramp6 is a Cd transporter, which mediates Cd transport from storage into the toxic cellular compartment. Gene transcription NcNramp1 in N. caerulescens regulates Cd influx across the endodermal plasma membrane, which implies possible root-to-shoot transport (Milner et al., 2014).

HMA1 is an efflux transporter localized in the chloroplast and controls the export of Cd from the chloroplast. HMA2 is a plasma membrane transporter involved in Cd root-to-shoot translocation, while overexpression of AtHMA3 enhanced Cd tolerance and increased its accumulation (Morel et al., 2009). AtHMA2 and AtHMA4, localized in the plasma membrane, are responsible for the xylem loading of Zn/Cd and play a key role in their accumulation in the shoots (Takahashi et al., 2012). Heavy-metal ATPase transporters are responsible for the long-distance transport of Cd from root to shoot. Additionally, gene expressions HMA4 and HMA2 regulate the influx of Cd into the stele to promote root-to-shoot transport in Arabidopsis Mishra et al. (2017).

ZIP transfers Zn to the stele in roots. For example, Noccaea caerulescen (J. Presl. & C. Presl.) and A. halleri exhibit improved Zn uptake (Assunção et al., 2001) and are represented by ZNT1 (Van de Mortel et al., 2006). The NcZNT1 gene expression and AtZIP4 for A. thaliana are active in the cortex, endodermis, and pericycle cells. These expressions are also in the same tissues of N. caerulescens but are not limited to Zn-deficient conditions (Van de Mortel et al., 2006; Lin et al., 2016). Zinc transporter 2 (ZNT2) and ZNT5 are also responsible for Zn²⁺ transport in the root cortex or by diffusion (Lin et al., 2016). The Zn ion is sequestered for vacuole storage and transported to the endodermis by ZIP23, ZIP19, ZIP5, and IRT3. Zinc ion transport stops by the apoplastic barrier (e.g., Casparian strip) and enters the endodermis via ZNT1/ZIP4. Transcriptional-level analysis shows that HMA2 and HMA4 form vital components of Zn hyperaccumulation and hyper-tolerance in A. halleri - AhHMA2 and AhHMA4 (Hanikenne et al., 2008; Frérot et al., 2018). Moreover, in the root pericycle, AhHMA2 and AhHMA4 promote Zn²⁺ efflux and loading in the root xylem (Hussain et al., 2004). Again, HMA3 mediates the sequestration of cationic Zn into the vacuole.

Zinc can transport from the root to shoot by ZIP4 and IRT3, form chelates, or possibly diffuse into the pericycle cells (the outermost part of the stele). Enhanced accumulation of Zn in the shoot by overexpression of IRT3 was suggested by Balafrej et al. (2020). Meanwhile, Zn enters the leaf cell either in chelation with low-molecular-weight ligands or as free Zn²⁺ complemented by ZIP4 and ZIP6 (Sinclair and Kramer, 2012). Several gene transcriptions from different transporters (e.g., MTP1 and 8, HMA3 and 4, and NRAMP3) promote the transport of Zn into the vacuole. The long-distance root-shoot translocation of Cd and Zn is solely responsible for HMA4 (Verret et al., 2004). Additionally, overexpression of HMA4 enhances Zn²⁺ efflux from the root symplast into the xylem vessels and promotes metal tolerance (Verret et al., 2004). After Zn loading in the xylem by different transporters: HMA, ZIP, and YLS, Zn reaches the leaves, where it binds to organic acids, e.g., malate and citrate, and sequesters in vacuoles. Unchelated Zn at the apoplastic barrier reaches the xylem through YSL or direct diffusion. Zn²⁺ crosses the xylem as free Zn or coupled with histidine, citrate, or malate (Tao and Lu, 2022). YSL transporters are also known for loading and unloading Zn in the xylem (Curie et al., 2009).

5 Persistence of hyperaccumulators under PTE stress

Plants, especially hyperaccumulators, either tolerate or detoxify PTEs to persist under high PTE (Dalvi and Bhalerao, 2013). Already taken ionic PTEs must undergo intracellular mechanisms to tolerance, including (a) cellular and subcellular compartmentalization of PTEs, (b) formation of chelates-reducing the toxicity of ionic forms of PTEs (Dalvi and Bhalerao, 2013), and (c) transportation capability. Meanwhile, other detoxification approaches involved in PTE tolerance in plants, such as PTE-immobilization in cell walls, impeded permeation across cell membranes, and active export into the apoplast (DalCorso et al., 2019).

6 The rhizosphere definition and its role

The rhizosphere elaborates on the root system and its close soils that foster biological and chemical activities, e.g., by exudation, for plant security and growth (Hartmann et al., 2009; Chamkhi et al., 2022). Rhizosphere represents nutrient-rich zones in soils that exhibit the capacity to perform extended functions for plants during stress (Chamkhi et al., 2022). However, the region supports beneficial and non-cooperative associations between rhizosphere microbes and plants (Figure 4). Due to the diverse root structure, the rhizosphere may exhibit varied size ranges. Hence, the properties of this region change only along roots. Meanwhile, about 90% of plants have roots extending from 0.27 to 0.9 m in soils, with a few reaching 1.82 m (Gilman, 1990).

FIGURE 4

The secretion of different bioactive (metabolites) compounds directing depends on the type of plant (genotype) and stress elicitor (e.g., abiotic and biotic). For example, roots can discharge their photosynthetically fixed C- into the soil (Sasse et al., 2018). The composition of exudates significantly impacts the activities and microbial count and diversity. Increased microbial count and activities in rhizosphere regions are a function of metabolite discharge (Sasse et al., 2018). Microbial preferences in the rhizosphere also depend on the influence of root exudates, which can affect the dissolution of PTEs for effective uptake. Hence, exudate patterns are vital drivers that shape the rhizosphere microbiome (Zhalnina et al., 2018) and are plant species-specific (Gianfreda, 2015).

Knowledge of the soil–root interface is pertinent to managing microorganisms, increasing plant growth, and reducing the effect of plant production. However, with the identification of plant genomes and the genes induced under different PTE stress, e.g., encoding for transporter proteins, metal sequestering peptides, and enzymes metabolism in plants, the principles governing PTEs uptake, accumulation, transport, chelation, and detoxification provide vital information for effective soil decontamination.

6.1 Rhizosphere microbe-plant interactions

Rhizosphere microbes exhibit movement to discharge pulses along plant roots (Hünninghaus et al., 2019) and play a vital role in regulating nutrition in plants, e.g., N fixation (Xiong et al., 2021). These microbes can compete and populate the root rhizosphere (Schreiter et al., 2018; Mulero-Aparicio et al., 2019). The attraction of microbes to the rhizosphere depends on the characteristics of the roots. Microbe-plant interaction in the rhizosphere involves chemical processes that partly account for the chelation and solubilization/dissolution of PTEs to promote mobility or immobilization (Figure 4). Although some microbes may not show a direct affinity for root exudates and many physicochemical properties of soils, especially toward the dissolution of PTEs, but contribute to their detoxification in soils. For example, Bacillus subtilis shows high tolerance and adsorption for Cd and Pb, a means of detoxification and elimination (Li et al., 2022). Soil properties, e.g., OM, organic C, and clay contents, influence microbial functional diversity (Li et al., 2022).

Microbes exhibiting resistance to the long-term effect of PTE contamination provide a basis for selecting suitable microbial species to assist in phytoremediation (Zubair et al., 2016; Table 2). Bacteria can help plants to resist stress and improve plant growth and productivity. For example, resistant bacteria can transform PTEs into less toxic forms and alter their availability for possible plant uptake or chelation (Whiting et al., 2001). Rhizosphere microbes such as Acinetobacter, Bacillus, Gluconacetobacter, and Pseudomonas affect the bioavailability of Zn (Costerousse et al., 2017), which involves pH reduction (acidic) and root growth. Additionally, the presence of mycelium fungi contributes to the increase in plants’ tolerance to excess Cd and Zn in Salix sp (Hrynkiewicz et al., 2012). Some rhizosphere microbes promote plant growth by direct interactions with plants or indirect antagonistic activities against plant pathogens. Pathogens affect many bacteria and fungi.

A typical example is endophyte resistance toward pathogenic space and nutrients in the rhizosphere and plant tissues (Vogel-Mikuš et al., 2006). The apical roots are involved in the active selection of specific microbe. Studies show that the polysaccharide composition of root mucilage for microbes with suitable glycosyl hydrolase composition (Amicucci et al., 2019) and further by extracellular DNA, antimicrobial proteins, and secondary metabolites (Haichar et al., 2014). Meanwhile, arbuscular mycorrhiza and ectomycorrhiza avoid PTEs from root uptake via absorption or chelation, indicating resistance (Hall, 2002).

Loading of PTEs in plant cell walls represents an approach to metal avoidance (Memon and Schroder, 2009; Krzeszowska et al., 2021). Cell wall pectin made of negative carboxylic groups of polygalacturonic acids can bond with cationic PTEs. The cation exchange reactions prevent free metallic ions from entering plant cells. Various interacting microbes produce phytohormones, which inhibit or promote root growth, protect plants against abiotic stress, and improve nutrient acquisition by roots (Gupta et al., 2014). One pertinent role of microbes in plant nutrition and health is the association between rhizosphere fluorescent pseudomonas and plants, while others suppress plant diseases and fungal pathogens from OM (Kumari and Kumar, 2018). For example, in soils suppressive to the fungal pathogen Rhizoctonia solani, Raza et al. (2016) reported that proteobacteria, firmicutes, and actinobacteria were prominent taxa involved in disease suppression.

Stable isotope study of plants and root-associated microbes shows dynamics in taxonomic composition and activities of microbial consumers. For example, Hünninghaus et al. (2019) pointed out that bacterial taxa with the highest abundance in the root of Zea mays L. were not necessarily those showing the highest enrichment of ¹³C from rhizodeposition, indicating substantial differences in consumption of exudates. Active and passive exudation of low molecular weight carbon compounds, e.g., sugars and organic acids, during root expansion and root hair zones (Canarini et al., 2019) constitutes microbial community modulation (Hu et al., 2018). These locations also modulate enzymatic activities (Zhang et al., 2020) and affect PTEs in soils and plant accessibility.

