Next Article in Journal
Assessing the Ecotoxicological Effects of Emerging Drug and Dye Pollutants on Plant–Soil Systems Pre- and Post-Photocatalytic Wastewater Treatment
Previous Article in Journal
Orchid Flora of the Guelma Region (North-Eastern Algeria), a Little-Known Group for Algerian Flora
Previous Article in Special Issue
Comparative Analysis of Ca2+/Cation Antiporter Gene Family in Rosa roxburghii and Enhanced Calcium Stress Tolerance via Heterologous Expression of RrCAX1a in Tobacco
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 14
Issue 24
10.3390/plants14243834
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Plant Responses to Heavy Metal Stresses: Mechanisms, Defense Strategies, and Nanoparticle-Assisted Remediation

by
Aysha Siddika Jarin
1,†,
Md Arifur Rahman Khan
1,2,*,†,
Tasfiqure Amin Apon
3,
Md Ashraful Islam
4,
Al Rahat
5,
Munny Akter
1,
Touhidur Rahman Anik
2,
Huong Mai Nguyen
2,
Thuong Thi Nguyen
6,
Chien Van Ha
2,* and
Lam-Son Phan Tran
2,*
1
Department of Agronomy, Gazipur Agricultural University, Gazipur 1706, Bangladesh
2
Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA
3
Agronomy and Farming Systems Division, Bangladesh Sugarcrop Research Institute, Ishwardi 6620, Bangladesh
4
Department of Genetics and Plant Breeding, Gazipur Agricultural University, Gazipur 1706, Bangladesh
5
Department of Agroforestry, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
6
Vietnam National University of Agriculture, Ha Noi 100000, Vietnam
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Plants 2025, 14(24), 3834; https://doi.org/10.3390/plants14243834
Submission received: 29 September 2025 / Accepted: 27 October 2025 / Published: 16 December 2025
(This article belongs to the Special Issue Genetic and Biochemical Mechanisms of Abiotic Stress Responses in Phototropic Organisms)
Browse Figures
Review Reports Versions Notes

Abstract

Heavy metal (HM) contamination threatens environmental sustainability, food safety, and agricultural productivity worldwide. HM toxicity adversely affects plant growth, reducing germination rates by 20–50%, impairing seedling establishment, and inhibiting shoot and root development by 30–60% in various crops. HM disrupts key physiological processes, including photosynthesis, stomatal regulation, membrane integrity, nutrient uptake, and enzymatic and nonenzymatic antioxidant activities. These disruptions largely result from oxidative stress, caused by the excessive accumulation of reactive oxygen species, which damage cellular components. To counteract HM toxicity, plants deploy a complex defense network involving antioxidant enzymes, metal chelation by phytochelatins and metallothioneins, vacuolar sequestration, and symbiotic interactions with arbuscular mycorrhizal fungi, which can retain 40–70% of metals in roots and reduce translocation to shoots. At the molecular level, MAPK (Mitogen-Activated Protein Kinase) signaling pathways, transcription factors (e.g., WRKY, MYB, bZIP, and NAC), and phytohormonal crosstalk regulate the expression of stress-responsive genes expression to enhance HM stress tolerance. Advances in nanotechnology offer promising strategies for the remediation of HM-contaminated soils and water sources (HM remediation); engineered and biogenic nanoparticles (e.g., ZnO, Fe3O4) improve metal immobilization, reduce bioavailability, and enhance plant growth by 15–35% under HM stresses, although excessive doses may induce phytotoxicity. Future applications of nanotechnology in HM remediation should consider nanoparticle transformation (e.g., dissolution and agglomeration) and environmentally relevant concentrations to ensure efficacy and minimize phytotoxicity. Integrating phytoremediation with nanoparticle-enabled strategies provides a sustainable approach for HM remediation. This review emphasizes the need for a multidisciplinary framework linking plant science, biotechnology, and nanoscience to advance HM remediation and safeguard agricultural productivity.

1. Introduction

Heavy metals (HMs) are dense metallic elements with densities exceeding 5 g cm−3 and relatively high atomic weights [1,2,3]. HMs are non-biodegradable and can persist in the environment for long periods, leading to prolonged biological half-lives [1,2,3]. Arsenic (As), cadmium (Cd), chromium (Cr), mercury (Hg), and lead (Pb) are common HMs found in soils, water, and wastewater, primarily introduced via natural processes, anthropogenic activities, and agricultural practices [4,5,6,7]. In the rhizosphere, HMs interact with root exudates, altering their solubility and bioavailability, which may impair nutrient uptake and induce mineral deficiencies in plants [8,9]. HMs disrupt physiological and biochemical processes by generating oxidative stress, impairing protein synthesis and cell division, and causing symptoms such as leaf chlorosis and growth inhibition [9,10,11,12,13,14,15,16,17,18,19]. Cellular components, including plasma membranes, mitochondria, and chloroplasts are particularly vulnerable to HM-induced toxicity [15,20]. To cope with HM stress, plants have evolved several adaptive mechanisms, such as regulating metal uptake, enhancing antioxidant defenses, chelating and compartmentalizing HMs, and activating stress-responsive signaling pathways [8,9,21,22]. Detoxification strategies include symbiotic associations with mycorrhizal fungi, immobilization of metal ions via root exudates or cell wall binding, active efflux of metals across membranes, chelation by metal-binding peptides such as phytochelatins and metallothioneins, and sequestration into vacuoles to prevent cytosolic toxicity [23,24,25]. Phytoremediation represents a sustainable strategy for mitigating HM contamination, utilizing the metal-accumulating capabilities of plants and their associated rhizosphere microorganisms [24,25]. Furthermore, the incorporation of nanotechnology into remediation strategies also shows potential to enhance HM removal efficiency. However, its effectiveness depends on the type of metal, soil characteristics, and nanoparticle properties [8,26,27]. To fully harness the potential of nanoparticle-assisted remediation, a comprehensive understanding of the nanoscale interactions and the associated cellular and molecular mechanisms is essential.
This review aims to explore the morphological, physiological, biochemical, and molecular responses of plants to HM stress, focusing on their underlying defense mechanisms and current strategies in phytoremediation and nanoparticle-assisted remediation. Furthermore, it highlights critical knowledge gaps and outlines future research directions for the effective management of HM contamination.

2. Roles of Heavy Metals in Plants

HM stress negatively affects plant growth and development [28,29]. Table 1 presents the roles as well as the adequate and toxic levels of heavy metals in plants. While some HMs serve as essential micronutrients at trace levels, their excessive accumulation in plant tissues causes toxicity [30,31,32]. The severity of HM toxicity depends on the specific metal species, its chemical form, concentration, and plant type [33,34]. Non-essential HMs, such as As (≥5 mg kg−1 dry weight, DW), Cd (≥5 mg kg−1 DW), Cr (≥5 mg kg−1 DW), Hg (≥1 mg kg−1 DW), and Pb (≥30 mg kg−1 DW) are toxic to plants (Table 1). For example, Cd accumulation at toxic levels disrupts water and nutrient uptake, induces oxidative stress, impairs root development, and ultimately reduces crop productivity and food safety [35,36]. Hg predominantly accumulates in roots, with possible translocation to shoots, where it interferes with photosynthesis, respiration, and overall cellular metabolism by generating reactive oxygen species (ROS) and damaging cellular membranes [37,38]. Cr inhibits seed germination by 20–50%, reduces amylase activity, alters sugar transport to embryos, and decreases photosynthetic efficiency through oxidative damage [39,40]. Pb interferes with root and shoot growth (30–60%) in various crops as well as chlorophyll synthesis, stomatal regulation, and photosystem II efficiency, thereby impairing CO2 assimilation [41,42]. As, particularly arsenite (As3+, AsO33–), is primarily taken up via aquaporin channels and binds to sulfhydryl groups in proteins, inhibiting respiration by targeting dehydrogenases, promoting ROS production, and causing intrachromosomal recombination. In contrast, arsenate (As5+, AsO43–) is taken up mainly through phosphate transporters and is largely reduced to As3+ in roots, resulting in limited translocation to shoots, whereas As3+ can translocate more readily depending on the plant species and metal detoxification mechanisms [43]. Furthermore, combined exposure to HMs can exacerbate leaf and stem wilting, in purple loosestrife (Lythrum salicaria) and maize (Zea mays) [44,45]. Essential micronutrients, including copper (Cu), iron (Fe), manganese (Mn), molybdenum (Mo), and zinc (Zn), are vital for optimal vegetative and reproductive development in plants. Both deficiencies and excesses of these elements can disrupt physiological and biochemical processes, resulting in impaired growth, reduced photosynthetic efficiency, nutrient imbalances, and decreased crop productivity [46,47]. For instance, Cu (5–30 mg kg−1 DW) and Zn (25–150 mg kg−1 DW) concentrations enhance enzyme activity, photosynthetic efficiency, and antioxidant defense systems, thereby supporting overall plant growth and productivity [46,47,48,49]. Additionally, Cu and Zn nanoparticles have been reported to promote seed germination, root elongation, and stress tolerance by modulating ROS homeostasis and enhancing nutrient uptake [46,47,48,49,50,51]. Excess Cu (>30 mg kg−1 DW) inhibits seed germination and sugar metabolism by suppressing α-amylase and invertase activities, resulting in growth retardation and leaf chlorosis [51]. Similarly, excessive Fe (>500 mg kg−1 DW) and Mn (>1000 mg kg−1 DW) promote ROS generation, leading to membrane, protein, and DNA damage, which manifests as bronzing, chlorosis, and inhibited plant growth [52,53]. Elevated Mo interferes with nitrogen fixation in legumes, resulting in stunted growth and floral abnormalities [54]. High Zn concentrations (>150 mg kg−1 DW) suppress enzymatic activities (α-amylase, protease, ribonuclease), impair the mobilization of food reserves and carbonic anhydrase activity, increase malondialdehyde (MDA) content and electrolyte leakage, and ultimately reduce plant biomass [55,56,57,58,59]. Mung bean (Vigna radiata) and tomato (Solanum lycopersicum) exhibit enhanced growth at cobalt (Co) 0.02–2 mg kg−1 DW levels, whereas concentrations of >10 mg kg−1 DW induce toxicity, causing stunted growth and physiological disturbances [49,50]. Figure 1 illustrates the varying impacts of HMs on plants at toxic concentrations.

3. Morphological, Physiological, and Biochemical Responses to Heavy Metal Stresses

HM stress adversely affects morphological, physiological, and biochemical processes in plants. An overview of HM-induced changes in plant morphological, physiological, and biochemical processes is provided in Table 2. One of the primary effects of HM stress is a reduction in intra-leaf CO2 levels, which refers to the concentration of CO2 within the leaf mesophyll and directly affects photosynthetic carbon assimilation and leaf gas exchange characteristics [71,72]. HM stress adversely affects stomatal function through both direct accumulation in leaf tissues and the indirect disruption of key physiological processes, ultimately reducing the rates of photosynthesis and transpiration [72,73,74]. The regulation of ionic fluxes within guard cells plays a pivotal role in HM-induced stomatal dysfunction [73,74]. Since stomatal conductance directly influences CO2 uptake and water vapor loss, any alteration in stomatal morphology such as changes in size, density, or opening behavior can significantly impact leaf gas exchange, nutrient acquisition, and plant water balance [74]. For instance, Pb accumulation in soybean (Glycine max) guard cells disrupts cytoplasmic membrane integrity, resulting in potassium ion efflux, reduced guard cell turgor, and stomatal closure [75]. Additionally, Pb stress reduces transpiration in tobacco (Nicotiana tabacum) [76] and stomatal conductance in wheat (Triticum aestivum) and broadleaf plantain (Plantago major) [77,78]. Cd exposure induces stomatal closure, leading to decreased rates of photosynthesis, respiration, and water use efficiency, ultimately disrupting the plant’s energy [79,80]. In wheat, Cd stress results in lowered CO2 assimilation, reduced stomatal conductance, and diminished water use efficiency [81]. Cr stress significantly reduces stomatal conductance in maize (Zea mays), thereby limiting leaf gas exchange and negatively affecting photosynthetic activity [82]. Similarly, Zn stress reduces stomatal conductance in pigeon pea (Cajanus cajan) [83].
Plants counteract HM toxicity through the synthesis of phytochelatins (PCs) and metallothioneins (MTs), which chelate metals and reduce cytosolic toxicity. PCs preferentially bind Cd2+ and As3+, forming stable vacuolar complexes that limit cytosolic accumulation and oxidative damage, while MTs exhibit variable metal-binding affinities depending on the plant species. The specificity of PCs and MTs influences detoxification efficiency; for example, Cd2+ is rapidly chelated in roots, reducing shoot translocation, whereas As3+ complexes may be redistributed gradually. These mechanisms vary across species, with Arabidopsis (Arabidopsis thaliana) accumulating Cd–PC complexes mainly in roots, while rice (Oryza sativa) shows greater root-to-shoot Cd translocation. Differences in MT expression further modulate tolerance to multi-metal stress, highlighting species-specific strategies in HM detoxification. HM stress increases abscisic acid (ABA) synthesis, which activates the OST1 (Open Stomata 1) protein kinase while inhibiting protein phosphatase 2C (PP2C) activity [96,97]. Blocking PP2Cs prevents protein dephosphorylation, thus relieving the suppression of ABA signaling [98]. The Open Stomata 1 (OST1) represents one of the main targets of PP2Cs, with OST1 being the best-characterized member [100,101]. OST1 transmits the ABA signal by phosphorylating downstream targets and enhancing ROS production via NADPH oxidase activation [102]. Additionally, nitric oxide (NO) and reactive nitrogen species (RNS) act as secondary messengers, amplifying the signaling cascade under HM stress. As a redox-active free radical, NO can neutralize HM-induced ROS directly or by activating antioxidant defenses. However, an imbalance between NO, ROS, and antioxidant activity can trigger oxidative stress [103]. HM stress also disrupts the photosynthetic electron transport chain, leading to decreased Photosystem II activity. At elevated concentrations, HM stress disturbs the light-harvesting complex, particularly the transition between its functional states. This results in antenna complex disorganization and compromised photochemical efficiency [104]. HM stress disrupts glucose metabolism, tricarboxylic acid cycle, and photosynthesis, while inducing ABA, ROS, and NO production, leading to signaling cascades including PP2C, OST1, and 8-Nitro-cGMP that cause turgor loss and stomatal closure. These processes collectively reduce the rates of photosynthesis, transpiration, respiration, nutrient and water uptake, and leaf area, while causing ion imbalance and cell membrane damage. The impact of HM stress on the physiological functions of plants is illustrated in Figure 2.

4. Disruption of Cell Membrane Integrity, Oxidative Homeostasis, and Enzymatic Activities Under Heavy Metal Stresses

HMs can penetrate cell membranes and bind to essential components such as proteins and phospholipids [105]. HMs interfere with membrane integrity, disrupt transport processes, displace calcium ions from critical binding sites, and reduce the availability of ATPase substrates by binding to adenosine triphosphate (ATP) [106,107]. HM stress strongly promotes the formation of hydroxyl free radicals, triggering lipid peroxidation through primary initiation as well as via the Haber–Weiss and Fenton reactions [108]. HM stress also leads to the accumulation of methylglyoxal in plants, which impairs antioxidant defense by depleting glutathione levels [109,110,111]. Redox-active metals such as Cu, Fe, and Cr can directly generate ROS [112], while redox-inactive metals such as Cd, Pb, and Zn promote ROS accumulation indirectly by impairing the plant’s antioxidant defense system, triggering calcium-dependent signaling pathways, and disturbing iron metabolism [111,112,113,114,115,116]. On the other hand, Cd, Pb, Ni, and Cr can substitute for vital cofactors like Mg, Zn, Fe, and Ca in enzymes such as RuBisCO and superoxide dismutases, resulting in impaired enzymatic activity and disrupted cellular signaling [117,118]. For example, Cd disrupts cellular functions by displacing Zn in zinc-finger transcription factors and Ca in calmodulin, thereby altering gene expression and impairing stomatal regulation, whereas Pb interferes with chlorophyll structure and photosystem II activity, ultimately reducing photosynthetic efficiency [119,120]. Additionally, arsenate (AsO43–) stress can mimic phosphate and disrupt ATP synthesis [121]. It also binds strongly to protein sulfhydryl (–SH) and carboxyl (–COOH) groups, leading to enzyme denaturation [105,122,123,124,125,126,127].

5. Plants’ Resistance Mechanisms to Heavy Metal Stresses

Plants cope with HM stress through two main resistance strategies: avoidance and tolerance. Avoidance mechanisms, such as mycorrhizal immobilization, root exudate complexation, and rhizosphere pH adjustment, function to prevent metal uptake and entry into root tissues. Among these avoidance strategies, immobilization by mycorrhizal associations is particularly effective for its role in restricting metal translocation and mitigating toxicity. When metals do enter plant cells, tolerance mechanisms are triggered, including the enhancement of antioxidant defenses, production of stress-associated proteins, and gene regulation to detoxify and compartmentalize the metals into less harmful forms in plants.

5.1. Immobilization by Mycorrhizal Associations

Mycorrhizal fungi, particularly arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (ECM), play a vital role in enhancing plant tolerance to HM stress by forming symbiotic associations with roots [128,129]. These fungi reduce HM uptake through chelation, adsorption, and the release of organic acids and glomalin [130,131]. Extraradical hyphae of AMF extend beyond the root zone, improving nutrients such as N, P, and K uptake, which in turn enhances plant growth and HM stress resistance [132,133]. AMF can retain 40–70% of metals in root tissues via chelation, while extraradical and intraradical hyphae provide additional binding surfaces containing glucan, chitin, and galactosamine polymers [134]. They also release organic acids such as citric, malic, and oxalic acids that immobilize HMs by forming stable complexes [131]. A major contribution of AMF is the secretion of glomalin, a glycoprotein with high metal-binding affinity, which stabilizes soil aggregates and reduces HM bioavailability. Evidence shows that AMF inoculation promotes HM retention in roots and reduces their movement to aerial tissues, often resulting in significantly lower concentrations in edible parts [135]. For example, Adeyemi et al. [134] reported that AMF inoculation enhanced P uptake and restricted HM transport to shoots in soybean (Glycine max), while eggplants (Solanum melongena) inoculated with AMF accumulated less Pb in fruits, improving growth and food safety. Although most studies confirm reduced translocation, small amounts of metals may still reach aboveground tissues at lower concentrations, and the precise mechanisms controlling long-distance movement remain only partly understood. In addition to AMF, ECM form a fungal sheath around roots and secrete extracellular polymers and organic acids that immobilize metals in the rhizosphere. ECM are particularly important for woody plants and act primarily as barriers to HM entry, whereas AMF combine nutrient acquisition with HM detoxification. Together, these two groups of fungi represent complementary strategies for enhancing plant tolerance to metal-contaminated soils. Through these mechanisms, mycorrhizal associations enhance nutrient transport, detoxify HMs, and improve biomass accumulation, especially during active phases of plant growth. They also block pathogen invasion, enrich beneficial rhizosphere microbes, and modulate phytohormone levels (e.g., IAA, cytokinins), further supporting root health and plant vigor [136,137,138,139]. Figure 3 illustrates the enhancement of HM detoxification, nutrient transport, and biomass accumulation in plants through microbial functions. Thus, mycorrhizal symbiosis functions as a critical plant defense strategy in HM-contaminated environments, providing both direct detoxification and indirect growth benefits. Nonetheless, knowledge gaps remain regarding the regulation of HM translocation from roots to shoots, warranting further research to fully elucidate these processes.

5.2. Root-Mediated Mechanisms and Phytochelatin-Driven Detoxification Under Heavy Metal Stresses

Among the diverse strategies employed by plants to withstand HM toxicity, root-mediated mechanisms and PC-driven detoxification play pivotal roles. Cellular mechanisms of HM detoxification and sequestration in plants are illustrated in Figure 4. Roots serve as the primary site for HM perception and uptake. One of the key defense strategies involves the secretion of root exudates, which include diffusates (e.g., peptides, carboxylic acids, and carbohydrates), excretions (e.g., protons, bicarbonates, and CO2), and secretions (e.g., mucilage, siderophores, and allelochemicals) [140]. These compounds contribute to the formation of stable metal complexes in the rhizosphere, thereby reducing HM solubility, mobility, and toxicity near the root surface [141]. Organic acids chelate metal ions and reduce their toxicity. Additionally, amino acids like histidine and nicotianamine act as metal chelators, enhancing the solubility and translocation of micronutrients such as Fe and Zn. Root-derived sugars and amino acids can also increase rhizosphere pH and modify redox conditions, encouraging metal precipitation and improving nutrient availability [142]. PCs and MTs play critical roles in chelating metal ions and mediating their compartmentalization particularly into vacuoles thereby minimizing cytosolic toxicity [143,144,145,146]. PCs can form stable complexes with a wide range of metal ions including Cd2+, As3+, Pb2+, and Zn2+ [147]. Their synthesis is rapidly upregulated following HM exposure, utilizing cytosolic glutathione present in millimolar concentrations as a substrate [148]. Once formed, PC-metal complexes are actively transported into the vacuole via tonoplast-localized ATP-Binding cassette transporters or metal/H+ antiporters, effectively sequestering toxic metals from the cytosol and protecting sensitive enzymatic processes [145]. Inside the vacuole, these complexes may undergo further stabilization through interactions with inorganic sulfide or sulfite ions, which shield them from proteolytic degradation. Over time, this compartmentalization may result in the formation of insoluble crystalline metal deposits, contributing to long-term immobilization and detoxification of HMs [148]. In addition to their detoxification function, PCs are also involved in metal homeostasis, particularly in regulating the uptake and distribution of essential micronutrients such as Zn and Cu [149,150]. In parallel, MTs serve as metal-binding ligands that assist in detoxifying excess metal ions while also regulating the availability of essential elements such as Zn and Cu. In plants, MTs are categorized into subfamilies (e.g., MT1 and MT2) based on the arrangement of their cysteine domains, which determine their metal-binding specificity and biological roles [151]. In addition to PC- and MT-mediated chelation, plants utilize several cellular barriers and strategies to limit HMs entry and toxicity:
i.
Plant’s cell wall, rich in pectin and lignin, can adsorb HMs through ion exchange, thereby reducing metal mobility and entry into cells [152].
ii.
Specific membrane transporters and channel proteins regulate HM uptake. Under HM stress, plants often downregulate these transporters to reduce metal influx [118].
iii.
Chelation is a widespread detoxification mechanism involving intracellular ligands such as PCs, MTs, organic acids (e.g., citric, malic, oxalic acids), and amino acids (e.g., histidine, nicotianamine), which bind free metal ions and prevent them from interfering with vital metabolic processes [153].
iv.
The tonoplast (vacuolar membrane) minimizes HM movement back into the cytoplasm via active permeability mechanisms, serving as a dynamic barrier against metal recirculation [147].
v.
Once PC-metal complexes are formed, they are transported into vacuoles and ultimately converted into insoluble metal deposits, stabilizing the intracellular environment and preventing oxidative damage [149,153].

5.3. Antioxidant Responses to Heavy Metal Stresses

Antioxidant enzymes play a central role in mitigating oxidative damage in plants exposed to HM stresses [112,113,114]. HM exposure induces the production of heat shock proteins (HSPs), which act as molecular chaperones, helping stabilize proteins and preserve membrane integrity. Studies show that various HSPs, including low-molecular-weight forms and HSP70, are upregulated in different plant species under HM stress [154,155,156,157]. Cd, Pb, Cr, and Hg induce overproduction of ROS, including superoxide radicals, hydrogen peroxide, and hydroxyl radicals, which disrupt cellular homeostasis [158,159]. In response, plants activate enzymatic defense mechanisms involving superoxide dismutase (SOD), catalase (CAT), peroxidases (POD), ascorbate peroxidase (APX), and glutathione reductase (GR) [160,161,162,163,164]. However, the intensity and efficiency of these responses vary with plant species, developmental stage, metal type, and exposure level. An overview of plant antioxidant enzyme responses to HM stress is provided in Table 3. In addition to enzymatic antioxidants, plants also accumulate secondary metabolites which further support ROS detoxification and improve stress resilience [161,165,166,167,168]. These metabolites help mitigate HM toxicity by chelating metals in the rhizosphere and scavenging ROS within the cells.

5.4. Regulation of Signaling Pathways and Gene Expression in Plants Under Heavy Metal Stresses

HM exposure triggers complex signaling pathways in plants that regulate gene expression and activate defense mechanisms. A major downstream signaling route is the mitogen-activated protein kinase cascade, which integrates signals from ROS, nitric oxide, and phytohormones to regulate stress-responsive genes [177]. These coordinated responses help initiate detoxification and stress adaptation processes. Crosstalk among signaling pathways ensures fine-tuned regulation, enabling plants to maintain metal homeostasis and resist toxicity [178]. Key signaling pathways and associated molecular players implicated in plant adaptation to HM stress are summarized in Table 4. Understanding these mechanisms is essential for advancing crop resilience to HM-contaminated environments.
Transcription factors (TFs) play a pivotal role in regulating plant responses to HM stress by modulating the expression of stress-responsive genes [185,186,187]. An overview of transcription factors activated during HM stress in plants is provided in Table 5. TFs act as molecular switches that activate or repress target genes involved in metal uptake, transport, sequestration, and detoxification. Key TF families, such as bZIP (basic leucine zipper transcription factor), MYB (myeloblastosis transcription factor), WRKY (tryptophan–arginine–lysine–tyrosine transcription factor), NAC, and AP2/ERF, coordinate a wide range of physiological and biochemical processes, including antioxidant defense, synthesis of metal-binding ligands (e.g., PCs and MTs), and regulation of ion transporters [187,188,189,190,191,192,193]. Mechanistically, WRKY TFs are frequently upregulated under Cd stress, where they activate downstream genes encoding antioxidant enzymes and phytochelatin synthases, thereby enhancing detoxification capacity. MYB TFs preferentially respond to Pb stress, regulating secondary metabolism and ion transport to limit Pb translocation to shoots [182,194,195]. bZIP TFs are strongly linked to redox homeostasis, integrating ROS signaling with metal-induced oxidative stress responses, while NAC and AP2/ERF TFs coordinate hormonal signaling pathways (e.g., ABA, ethylene) that fine-tune stress-responsive gene expression [182,195]. Under combined metal exposure (e.g., Cd + Pb), crosstalk among these TFs integrates overlapping yet distinct signaling networks, synchronizing antioxidant defenses, metal chelation, and ion homeostasis [194,195,196,197,198,199]. This integrated regulation highlights how plants orchestrate both metal-specific and multi-metal tolerance strategies, providing mechanistic insights valuable for engineering crops with enhanced resilience to HM stress.
Transgenic approaches have proven effective in improving plant tolerance HM stress. Overexpression of genes such as phytochelatin synthase or metal transporters (HMA3, Nramp) enhances HM sequestration and limits translocation to shoots, reducing cytosolic toxicity [185,186,187,188,189,190,191]. Antioxidant genes further mitigate oxidative damage and preserve photosynthetic efficiency [158,159,160,165,166,167,168]. Combining these genetic strategies with nanoparticle-assisted remediation offers synergistic benefits: nanoparticles immobilize HMs in the rhizosphere, while transgenic plants efficiently chelate and compartmentalize metals intracellularly. This integrated approach enhances plant growth, stress tolerance, and HM removal efficiency, highlighting the potential of biotechnology in conjunction with nanotechnology for HM-contaminated soils.
CRISPR/Cas9 genome editing offers a precise approach to improve plant tolerance to HM stress. By targeting key genes, transcription factors (e.g., WRKY, MYB, bZIP), and metal transporters, CRISPR/Cas9 can reduce metal uptake and translocation, enhance antioxidant defenses, and strengthen PC or MT-mediated detoxification [182,194]. Studies in rice, Arabidopsis, and wheat have shown that such modifications can improve growth, stress tolerance, and yield under HM exposure, providing an efficient strategy to develop HM-resilient crops.