Arsenic reduction, methylation, and demethylation depend on the type of microbes in the soil. Under anaerobic conditions, organoarsenicals reduce to volatile arsine, such as monomethylarsonous acid [MMA^(III)], dimethylarsinous acid [DMA^(III)], and trimethylarsine TMA^(III) (Zhang et al., 2021). Microbial As methylation is an effective method for As detoxification in microbes as a bioremediation approach.

6.2 Effects of PTEs on rhizosphere microbes during hyperaccumulation

Many rhizosphere microbiomes can tolerate high contents of Zn, As, Cd, and Pb (Abou-shanab et al., 2019), which contribute significantly to the mobility and immobilization of PTE in soils.

Rhizosphere microbes, such asbacterial siderophores, can increase PTE accumulation and induce tolerance during phytoremediation (Benizri and Kidd, 2018). For instance, rhizobacteria, endophytes, siderophores, carboxylic acids, and phosphate solubilizers can contribute to the dissolution of As for plant uptake (He et al., 2013; Cabello-Conejo et al., 2014). Plant-associated microbes protect host plants by releasing phytohormones to combat biotic and abiotic elicitors that cause adverse effects on plants.

Moreover, the secretion of root exudates by hyperaccumulating plants and the attraction of rhizosphere microorganisms can significantly affect the availability of PTEs (Figure 4). For example, a Cd content of 7 mg kg^-1 in soil caused a reduction in rhizobium populations (Chaudri et al., 1992). Thus, high contents of some PTE can reduce microbial diversity and abundance (Abou-Shanab et al., 2005). For instance, the inoculation of Bacillus sp., Delftia sp., Pseudomonas sp., Pseudoxanthomonas sp., and Variovorax sp. on P. vittata plants under As stress resulted in increased plant biomass and As removal efficiency in soils (Yang et al., 2012).

Changes in pH affect microbial abundance and diversity, which are directly associated with the solubility of PTEs. According to Delorme et al. (2001), a high alkaline pH by adding lime increased bacteria count reduced Zn toxicity and enabled the growth of N. caerulescens and Trifolium pratense L. Meanwhile, increasing acidity promotes the high solubility of PTE for effective bioaccumulation (Becker and Skaar, 2014). Microbial counts also affect hyperaccumulators, probably because of the different secretions.

For example, N. caerulescens recorded a higher microbial population in Zn-contaminated soil than Trifolium pratense L. (Delorme et al., 2001) via acidification by microbes, which improves Zn availability, uptake, and selection for metal-resistant bacteria. Bacterial strains with Hexa-, Penta-, Tetra-, and Trivalent-metal ions tolerant are often abundant in the rhizosphere zone, where they can resist high Cd and Pb contents (Abou-Shanab et al., 2005). A unified multi-microbial influence on PTEs may result in fast stabilization or dissolution. These multi-facet abilities of diversified microbes in the rhizosphere are helpful during high levels of PTEs, as this can affect the uptake (Gremion et al., 2004). Antibiotics, phosphate solubilizers, hydrocyanic and indoleacetic acids, and siderophores obtained from some rhizobacteria increase Cd availability and facilitate absorption in plant roots (Sharma and Archana, 2016; He et al., 2020). Microbial populations often establish some positive relationship with the host plant system. Soil contaminated with PTEs can lead to the appearance of resistant rhizobacteria (Henao and Ghneim-Herrera, 2021; Table 3). Hyperaccumulating plant species of PTEs can significantly shape the rhizosphere ecosystem and impact the microbial community to favor the reduction of As, Cd, Pb, Zn, and many other pollutants. For example, Actinobacteria, Bacteroidetes, and genus Streptomyces were well-detected as dominant traits in Cd-stressed hyperaccumulator Sedum alfredii compared to non-hyperaccumulating ecotypes (Hou et al., 2018). Thus, S. alfredii and Cd exposure select suitable microbes for hyperaccumulation. According to Lu et al. (2023), Acidobacteria, Bacteroidetes, Deltaproteobacteria, and Gemmatimonadetes regulate excess Cd uptake and accumulation in Triticum aestivumL. with microbes partly influenced by soils with high OM.

Studies have shown that a high proportion of Zn-resistant bacteria persist in the rhizosphere of the hyperaccumulator N. caerulescens (Delorme et al., 2001; Whiting et al., 2001) and Alyssum bertolonii Desv (Sessitsch et al., 2013) or Alyssum murale M. Bieb (Abou-Shanab et al., 2003) grown in soil contaminated with Zn. The addition of bacteria increased the shoot Zn content in N caerulescens about two times and the rate of soluble Zn transport compared to axenic controls (Whiting et al., 2001). Enzymatic processes during detoxification and activation of chemicals in plants are similar to microbial biotransformation pathways in soils.

The comparison of biochemical isolates such as phosphate solubilizers, siderophore, and acids showed that phosphate solubilizers dissolve 82.2% Zn and 68.2% of Pb, siderophores (71.02% Zn and 61.6% Pb), and acids—53.3% Zn and 42.9% Pb (Abou-Shanab et al., 2005). Hence, several organic materials released by microbes in the root rhizospheres are responsible for the dissolution of PTEs for plants’ availability. According to Singh et al. (2022), the presence of siderophores decreased the uptake of metals by plants. Siderophores produced by Pseudomonas sp., Serratia marcescens, and Streptomyces sp. had either no effect or negatively affected Zn uptake by Salix capreastrum. These effects indicate that the principles underlying metal uptake are also plant-dependent. The efficiency of siderophore producers in mobilizing or immobilizing soil PTEs depends on the binding form of metal/(loid)s, the charge of siderophores, soil pH, mineral composition, and organic content (Jing et al., 2007). Soil microbiome, particularly bacteria, containing enzymes, such as 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, limits secretion in stressed plants (Tiwari et al., 2018). Moreover, arbuscular mycorrhizal fungi contribute to plant PTE uptake (Kranner and Colville, 2011). Therefore, mycorrhizal fungi with high metal contents tolerance and biomass production can be applied for phytoextraction (Sagardoy et al., 2010). Thus, it is pertinent to co-inoculate PTE hyperaccumulators with desired microbes, e.g., Arthrobacter and other Microbacterium, that can improve uptake and translocation (Visioli et al., 2015).

7 Future perspectives

Microbes exhibit preference for specific PTE during hyperaccumulation. These attractions result from the secretion of exudates into the root rhizosphere region. Meanwhile, the entire microbial community may not necessarily benefit from the chelation or dissolution of PTEs for effective uptake by plants. Culturomics purposed on adapting beneficial microbes can improve the accessibility of PTEs.

Gene encoding involved in the uptake and translocation of Pb remains less published among crops such as Oryza sativa (Gong et al., 2022), while so far neglected in the hyperaccumulation of risk elements from contaminated sites. The induction of many of these transporter families and the use of suitable nano/microparticles remain the next level of concern for the remediation of PTE-contaminated sites. Mutation and ionome modifications of plant species with effective uptake and above-ground accumulation offer another innovative approach to PTE management in contaminated soils for sustainable use (Navarrete and De La Fuente, 2015).

8 Conclusion

Anthropogenic interferences contribute significantly to excess potentially toxic elements (PTES; As, Cd, Pb, and Zn) above the threshold of agricultural soils. Hyperaccumulating plants (above-ground accumulators of PTEs) possess uptake ability and accumulate the accessible portion of PTEs associated with the exchange complexes and soluble forms in the soil solution.

Additionally, soil characteristics, including high organic matter, carbon, and clay content increases microbial biomass and functionality and induce changes that regulate soil microbial community. These properties affect microbial abundance and increase the chances of high PTE reworking to ease uptake.

Root exudations of hyperaccumulators contribute to microbes’ selection. Microbial stimulation (chemotaxis and excretion), e.g., flavonoids, also provide an anchor to colonize the root surface to support the solubilization and uptake of PTEs. The production rate of root exudate by hyperaccumulators and the attraction of rhizosphere microbes can significantly affect the bioavailability and bioaccumulation of PTEs, which enhances phytoextraction by hyperaccumulators. Changes in soil physicochemical properties (e.g., pH and redox potential) and root exudation affect microbial abundance and diversity, which also influence the solubility, mobility, and accessibility of PTEs. Multiple resistance of As, Cd, Pb, and Zn by microbes can assist many hyperaccumulators during PTE uptake. Diversified microbes in the root rhizosphere are vital during high levels of PTEs, as this can increase metal uptake while plants utilize them to avoid toxicity.

Meanwhile, different transporters, including Zinc-iron protein (ZIP), Metal Tolerance Protein (MTP), Heavy metal ATPases (HMA), Yellow Strip-like (YSL), and Natural resistance-associated macrophage proteins (NRAMPs) and their transcription genes are responsible for the influx/efflux of PTEs to plant compartments. Many hyperaccumulators show unique transcriptional transporters associated with fast uptake of high contents of PTEs and subsequent translocation to the aerial parts. Part of the bioavailable fractions of the PTEs is chelated with intracellular organs of hyperaccumulators as a means of detoxification, while exudation contributes to tolerance.

Thus, hyperaccumulation depends on the availability of mobilized metal ions in soils, enhanced activity of metal transporters, and metal chelates/solubilizers provided by plants or their associated microbes.

Incorporating different transporter genes into plants to improve the ability for PTEs hyperaccumulation needs attention. The microbial community in the root rhizosphere during PTE hyperaccumulation is not well-studied. The inoculation of suitable transporter genes and rhizosphere microbes for an effective hyperaccumulation of PTEs requires critical studies.