6. Nanoparticle-Mediated Alleviation of Heavy Metal Stresses in Plants

Nanoparticles (NPs) have demonstrated significant potential in alleviating the adverse effects of HM stress in plants [205]. At low concentrations, NPs can stimulate plant growth, enhance stress resistance, and improve photosynthetic efficiency. However, excessive exposure may cause phytotoxicity, including oxidative damage, growth inhibition, and impaired nutrient uptake [206]. Understanding the dose-dependent behavior of NPs is therefore critical for their safe and effective application. NPs can affect HM root-to-shoot translocation by immobilizing metals in the rhizosphere or binding them within root tissues, thus reducing their translocation to shoots [207,208]. For example, Fe3O4 NPs reduce Cd mobility in wheat roots and shoots, while mercapto-functionalized silica nanoparticles (SiNPs) stabilize Cd in less bioavailable forms [209,210]. ZnO NPs enhance antioxidant defenses in white leadtree (Leucaena leucocephala), mitigating Cd and Pb toxicity, and can interact with endogenous phytochelatins and metallothioneins to form stable metal-ligand complexes, further reducing cytosolic toxicity [211,212,213]. These interactions are often concentration-dependent, with optimal NP levels promoting growth and metal detoxification, whereas excessive doses can disrupt cellular redox homeostasis and metal chelation, highlighting the need to determine safe application thresholds. Beyond plant-level effects, the environmental fate of nanoparticles must be considered. Uncontrolled or excessive NP application may affect soil microbial communities, bioaccumulate in non-target organisms, or contaminate soil and water ecosystems. Therefore, careful monitoring, dose optimization, and ecological risk assessment are essential for the sustainable use of nanoparticles in HM remediation. Table 6 presents different nanoparticles used to mitigate HM stress in plants, highlighting their roles in enhancing tolerance and reducing toxicity.

7. Nanoparticle-Assisted Bioremediation Against Heavy Metal Stresses

Nanoparticle-assisted bioremediation represents a promising and eco-friendly strategy that merges nanotechnology with biological approaches, particularly the use of microorganisms to detoxify HMs stress [222,223]. For example, bacteria such as Pseudomonas aeruginosa, Bacillus subtilis, Rhizobium spp., and Staphylococcus aureus can biosynthesize NPs with high adsorption capacity, enabling effective HM immobilization [224]. Fungal genera like Aspergillus, Rhizopus, and Penicillium contribute to HM remediation [225]. Plant-derived NPs, synthesized using extracts from Camellia sinensis, Citrus limon, and Mangifera indica, benefit from stabilization by secondary metabolites, enhancing their biocompatibility and remediation potential [226]. Polyvinylpyrrolidone (PVP)-coated iron oxide NPs combined with Halomonas sp. achieved 100% removal of Cd2+ and 80% removal of Pb2+ within 24 h, far outperforming NPs used alone [227]. Biogenic manganese oxide (MnO) NPs synthesized by bacteria and fungi have demonstrated excellent cation exchange and redox capacity, enabling effective reduction of Cd, Cu, Pb, and Zn in contaminated soils [228,229]. Remarkably, biogenic MnO from Pseudomonas putida MnB1 exhibits 7–8 times greater HM adsorption across diverse environmental conditions. However, the potential ecological risks of nanoparticles should not be overlooked. Excessive or uncontrolled NP application may lead to phytotoxicity, disruption of soil microbial communities, bioaccumulation in non-target organisms, and contamination of water and soil ecosystems. Therefore, careful dose optimization, environmental risk assessment, and monitoring are essential for the safe and sustainable implementation of nanoparticle-assisted remediation strategies. Table 7 summarizes the microbial isolates used for NP biosynthesis and their applications in mitigating HM stress in plants.

8. Conclusions and Future Research Directions

Growing prevalence of HM contamination in agricultural ecosystems poses a significant threat to ecosystem health and the sustainability of food production systems. HM stress disrupts essential plant functions by restricting shoot and root development, delaying seedling establishment, while impairing key physiological and metabolic processes including photosynthesis, respiration, water and nutrient uptake, enzymatic activities, and hormonal signaling pathways. These disruptions lead to the excessive generation of ROS, resulting in oxidative stress that causes cellular damage, growth inhibition, and substantial reductions in crop yield and quality. To counteract HM toxicity, plants have evolved a complex network of defense mechanisms operating at physiological, biochemical, and molecular levels. Physiological strategies include root exudation, modulation of ion transport, and regulation of stomatal conductance to limit metal uptake and mitigate stress impacts. Biochemical responses to HM stress involve the synthesis of phytochelatins and metallothioneins for metal chelation and sequestration, alongside the activation of enzymatic (e.g., SOD, CAT, POD) and non-enzymatic (e.g., AsA, GSH) antioxidant systems to scavenge ROS and maintain cellular redox balance. At the molecular level, plants employ transcriptional reprogramming, signal transduction cascades that regulate stress-responsive genes and pathways. Key transcription factors, including WRKY, MYB, bZIP, and NAC families, along with MAPK signaling cascades, play pivotal roles in orchestrating gene expression and enhancing plant resilience under HM stress. Moreover, the advent of engineered NPs and nanoparticle-assisted bioremediation offers promising avenues for enhancing HM immobilization, reducing bioavailability, and promoting safer crop production. Nanoparticle-assisted bioremediation, which integrates biologically synthesized nanoparticles with traditional bioremediation approaches, holds promise for increasing reactivity, improving microbial resilience, and targeting specific contaminants. To bridge existing gaps and advance sustainable HM remediation strategies, future research should focus on:
i.
Deciphering complex plant–microbiome–NPs interactions to optimize rhizosphere processes for HM detoxification.
ii.
Applying synthetic biology and CRISPR/Cas9-based gene editing to enhance key regulatory genes, transcription factors, and transporters for improved HM stress tolerance.
iii.
Integrating multi-omics tools to unravel the regulatory networks and crosstalk between physiological, biochemical, and molecular pathways involved in HM stress tolerance.
iv.
Evaluating the long-term ecological risks and field performance of NPs, with emphasis on safe design, environmental fate, and regulatory frameworks.
v.
Developing scalable, field-applicable nanoparticle-assisted phytoremediation protocols that combine engineered plants, beneficial microbes, and smart nanomaterials for site-specific remediation.
Collectively, these efforts will help transform laboratory advances into practical, sustainable solutions for managing HM stress in agroecosystems, ensuring resilient food production systems and safeguarding the environment for future generations.

Author Contributions

Conceptualization, A.S.J. and M.A.R.K.; visualization, A.S.J. and M.A.R.K.; writing—original draft, A.S.J. and M.A.R.K.; supervision, M.A.R.K.; writing—review and editing, M.A.R.K., T.A.A., M.A.I., A.R., M.A., T.R.A., H.M.N., T.T.N., C.V.H. and L.-S.P.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Acknowledgments

The authors express their heartfelt gratitude to the University Grants Commission of Bangladesh for supporting the project titled “Morpho-physiological and biochemical changes of cowpea genotypes under saline conditions”, to the Ministry of Science and Technology for the special research grant (2022–2023, SRG-221152), and to the Research Management Wing of Gazipur Agricultural University, Gazipur 1706, Bangladesh (Project ID: 05/2020), for their contributions to this work. During the preparation of this manuscript, the authors used OpenAI’s ChatGPT (GPT-5-mini) for the purposes of language refinement and grammar correction of the manuscript text. The authors have reviewed and edited the output and take full responsibility for the content of this publication.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships which influenced the work composing this paper. No data was used for the research described in the article.

References

  1. Baker, A.J.M. Accumulators and excluders-strategies in the response of plants to heavy metals. J. Plant Nutr. 1981, 3, 643–654. [Google Scholar] [CrossRef]
  2. Hanikenne, M.; Nouet, C. Metal hyperaccumulation and hypertolerance: A model for plant evolutionary genomics. Curr. Opin. Plant Biol. 2011, 14, 252–259. [Google Scholar] [CrossRef]
  3. Luo, X.S.; Yu, S.; Zhu, Y.G.; Li, X.D. Trace metal contamination in urban soils of China. Sci. Total Environ. 2012, 421, 17–30. [Google Scholar] [CrossRef]
  4. Fu, Z.; Guo, W.; Dang, Z.; Hu, Q.; Wu, F.; Feng, C.; Zhao, X.; Meng, W.; Xing, B.; Giesy, J.P. Refocusing on nonpriority toxic metals in the aquatic environment in China. Environ. Sci. Technol. 2017, 51, 13960–13962. [Google Scholar] [CrossRef]
  5. Burakov, A.E.; Galunin, E.V.; Burakova, I.V.; Kucherova, A.E.; Agarwal, S.; Tkachev, A.G.; Gupta, V.K. Adsorption of heavy metals on conventional and nanostructured materials for wastewater treatment purposes: A review. Ecotoxicol. Environ. Saf. 2017, 148, 702–712. [Google Scholar] [CrossRef]
  6. Singh, S.; Kapoor, D.; Khasnabis, S.; Singh, J.; Ramamurthy, P.C. Mechanism and kinetics of adsorption and removal of heavy metals from wastewater using nanomaterials. Environ. Chem. Lett. 2021, 19, 2351–2381. [Google Scholar] [CrossRef]
  7. Nazar, R.; Iqbal, N.; Masood, A.; Khan, M.I.R.; Syeed, S.; Khan, N.A. Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am. J. Plant Sci. 2012, 3, 1476–1489. [Google Scholar] [CrossRef]
  8. Ali, Q.; Zia, M.A.; Kamran, M.; Shabaan, M.; Zulfiqar, U.; Ahmad, M.; Maqsood, M.F. Nanoremediation for heavy metal contamination: A review. Hybrid Adv. 2023, 4, 100091. [Google Scholar] [CrossRef]
  9. Saeed, M.; Ilyas, N.; Bibi, F.; Shabir, S.; Mehmood, S.; Akhtar, N.; Eldin, S.M. Nanoremediation approaches for the mitigation of heavy metal contamination in vegetables: An overview. Nanotechnol. Rev. 2023, 12, 20230156. [Google Scholar] [CrossRef]
  10. Małkowski, E.; Sitko, K.; Zieleźnik-Rusinowska, P.; Gieroń, Ż.; Szopiński, M. Heavy metal toxicity: Physiological implications of metal toxicity in plants. In Plant Metallomics and Functional Omics; Springer: Cham, Switzerland, 2019; pp. 253–301. [Google Scholar] [CrossRef]
  11. Ghori, N.; Ghori, T.; Hayat, M.Q.; Imadi, S.R.; Gul, A.; Altay, V.; Ozturk, M. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 2019, 16, 1807–1828. [Google Scholar] [CrossRef]
  12. Krämer, U. Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 2010, 61, 517–534. [Google Scholar] [CrossRef]
  13. Verbruggen, N.; Hermans, C.; Schat, H. Mechanisms to cope with arsenic or cadmium excess in plants. Curr. Opin. Plant Biol. 2009, 12, 364–372. [Google Scholar] [CrossRef] [PubMed]
  14. Schat, H.; Llugany, M.; Bernhard, R. Metal-specific patterns of tolerance, uptake, and transport of heavy metals in hyperaccumulating and nonhyperaccumulating metallophytes. In Phytoremediation of Contaminated Soil and Water, 1st ed.; CRC Press: Boca Raton, FL, USA, 2020; pp. 171–188. [Google Scholar] [CrossRef]
  15. Khan, S.; Rehman, S.; Khan, A.Z.; Khan, M.A.; Shah, M.T. Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan. Ecotoxicol. Environ. Saf. 2010, 73, 1820–1827. [Google Scholar] [CrossRef] [PubMed]
  16. Shahid, M.; Pinelli, E.; Pourrut, B.; Silvestre, J.; Dumat, C. Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol. Environ. Saf. 2010, 74, 78–84. [Google Scholar] [CrossRef] [PubMed]
  17. Wu, S.; Zhang, X.; Chen, B.; Wu, Z.; Li, T.; Hu, Y.; Sun, Y.; Wang, Y. Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environ. Exp. Bot. 2016, 122, 10–18. [Google Scholar] [CrossRef]
  18. Bini, C.; Wahsha, M.; Fontana, S.; Maleci, L. Effects of heavy metals on morphological characteristics of Taraxacum officinale Web growing on mine soils in NE Italy. J. Geochem. Explor. 2012, 123, 101–108. [Google Scholar] [CrossRef]
  19. Khan, A.; Khan, S.; Khan, M.A.; Qamar, Z.; Waqas, M. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environ. Sci. Pollut. Res. 2015, 22, 13772–13799. [Google Scholar] [CrossRef]
  20. Mellem, J.J.; Baijnath, H.; Odhav, B. Translocation and accumulation of Cr, Hg, As, Pb, Cu and Ni by Amaranthus dubius (Amaranthaceae) from contaminated sites. J. Environ. Sci. Health Part A 2009, 44, 568–575. [Google Scholar] [CrossRef]
  21. Maleki, M.; Ghorbanpour, M.; Kariman, K. Physiological and antioxidative responses of medicinal plants exposed to heavy metals stress. Plant Gene 2017, 11, 247–254. [Google Scholar] [CrossRef]
  22. Michalak, A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol. J. Environ. Stud. 2006, 15, 523–530. [Google Scholar]
  23. Delmar, J.A.; Su, C.C.; Yu, E.W. Heavy metal transport by the CusCFBA efflux system. Protein Sci. 2015, 24, 1720–1736. [Google Scholar] [CrossRef]
  24. Dhalaria, R.; Kumar, D.; Kumar, H.; Nepovimova, E.; Kuča, K.; Torequl Islam, M.; Verma, R. Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy 2020, 10, 815. [Google Scholar] [CrossRef]
  25. Agarwal, P.; Vibhandik, R.; Agrahari, R.; Daverey, A.; Rani, R. Role of root exudates on the soil microbial diversity and biogeochemistry of heavy metals. Appl. Biochem. Biotechnol. 2024, 196, 2673–2693. [Google Scholar] [CrossRef]
  26. Ma, Y.; Zhang, C.; Oliveira, R.S.; Freitas, H.; Luo, Y. Bioaugmentation with endophytic bacterium E6S homologous to Achromobacter piechaudii enhances metal Rhizoaccumulation in host Sedum plumbizincicola. Front. Plant Sci. 2016, 7, 75. [Google Scholar] [CrossRef]
  27. Muthusaravanan, S.; Sivarajasekar, N.; Vivek, J.S.; Paramasivan, T.; Naushad, M.; Prakashmaran, J.; Gayathri, V.; Al-Duaij, O.K. Phytoremediation of heavy metals: Mechanisms, methods and enhancements. Environ. Chem. Lett. 2018, 16, 1339–1359. [Google Scholar] [CrossRef]
  28. Hussain, A.; Abbas, N.; Arshad, F.; Akram, M.; Khan, Z.I.; Ahmad, K.; Mansha, M.; Mirzaei, F. Effects of diverse doses of lead (Pb) on different growth attributes of Zea mays L. Agric. Sci. 2013, 4, 262–265. [Google Scholar] [CrossRef]
  29. Bharti, R.; Sharma, R. Effect of heavy metals: An overview. Mater. Today Proc. 2022, 51, 880–885. [Google Scholar] [CrossRef]
  30. Djingova, R.; Kuleff, I. Instrumental techniques for trace analysis. In Trace Metals in the Environment; Elsevier: Amsterdam, The Netherlands, 2000; Volume 4, pp. 137–185. [Google Scholar] [CrossRef]
  31. Raskin, I.; Ensley, B.D. Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment; John Wiley & Sons: Hoboken, NJ, USA, 2000; Available online: http://ci.nii.ac.jp/ncid/BA45677643 (accessed on 28 September 2025).
  32. Jadia, C.D.; Fulekar, M.H. Phytoremediation of heavy metals: Recent techniques. Afr. J. Biotechnol. 2009, 8, 921–928. [Google Scholar]
  33. Upadhyay, M.K.; Majumdar, A. Heavy metals’ stress responses in field crops. In Response of Field Crops to Abiotic Stress; CRC Press: Boca Raton, FL, USA, 2022; pp. 45–54. [Google Scholar] [CrossRef]
  34. Taiz, L.; Zeiger, E. Plant Physiology, 3rd ed.; Sinauer Associates: Sunderland, MA, USA, 2002. [Google Scholar]
  35. Farooq, M.A.; Detterbeck, A.; Clemens, S.; Dietz, K.J. Silicon-induced reversibility of cadmium toxicity in rice. J. Exp. Bot. 2016, 67, 3573–3585. [Google Scholar] [CrossRef]
  36. Ruyter-Hooley, M.; Larsson, A.C.; Johnson, B.B.; Antzutkin, O.N.; Angove, M.J. The effect of inositol hexaphosphate on cadmium sorption to gibbsite. J. Colloid Interface Sci. 2016, 474, 159–170. [Google Scholar] [CrossRef]
  37. Fernández-Martínez, R.; Larios, R.; Gómez-Pinilla, I.; Gómez-Mancebo, B.; López-Andrés, S.; Loredo, J.; Ordóñez, A.; Rucandio, I. Mercury accumulation and speciation in plants and soils from abandoned cinnabar mines. Geoderma 2015, 253–254, 30–38. [Google Scholar] [CrossRef]
  38. Messer, R.L.; Lockwood, P.E.; Tseng, W.Y.; Edwards, K.; Shaw, M.; Caughman, G.B.; Lewis, J.B.; Wataha, J.C. Mercury (II) alters mitochondrial activity of monocytes at sublethal doses via oxidative stress mechanisms. J. Biomed. Mater. Res. Part B Appl. Biomater. 2005, 75, 257–263. [Google Scholar] [CrossRef] [PubMed]
  39. Zeid, I. Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol. Plant. 2001, 44, 111–115. [Google Scholar] [CrossRef]
  40. Srivastava, D.; Tiwari, M.; Dutta, P.; Singh, P.; Chawda, K.; Kumari, M.; Chakrabarty, D. Chromium stress in plants: Toxicity, tolerance and phytoremediation. Sustainability 2021, 13, 4629. [Google Scholar] [CrossRef]
  41. Pourrut, B.; Jean, S.; Silvestre, J.; Pinelli, E. Lead-induced DNA damage in Vicia faba root cells: Potential involvement of oxidative stress. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2011, 726, 123–128. [Google Scholar] [CrossRef]
  42. Dao, L.H.; Beardall, J. Effects of lead on two green microalgae Chlorella and Scenedesmus: Photosystem II activity and heterogeneity. Algal Res. 2016, 16, 150–159. [Google Scholar] [CrossRef]
  43. Helleday, T.; Nilsson, R.; Jenssen, D. Arsenic [III] and heavy metal ions induce intrachromosomal homologous recombination in the hprt gene of V79 Chinese hamster cells. Environ. Mol. Mutagen. 2000, 35, 114–122. [Google Scholar] [CrossRef]
  44. Nicholls, A.M.; Mal, T.K. Effects of lead and copper exposure on growth of an invasive weed, Lythrum salicaria L. (Purple Loosestrife). Ohio J. Sci. 2003, 103, 129–133. [Google Scholar]
  45. Abdul, G. Toxic effects of heavy metals on plant growth and metal accumulation in maize (Zea mays L.). Iran. J. Toxicol. 2010, 3, 325–334. [Google Scholar]
  46. Van Nguyen, D.; Nguyen, H.M.; Le, N.T.; Nguyen, K.H.; Nguyen, H.T.; Le, H.M.; Nguyen, A.T.; Dinh, N.T.T.; Hoang, S.A.; Van Ha, C. Copper nanoparticle application enhances plant growth and grain yield in maize under drought stress conditions. J. Plant Growth Regul. 2022, 41, 364–375. [Google Scholar] [CrossRef]
  47. Hänsch, R.; Mendel, R.R. Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr. Opin. Plant Biol. 2009, 12, 259–266. [Google Scholar] [CrossRef]
  48. Rahman Anik, T.; Mostofa, M.G.; Rahman, M.M.; Keya, S.S.; Ha, C.V.; Khan, M.A.R.; Abdelrahman, M.; Dao, M.N.K.; Chu, H.D.; Tran, L.-S.P. Comparative effects of ZnSO4 and ZnO-NPs in improving cotton growth and yield under drought stress at early reproductive stage. Plant Sci. 2025, 359, 112589. [Google Scholar] [CrossRef]
  49. Chatterjee, J.; Chatterjee, C. Management of phytotoxicity of cobalt in tomato by chemical measures. Plant Sci. 2003, 164, 793–801. [Google Scholar] [CrossRef]
  50. Jayakumar, K.; Jaleel, C.A.; Municipality, A.; Emirates, E.; Emirates, A.; Arabia, S. Phytochemical changes in green gram (Vigna radiata) under cobalt stress. Glob. J. Mol. Sci. 2008, 3, 46–49. [Google Scholar]
  51. Katare, J.; Pichhode, M.; Kumar, N. Growth of Terminalia bellirica [(Gaertn.) Roxb.] on the Malanjkhand copper mine overburden dump spoil material. Int. J. Res.-Granthaalayah 2015, 3, 14–24. [Google Scholar] [CrossRef]
  52. Arora, A.; Sairam, R.K.; Srivastava, G.C. Oxidative stress and antioxidative system in plants. Curr. Sci. 2002, 82, 1227–1238. [Google Scholar]
  53. De Dorlodot, S.; Lutts, S.; Bertin, P. Effects of ferrous iron toxicity on the growth and mineral composition of an interspecific rice. J. Plant Nutr. 2005, 28, 1–20. [Google Scholar] [CrossRef]
  54. Yang, J.; Song, Z.; Ma, J.; Han, H. Toxicity of molybdenum-based nanomaterials on the soybean–rhizobia symbiotic system: Implications for nutrition. ACS Appl. Nano Mater. 2020, 3, 5773–5782. [Google Scholar] [CrossRef]
  55. Ahmad, M.S.A.; Ashraf, M. Essential roles and hazardous effects of nickel in plants. Rev. Environ. Contam. Toxicol. 2011, 214, 125–167. [Google Scholar] [CrossRef]
  56. Shi, G.R.; Cai, Q.S. Photosynthetic and anatomic responses of peanut leaves to zinc stress. Biol. Plant. 2009, 53, 391–394. [Google Scholar] [CrossRef]