References

• 1

  AbolghassemE.DingY.MokhberdoranF.XieY. F. (2015). Heavy metal stress and some mechanisms of plant defense response. Sci. World J.2015, 756120. 10.1155/2015/756120

  • CrossRef
  • Google Scholar
  • View reference in article

• 2

  Abou-ShanabR. A.AngleJ. S.DelormeT. A.ChaneyR. L.Van BerkumP.MoawadH.et al (2003). Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol.158, 219–224. 10.1046/j.1469-8137.2003.00721.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 3

  Abou-ShanabR. A.GhozlanH.GhanemK.MoawadH. (2005). Behaviour of bacterial populations isolated from rhizosphere of diplachne fusca dominant in industrial sites. World J. Microbiol. Biotechnol.21, 1095–1101. 10.1007/s11274-004-0005-6

  • CrossRef
  • Google Scholar
  • View reference in article

• 4

  Abou-shanabR.El-SheekhM.SadowskyM. J. (2019). ““Role of rhizobacteria in phytoremediation of metal-impacted sites”,” in Emerging and eco-friendly approaches for waste management. Editors BharagavaR.ChowdharP. (Singapore: Springer). 10.1007/978-981-10-8669-4_14

  • CrossRef
  • Google Scholar
  • View reference in article

• 5

  AliH.KhanE.SajadM. A. (2013). Phytoremediation of heavy metals-concepts and applications. Chemosphere91, 869–881. 10.1016/j.chemosphere.2013.01.075

  • CrossRef
  • Google Scholar
  • View reference in article

• 6

  AmicucciM. J.GalermoA. G.GuerreroA.TrevesG.NanditaE.KailemiaM. J.et al (2019). Strategy for structural elucidation of polysaccharides: Elucidation of a maize mucilage that harbors diazotrophic bacteria. Anal. Chem.91, 7254–7265. 10.1021/acs.analchem.9b00789

  • CrossRef
  • Google Scholar
  • View reference in article

• 7

  AsareM. O.SzákováJ.TlustošP. (2023). The fate of secondary metabolites in plants growing on Cd-As-and Pb-contaminated soils-a comprehensive review. Environ. Sci. Pollut. Res. Int.30, 11378–11398. 10.1007/s11356-022-24776-x

  • CrossRef
  • Google Scholar
  • View reference in article

• 8

  AshrafS.AliQ.ZahirZ. A.AshrafS.AsgharH. N. (2019). Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol. Environ. Safe174, 714–727. 10.1016/j.ecoenv.2019.02.068

  • CrossRef
  • Google Scholar
  • View reference in article

• 9

  AssunçãoA.MartinsP. D. C.De FolterS.VooijsR.SchatH.AartsM. (2001). Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens: Zinc transporters of Thlaspi caerulescens. Thlaspi Caerulescens. Plant, Cell. Environ.24, 217–226. 10.1111/j.13653040.2001.00666.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 10

  BakerA. J. M.WhitingS. N. (2002). In search of the Holy Grail - a further step in understanding metal hyperaccumulation?New Phytol.155, 1–4. 10.1046/j.1469-8137.2002.00449_1.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 11

  BakerA. J. M.McGrathS. P.ReevesR. D.SmithJ. A. C. (2000). “Hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils,” in Phytoremediation of contaminated soil and water. Editors TerryN.BanuelosG. (London: Lewis Publishers), 85–107.

  • Google Scholar
  • View reference in article

• 12

  BalafrejH.BoguszD.TriquiZ. A.GuediraA.BendaouN.SmouniA.et al (2020). Zinc hyperaccumulation in plants: A review. Plants9, 562. 10.3390/plants9050562

  • CrossRef
  • Google Scholar
  • View reference in article

• 13

  BastowE. L.Garcia De La TorreV. S.MacleanA. E.GreenR. T.MerlotS.ThomineS.et al (2018). Vacuolar iron stores gated by NRAMP3 and NRAMP4 are the primary source of iron in germinating seeds. Plant Physiol.177, 1267–1276. 10.1104/pp.18.00478

  • CrossRef
  • Google Scholar
  • View reference in article

• 14

  BeckerK. W.SkaarE. P. (2014). Metal limitation and toxicity at the interface between host and pathogen. FEMS. Microbiol. Rev.38, 1235–1249. 10.1111/15746976.12087

  • CrossRef
  • Google Scholar
  • View reference in article

• 15

  BenizriE.KiddP. (2018). The role of the rhizosphere and microbes associated with hyperaccumulator plants in metal accumulation, in Agromining: Farming for metals. Mineral resource reviews. Editors Van der EntA.EchevarriaG.BakerA.MorelJ. (Cham: Springer). 10.1007/978-3-319-61899-9_9

  • CrossRef
  • Google Scholar
  • View reference in article

• 16

  BerhongarayG.VerlindenM. S.BroeckxL. S.CeulemansR. (2015). Changes in belowground biomass after coppice in two Populus genotypes. Forest Ecology and Management337, 1–10.

  • Google Scholar

• 17

  BienertG. P.ThorsenM.SchüsslerM. D.NilssonH. R.WagnerA.TamásM. J.et al (2008). A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3across membranes. Bmc. Biol.6, 26. 10.1186/1741-7007-6-26

  • CrossRef
  • Google Scholar
  • View reference in article

• 18

  BishtN.ChauhanP. S. (2020). “Excessive and disproportionate use of chemicals cause soil contamination and nutritional stress,” in Soil contamination - threats and sustainable solutions. Editors LarramendyM. L.SoloneskiS. (Rijeka: IntechOpen). 10.5772/intechopen.94593

  • CrossRef
  • Google Scholar
  • View reference in article

• 19

  BoenteC.SierraC.MartínezJ.Rodríguez-ValdésE.AfifE.ReyJ.et al (2022). Impact of old Pb mining and metallurgical production in soils from the Linares mining district (Spain). Environ.9, 24. 10.3390/environments9020024

  • CrossRef
  • Google Scholar
  • View reference in article

• 20

  BridgwaterA. V.MeierD.RadleinD. (1999). An overview of fast pyrolysis of biomass. Org. Geochem.30, 1479–1493. 10.1016/s0146-6380(99)00120-5

  • CrossRef
  • Google Scholar
  • View reference in article

• 21

  Cabello-ConejoM.Becerra-CastroC.Prieto-FernándezA.MonterrosoC.Saavedra-FerroA.MenchM.et al (2014). Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Alyssum Pintodasilvae. Plant Soil379, 35–50. 10.1007/s11104-014-2043-7

  • CrossRef
  • Google Scholar
  • View reference in article

• 22

  CanariniA.KaiserC.MerchantA.RichterA.WanekW. (2019). Root exudation of primary metabolites: Mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci.10, 157. 10.3389/fpls.2019.00157

  • CrossRef
  • Google Scholar
  • View reference in article

• 23

  CastaňaresE.LojkaB. (2020). .Potential hyperaccumulator plants for sustainable environment in tropical habitats. IOP. Conf. Ser. Earth. Environ. Sci.528, 012045. 10.1088/17551315/528/1/012045

  • CrossRef
  • Google Scholar
  • View reference in article

• 24

  CempelM.NikelG. (2006). Nickel: A review of its sources and environmental toxicology. Pol. J. Environ. Stud.15, 375–382.

  • Google Scholar
  • View reference in article

• 25

  ChamkhiI.El OmariN.BalahbibA.El MenyiyN.BenaliT.GhoulamC. (2022). Is the rhizosphere a source of applicable multi-beneficial microorganisms for plant enhancement?Saudi J. Biol. Sci.29, 1246–1259. 10.1016/j.sjbs.2021.09.032

  • CrossRef
  • Google Scholar
  • View reference in article

• 26

  ChaudriA. M.McGrathS. P.GillerK. E. (1992). Survival of the indigenous population of Rhizobium leguminosarum biovar trifolii in soil spiked with Cd, Zn, Cu, and Ni salts. Soil Biol. biochem.24, 625–632. 10.1016/0038-0717(92)90040-5

  • CrossRef
  • Google Scholar
  • View reference in article

• 27

  ChenY.FuJ. W.HanY. H.RathinasabapathiB.MaL. Q. (2016). High as exposure induced substantial arsenite efflux in As-hyperaccumulator Pteris vittata. Chemosphere144, 2189–2194. 10.1016/j.chemosphere.2015.11.001

  • CrossRef
  • Google Scholar
  • View reference in article

• 28

  CosterousseB.Schönholzer-MauclaireL.FrossardE.ThonarC. (2017). Identification of heterotrophic zinc mobilization processes among bacterial strains isolated from wheat rhizosphere (Triticum aestivum L.). Appl. Environ. Microbiol.84, e01715–e01717. 10.1128/AEM.01715-17

  • CrossRef
  • Google Scholar
  • View reference in article

• 29

  CurieC.CassinG.CouchD.DivolF.HiguchiK.Le JeanM.et al (2009). Metal movement within the plant: Contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot.103, 1–11. 10.1093/aob/mcn207

  • CrossRef
  • Google Scholar
  • View reference in article

• 30

  da SilvaE. B.de OliveiraL. M.WilkieA. C.LiuY.MaL. Q. (2018). Arsenic removal from As-hyperaccumulator Pteris vittata biomass: Coupling extraction with precipitation. Chemosphere193, 288–294. 10.1016/j.chemosphere.2017.10.116

  • CrossRef
  • Google Scholar
  • View reference in article

• 31

  DalCorsoG.FasaniE.ManaraA.VisioliG.FuriniA. (2019). Heavy metal pollutions: State of the art and innovation in phytoremediation. Int. J. Mol. Sci.20 (14), 3412. 10.3390/ijms20143412

  • CrossRef
  • Google Scholar
  • View reference in article

• 32

  DalviA. A.BhaleraoS. A. (2013). Response of plants towards heavy metal toxicity: An overview of avoidance, tolerance, and uptake mechanism. Ann. Plant. Sci.2, 362–368.