  57. Siddiqui, M.H.; Al-Whaibi, M.H.; Basalah, M.O. Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 2011, 248, 503–511. [Google Scholar] [CrossRef]
  58. Schutzendubel, A.; Schwanz, P.; Teichmann, T.; Gross, K.; Langenfeld-Heyser, R.; Godbold, D.L.; Polle, A. Cadmium-induced changes in antioxidative systems, H2O2 content and differentiation in pine (Pinus sylvestris) roots. Plant Physiol. 2001, 127, 887–892. [Google Scholar] [CrossRef] [PubMed]
  59. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef]
  60. Sarwar, N.; Saifullah; Malhi, S.S.; Zia, M.H.; Naeem, A.; Bibi, S.; Farid, G. Role of mineral nutrition in minimizing cadmium accumulation by plants. J. Sci. Food Agric. 2010, 90, 925–937. [Google Scholar] [CrossRef]
  61. Zunaidi, A.A.; Lim, L.H.; Metali, F. Heavy metal tolerance and accumulation in the Brassica species (Brassica chinensis var. parachinensis and Brassica rapa L.): A pot experiment. Heliyon 2024, 10, e29528. [Google Scholar] [CrossRef] [PubMed]
  62. Pourrut, B.; Shahid, M.; Dumat, C.; Winterton, P.; Pinelli, E. Lead uptake, toxicity, and detoxification in plants. Rev. Environ. Contam. Toxicol. 2011, 213, 113–136. [Google Scholar] [CrossRef] [PubMed]
  63. Dawood, M.F.; Sofy, M.R.; Mohamed, H.I.; Sofy, A.R.; Abdel-Kader, H.A. N-or/and P-deprived Coccomyxa chodatii SAG 216–2 extracts instigated mercury tolerance of germinated wheat seedlings. Plant Soil 2023, 483, 225–253. [Google Scholar] [CrossRef]
  64. Osman, H.E.; Fadhlallah, R.S. Impact of lead on seed germination, seedling growth, chemical composition, and forage quality of different varieties of Sorghum. J. Umm Al-Qura Univ. Appl. Sci. 2023, 9, 77–86. [Google Scholar] [CrossRef]
  65. Marschner, H. (Ed.) Marschner’s Mineral Nutrition of Higher Plants; Academic Press: Cambridge, MA, USA, 2011. [Google Scholar] [CrossRef]
  66. Aqeel, U.; Aftab, T.; Khan, M.M.A.; Naeem, M. Excessive copper induces toxicity in Mentha arvensis L. by disturbing growth, photosynthetic machinery, oxidative metabolism and essential oil constituents. Plant Stress 2023, 8, 100161. [Google Scholar] [CrossRef]
  67. Broadley, M.R.; White, P.J.; Hammond, J.P.; Zelko, I.; Lux, A. Zinc in plants. New Phytol. 2007, 173, 677–702. [Google Scholar] [CrossRef]
  68. Mathur, J.; Panwar, R. Synergistic effect of pyrene and heavy metals (Zn, Pb, and Cd) on phytoremediation potential of Medicago sativa L. (alfalfa) in multi-contaminated soil. Environ. Sci. Pollut. Res. 2024, 31, 21012–21027. [Google Scholar] [CrossRef]
  69. Kabata-Pendias, A. Trace Elements in Soils and Plants; CRC Press: Boca Raton, FL, USA, 2010. [Google Scholar] [CrossRef]
  70. Shahzad, A.; Aslam, U.; Ferdous, S.; Qin, M.; Siddique, A.; Billah, M.; Naeem, M.; Mahmood, Z.; Kayani, S. Combined effect of endophytic Bacillus mycoides and rock phosphate on the amelioration of heavy metal stress in wheat plants. BMC Plant Biol. 2024, 24, 125. [Google Scholar] [CrossRef]
  71. Dong, J.; Wu, F.-B.; Zhang, G.-P. Effect of cadmium on growth and photosynthesis of tomato seedlings. J. Zhejiang Univ. Sci. B 2005, 6, 974–980. [Google Scholar] [CrossRef] [PubMed]
  72. Gao, T.; Wang, H.; Li, C.; Zuo, M.; Wang, X.; Liu, Y.; Yang, Y.; Xu, D.; Liu, Y.; Fang, X. Effects of heavy metal stress on physiology, hydraulics, and anatomy of three desert plants in the Jinchang mining area, China. Int. J. Environ. Res. Public Health 2022, 19, 15873. [Google Scholar] [CrossRef]
  73. Liu, L.N. Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta (BBA)-Bioenerg 2016, 1857, 256–265. [Google Scholar] [CrossRef]
  74. Guo, Z.; Gao, Y.; Yuan, X.; Yuan, M.; Huang, L.; Wang, S.; Duan, C. Effects of heavy metals on stomata in plants: A review. Int. J. Mol. Sci. 2023, 24, 9302. [Google Scholar] [CrossRef]
  75. Weryszko-Chmielewska, E.; Chwil, M. Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr.). Soil Sci. Plant Nutr. 2005, 51, 203–212. [Google Scholar] [CrossRef]
  76. Alkhatib, R.; Maruthavanan, J.; Ghoshroy, S.; Steiner, R.; Sterling, T.; Creamer, R. Physiological and ultrastructural effects of lead on tobacco. Biol. Plant. 2012, 56, 711–716. [Google Scholar] [CrossRef]
  77. Kanwal, A.; Farhan, M.; Sharif, F.; Hayyat, M.U.; Shahzad, L.; Ghafoor, G.Z. Effect of industrial wastewater on wheat germination, growth, yield, nutrients and bioaccumulation of lead. Sci. Rep. 2020, 10, 11361. [Google Scholar] [CrossRef] [PubMed]
  78. Kosobrukhov, A.; Knyazeva, I.; Mudrik, V. Plantago major plants responses to increased content of lead in soil: Growth and photosynthesis. Plant Growth Regul. 2004, 42, 145–151. [Google Scholar] [CrossRef]
  79. Yang, S.; Zhang, J.; Chen, L. Growth and physiological responses of Pennisetum sp. to cadmium stress under three different soils. Environ. Sci. Pollut. Res. 2021, 28, 14867–14881. [Google Scholar] [CrossRef]
  80. Hamanishi, E.T.; Thomas, B.R.; Campbell, M.M. Drought induces alterations in the stomatal development program in Populus. J. Exp. Bot. 2012, 63, 4959–4971. [Google Scholar] [CrossRef] [PubMed]
  81. Abo-Kassem, E.; Sharaf-El-Din, A.; Rozema, J.; Foda, E.A. Synergistic effects of cadmium and NaCl on the growth, photosynthesis and ion content in wheat plants. Biol. Plant. 1995, 37, 241–249. [Google Scholar] [CrossRef]
  82. Anjum, S.A.; Ashraf, U.; Khan, I.; Saleem, M.F. Chromium toxicity induced alterations in growth, photosynthesis, gas exchange attributes and yield formation in maize. Pak. J. Agric. Sci. 2016, 53, 751–757. [Google Scholar] [CrossRef]
  83. Khudsar, T.; Arshi, A.; Siddiqi, T.O.; Mahmooduzzafar; Iqbal, M. Zinc-induced changes in growth characters, foliar properties, and Zn-accumulation capacity of pigeon pea at different stages of plant growth. J. Plant Nutr. 2008, 31, 281–306. [Google Scholar] [CrossRef]
  84. Chen, J.; Zhu, C.; Lin, D.; Sun, Z.X. The effects of Cd on lipid peroxidation, hydrogen peroxide content and antioxidant enzyme activities in Cd-sensitive mutant rice seedlings. Can. J. Plant Sci. 2007, 87, 49–57. [Google Scholar] [CrossRef]
  85. Maheshwari, R.; Dubey, R.S. Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul. 2009, 59, 37–49. [Google Scholar] [CrossRef]
  86. Verma, S.; Dubey, R.S. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 2003, 164, 645–655. [Google Scholar] [CrossRef]
  87. Kibra, M.G. Effects of mercury on some growth parameters of rice (Oryza sativa L.). Soil Environ. 2008, 27, 23–28. [Google Scholar]
  88. Gajewska, E.; Bernat, P.; Długoński, J.; Skłodowska, M. Effect of nickel on membrane integrity, lipid peroxidation and fatty acid composition in wheat seedlings. J. Agron. Crop Sci. 2012, 198, 286–294. [Google Scholar] [CrossRef]
  89. Ahmad, I.; Akhtar, M.J.; Zahir, Z.A.; Jamil, A. Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pak. J. Bot. 2012, 44, 1569–1574. [Google Scholar]
  90. Lukatkin, A.S.; Kashtanova, N.N.; Duchovskis, P. Changes in maize seedlings growth and membrane permeability under the effect of epibrassinolide and heavy metals. Russ. Agric. Sci. 2013, 39, 307–310. [Google Scholar] [CrossRef]
  91. Kumar, D.; Seth, C.S. Photosynthesis, lipid peroxidation, and antioxidative responses of Helianthus annuus L. against chromium (VI) accumulation. Int. J. Phytoremediat. 2022, 24, 590–599. [Google Scholar] [CrossRef] [PubMed]
  92. Ashraf, M.Y.; Sadiq, R.; Hussain, M.; Ashraf, M.; Ahmad, M.S.A. Toxic effect of nickel (Ni) on growth and metabolism in germinating seeds of sunflower (Helianthus annuus L.). Biol. Trace Elem. Res. 2011, 143, 1695–1703. [Google Scholar] [CrossRef] [PubMed]
  93. Janas, K.M.; Zielińska-Tomaszewska, J.; Rybaczek, D.; Maszewski, J.; Posmyk, M.M.; Amarowicz, R.; Kosińska, A. The impact of copper ions on growth, lipid peroxidation, and phenolic compound accumulation and localization in lentil (Lens culinaris Medic.) seedlings. J. Plant Physiol. 2010, 167, 270–276. [Google Scholar] [CrossRef]
  94. Sheoran, I.S.; Singal, H.R.; Singh, R. Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanus cajan L.). Photosynth. Res. 1990, 23, 345–351. [Google Scholar] [CrossRef]
  95. Farooqi, Z.R.; Iqbal, M.Z.; Kabir, M.; Shafiq, M. Toxic effects of lead and cadmium on germination and seedling growth of Albizia lebbeck (L.) Benth. Pak. J. Bot. 2009, 41, 27–33. [Google Scholar]
  96. Zhu, J.-K. Abiotic stress signaling and responses in plants. Cell 2016, 167, 313–324. [Google Scholar] [CrossRef]
  97. Vishwakarma, K.; Upadhyay, N.; Kumar, N.; Yadav, G.; Singh, J.; Mishra, R.K.; Kumar, V.; Verma, R.; Upadhyay, R.G.; Pandey, M.; et al. Abscisic acid signaling and abiotic stress tolerance in plants: A review on current knowledge and future prospects. Front. Plant Sci. 2017, 8, 161. [Google Scholar] [CrossRef]
  98. Park, S.Y.; Fung, P.; Nishimura, N.; Jensen, D.R.; Fujii, H.; Zhao, Y.; Lumba, S.; Santiago, J.; Rodrigues, A.; Chow, T.-F.F.; et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 2009, 324, 1068–1071. [Google Scholar] [CrossRef]
  99. Panda, S.K. Impact of copper on reactive oxygen species, lipid peroxidation and antioxidants in Lemna minor. Biol. Plant. 2008, 52, 561–564. [Google Scholar] [CrossRef]
  100. Mustilli, A.C.; Merlot, S.; Vavasseur, A.; Fenzi, F.; Giraudat, J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 2002, 14, 3089–3099. [Google Scholar] [CrossRef]
  101. Postiglione, A.E.; Muday, G.K. The role of ROS homeostasis in ABA-induced guard cell signaling. Front. Plant Sci. 2020, 11, 968. [Google Scholar] [CrossRef]
  102. Pei, Z.M.; Murata, Y.; Benning, G.; Thomine, S.; Klusener, B.; Allen, G.J.; Grill, E.; Schroeder, J.I. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 2000, 406, 731–734. [Google Scholar] [CrossRef]
  103. Sahay, S.; Gupta, M. An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 2017, 67, 39–52. [Google Scholar] [CrossRef] [PubMed]
  104. Linger, P.; Ostwald, A.; Haensler, J. Cannabis sativa L. growing on heavy metal contaminated soil: Growth, cadmium uptake and photosynthesis. Biol. Plant. 2005, 49, 567–576. [Google Scholar] [CrossRef]
  105. Emamverdian, A.; Ding, Y. Effects of heavy metals’ toxicity on plants and enhancement of plant defense mechanisms of Si-mediation “review”. Int. J. Environ. Agric. Res. 2017, 3, 41–51. [Google Scholar]
  106. Llamas, A.; Ullrich, C.I.; Sanz, A. Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L.) roots. Plant Soil 2000, 219, 21–28. [Google Scholar] [CrossRef]
  107. Amiri, S.; Mehrnia, M.; Azami, H.; Barzegari, D.; Shavandi, M.; Sarrafzadeh, M. Effect of heavy metals on fouling behavior in membrane bioreactors. J. Environ. Health Sci. Eng. 2010, 7, 377–384. [Google Scholar]
  108. Sharma, R.K.; Agrawal, M. Biological effects of heavy metals: An overview. J. Environ. Biol. 2005, 26, 301–313. [Google Scholar] [PubMed]
  109. Hossain, M.A.; Hossain, M.Z.; Fujita, M. Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust. J. Crop Sci. 2009, 3, 53–64. [Google Scholar]
  110. Hossain, M.A.; Hossain, M.Z.; Fujita, M. Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol. Mol. Biol. Plants 2010, 16, 259–272. [Google Scholar] [CrossRef]
  111. Shah, K.; Kumar, R.G.; Verma, S.; Dubey, R.S. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci. 2001, 161, 1135–1144. [Google Scholar] [CrossRef]
  112. Gill, M. Heavy metal stress in plants: A review. Int. J. Adv. Res. 2014, 2, 1043–1055. [Google Scholar]
  113. Rao, M.J.; Duan, M.; Zhou, C.; Jiao, J.; Cheng, P.; Yang, L.; Wei, W.; Shen, Q.; Ji, P.; Yang, Y.; et al. Antioxidant defense system in plants: Reactive oxygen species production, signaling, and scavenging during abiotic Stress-Induced oxidative damage. Horticulturae 2025, 11, 477. [Google Scholar] [CrossRef]
  114. Shi, X.; Dalal, N.S. Evidence for a Fenton-type mechanism for the generation of OH radicals in the reduction of Cr (VI) in cellular media. Arch. Biochem. Biophys. 1990, 281, 90–95. [Google Scholar] [CrossRef]
  115. Zhang, M.; Jin, Z.Q.; Zhao, J.; Zhang, G.; Wu, F. Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley. Plant Growth Regul. 2015, 75, 567–574. [Google Scholar] [CrossRef]
  116. Wu, H.; Tito, N.; Giraldo, J.P. Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano 2017, 11, 11283–11297. [Google Scholar] [CrossRef] [PubMed]
  117. Mohamed, H.I.; Ullah, I.; Toor, M.D.; Tanveer, N.A.; Din, M.M.U.; Basit, A.; Sultan, Y.; Muhammad, M.; Rehman, M.U. Heavy metals toxicity in plants: Understanding mechanisms and developing coping strategies for remediation: A review. Bioresour. Bioprocess. 2025, 12, 95. [Google Scholar] [CrossRef] [PubMed]
  118. DalCorso, G.; Farinati, S.; Maistri, S.; Furini, A. How plants cope with cadmium: Staking all on metabolism and gene expression. J. Integr. Plant Biol. 2008, 50, 1268–1280. [Google Scholar] [CrossRef] [PubMed]
  119. Patra, M.; Bhowmik, N.; Bandopadhyay, B.; Sharma, A. Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ. Exp. Bot. 2004, 52, 199–223. [Google Scholar] [CrossRef]
  120. Van Assche, F.; Clijsters, H. Inhibition of photosynthesis in Phaseolus vulgaris by treatment with toxic concentrations of zinc: Effects on electron transport and photophosphorylation. Physiol. Plant. 1986, 66, 717–721. [Google Scholar] [CrossRef]
  121. Meharg, A.A.; Hartley-Whitaker, J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol. 2002, 154, 29–43. [Google Scholar] [CrossRef]
  122. Quig, D. Cysteine metabolism and metal toxicity. Altern. Med. Rev. 1998, 3, 262–270. [Google Scholar]
  123. Chander, K.P.C.B.; Brookes, P.C.; Harding, S.A. Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam. Soil Biol. Biochem. 1995, 27, 1409–1421. [Google Scholar] [CrossRef]
  124. Chillé, D.; Mollica-Nardo, V.; Giuffrè, O.; Ponterio, R.C.; Saija, F.; Sponer, J.; Trusso, S.; Cassone, G.; Foti, C. Binding of arsenic by common functional groups: An experimental and quantum-mechanical study. Appl. Sci. 2022, 12, 3210. [Google Scholar] [CrossRef]
  125. Kucharski, J.; Boros, E.; Wyszkowska, J. Biochemical activity of nickel-contaminated soil. Pol. J. Environ. Stud. 2009, 18, 1039–1044. [Google Scholar]
  126. Kumchai, J.; Huang, J.Z.; Lee, C.Y.; Chen, F.C.; Chin, S.W. Proline partially overcomes excess molybdenum toxicity in cabbage seedlings grown in vitro. Genet. Mol. Res. 2013, 12, 5589–5601. [Google Scholar] [CrossRef]
  127. Singh, J.; Kalamdhad, A.S. Effects of heavy metals on soil, plants, human health and aquatic life. Int. J. Res. Chem. Environ. 2011, 1, 15–21. [Google Scholar]
  128. Jentschke, G.; Godbold, D.L. Metal toxicity and ectomycorrhizas. Physiol. Plant. 2000, 109, 107–116. [Google Scholar] [CrossRef]
  129. Leyval, C.; Turnau, K.; Haselwandter, K. Effect of heavy metal pollution on mycorrhizal colonization and function: Physiological, ecological and applied aspects. Mycorrhiza 1997, 7, 139–153. [Google Scholar] [CrossRef]
  130. Hall, J.Á. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 2002, 53, 1–11. [Google Scholar] [CrossRef] [PubMed]
  131. Shi, W.; Zhang, Y.; Chen, S.; Polle, A.; Rennenberg, H.; Luo, Z.B. Physiological and molecular mechanisms of heavy metal accumulation in nonmycorrhizal versus mycorrhizal plants. Plant Cell Environ. 2019, 42, 1087–1103. [Google Scholar] [CrossRef]
  132. Millar, N.S.; Bennett, A.E. Stressed out symbiotes: Hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 2016, 182, 625–641. [Google Scholar] [CrossRef]
  133. Liao, D.; Sun, C.; Li, S.; Tauqeer, A.; Bian, X.; Shen, J.; Wu, S. The utilization and molecular mechanism of arbuscular mycorrhizal symbiosis in vegetables. Veg. Res. 2023, 3, 1. [Google Scholar] [CrossRef]
  134. Adeyemi, N.O.; Atayese, M.O.; Sakariyawo, O.S.; Azeez, J.O.; Sobowale, S.P.A.; Olubode, A.; Adeoye, S. Alleviation of heavy metal stress by arbuscular mycorrhizal symbiosis in Glycine max (L.) grown in copper, lead and zinc contaminated soils. Rhizosphere 2021, 18, 100325. [Google Scholar] [CrossRef]
  135. Chaturvedi, R.; Favas, P.J.; Pratas, J.; Varun, M.; Paul, M.S. Effect of Glomus mosseae on accumulation efficiency, hazard index and antioxidant defense mechanisms in tomato under metal(loid) stress. Int. J. Phytoremediat. 2018, 20, 885–894. [Google Scholar] [CrossRef]
  136. Riaz, M.; Kamran, M.; Fang, Y.; Wang, Q.; Cao, H.; Yang, G.; Deng, L.; Wang, Y.; Zhou, Y.; Anastopoulos, I.; et al. Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. J. Hazard. Mater. 2021, 402, 123919. [Google Scholar] [CrossRef]
  137. Borowicz, V.A. Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 2001, 82, 3057–3068. [Google Scholar] [CrossRef]
  138. Abd_Allah, E.F.; Hashem, A.; Alqarawi, A.A.; Bahkali, A.H.; Alwhibi, M.S. Enhancing growth performance and systemic acquired resistance of medicinal plant Sesbania sesban (L.) Merr using arbuscular mycorrhizal fungi under salt stress. Saudi J. Biol. Sci. 2015, 22, 274–283. [Google Scholar] [CrossRef] [PubMed]
  139. Bi, Y.; Zhang, J.; Song, Z.; Wang, Z.; Qiu, L.; Hu, J.; Gong, Y. Arbuscular mycorrhizal fungi alleviate root damage stress induced by simulated coal mining subsidence ground fissures. Sci. Total Environ. 2019, 652, 398–405. [Google Scholar] [CrossRef]
  140. Marschner, H. Mineral Nutrition of Higher Plants, 2nd ed.; Academic Press: London, UK, 1995. [Google Scholar] [CrossRef]
  141. Dalvi, A.A.; Bhalerao, S.A. Response of plants towards heavy metal toxicity: An overview of avoidance, tolerance and uptake mechanism. Ann. Plant Sci. 2013, 2, 362–368. [Google Scholar]
  142. Jarin, A.S.; Islam, M.M.; Rahat, A.; Ahmed, S.; Ghosh, P.; Murata, Y. Drought stress tolerance in rice: Physiological and biochemical insights. Int. J. Plant Biol. 2024, 15, 692–718. [Google Scholar] [CrossRef]
  143. Grill, E.; Löffler, S.; Winnacker, E.L.; Zenk, M.H. Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA 1989, 86, 6838–6842. [Google Scholar] [CrossRef]
  144. Rauser, W.E. Phytochelatins. Annu. Rev. Biochem. 1990, 59, 61–86. [Google Scholar] [CrossRef]
  145. Cobbett, C.S. Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr. Opin. Plant Biol. 2000, 3, 211–216. [Google Scholar] [CrossRef] [PubMed]
  146. Tong, Y.; Kneer, R.; Zhu, Y. Vacuolar compartmentalization: A second-generation approach to engineering plants for phytoremediation. Trends Plant Sci. 2003, 9, 7–9. [Google Scholar] [CrossRef] [PubMed]
  147. Clemens, S.; Kim, E.J.; Neumann, D.; Schroeder, J.I. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 1999, 18, 3325–3333. [Google Scholar] [CrossRef]
  148. Bertrand, M.; Guary, J.C.; Schoefs, B. How plants adapt their physiology to an excess of metals. In Handbook of Plant and Crop Physiology; Pessarakli, M., Ed.; CRC Press: Boca Raton, FL, USA, 2001; pp. 773–784. [Google Scholar] [CrossRef]
  149. Salt, D.E.; Rauser, W.E. MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 1995, 107, 1293–1301. [Google Scholar] [CrossRef]
  150. Ebbs, S.; Lau, I.; Ahner, B.; Kochian, L. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 2002, 214, 635–640. [Google Scholar] [CrossRef] [PubMed]
  151. Goldsbrough, P. Metal tolerance in plants: The role of phytochelatins and metallothioneins. In Phytoremediation of Contaminated Soil and Water; CRC Press: Boca Raton, FL, USA, 2020; pp. 221–233. [Google Scholar] [CrossRef]
  152. Wang, Y.; Wang, L.; Ma, C.; Wang, K.; Hao, Y.; Chen, Q.; Mo, Y.; Rui, Y. Effects of Cerium Oxide on Rice Seedlings as Affected by Co-Exposure of Cadmium and Salt. Environ. Pollut. 2019, 252, 1087–1096. [Google Scholar] [CrossRef] [PubMed]
  153. Sharma, S.S.; Dietz, K.J. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009, 14, 43–50. [Google Scholar] [CrossRef]
  154. Tseng, T.S.; Tzeng, S.S.; Yeh, K.W.; Yeh, C.H.; Chang, F.C.; Chen, Y.M.; Lin, C.Y. The heat-shock response in rice seedlings: Isolation and expression of cDNAs that encode class I low-molecular-weight heat-shock proteins. Plant Cell Physiol. 1993, 34, 165–168. [Google Scholar] [CrossRef]
  155. Wollgiehn, R.; Neumann, D. Metal stress response and tolerance of cultured cells from Silene vulgaris and Lycopersicon peruvianum: Role of heat stress proteins. J. Plant Physiol. 1999, 154, 547–553. [Google Scholar] [CrossRef]
  156. Neumann, D.; Lichtenberger, O.; Günther, D.; Tschiersch, K.; Nover, L. Heat-shock proteins induce heavy-metal tolerance in higher plants. Planta 1994, 194, 360–367. [Google Scholar] [CrossRef]
  157. Lewis, S.; Donkin, M.E.; Depledge, M.H. Hsp70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat. Toxicol. 2001, 51, 277–291. [Google Scholar] [CrossRef]
  158. Rao, K.M.; Sresty, T.V.S. Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci. 2000, 157, 113–128. [Google Scholar] [CrossRef] [PubMed]
  159. Schützendübel, A.; Polle, A. Plant responses to abiotic stresses: Heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 2002, 53, 1351–1365. [Google Scholar] [CrossRef]
  160. Bhaduri, A.M.; Fulekar, M.H. Antioxidant enzyme responses of plants to heavy metal stress. Rev. Environ. Sci. Bio/Technol. 2012, 11, 55–69. [Google Scholar] [CrossRef]
  161. Okem, A.; Stirk, W.A.; Street, R.A.; Southway, C.; Finnie, J.F.; Van Staden, J. Effects of Cd and Al stress on secondary metabolites, antioxidant and antibacterial activity of Hypoxis hemerocallidea Fisch. & C.A. Mey. Plant Physiol. Biochem. 2015, 97, 147–155. [Google Scholar] [CrossRef] [PubMed]
  162. Malekzadeh, P.; Khara, J.; Farshian, S.; Jamal-Abad, A.K.; Rahmatzade, S. Cadmium toxicity in maize seedlings: Changes in antioxidant enzyme activities and root growth. Pak. J. Biol. Sci. 2007, 10, 127–131. [Google Scholar] [CrossRef]
  163. Cui, Y.; Zhao, N. Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant Soil Environ. 2011, 57, 34–39. [Google Scholar] [CrossRef]
  164. Chen, F.; Wang, F.; Wu, F.; Mao, W.; Zhang, G.; Zhou, M. Modulation of exogenous glutathione in antioxidant defense system against Cd stress in two barley genotypes differing in Cd tolerance. Plant Physiol. Biochem. 2010, 48, 663–672. [Google Scholar] [CrossRef]
  165. Lobo, V.; Patil, A.; Phatak, A.; Chandra, N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn. Rev. 2010, 4, 118–126. [Google Scholar] [CrossRef]
  166. Sharma, P.; Jha, A.B.; Dubey, R.S.; Pessarakli, M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, 2012, 217037. [Google Scholar] [CrossRef]
  167. Bali, A.S.; Sidhu, G.P.S.; Kumar, V. Root exudates ameliorate cadmium tolerance in plants: A review. Environ. Chem. Lett. 2020, 18, 1243–1275. [Google Scholar] [CrossRef]
  168. Bartwal, A.; Mall, R.; Lohani, P.; Guru, S.K.; Arora, S. Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J. Plant Growth Regul. 2013, 32, 216–232. [Google Scholar] [CrossRef]
  169. Shanker, K.A.; Djanaguiraman, M.; Sudhagar, R.; Chandrashekar, C.N.; Pathmanabhan, G. Differential antioxidative response of ascorbate-glutathione pathway enzymes and metabolites to chromium speciation stress in green gram (Vigna radiata L. cv. CO 4) roots. Plant Sci. 2004, 166, 1035–1043. [Google Scholar] [CrossRef]
  170. Mazhoudi, S.; Chaoui, A.; Ghorbal, M.H.; El Ferjani, E. Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum Mill.). Plant Sci. 1997, 127, 129–137. [Google Scholar] [CrossRef]
  171. Prasad, K.V.S.K.; Saradhi, P.P.; Sharmila, P. Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ. Exp. Bot. 1999, 42, 1–10. [Google Scholar] [CrossRef]
  172. Hameed, A.; Qadri, T.N.; Siddiqi, T.O.; Iqbal, M. Differential activation of the enzymatic antioxidant system of Abelmoschus esculentus L. under CdCl2 and HgCl2 exposure. Braz. J. Plant Physiol. 2011, 23, 46–54. [Google Scholar] [CrossRef]