  • Google Scholar
  • View reference in article

• 33

  DanhL. T.TruongP.MammucariR.FosterN. (2014). A critical review of the arsenic uptake mechanisms and phytoremediation potential ofPteris vittata. Pteris Vittata. Int. J. Phytoremed.16, 429–453. 10.1080/15226514.2013.798613

  • CrossRef
  • Google Scholar
  • View reference in article

• 34

  DaryM.Chamber-PérezM.PalomaresA. J.PajueloE. (2010). “Insitu” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal-resistant plant-growth-promoting rhizobacteria. J. Hazard. Mat.177, 323–330. 10.1016/j.jhazmat.2009.12.035

  • CrossRef
  • Google Scholar
  • View reference in article

• 35

  DelormeT. A.GagliardiJ. V.AngleJ. S.ChaneyR. L. (2001). Influence of the zinc hyperaccumulator Thlaspi caerulescens J. & C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can. J. Microbiol.47, 773–776. 10.1139/w01-067

  • CrossRef
  • Google Scholar
  • View reference in article

• 36

  Desbrosses-FonrougeA-G.VoigtK.SchröderA.ArrivaultS.ThomineS.KrämerU. (2005). Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. Febs. Lett.579, 4165–4174. 10.1016/j.febslet.2005.06.046

  • CrossRef
  • Google Scholar
  • View reference in article

• 37

  DiX.BeesleyL.ZhangZ.ZhiS.JiaY.DingY. (2019). Microbial arsenic methylation in soil and uptake and metabolism of methylated arsenic in plants: A review. Int. J. Environ. Res. Public Health16, 5012. 10.3390/ijerph16245012

  • CrossRef
  • Google Scholar
  • View reference in article

• 38

  DiDonatoR. J.JrRobertsL. A.SandersonT.Robynn EisleyB.WalkerE. L. (2004). Arabidopsis yellow stripe-like2 (YSL2): A metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J Cell. microbiol.39 (3), 403–414. 10.1111/j.1365313X.2004.02128.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 39

  DivolF.CouchD.ConéjéroG.RoschzttardtzH.MariS.CurieC. (2013). The Arabidopsis YELLOW STRIPE LIKE4 and 6 transporters control iron release from the chloroplast. Plant Cell.25 (3), 1040–1055. 10.1105/tpc.112.107672

  • CrossRef
  • Google Scholar
  • View reference in article

• 40

  DixitP.MukherjeeP. K.RamachandranV.EapenS. (2011). Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One.6 (1), e16360. 10.1371/journal.pone.0016360

  • CrossRef
  • Google Scholar
  • View reference in article

• 41

  ĐurićM.OprčkalP.ZalarS. V.PranjićA. M.ŠčančarJ.MilačičR.et al (2021). Environmental impacts and immobilization mechanisms of cadmium, lead, and zinc in geotechnical composites made from contaminated soil and paper-ash. Appl. Sci.11, 11822. 10.3390/app112411822

  • CrossRef
  • Google Scholar
  • View reference in article

• 42

  EapenS.D’souzaS. (2005). Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol. Adv.23, 97–114. 10.1016/j.biotechadv.2004.10.001

  • CrossRef
  • Google Scholar
  • View reference in article

• 43

  Estrella-GómezN.Mendoza-CózatlD.Moreno-SánchezR.González-MendozaD.Zapata-PérezO.Martínez-HernándezA.et al (2009). The Pb-hyperaccumulator aquatic fern Salvinia minima Baker, responds to Pb²⁺ by increasing phytochelatins via changes in SmPCS expression and phytochelatin synthase activity. Aquat. Toxicol.91, 320–328. 10.1016/j.aquatox.2008.11.002

  • CrossRef
  • Google Scholar
  • View reference in article

• 44

  FAO/UN (2018). Report sounds alarm on soil pollution. https://www.fao.org/news/story/en/item/1126971/icode/ (Assessed 29 October 2022).

  • Google Scholar
  • View reference in article

• 45

  FayigaA. O.SahaU. K. (2016). Arsenic hyperaccumulating fern: Implications for remediation of arsenic contaminated soils. Geoderma.284, 132–143. 10.1016/j.geoderma.2016.09.003

  • CrossRef
  • Google Scholar
  • View reference in article

• 46

  Flores-CáceresM. L.HattabS.HattabS.BoussettaH.BanniM.HernándezL. E. (2015). Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Sci.233, 165–173. 10.1016/j.plantsci.2015.01.013

  • CrossRef
  • Google Scholar
  • View reference in article

• 47

  FrérotH.HautekèeteN-C.DecombeixI.BouchetM-H.CréachA.Saumitou-LapradeetP.et al (2018). Habitat heterogeneity in the pseudometallophyte Arabidopsis halleri and its structuring effect on natural variation of zinc and cadmium hyperaccumulation. Plant Soil.423, 157–174. 10.1007/s11104-017-3509-1

  • CrossRef
  • Google Scholar
  • View reference in article

• 48

  FullerR.LandriganP. J.BalakrishnanK.BathanG.Bose-O’ReillyS.BrauerM.et al (2022). Pollution and health: A progress update. Lancet6, E535–E547. 10.1016/s2542-5196(22)00090-0

  • CrossRef
  • Google Scholar
  • View reference in article

• 49

  GengH.WangF.YanC.MaS.ZhangY.QinQ.et al (2022). Rhizosphere microbial community composition and survival strategies in oligotrophic and metal(loid) contaminated iron tailings areas. Hazard. Mat.436, 129045. 10.1016/j.jhazmat.2022.129045

  • CrossRef
  • Google Scholar
  • View reference in article

• 50

  GhoriZ.IftikharH.BhattiM. F.Nasar-um-MinullahSharmaI.KaziA. G.et al (2016). “Phytoextraction: The use of plants to remove heavy metals from the soil,” in Plant metal interaction: Emerging remediation techniques. Editor AhmadP. (Amsterdam: Elsevier), 385–409.

  • Google Scholar
  • View reference in article

• 51

  GianfredaL. (2015). Enzymes of importance to rhizosphere processes. J. Soil Sci. Plant Nutr.15, 0. 10.4067/S0718-95162015005000022

  • CrossRef
  • Google Scholar
  • View reference in article

• 52

  GilmanE. F. (1990). Tree root growth and development. I. Form, spread, depth, and periodicity. J. Environ. Hort.8, 215–220. 10.24266/0738-2898-8.4.215

  • CrossRef
  • Google Scholar
  • View reference in article

• 53

  GlickB. R. (2010). Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv.28, 367–374. 10.1016/j.biotechadv.2010.02.001

  • CrossRef
  • Google Scholar
  • View reference in article

• 54

  GongL.WangJ.AbbasT.ZhangQ.CaiM.TahirM.et al (2021). Immobilization of exchangeable Cd in soil using mixed amendment and its effect on soil microbial communities under paddy upland rotation system. Chemosphere262, 127828. 10.1016/j.chemosphere.2020.127828

  • CrossRef
  • Google Scholar
  • View reference in article

• 55

  GongX.YangF.PanX.ShaoJ. F. (2022). Accumulation of silicon in shoots is required for reducing lead uptake in rice. Crop J.262, 12782810.1016/j.cj.2022.09.014

  • CrossRef
  • Google Scholar

• 56

  GremionF.ChatzinotasA.KaufmannK.von SiglerW.HarmsH. (2004). Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS. Microbiol. Ecol.48 (2), 273–283. 10.1016/j.femsec.2004.02.004

  • CrossRef
  • Google Scholar

• 57

  GuerinotM. L. (2000). The ZIP family of metal transporters. Biochimica Biophysica. Acta (BBA). – Biomemb.1465, 190–198. 10.1016/S00052736(00)00138-3

  • CrossRef
  • Google Scholar

• 58

  GuerraF. P.Gainza-CortésF. I.Pérez-CastroR.ZamudioF. (2011). “Phytoremediation of heavy metals using poplars (Populus spp.): A glimpse of the plant responses to copper, cadmium and zinc stress,” in Handbook of phytoremediation (Chile: Nova Science Publishers Inc.), 387–414.

  • Google Scholar

• 59

  GullapM. K.DasciM.Erkovanİ.H.KocA.TuranM. (2014). Plant Growth-Promoting Rhizobacteria (PGPR) and phosphorus fertilizer-assisted phytoextraction of toxic heavy metals from contaminated soils. Commun. Soil Sci. Plant Anal.45, 2593–2606. 10.1080/00103624.2014.929702

  • CrossRef
  • Google Scholar

• 60

  GuptaA.GopalM.ThomasG. V.ManikandanV.GajewskiJ.ThomasG.et al (2014). Whole-genome sequencing and analysis of plant growth-promoting bacteria isolated from the rhizosphere of plantation crops coconut, cocoa, and arecanut. PLoS ONE.9, e104259. 10.1371/journal.pone.0104259

  • CrossRef
  • Google Scholar

• 61

  GutschA.ZouaghiS.RenautJ.CuypersA.HausmanJ. F.SergeantK. (2018). Changes in the proteome of medicago sativa leaves in response to long-term cadmium exposure using a cell-wall targeted approach. Int. J. Mol. Sci.19, 2498. 10.3390/ijms19092498

  • CrossRef
  • Google Scholar

• 62

  HaicharF. E. Z.SantaellaC.HeulinT.AchouakW. (2014). Root exudates mediated interactions belowground. Soil Biol. Biochem.77, 69–80. 10.1016/j.soilbio.2014.06.017

  • CrossRef
  • Google Scholar

• 63

  HallJ. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot.53, 1–11. 10.1093/jexbot/53.366.1

  • CrossRef
  • Google Scholar

• 64

  HanikenneM.BaurainD. (2014). Origin and evolution of metal P-type ATPases in plantae (archaeplastida). Front. Plant Sci.4, 544. 10.3389/fpls.2013.00544

  • CrossRef
  • Google Scholar

• 65

  HanikenneM.TalkeI. N.HaydonM. J.LanzC.NolteA.MotteP.et al (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature453, 391–395. 10.1038/nature06877

  • CrossRef
  • Google Scholar

• 66

  HardyJ. T. (2003). Climate change: Causes, effects, and solutions (1st ed.). New Jersey: Wiley, Chischester.