  173. Luo, Z.-B.; He, X.-J.; Chen, L.; Tang, L.; Gao, S.; Chen, F. Effects of zinc on growth and antioxidant responses in Jatropha curcas seedlings. Int. J. Agric. Biol. 2010, 12, 119–124. [Google Scholar]
  174. Gomes-Junior, R.A.; Moldes, C.A.; Delite, F.S.; Gratão, P.L.; Mazzafera, P.; Lea, P.J.; Azevedo, R.A. Nickel Elicits a Fast Antioxidant Response in Coffea arabica Cells. Plant Physiol. Biochem. 2006, 44, 420–429. [Google Scholar] [CrossRef]
  175. Odjegba, V.J.; Fasidi, I.O. Changes in antioxidant enzyme activities in Eichhornia crassipes (Pontederiaceae) and Pistia stratiotes (Araceae) under heavy metal stress. Rev. De Biol. Trop. 2007, 55, 815–823. [Google Scholar] [CrossRef] [PubMed]
  176. Boojar, M.M.A. Role of antioxidant enzyme responses and phytochelatins in tolerance strategies of Alhagi camelorum Fisch growing on copper mine. Acta Bot. Croat. 2010, 69, 107–121. [Google Scholar]
  177. Niekerk, L.A.; Gokul, A.; Basson, G.; Badiwe, M.; Nkomo, M.; Klein, A.; Keyster, M. Heavy metal stress and mitogen activated kinase transcription factors in plants: Exploring heavy metal–ROS influences on plant signalling pathways. Plant Cell Environ. 2024, 47, 2793–2810. [Google Scholar] [CrossRef] [PubMed]
  178. Kumar, S.; Trivedi, P.K. Heavy metal stress signaling in plants. In Plant Metal Interaction; Elsevier: Amsterdam, The Netherlands, 2016; pp. 585–603. [Google Scholar] [CrossRef]
  179. Ali, S.; Mir, R.A.; Tyagi, A.; Manzar, N.; Kashyap, A.S.; Mushtaq, M.; Raina, A.; Park, S.; Sharma, S.; Mir, Z.A.; et al. Chromium toxicity in plants: Signaling, mitigation, and future perspectives. Plants 2023, 12, 1502. [Google Scholar] [CrossRef]
  180. Chakrabarty, D.; Trivedi, P.K.; Misra, P.; Tiwari, M.; Shri, M.; Shukla, D.; Kumar, S.; Rai, A.; Pandey, A.; Nigam, D.; et al. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 2009, 74, 688–702. [Google Scholar] [CrossRef]
  181. Liu, Y.; Liu, L.; Qi, J.; Dang, P.; Xia, T. Cadmium activates ZmMPK3-1 and ZmMPK6-1 via induction of reactive oxygen species in maize roots. Biochem. Biophys. Res. Commun. 2019, 516, 747–752. [Google Scholar] [CrossRef]
  182. Zhao, F.Y.; Hu, F.; Zhang, S.Y.; Wang, K.; Zhang, C.R.; Liu, T. MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environ. Sci. Pollut. Res. 2013, 20, 5449–5460. [Google Scholar] [CrossRef]
  183. Mansoor, S.; Ali, A.; Kour, N.; Bornhorst, J.; AlHarbi, K.; Rinklebe, J.; Abd El Moneim, D.; Ahmad, P.; Chung, Y.S. Heavy Metal Induced Oxidative Stress Mitigation and ROS Scavenging in Plants. Plants 2023, 12, 3003. [Google Scholar] [CrossRef]
  184. Trinh, N.-N.; Huang, T.-L.; Chi, W.-C.; Fu, S.-F.; Chen, C.-C.; Huang, H.-J. Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol. Plant. 2013, 149, 264–276. [Google Scholar] [CrossRef]
  185. Mitra, M.; Agarwal, P.; Roy, S. Plant response to heavy metal stress: An insight into the molecular mechanism of transcriptional regulation. In Plant Transcription Factors; Academic Press: Cambridge, MA, USA, 2022; pp. 337–367. [Google Scholar] [CrossRef]
  186. Hasan, M.K.; Cheng, Y.; Kanwar, M.K.; Chu, X.Y.; Ahammed, G.J.; Qi, Z.Y. Responses of plant proteins to heavy metal stress—A review. Front. Plant Sci. 2017, 8, 1492. [Google Scholar] [CrossRef]
  187. Çelik, Ö.; Ayan, A.; Meriç, S.; Atak, Ç. Heavy metal stress-responsive phyto-miRNAs. In Cellular and Molecular Phytotoxicity of Heavy Metals; Hasanuzzaman, M., Fujita, M., Eds.; Springer: Cham, Switzerland, 2020; pp. 137–155. [Google Scholar] [CrossRef]
  188. Kaur, H.; Kohli, S.K.; Khanna, K.; Dhiman, S.; Kour, J.; Bhardwaf, T.; Bhardwaf, R. Deciphering the role of metal binding proteins and metal transporters for remediation of toxic metals in plants. In Bioremediation of Toxic Metal(loid)s; CRC Press: Boca Raton, FL, USA, 2022; pp. 257–272. [Google Scholar] [CrossRef]
  189. Osborne, W.J.; Sharma, S. Genomic instability in medicinal plants in response to heavy metal stress. In Stress-Responsive Factors and Molecular Farming in Medicinal Plants; Springer: Singapore, 2023; pp. 207–226. [Google Scholar] [CrossRef]
  190. Iqbal, B.; Ahmad, N.; Li, G.; Jalal, A.; Khan, A.R.; Zheng, X.; Du, D. Unlocking plant resilience: Advanced epigenetic strategies against heavy metal and metalloid stress. Plant Sci. 2024, 349, 112265. [Google Scholar] [CrossRef]
  191. Lanciano, S.; Mirouze, M. DNA methylation in rice and relevance for breeding. Epigenomes 2017, 1, 10. [Google Scholar] [CrossRef]
  192. Gallo-Franco, J.J.; Sosa, C.C.; Ghneim-Herrera, T.; Quimbaya, M. Epigenetic control of plant response to heavy metal stress: A new view on aluminum tolerance. Front. Plant Sci. 2020, 11, 602625. [Google Scholar] [CrossRef]
  193. Zhou, Y.Y.; Wang, Y.S.; Sun, C.C. Molecular cloning and expression analysis of the typical class III chitinase genes from three mangrove species under heavy metal stress. Plants 2023, 12, 1681. [Google Scholar] [CrossRef] [PubMed]
  194. Zhou, M.; Zheng, S.; Liu, R.; Lu, J.; Lu, L.; Zhang, C.; Liu, Z.; Lue, C.; Zhang, L.; Yant, L.; et al. Genome-wide identification, phylogenetic and expression analysis of the heat shock transcription factor family in bread wheat (Triticum aestivum L.). BMC Genom. 2019, 20, 505. [Google Scholar] [CrossRef] [PubMed]
  195. Hu, S.; Yu, Y.; Chen, Q.; Mu, G.; Shen, Z.; Zheng, L. OsMYB45 plays an important role in rice resistance to cadmium stress. Plant Sci. 2018, 269, 110–118. [Google Scholar] [CrossRef] [PubMed]
  196. Sapara, K.K.; Khedia, J.; Agarwal, P.; Gangapur, D.R.; Agarwal, P.K. SbMYB15 transcription factor mitigates cadmium and nickel stress in transgenic tobacco by limiting uptake and modulating antioxidative defence system. Functi. Plant Biol. 2019, 46, 702–714. [Google Scholar] [CrossRef]
  197. Xu, Z.; Ge, Y.; Zhang, W.; Zhao, Y.; Yang, G. The walnut JrVHAG1 gene is involved in cadmium stress response through ABA-signal pathway and MYB transcription regulation. BMC Plant Biol. 2018, 18, 19. [Google Scholar] [CrossRef] [PubMed]
  198. Xing, Q.; Hasan, M.K.; Li, Z.; Yang, T.; Jin, W.; Qi, Z.; Yang, P.; Wang, G.; Ahammed, G.J.; Zhou, J. Melatonin-induced plant adaptation to cadmium stress involves enhanced phytochelatin synthesis and nutrient homeostasis in Solanum lycopersicum L. J. Hazard. Mater. 2023, 456, 131670. [Google Scholar] [CrossRef]
  199. Zhou, Y.; Xu, D.; Jia, L.; Huang, X.; Ma, G.; Wang, S.; Zhu, M.; Zhang, A.; Guan, M.; Lu, K.; et al. Genome-wide identification and structural analysis of bZIP transcription factor genes in Brassica napus. Genes 2017, 8, 288. [Google Scholar] [CrossRef]
  200. Agarwal, P.; Mitra, M.; Banerjee, S.; Roy, S. MYB4 transcription factor, a member of R2R3-subfamily of MYB domain protein, regulates cadmium tolerance via enhanced protection against oxidative damage and increases expression of PCS1 and MT1C in Arabidopsis. Plant Sci. 2020, 297, 110501. [Google Scholar] [CrossRef] [PubMed]
  201. Han, Y.; Fan, T.; Zhu, X.; Wu, X.; Ouyang, J.; Jiang, L.; Cao, S. WRKY12 represses GSH1 expression to negatively regulate cadmium tolerance in Arabidopsis. Plant Mol. Biol. 2019, 99, 149–159. [Google Scholar] [CrossRef]
  202. Sheng, Y.; Yan, X.; Huang, Y.; Han, Y.; Zhang, C.; Ren, Y.; Fan, T.; Xiao, F.; Liu, Y.; Cao, S. The WRKY transcription factor, WRKY13, activates PDR8 expression to positively regulate cadmium tolerance in Arabidopsis. Plant Cell Environ. 2019, 42, 891–903. [Google Scholar] [CrossRef]
  203. Zhang, C.; Tong, C.; Cao, L.; Zheng, P.; Tang, X.; Wang, L.; Miao, M.; Liu, Y.; Cao, S. Regulatory module WRKY33–ATL31–IRT1 mediates cadmium tolerance in Arabidopsis. Plant Cell Environ. 2023, 46, 1653–1670. [Google Scholar] [CrossRef]
  204. Zhang, P.; Wang, R.; Ju, Q.; Li, W.; Tran, L.-S.P.; Xu, J. The R2R3-MYB transcription factor MYB49 regulates cadmium accumulation. Plant Physiol. 2019, 180, 529–542. [Google Scholar] [CrossRef]
  205. Moharem, M.; Elkhatib, E.; Mesalem, M. Remediation of chromium and mercury polluted calcareous soils using nanoparticles: Sorption–desorption kinetics, speciation and fractionation. Environ. Res. 2019, 170, 366–373. [Google Scholar] [CrossRef]
  206. Cao, F.; Dai, H.; Hao, P.F.; Wu, F. Silicon regulates the expression of vacuolar H⁺-pyrophosphatase 1 and decreases cadmium accumulation in rice (Oryza sativa L.). Chemosphere 2020, 240, 124907. [Google Scholar] [CrossRef]
  207. Khan, M.N.; Mobin, M.; Abbas, Z.K.; AlMutairi, K.A.; Siddiqui, Z.H. Role of nanomaterials in plants under challenging environments. Plant Physiol. Biochem. 2017, 110, 194–209. [Google Scholar] [CrossRef] [PubMed]
  208. Mingyu, S.; Fashui, H.; Chao, L.; Xiao, W.; Xiaoqing, L.; Liang, C.; Zhongrui, L. Effects of nano-anatase TiO2 on absorption, distribution of light, and photoreduction activities of chloroplast membrane of spinach. Biol. Trace Elem. Res. 2007, 118, 120–130. [Google Scholar] [CrossRef] [PubMed]
  209. Sebastian, A.; Nangia, A.; Prasad, M.N.V. Cadmium and sodium adsorption properties of magnetite nanoparticles synthesized from Hevea brasiliensis bark: Relevance in amelioration of metal stress in rice. J. Hazard. Mater. 2019, 371, 261–272. [Google Scholar] [CrossRef]
  210. Wang, G.; Pan, X.; Zhang, S.; Zhong, Q.; Zhou, W.; Zhang, X.; Peijnenburg, W.J. Remediation of heavy metal-contaminated soil by biodegradable chelator–induced washing: Efficiencies and mechanisms. Environ. Res. 2020, 186, 109554. [Google Scholar] [CrossRef]
  211. Zhou, P.; Adeel, M.; Shakoor, N.; Guo, M.; Hao, Y.; Azeem, I.; Rui, Y. Application of nanoparticles alleviates heavy metals stress and promotes plant growth: An overview. Nanomaterials 2020, 11, 26. [Google Scholar] [CrossRef]
  212. Singh, J.; Lee, B.K. Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max), a possible mechanism for the removal of Cd from the contaminated soil. J. Environ. Manag. 2016, 170, 88–96. [Google Scholar] [CrossRef]
  213. Venkatachalam, P.; Jayaraj, M.; Manikandan, R.; Geetha, N.; Rene, E.R.; Sharma, N.C.; Sahi, S.V. Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: A physiochemical analysis. Plant Physiol. Biochem. 2017, 110, 59–69. [Google Scholar] [CrossRef]
  214. Shaik, A.M.; David Raju, M.; Rama Sekhara Reddy, D. Green synthesis of zinc oxide nanoparticles using aqueous root extract of Sphagneticola trilobata and its role in toxic metal removal and plant growth promotion. Inorg. Nano-Met. Chem. 2020, 50, 569–579. [Google Scholar] [CrossRef]
  215. Dai, S.; Wang, B.; Song, Y.; Xie, Z.; Li, C.; Li, S.; Jiang, M. Astaxanthin and its gold nanoparticles mitigate cadmium toxicity in rice by inhibiting cadmium translocation and uptake. Sci. Total Environ. 2021, 786, 147496. [Google Scholar] [CrossRef] [PubMed]
  216. Cai, F.; Wu, X.; Zhang, H.; Shen, X.; Zhang, M.; Chen, W.; Wang, X. Impact of TiO2 nanoparticles on lead uptake and bioaccumulation in rice (Oryza sativa L.). NanoImpact 2017, 5, 101–108. [Google Scholar] [CrossRef]
  217. Song, C.; Ye, F.; Zhang, H.; Hong, J.; Hua, C.; Wang, B.; Zhao, L. Metal(loid) oxides and metal sulfides nanomaterials reduced heavy metals uptake in soil cultivated cucumber plants. Environ. Pollut. 2019, 255, 113354. [Google Scholar] [CrossRef]
  218. Konate, A.; He, X.; Zhang, Z.; Ma, Y.; Zhang, P.; Alugongo, G.M.; Rui, Y. Magnetic (Fe3O4) nanoparticles reduce heavy metals uptake and mitigate their toxicity in wheat seedling. Sustainability 2017, 9, 790. [Google Scholar] [CrossRef]
  219. Sardar, R.; Ahmed, S.; Shah, A.A.; Yasin, N.A. Selenium nanoparticles reduced cadmium uptake, regulated nutritional homeostasis and antioxidative system in Coriandrum sativum grown in cadmium toxic conditions. Chemosphere 2022, 287, 132332. [Google Scholar] [CrossRef]