  • Google Scholar

• 67

  HartmannA.SchmidM.van TuinenD.BergG. (2009). Plant-driven selection of microbes. Plant Soil321, 235–257. 10.1007/s11104-008-9814-y

  • CrossRef
  • Google Scholar

• 68

  HasanM. K.ChengY.KanwarM. K.ChuX.-Y.AhammedG. J.QiZ.-Y. (2017). Responses of plant proteins to heavy metal stress—a review. Front. Plant Sci.8, 1492. 10.3389/fpls.2017.01492

  • CrossRef
  • Google Scholar

• 69

  HeH.YeZ.YangD.YanJ.XiaoL.ZhongT.et al (2013). Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere90, 1960–1965. 10.1016/j.chemosphere.2012.10.057

  • CrossRef
  • Google Scholar

• 70

  HeZ.YanH.ChenY.ShenH.XuW.ZhangH.et al (2016). An aquaporin PvTIP4;1 from Pteris vittata may mediate arsenite uptake. New Phytol.209, 746–761. 10.1111/nph.13637

  • CrossRef
  • Google Scholar

• 71

  HeX.XuM.WeiQ.TangM.GuanL.LouL.et al (2020). Promotion of growth and phytoextraction of cadmium and lead in Solanum nigrum L. mediated by plant-growth promoting rhizobacteria. Ecotoxicol. Enviro. Saf.205, 111333. 10.1016/j.ecoenv.2020.111333

  • CrossRef
  • Google Scholar

• 72

  HenaoS. G.Ghneim-HerreraT. (2021). Heavy metals in soils and the remediation potential of bacteria associated with the plant microbiome. Front. Environ. Sci.9. 10.3389/fenvs.2021.604216

  • CrossRef
  • Google Scholar

• 73

  HouD.LinZ.WangR.GeJ.WeiS.XieR.et al (2018). Cadmium exposure-Sedum alfredii planting interactions shape the bacterial community in the hyperaccumulator plant rhizosphere. Appl. Environ. Microbiol.84, e02797–17. 10.1128/AEM.02797-17

  • CrossRef
  • Google Scholar

• 74

  HrynkiewiczK.DabrowskaG.BaumC.NiedojadloK.LeinweberP. (2012). Interactive and single effects of ectomycorrhiza formation and Bacillus cereus on metallothionein MT1 expression and phytoextraction of Cd and Zn by willows. Water Air Soil Pollut.223 (3), 957–968. 10.1007/s11270-011-0915-5

  • CrossRef
  • Google Scholar

• 75

  HsiehT. F.IbarraC. A.SilvaP.ZemachA.Eshed-WilliamsL.FischerR. L.et al (2009). Genome-wide demethylation of Arabidopsis endosperm. Sci.324, 1451–1454. 10.1126/science.1172417

  • CrossRef
  • Google Scholar

• 76

  HuL.RobertC. A. M.CadotS.ZhangX.YeM.LiB.et al (2018). Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Comm.9, 2738. 10.1038/s41467-018-05122-7

  • CrossRef
  • Google Scholar

• 77

  HünninghausM.DibbernD.KramerS.KollerR.PauschJ.Schloter-HaiB.et al (2019). Disentangling carbon flow across microbial kingdoms in the rhizosphere of maize. Soil Biol. biochem.134, 122–130. 10.1016/j.soilbio.2019.03.007

  • CrossRef
  • Google Scholar

• 78

  HussainD.HaydonM. J.WangY.WongE.ShersonS. M.YoungJ.et al (2004). P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell.16 (5), 1327–1339. 10.1105/tpc.020487

  • CrossRef
  • Google Scholar

• 79

  IzquierdoM.TyeA. M.CheneryS. R. (2017). Using isotope dilution assays to understand speciation changes in Cd, Zn, Pb, and Fe in a soil model system under simulated flooding conditions. Geoderma295, 41–52. 10.1016/j.geoderma.2017.02.006

  • CrossRef
  • Google Scholar

• 80

  JacobJ. M.KarthikC.SarataleR. G.KumarS. S.PrabakarD.KadirveluK.et al (2018). Biological approaches to tackle heavy metal pollution: A survey of literature. J. Environ. Manage.217, 56–70. 10.1016/j.jenvman.2018.03.077

  • CrossRef
  • Google Scholar

• 81

  JiX.AbakumovE.ChigrayS.SaparovaS.PolyakovV.WangW.et al (2021). Response of carbon and microbial properties to risk elements pollution in arctic soils. J. Hazard. Mat.408, 124430. 10.1016/j.jhazmat.2020.124430

  • CrossRef
  • Google Scholar

• 82

  JingY. D.HeZ. L.YangX. E. (2007). Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. Sci. B8, 192–207. 10.1631/jzus.2007.B0192

  • CrossRef
  • Google Scholar

• 83

  JingY. X.YanJ. L.HeH. D.YangD. J.XiaoL.ZhongT.et al (2014). Characterization of bacteria in the rhizosphere soils of Polygonum pubescens and their potential in promoting growth and Cd. Pb. Zn. uptake by Brassica Napus. Int. J. Phytol.16, 321–333. 10.1080/15226514.2013.773283

  • CrossRef
  • Google Scholar

• 84

  JosephT.DubeyB.McBeanE. A. (2015). Human health risk assessment from arsenic exposures in Bangladesh. Sci. Total. Environ.527, 552–560. 10.1016/j.scitotenv.2015.05.053

  • CrossRef
  • Google Scholar

• 85

  KarimiN.SouriZ. (2015). Effect of phosphorus on arsenic accumulation and detoxification in arsenic hyperaccumulator, Isatis cappadocica. J. Plant. Growth Reg.34, 88–95. 10.1007/s00344-014-9445-x

  • CrossRef
  • Google Scholar

• 86

  KarimiN.GhaderianS. M.RaabA.FeldmannJ.MehargA. A. (2009). An arsenic‐accumulating, hypertolerant brassica, Isatis capadocica. Isatis Cappadocica. New Phytol.184, 41–47. 10.1111/j.14698137.2009.02982.x

  • CrossRef
  • Google Scholar

• 87

  KhalidS.ShahidM.DumatC.NiaziN. K.BibiI.BakhatG. H. F. S.et al (2017). Influence of ground-water and wastewater irrigation on lead accumulation in soil and vegetables: Implications for health risk assessment and phytoremediation. Int. J. Phytoremed.19, 1037–1046. 10.1080/15226514.2017.1319330

  • CrossRef
  • Google Scholar

• 88

  KhanS.NaushadM.LimaE. C.ZhangS.ShaheenS. M.RinklebeJ. (2021). Global soil pollution by toxic elements: Current status and future perspectives on the risk assessment and remediation strategies – a review. J. Hazard. Mater417, 126039. 10.1016/j.jhazmat.2021.126039

  • CrossRef
  • Google Scholar

• 89

  KicińskaA.PomykałamR.Izquierdo-DiazM. (2021). Changes in soil pH and mobility of heavy metals in contaminated soils. Eur. J. Soil. Sci.73, e13203. 10.1111/ejss.13203

  • CrossRef
  • Google Scholar

• 90

  KnabbK. A.ErelY.TiroshO.RittenourT.LaparidouS.NajjarM.et al (2016). Environmental impacts of ancient copper mining and metallurgy: Multi-proxy investigation of human-landscape dynamics in the Faynan valley, southern Jordan. J. Archaeol. Sci.74, 85–101. 10.1016/j.jas.2016.09.003

  • CrossRef
  • Google Scholar

• 91

  KoptsikG. N. (2014). Problems and prospects concerning the phytoremediation of heavy metal polluted soils: A review. Eurasian Soil Sci.47, 923–939. 10.1134/S1064229314090075

  • CrossRef
  • Google Scholar

• 92

  KoulB.TaakP. (2018). Biotechnological strategies for effective remediation of polluted soils. Springer. 10.1007/978-981-13-2420

  • CrossRef
  • Google Scholar

• 93

  KrannerI.ColvilleL. (2011). Metals and seeds: Biochemical and molecular implications and their significance for seed germination. Environ. Exp. Bot.7, 93–105. 10.1016/j.envexpbot.2010.05.005

  • CrossRef
  • Google Scholar

• 94

  KrzeszowskaE.Kokowska-PawłowskaM.KandrzeszowskiS. (2021). Distribution of selected critical elements in the carboniferous coal-bearing series of the upper silesian and lublin coal basins (Poland). Acta. Geol. Sin.96, 273–292. 10.1111/17556724.14811

  • CrossRef
  • Google Scholar

• 95

  KumarA.PrasadM. N. V. (2018). Plant-lead interactions: Transport, toxicity, tolerance, and detoxification mechanisms. Ecotoxicol. Environ. Saf.166, 401–418. 10.1016/j.ecoenv.2018.09.113

  • CrossRef
  • Google Scholar

• 96

  KumarS.DubeyR. S.TripathiR. D.ChakrabartyD.TrivediP. K. (2015). Omics and biotechnology of arsenic stress and detoxification in plants: Current updates and prospective. Environ. Int.7, 221–230. 10.1016/j.envint.2014.10.019

  • CrossRef
  • Google Scholar

• 97

  KumariA.KumarR.shmiR.JangraR. (2018). Exploring phyllosphere bacteria for growth promotion and yield of potato (Solanum tuberosum L.). Int. J. Curr. Microbiol. Appl. Sci.7 (4), 1065–1071. 10.20546/ijcmas.2018.704.117

  • CrossRef
  • Google Scholar

• 98

  LandriganP. J.FullerR.AcostaN. J. R.AdeyiO.ArnoldR.BasuN.et al (2018). The Lancet Commission on pollution and health. Lancet39, 462–512. 10.1016/S0140-6736(17)32345-0

  • CrossRef
  • Google Scholar

• 99

  LapieC.LeglizeP.ParisC. (2019). Profiling of main metabolites in root exudates and mucilage collected from maize submitted to cadmium stress. Environ. Sci. Pollut. Res.26, 17520–17534. 10.1007/s11356-019-05168-0

  • CrossRef
  • Google Scholar

• 100

  LeBlancM. S.McKinneyE. C.MeagherR. B.SmithA. P. (2013). Hijacking membrane transporters for arsenic phytoextraction. J. Biotechnol. 163, 1–9. 10.1016/j.jbiotec.2012.10.013

  • CrossRef
  • Google Scholar

• 101

  LeeS.AnG. (2009). Over−expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell. Environ.32, 408–416. 10.1111/j.1365-3040.2009.01935.x

  • CrossRef
  • Google Scholar

• 102

  LiX.SunM.ZhangL.FinlayR. D.LiuR.LianB. (2022). Widespread bacterial responses and their mechanism of bacterial metallogenic detoxification under high concentrations of heavy metals. Environ. Saf.246, 114193. 10.1016/j.ecoenv.2022.114193

  • CrossRef
  • Google Scholar

• 103

  LiaoZ.ChenY.MaJ.IslamM. S.WengL.LiY. (2019). Cd, Cu, and Zn accumulations caused by long-term fertilization in greenhouse soils and their potential risk assessment. Int. J. Environ. Res. Public Health16, 2805. 10.3390/ijerph16152805

  • CrossRef
  • Google Scholar

• 104

  LimaL. W.CastleberryM.WangelineA. L.AguirreB.Dall’AcquaS.Pilon-SmitsE. A. H.et al (2022). HyperaccumulatorStanleya pinnata: In situ fitness in relation to tissue selenium concentration. Plants11, 690. 10.3390/plants11050690

  • CrossRef
  • Google Scholar

• 105

  LimmerM.BurkenJ. (2016). Phytovolatilization of organic contaminants. Environ. Sci. Technol.50, 6632–6643. 10.1021/acs.est.5b04113

  • CrossRef
  • Google Scholar

• 106

  LinY-F.HassanZ.TalukdarS.SchatH.AartsM. G. (2016). Expression of the ZNT1 zinc transporter from the metal hyperaccumulator Noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana. PLoS ONE11, e0149750. 10.1371/journal.pone.0149750

  • CrossRef
  • Google Scholar

• 107

  LiuW.ShuW.LanC. (2004). Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin. Sci. Bull.49, 29–32. 10.1007/BF02901739

  • CrossRef
  • Google Scholar

• 108

  LiuL.LiW.SongW.GuoM. (2018). Remediation techniques for heavy metal-contaminated soils: Principles and applicability. Sci. Total. Environ.633, 206–219. 10.1016/j.scitotenv.2018.03.161

  • CrossRef
  • Google Scholar

• 109

  LiuJ.ZhaoL.LiuQ.LiJ.QiaoZ.SunP.et al (2022). A critical review on soil washing during soil remediation for heavy metals and organic pollutants. Int. J. Environ. Sci. Technol.19, 601–624. 10.1007/s13762-021-03144-1

  • CrossRef
  • Google Scholar

• 110

  LodyginE. D.AlekseevI. I.VasilevichR. S.AbakumovE. V. (2020). Complexation of lead and cadmium ions with humic acids from arctic peat soils. Environ. Res.191, 110058. 10.1016/j.envres.2020.110058

  • CrossRef
  • Google Scholar

• 111

  LombiE.TearallK. L.HowarthJ. R.ZhaoF. J.HawkesfordM. J.McGrathS. P. (2002). Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Thlaspi Caerulescens. Plant Physiol.128, 1359–1367. 10.1104/pp.010731

  • CrossRef
  • Google Scholar

• 112

  LuM.HuangL.WangQ.CaoX.LinQ.HeZ.et al (2023). Soil properties drive the bacterial community to cadmium contamination in the rhizosphere of two contrasting wheat (Triticum aestivum L.) genotypes. J. Environ. Sci.128, 117–128. 10.1016/j.jes.2022.07.028

  • CrossRef
  • Google Scholar

• 113

  LuoJ-S.ZhangZ. (2021). Mechanisms of cadmium phytoremediation and detoxification in plants. Crop J9, 521–529. 10.1016/j.cj.2021.02.001

  • CrossRef
  • Google Scholar

• 114

  MaL.KomarK.TuC.ZhangW.CaiY.KennelleyE. D. (2001). A fern that hyperaccumulates arsenic. Nature409, 579. 10.1038/35054664

  • CrossRef
  • Google Scholar

• 115

  MaL.LiJ.ZhanZ.ChenL.LiD.BaiQ.et al (2016). Specific histone modification responds to arsenic-induced oxidative stress. Toxicol. Appl. Pharmacol.302, 52–61. 10.1016/j.taap.2016.03.015

  • CrossRef
  • Google Scholar

• 116

  MałeckaA.KonkolewskA.HanćA.BarałkiewiczD.CiszewskaL.RatajczakE.et al (2019). Insight into the phytoremediation capability of Brassica juncea (v. Malopolska): Metal accumulation and antioxidant enzyme activity. Int. J. Mol. Sci.20, 4355. 10.3390/ijms20184355

  • CrossRef
  • Google Scholar

• 117

  Matec Industries (2021). Soil washing – remediation of contaminated sites. https://www.matecindustries.com/en/soil-washing-remediation-of-contaminated-sites/ ([Accessed 21 February 2023].

  • Google Scholar

• 118

  MemonA. R.SchröderP. (2009). Implications of metal accumulation mechanisms to phytoremediation. Environ. Sci. Pollut. Res. Int.16, 162–175. 10.1007/s11356-008-0079-z

  • CrossRef
  • Google Scholar

• 119

  MertensJ.SmoldersE. (2013). “Zinc,” in Heavy metals in soils. Environmental pollution. Editor AllowayB. (Dordrecht: Springer), 22. 10.1007/978-94-007-4470-7_17

  • CrossRef
  • Google Scholar

• 120

  Mesjasz-PrzybyłowiczJ.NakoniecznyM.MigulaP.AugustyniakM.TarnawskaM.ReimoldW. U.et al (2004). Uptake of Cadmium, Lead, Nickel, and Zinc from soil and water solutions by the nickel hyperaccumulator. Berkheya Coddii. Acta Biol. Cracoviensia Ser. Bot.46, 75–85.

  • Google Scholar

• 121

  MilnerM. J.Mitani-UenoN.YamajiN.YokoshoK.CraftE.FeiZ.et al (2014). Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. Plant J.78, 398–410. 10.1111/tpj.12480

  • CrossRef
  • Google Scholar

• 122

  MishraS.MishraA.KüpperH. (2017). Protein biochemistry and expression regulation of cadmium/zinc pumping ATPases in the hyperaccumulator plantsArabidopsis halleri and. Noccaea Caerulescens. Front. Plant. Sci.8, 835. 10.3389/fpls.2017.00835

  • CrossRef
  • Google Scholar

• 123

  MiyadateH.AdachiS.HiraizumiA.TezukaK.NakazawaN.KawamotoT.et al (2010). OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol.189, 190–199. 10.1111/j.1469-8137.2010.03459.x

  • CrossRef
  • Google Scholar

• 124

  MleczekM.GąseckaM.WaliszewskaB.MagdziakZ.SzostekM.RutkowskiP.et al (2018). Salix viminalis L. - a highly effective plant in phytoextraction of elements. Chemosphere212, 67–78. 10.1016/j.chemosphere.2018.08.055

  • CrossRef
  • Google Scholar

• 125

  MohileyA.LaaserT.HörethS.ClemensS.TielbörgerK.GruntmanM. (2021). Between the devil and the deep blue sea: Herbivory induces foraging for and uptake of cadmium in a metal hyperaccumulating plant. Proc. R. Soc. B288, 20211682. 10.1098/rspb.2021.1682

  • CrossRef
  • Google Scholar

• 126

  MondilloN.WilkinsonJ. J.BoniM.WeissD. J.MathurR. (2018). A global assessment of Zn isotope fractionation in secondary Zn minerals from sulfide and non-sulfide ore deposits and model for fractionation control. Chem. Geol.500, 182–193. 10.1016/j.chemgeo.2018.09.033

  • CrossRef
  • Google Scholar

• 127

  MorelM.CrouzetJ.GravotA.AuroyP.LeonhardtN.VavasseurA.et al (2009). AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol.149, 894–904. 10.1104/pp.108.130294

  • CrossRef
  • Google Scholar

• 128

  Mulero-AparicioA.CernavaT.TurràD.SchaeferA.Di PietroA.López-EscuderoF. J.et al (2019). The role of volatile organic compounds and rhizosphere competence in mode of action of the non-pathogenic Fusarium oxysporum FO12 toward Verticillium wilt. Front. Microbiol.10, 1808. 10.3389/fmicb.2019.01808

  • CrossRef
  • Google Scholar

• 129

  National Academy of Sciences (2020). Climate change: Evidence and causes: Update 2020. Washington, DC: The National Academies Press, 7. 10.17226/25733

  • CrossRef
  • Google Scholar

• 130

  NavarreteF.De La FuenteL. (2015). Zinc detoxification is required for full virulence and modification of the host leaf ionome by Xylella fastidiosa. Mol. Plant Microbe. Interact.28, 497–507. 10.1094/MPMI-07-14-0221-R

  • CrossRef
  • Google Scholar

• 131

  ParvinS.HaqueM. E.AkhterF.AliM.ShafinM. S. (2021). Determination of arsenic in minor cereals (barley, foxtail millet, proso-millet, finger- millet, pearl -millet, buckwheat. Oat, quinoa, and sorghum) in gazipur. Biomed. J. Sci. Tech. Res.40, 32251–32253.

  • Google Scholar

• 132

  PineauC.LoubetS.LefoulonC.ChaliesC.FizamesC.LacombeB.et al (2012). Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Gene.8, e1003120. 10.1371/journal.pgen.1003120

  • CrossRef
  • Google Scholar

• 133

  PunamiyaP.DattaR.SarkarD.BarberS.PatelM.DasP. (2010). Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J. Hazard Mat.177, 465–474. 10.1016/j.jhazmat.2009.12.056

  • CrossRef
  • Google Scholar

• 134

  QiaoS. Y.TaoY.ShanQ. H.WangJ. G.ChaiT. Y.GongS. F.et al (2021). Physiological and gene expression responses of six annual ryegrass cultivars to cobalt, lead, and nickel stresses. Int. J. Mol. Sci.22, 13583. 10.3390/ijms222413583

  • CrossRef
  • Google Scholar

• 135

  RaiV. (2002). Role of amino acids in plant responses to stresses. Biol. Plant45, 481–487. 10.1023/A:1022308229759

  • CrossRef
  • Google Scholar

• 136

  RazaW.YousafS.RajerF. U. (2016). Plant growth-promoting activity of volatile organic compounds produced by Bio-control strains. Sci. Lett.4, 40–43.

  • Google Scholar

• 137

  ReevesR. D.BakerA. J. M. (2000). ““Metal accumulating plants”,” in Phytoremediation of toxic metals: Using plants to clean up the environment. Editors RaskinI.FinsleyB. D. (New York: Wiley), 193–229.

  • Google Scholar

• 138

  RicachenevskyF. K.MenguerP. K.SperottoR. A.WilliamsL. E.FettJ. P. (2013). Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front. Plant. Sci.144, 144. 10.3389/fpls.2013.00144

  • CrossRef
  • Google Scholar

• 139

  RicachenevskyF. K.PunshonT.SaltD. E.FettJ. P.GuerinotM. L. (2021). Arabidopsis thaliana zinc accumulation in leaf trichomes is correlated with zinc concentration in leaves. Sci. Rep.11, 5278. 10.1038/s41598-021-84508-y

  • CrossRef
  • Google Scholar

• 140

  RoyS. B.BeraA. (2002). Individual and combined effect of mercury and manganese on phenol and proline content in leaf and stem of mungbean seedlings. J. Environ. Biol.23, 433–435.

  • Google Scholar

• 141

  SagardoyR.MoralesF. E.Rellán-ÁlvarezR.AbadíaA.AbadíaJ.López-MillánA. (2010). Carboxylate metabolism in sugar beet plants grown with excess Zn. J. Plant Physiol.168, 730–733. 10.1016/j.jplph.2010.10.012

  • CrossRef
  • Google Scholar

• 142

  SalmanS. A.El-AnwarE. A. A.AsmoayA.MekkyH.IbrahemW. A.ElnazerA. (2021). Chemical fractionation and risk assessment of some heavy metals in soils, assiut governorate, Egypt. Egypt. J. Chem.64. 10.21608/ejchem.2021.59371.3276

  • CrossRef
  • Google Scholar

• 143

  SarkarB.MukhopadhyayR.RamanayakaS.BolanN.OkY. S. (2021). The role of soils in the disposition, sequestration, and decontamination of environmental contaminants. Phil. Trans. R. Soc. B376, 20200177. 10.1098/rstb.2020.0177

  • CrossRef
  • Google Scholar

• 144

  SasseJ.MartinoiaE.NorthernT. (2018). Feed your friends: Do plant exudates shape the root microbiome?Trends Plant Sci.23, 25–41. 10.1016/j.tplants.2017.09.003

  • CrossRef
  • Google Scholar

• 145

  SchreiterS. S.BabinD. D.SmallaK. K.GroschR. R. (2018). Rhizosphere competence and biocontrol effect of Pseudomonas sp. RU47 independent from plant species and soil type at the field scale. Front. Microbiol.9, 97. 10.3389/fmicb.2018.00097

  • CrossRef
  • Google Scholar

• 146

  SessitschA.KuffnerM.KiddP.VangronsveldJ.WenzelW. W.FallmannK.et al (2013). The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol. Biochem.60, 182–194. 10.1016/j.soilbio.2013.01.012

  • CrossRef
  • Google Scholar

• 147

  ShahidM.DumatC.PourrutB.SilvestreJ.LaplancheC.PinelliE. (2014). Influence of EDTA and citric acid on lead-induced oxidative stress toVicia faba roots. J. Soils Sed.14, 835–843. 10.1007/s11368-013-0724-0

  • CrossRef
  • Google Scholar

• 148

  ShahzadZ.GostiF.FrérotH.LacombeE.RoosensN.Saumitou-LapradeP.et al (2010). The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet.6, e1000911. 10.1371/journal.pgen.1000911

  • CrossRef
  • Google Scholar

• 149

  ShanmugamV.LoJ-C.YehK-C. (2013). Control of Zn uptake in Arabidopsis halleri: A balance between Zn and Fe. Front. Plant Sci.14, 281. 10.3389/fpls.2013.00281

  • CrossRef
  • Google Scholar

• 150

  SharmaR. K.ArchanaG. (2016). Cadmium minimization in food crops by cadmium resistant plant growth promoting rhizobacteria. Appl. Soil Ecol.107, 66–78. 10.1016/j.apsoil.2016.05.009

  • CrossRef
  • Google Scholar

• 151

  SharmaA.PatniB.ShankhdharD.ShankhdharS. C. (2013). Zinc – An indispensable micronutrient. Physiol. Mol. Biol. Plants.19, 11–20. 10.1007/s12298-012-0139-1

  • CrossRef
  • Google Scholar

• 152

  ShenZ.ZhangJ.HouD.TsangD. W. C.OkY. S.AlessiD. S. (2019). Synthesis of MgO-coated corncob biochar and its application in lead stabilization in a soil washing residue. Environ. Int.122, 357–362. 10.1016/j.envint.2018.11.045

  • CrossRef
  • Google Scholar

• 153

  ShinJ.NatansonA.KhunJ.OdorizziN.DeCreny-JacksonJ.FowoweH.et al (2017). Research Article: Assessing the impact of coal ash exposure on soil microbes in the Dan River. BIOS. J.88, 72–85. 10.1893/bios-d-16-00006.1

  • CrossRef
  • Google Scholar

• 154

  ShiraziZ.AbediA.KordrostamiM.BurrittD. J.HossainM. A. (2019). Genome-wide identification and characterization of the metal tolerance protein (MTP) family in grape (Vitis vinifera L.). 3 Biotech.9, 199. 10.1007/s13205-019-1728-2

  • CrossRef
  • Google Scholar

• 155

  ShrivastavaA.GhoshD.DashA.BoseS. (2015). Arsenic contamination in soil and sediment in India: Sources, effects, and remediation. Curr. Pollut. Rep.1, 35–46. 10.1007/s40726-015-0004-2

  • CrossRef
  • Google Scholar

• 156

  SinclairS. A.KrämerU. (2012). The zinc homeostasis network of land plants. Biochim. Biophys. Acta.1823, 1553–1567. 10.1016/j.bbamcr.2012.05.016

  • CrossRef
  • Google Scholar

• 157

  SinghS.PariharP.SinghR.SinghV. P.PrasadS. M. (2016). Heavy metal tolerance in plants: Role of transcriptomics, proteomics, metabolomics, and ionomics. Front. Plant Sci.6, 1143. 10.3389/fpls.2015.01143

  • CrossRef
  • Google Scholar

• 158

  SinghP.ChauhanP. K.UpadhyayS. K.SinghR. K.DwivediP.WangJ.et al (2022). Mechanistic insights and potential use of siderophores producing microbes in rhizosphere for mitigation of stress in plants grown in degraded land. Front. Microbiol.13, 898979. 10.3389/fmicb.2022.898979

  • CrossRef
  • Google Scholar

• 159

  SochaA. L.GuerinotM. L. (2014). Mn-euvering manganese: The role of transporter gene family members in manganese uptake and mobilization in plants. Front. Plant Sci.5, 106. 10.3389/fpls.2014.00106

  • CrossRef
  • Google Scholar

• 160

  SongW. Y.ParkJ.Mendoza-CózatlD. G.Suter-GrotemeyerM.ShimD.HörtensteinerS.et al (2010). Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. U. S. A.107, 21187–21192. 10.1073/pnas.1013964107

  • CrossRef
  • Google Scholar

• 161

  SouriZ.KarimiN.SandalioL. M. (2017). Arsenic hyperaccumulation strategies: An overview. Front. Cell. Dev. Biol.5, 67. 10.3389/fcell.2017.00067

  • CrossRef
  • Google Scholar

• 162

  SridharB. B. M.HanF. X.DiehlS. V.MontsD. L.SuY. (2011). Effect of phytoaccumulation of arsenic and chromium on structural and ultrastructural changes of brake fern (Pteris vittata). Bra. J. Plant. Physiol.23, 285–293. 10.1590/S1677-04202011000400006

  • CrossRef
  • Google Scholar

• 163

  SuY. H.McGrathS. P.ZhuY. G.ZhaoF. J. (2008). Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol.180, 434–441. 10.1111/j.14698137.2008.02584.x

  • CrossRef
  • Google Scholar

• 164

  SumanJ.UhlikO.ViktorovaJ.MacekT. (2018). Phytoextraction of heavy metals: A promising tool for clean-up of polluted environment?Front. Plant Sci.9, 1476. 10.3389/fpls.2018.01476

  • CrossRef
  • Google Scholar

• 165

  SungurA.KavdirY.ÖzcanH.İlayR.SoylakM. (2020). Geochemical fractions of trace metals in surface and core sections of aggregates in agricultural soils. Catena197, 104995. 10.1016/j.catena.2020.104995

  • CrossRef
  • Google Scholar

• 166

  TakahashiR.BashirK.IshimaruY.NishizawaN. K.NakanishiH. (2012). The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav.7, 1605–1607. 10.4161/psb.22454

  • CrossRef
  • Google Scholar

• 167

  TaoJ.LuL. (2022). Advances in genes-encoding transporters for cadmium uptake, translocation, and accumulation in plants. Toxics10, 411. 10.3390/toxics10080411

  • CrossRef
  • Google Scholar

• 168

  ThakurS.SinghL.WahidZ. A.SiddiquiM. F.AtnawS. M.DinM. F. M. (2016). Plant-driven removal of heavy metals from soil: Uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ. Monit. Assess.188, 206. 10.1007/s10661-016-5211-9

  • CrossRef
  • Google Scholar

• 169

  ThounaojamT. C.KhanZ.MeeteiT. T.SrivastavaS.PandaK. S.UpadhyayaH. (2021). Transporters: The molecular drivers of arsenic stress tolerance in plants. J. Plant Biochem. Biotechnol.30, 730–743. 10.1007/s13562-021-00748-z

  • CrossRef
  • Google Scholar

• 170

  TiwariG.DuraivadivelP.SharmaS.HariprasadP. (2018). 1-Aminocyclopropane-1-carboxylic acid deaminase producing beneficial rhizobacteria ameliorate the biomass characters of Panicum maximum Jacq. by mitigating drought and salt stress. Sci. Rep.8, 17513. 10.1038/s41598-018-35565-3

  • CrossRef
  • Google Scholar

• 171

  TongY-P.KneerR.ZhuY-G. (2004). Vacuolar compartmentalization: A second-generation approach to engineering plants for phytoremediation. Trends Plant Sci.9, 7–9. 10.1016/j.tplants.2003.11.009

  • CrossRef
  • Google Scholar

• 172

  Van de MortelJ. E.VillanuevaL. A.SchatH.KwekkeboomJ.CoughlanS.MoerlandP. D.et al (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator. Thlaspi Caerulescens. Plant Physiol.142, 1127–1147. 10.1104/pp.106.082073

  • CrossRef
  • Google Scholar

• 173

  VatamaniukO. K.MariS.LuY. P.ReaP. A. (2000). Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: Blocked thiols are sufficient for PC synthase catalyzed transpeptidation of glutathione and related thiol peptides. J. Biol. Chem.275, 31451–31459. 10.1074/jbc.m002997200

  • CrossRef
  • Google Scholar

• 174

  VerretF.GravotA.AuroyP.LeonhardtN.DavidP.NussaumeL.et al (2004). Overexpression of AtHMA4 enhances root−to−shoot translocation of zinc and cadmium and plant metal tolerance. Febs. Lett.576, 306–312. 10.1016/j.febslet.2004.09.023

  • CrossRef
  • Google Scholar

• 175

  VisioliG.D'EgidioS.SanangelantoniA. M. (2015). The bacterial rhizobiome of hyperaccumulators: Future perspectives based on omics analysis and advanced microscopy. Front. Plant Sci.5, 752. 10.3389/fpls.2014.00752

  • CrossRef
  • Google Scholar

• 176

  VisoottivisethaP.FrancesconibK.SridokchanW. (2002). The potential of Thai indigenous plant species for the phytoremediation of arsenic-contaminated land. Environ. Pollut.118, 453–461. 10.1016/s0269-7491(01)00293-7

  • CrossRef
  • Google Scholar

• 177

  Vogel-MikušK.PongracP.KumpP.NečemerM.RegvarM. (2006). Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ. Pollut.139, 362–371. 10.1016/j.envpol.2005.05.005

  • CrossRef
  • Google Scholar

• 178

  WangS.MulliganC. N. (2006). Effect of natural organic matter on arsenic release from soils and sediments into groundwater. Environ. Geochem. Health28, 197–214. 10.1007/s10653-005-9032-y

  • CrossRef
  • Google Scholar

• 179

  WangS. L.LiaoW.YuF. Q.LiaoB.ShuW. S. (2009). Hyperaccumulation of lead, zinc, and cadmium in plants growing on a lead/zinc outcrop in Yunnan Province, China. Environ. Earth Sci.58, 471–476. 10.1007/s00254-008-1519-2

  • CrossRef
  • Google Scholar

• 180

  WangX.TamN. F-Y.HeH.YeZ. (2015). The role of root anatomy, organic acids, and iron plaque on mercury accumulation in rice. Plant Soil.394, 301–313. 10.1007/s11104-015-2537-y

  • CrossRef
  • Google Scholar

• 181

  WhitingS. N.de SouzaM. P.TerryN. (2001). Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ. Sci. Technol.35, 3144–3150. 10.1021/es001938v

  • CrossRef
  • Google Scholar

• 182

  WiggenhauserM.AucourA. M.BureauS.CampilloS.TeloukP.RomaniM.et al (2021). Cadmium transfer in contaminated soil-rice systems: Insights from solid-state speciation analysis and stable isotope fractionation. Environ. Pollut.26, 115934. 10.1016/j.envpol.2020.115934

  • CrossRef
  • Google Scholar

• 183

  WilkinsK. A.MatthusE.SwarbreckM. S.DaviesJ. M. (2016). Calcium-mediated abiotic stress signaling in roots. Front. Plant Sci.7, 1296. 10.3389/fpls.2016.01296

  • CrossRef
  • Google Scholar

• 184

  WilliamsL. E.MillsR. F. (2005). P1B ATPases—An ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci.10, 491–502. 10.1016/j.tplants.2005.08.008

  • CrossRef
  • Google Scholar

• 185

  WioletaW.AnnaD.IlonaB.KamilaK.ElżbietaR. (2015). Lead-induced changes in phosphorylation of PSII proteins in low-light grown pea plants. Biometals28, 151–162. 10.1007/s10534-014-9811-y

  • CrossRef
  • Google Scholar

• 186

  WojcikM.TukiendorfA. (2005). Cadmium uptake, localization and detoxification in Zea mays. Zea Mays. Biol. Plant49, 237–245. 10.1007/s10535-005-7245-7

  • CrossRef
  • Google Scholar

• 187

  WoldetsadikD.DrechselP.KeraitaB.ItannaF.GebrekidanH. (2017). Heavy metal accumulation, and health risk assessment in wastewater-irrigated urban vegetable farming sites of Addis Ababa, Ethiopia. Int. J. Food. Contam.4, 9. 10.1186/s40550-017-0053-y

  • CrossRef
  • Google Scholar

• 188

  World Health Organization (1996). Permissible limits of heavy metals in soil and plants. Geneva, Switzerland: WHO.

  • Google Scholar

• 189

  WuC.LiaoB.WangS-L.ZhangJ.LiJ-T. (2010). Pb and Zn accumulation in a Cd-hyperaccumulator (Viola baoshanensis). Int. J. Phytol.12, 574–585. 10.1080/15226510903353195

  • CrossRef
  • Google Scholar

• 190

  WuC.ShiL.XueS.LiW.JiangX.RajendranM.et al (2019). Effect of sulfur-iron modified biochar on the available cadmium and bacterial community structure in contaminated soils. Sci. Total Environ.647, 1158–1168. 10.1016/j.scitotenv.2018.08.087

  • CrossRef
  • Google Scholar

• 191

  XiongQ.HuJ.WeiH.ZhangH.ZhuJ. (2021). Relationship between plant roots, rhizosphere microorganisms, and nitrogen and its special focus on rice. Agric.11, 234. 10.3390/agriculture11030234

  • CrossRef
  • Google Scholar

• 192

  XuW.DaiW.YanH.LiS.ShenH.ChenY.et al (2015). Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol. Plant8, 722–733. 10.1016/j.molp.2015.01.005

  • CrossRef
  • Google Scholar

• 193

  YamajiN.SasakiA.XiaJ.YokoshoK.MaJ. F. (2013). A node-based switch for preferential distribution of manganese in rice. Nat. Commun.4, 2442. 10.1038/ncomms3442

  • CrossRef
  • Google Scholar

• 194

  YanA.WangY.TanS. N.YusofM. L.GhoshS.ChenZ. (2020). Phytoremediation: A promising approach for revegetation of heavy metal-polluted land. Front. Plant Sci.11, 359. 10.3389/fpls.2020.00359Phytoremediation

  • CrossRef
  • Google Scholar

• 195

  YangQ.TuS.WangG.LiaoX.YanX. (2012). Effectiveness of applying arsenate-reducing bacteria to enhance arsenic removal from polluted soils by Pteris vittata L. Int. J. Phytoremed.14, 89–99. 10.1080/15226510903567471

  • CrossRef
  • Google Scholar

• 196

  YuanL.YangS.LiuB.ZhangM.WuK. (2012). Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell. Rep.31, 67–79. 10.1007/s00299-011-1140-9

  • CrossRef
  • Google Scholar

• 197

  ZemanováV.PavlíkováD.HniličkaF.PavlíkM. (2021). Arsenic toxicity-induced physiological and metabolic changes in the shoots of Pteris cretica and spinacia oleracea. Plants10, 2009. 10.3390/plants10102009

  • CrossRef
  • Google Scholar

• 198

  ZengX.XuH.LuJ.LiW.WuL.TangJ.et al (2020). The immobilization of soil cadmium by the combined amendment of bacteria and hydroxyapatite. Rep10, 2189. 10.1038/s41598-020-58259-1

  • CrossRef
  • Google Scholar

• 199

  ZhalninaK.ZenglerK.NewmanD.NorthernT. R. (2018). Need for laboratory ecosystems to unravel the structures and functions of soil microbial communities mediated by chemistry. mBio9, 011755–e1218. 10.1128/mBio.01175-18

  • CrossRef
  • Google Scholar

• 200

  ZhangY.CougnonF. B. L.WanniarachchiY. A.HaydenJ. A.NolanE. M. (2013). Reduction of human defensin 5 affords a high-affinity zinc chelating peptide. ACS Chem. Biol.8, 1907–1911. 10.1021/cb400340k

  • CrossRef
  • Google Scholar

• 201

  ZhangJ.MartinoiaE.LeeY. (2018). Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development. Plant Cell. Physiol.59, 1317–1325. 10.1093/pcp/pcy006

  • CrossRef
  • Google Scholar

• 202

  ZhangX.KuzyakovY.ZangH.MichaelaD. A.LinglingS.SpielvogelS.et al (2020). Rhizosphere hotspots: Root hairs and warming control microbial efficiency, carbon utilization, and energy production. Soil Biol. biochem.148, 107872. 10.1016/j.soilbio.2020.107872

  • CrossRef
  • Google Scholar

• 203

  ZhangJ.ChenJ.WuY-F.WangZ. P.QiuJ. G.LiX. L.et al (2021). Oxidation of organoarsenicals and antimonite by a novel flavin monooxygenase widely present in soil bacteria. Environ. Microbiol.24, 752–761. 10.1111/1462-2920.15488

  • CrossRef
  • Google Scholar

• 204

  ZhaoF. J.MaJ. F.MehargA. A.McGrathS. P. (2008). Arsenic uptake and metabolism in plants. New Phytol.181, 777–794. 10.1111/j.14698137.2008.02716.x

  • CrossRef
  • Google Scholar

• 205

  ZhuL-J.GuanD. X.LuoJ.RathinasabapathiB.MaL. Q. (2014). Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and. Pteris Multifida. Chemosphere113, 9–16. 10.1016/j.chemosphere.2014.03.081

  • CrossRef
  • Google Scholar

• 206

  ZubairM.ShakirM.AliQ.RaniN.FatimaN.FarooqS.et al (2016). Rhizobacteria and phytoremediation of heavy metals. Environ. Technol. Rev.5. 112–119. 10.1080/21622515.2016.1259358

  • CrossRef
  • Google Scholar