  220. Zhu, Y.; Dong, Y.; Zhu, N.; Jin, H. Foliar application of biosynthetic nano-selenium alleviates the toxicity of Cd, Pb, and Hg in Brassica chinensis by inhibiting heavy metal adsorption and improving antioxidant system in plant. Ecotoxicol. Environ. Saf. 2022, 240, 113681. [Google Scholar] [CrossRef]
  221. Gao, M.; Chang, X.; Yang, Y.; Song, Z. Foliar graphene oxide treatment increases photosynthetic capacity and reduces oxidative stress in cadmium-stressed lettuce. Plant Physiol. Biochem. 2020, 154, 287–294. [Google Scholar] [CrossRef] [PubMed]
  222. Bayat, Z.; Hassanshahian, M.; Cappello, S. Immobilization of microbes for bioremediation of crude oil polluted environments: A mini review. Open Microbiol. J. 2015, 9, 48–54. [Google Scholar] [PubMed]
  223. Ken, D.S.; Sinha, A. Recent developments in surface modification of nano zero-valent iron (nZVI): Remediation, toxicity and environmental impacts. Environ. Nanotechnol. Monit. Manag. 2020, 14, 100344. [Google Scholar] [CrossRef]
  224. Gnanaprakasam, P.; Jeena, S.E.; Premnath, D.; Selvaraju, T. Simple and robust green synthesis of Au NPs on reduced graphene oxide for the simultaneous detection of toxic heavy metal ions and bioremediation using bacterium as the scavenger. Electroanalysis 2016, 28, 1885–1893. [Google Scholar] [CrossRef]
  225. Ghosh, S.; Rusyn, I.; Dmytruk, O.V.; Dmytruk, K.V.; Onyeaka, H.; Gryzenhout, M.; Gafforov, Y. Filamentous fungi for sustainable remediation of pharmaceutical compounds, heavy metal and oil hydrocarbons. Front. Bioeng. Biotechnol. 2023, 11, 1106973. [Google Scholar] [CrossRef]
  226. Nakhjavani, M.; Nikkhah, V.; Sarafraz, M.M.; Shoja, S.; Sarafraz, M. Green synthesis of silver nanoparticles using green tea leaves: Experimental study on the morphological, rheological and antibacterial behaviour. Heat Mass Transf. 2017, 53, 3201–3209. [Google Scholar] [CrossRef]
  227. Cao, X.; Alabresm, A.; Chen, Y.P.; Decho, A.W.; Lead, J. Improved metal remediation using a combined bacterial and nanoscience approach. Sci. Total Environ. 2020, 704, 135378. [Google Scholar] [CrossRef]
  228. Della Puppa, L.; Komárek, M.; Bordas, F.; Bollinger, J.C.; Joussein, E. Adsorption of copper, cadmium, lead and zinc onto a synthetic manganese oxide. J. Colloid Interface Sci. 2013, 399, 99–106. [Google Scholar] [CrossRef]
  229. Watanabe, J.I.; Tani, Y.; Chang, J.; Miyata, N.; Naitou, H.; Seyama, H. As (III) oxidation kinetics of biogenic manganese oxides formed by Acremonium strictum strain KR21-2. Chem. Geol. 2013, 347, 227–232. [Google Scholar] [CrossRef]
  230. Rafique, M.; Sadaf, I.; Rafique, M.S.; Tahir, M.B. A review on green synthesis of silver nanoparticles and their applications. Artif. Cells Nanomed. Biotechnol. 2017, 45, 1272–1291. [Google Scholar] [CrossRef]
  231. Klaus, T.; Joerger, R.; Olsson, E.; Granqvist, C.G. Silver-based crystalline nanoparticles, microbially fabricated. Proc. Natl. Acad. Sci. USA 1999, 96, 13611–13614. [Google Scholar] [CrossRef]
  232. Amin, M.; Anwar, F.; Janjua, M.R.S.A.; Iqbal, M.A.; Rashid, U. Green synthesis of silver nanoparticles through reduction with Solanum xanthocarpum L. berry extract: Characterization, antimicrobial and urease inhibitory activities against Helicobacter pylori. Int. J. Mol. Sci. 2012, 13, 9923–9941. [Google Scholar] [CrossRef]
  233. Al-Senani, G.M.; Al-Kadhi, N. The synthesis and effect of silver nanoparticles on the adsorption of Cu2+ from aqueous solutions. Appl. Sci. 2020, 10, 4840. [Google Scholar] [CrossRef]
  234. Shedbalkar, U.; Singh, R.; Wadhwani, S.; Gaidhani, S.; Chopade, B.A. Microbial synthesis of gold nanoparticles: Current status and future prospects. Adv. Colloid Interface Sci. 2014, 209, 40–48. [Google Scholar] [CrossRef] [PubMed]
  235. Bhargava, A.; Jain, N.; Gangopadhyay, S.; Panwar, J. Development of gold nanoparticle-fungal hybrid based heterogeneous interface for catalytic applications. Process Biochem. 2015, 50, 1293–1300. [Google Scholar] [CrossRef]
  236. Shankar, S.S.; Ahmad, A.; Pasricha, R.; Sastry, M. Bioreduction of chloroaurate ions by geranium leaves and its endophytic fungus yields gold nanoparticles of different shapes. J. Mater. Chem. 2003, 13, 1822–1826. [Google Scholar] [CrossRef]
  237. Agarwal, H.; Kumar, S.V.; Rajeshkumar, S. A review on green synthesis of zinc oxide nanoparticles—An eco-friendly approach. Resour.-Effic. Technol. 2017, 3, 406–413. [Google Scholar] [CrossRef]
  238. Hossain, A.; Abdallah, Y.; Ali, M.A.; Masum, M.M.I.; Li, B.; Sun, G.; An, Q. Lemon-fruit-based green synthesis of zinc oxide nanoparticles and titanium dioxide nanoparticles against soft rot bacterial pathogen Dickeya dadantii. Biomolecules 2019, 9, 863. [Google Scholar] [CrossRef]
  239. Chidambaram, D.; Hennebel, T.; Taghavi, S.; Mast, J.; Boon, N.; Verstraete, W.; Fitts, J.P. Concomitant microbial generation of palladium nanoparticles and hydrogen to immobilize chromate. Environ. Sci. Technol. 2010, 44, 7635–7640. [Google Scholar] [CrossRef]
  240. Subramaniyam, V.; Subashchandrabose, S.R.; Thavamani, P.; Megharaj, M.; Chen, Z.; Naidu, R. Chlorococcum sp. MM11—A novel phyco-nanofactory for the synthesis of iron nanoparticles. J. Appl. Phycol. 2015, 27, 1861–1869. [Google Scholar] [CrossRef]
  241. Tarafdar, J.C.; Raliya, R. Rapid, low-cost, and ecofriendly approach for iron nanoparticle synthesis using Aspergillus oryzae TFR9. J. Nanopart. 2013, 2013, 141274. [Google Scholar] [CrossRef]
  242. Kumar, D.; Dhankher, O.P.; Tripathi, R.D.; Seth, C.S. Titanium dioxide nanoparticles potentially regulate the mechanisms for photosynthetic attributes, genotoxicity, antioxidants defense machinery, and phytochelatins synthesis in relation to hexavalent chromium toxicity in Helianthus annuus L. J. Hazard. Mater. 2023, 454, 131418. [Google Scholar] [CrossRef]
  243. Bai, Y.; Yang, T.; Liang, J.; Qu, J. The role of biogenic Fe-Mn oxides formed in situ for arsenic oxidation and adsorption in aquatic ecosystems. Water Res. 2016, 98, 119–127. [Google Scholar] [CrossRef]
  244. Raj, R.; Dalei, K.; Chakraborty, J.; Das, S. Extracellular polymeric substances of a marine bacterium mediated synthesis of CdS nanoparticles for removal of cadmium from aqueous solution. J. Colloid Interface Sci. 2016, 462, 166–175. [Google Scholar] [CrossRef] [PubMed]
Plants 14 03834 g001
Figure 1. Impact of essential and nonessential metals on plants. Toxicity levels are presented in Table 1. As, arsenic; Cd, cadmium; Co, cobalt; Cr, chromium; Cu, copper; Fe, iron; Hg, mercury; Mn, manganese; Pb, lead; Zn, zinc. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Figure 1. Impact of essential and nonessential metals on plants. Toxicity levels are presented in Table 1. As, arsenic; Cd, cadmium; Co, cobalt; Cr, chromium; Cu, copper; Fe, iron; Hg, mercury; Mn, manganese; Pb, lead; Zn, zinc. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Plants 14 03834 g001
Plants 14 03834 g002
Figure 2. Effects of heavy metal (HM) stresses on physiological functions of plants. HM exposure disrupts glucose metabolism, TCA cycle, stomatal regulation, and multiple signaling pathways, ultimately impairing plant growth and productivity. Blue boxes represent upstream biochemical and signaling disruptions triggered by HM exposure, while pink boxes indicate downstream physiological and growth-related impairments. Horizontal arrows indicate causal relationships or signaling pathways among components. Curved arrows represent feedback effects on stomatal regulation. ABA, abscisic acid; ABI1/PYR/PYL, ABA receptors (ABA insensitive 1/pyrabactin resistance/PYR1-like); cGMP, cyclic guanosine monophosphate; NO, nitric oxide; PP2C, protein phosphatase 2C; OST1, Open Stomata 1; RNS, reactive nitrogen species; ROS, reactive oxygen species; TCA, tricarboxylic acid; Plants 14 03834 i001, heavy metals. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Figure 2. Effects of heavy metal (HM) stresses on physiological functions of plants. HM exposure disrupts glucose metabolism, TCA cycle, stomatal regulation, and multiple signaling pathways, ultimately impairing plant growth and productivity. Blue boxes represent upstream biochemical and signaling disruptions triggered by HM exposure, while pink boxes indicate downstream physiological and growth-related impairments. Horizontal arrows indicate causal relationships or signaling pathways among components. Curved arrows represent feedback effects on stomatal regulation. ABA, abscisic acid; ABI1/PYR/PYL, ABA receptors (ABA insensitive 1/pyrabactin resistance/PYR1-like); cGMP, cyclic guanosine monophosphate; NO, nitric oxide; PP2C, protein phosphatase 2C; OST1, Open Stomata 1; RNS, reactive nitrogen species; ROS, reactive oxygen species; TCA, tricarboxylic acid; Plants 14 03834 i001, heavy metals. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Plants 14 03834 g002
Plants 14 03834 g003
Figure 3. An overview of heavy metals detoxification, nutrient transport, and biomass accumulation in plants by microbial functions. AMF, arbuscular mycorrhizal fungi; Co, cobalt; Cu, copper; ECM, ectomycorrhizal fungi; Fe, iron; Mn, manganese; Pb, lead; Zn, zinc. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Figure 3. An overview of heavy metals detoxification, nutrient transport, and biomass accumulation in plants by microbial functions. AMF, arbuscular mycorrhizal fungi; Co, cobalt; Cu, copper; ECM, ectomycorrhizal fungi; Fe, iron; Mn, manganese; Pb, lead; Zn, zinc. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Plants 14 03834 g003
Plants 14 03834 g004
Figure 4. Cellular mechanisms of heavy metals detoxification and sequestration in plants. HMs first interact with the cell wall (1), followed by regulated transport across the plasma membrane (2) into the cytosol (3), where they are chelated by phytochelatins and metallothioneins. The resulting PC-HM complexes are then transported across the tonoplast (4) into the vacuole (5) for sequestration and detoxification, utilizing proton gradients to drive transport and stabilizing HMs in less toxic forms within the vacuole. HMs, heavy metals; MTs, metallothioneins; PCs, phytochelatins; PC-HM, phytochelatin-heavy metal complex; PC-HM-S, stabilized phytochelatin-heavy metal complex. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Figure 4. Cellular mechanisms of heavy metals detoxification and sequestration in plants. HMs first interact with the cell wall (1), followed by regulated transport across the plasma membrane (2) into the cytosol (3), where they are chelated by phytochelatins and metallothioneins. The resulting PC-HM complexes are then transported across the tonoplast (4) into the vacuole (5) for sequestration and detoxification, utilizing proton gradients to drive transport and stabilizing HMs in less toxic forms within the vacuole. HMs, heavy metals; MTs, metallothioneins; PCs, phytochelatins; PC-HM, phytochelatin-heavy metal complex; PC-HM-S, stabilized phytochelatin-heavy metal complex. Figure created using Adobe Photoshop (Adobe Systems, San Jose, CA, USA).
Plants 14 03834 g004
Table 1. Roles and adequate/toxic levels of heavy metals in plants.
Table 1. Roles and adequate/toxic levels of heavy metals in plants.
MetalsEssentiality and Roles in PlantsAdequate/Beneficial Levels (mg kg−1 DW)Toxic Levels (mg kg−1 DW)References
Arsenic (As)Non-essential toxic heavy metal–≥5[60]
Cadmium (Cd)–≥5[60,61]
Chromium (Cr)–≥5[62]
Mercury (Hg)–≥1[60,63]
Lead (Pb)–≥30[62,64]
Copper (Cu)Essential micronutrient5–30>30[65,66]
Iron (Fe)50–250>500[65]
Manganese (Mn)20–500>1000[65]
Molybdenum (Mo)0.1–5>10[65]
Zinc (Zn)25–150>150[67,68]
Nickel (Ni)0.1–10>50[69,70]
Cobalt (Co)Beneficial for nitrogen fixation in legumes0.02–2>10[65]
Adequate/beneficial levels indicate concentrations typically required for normal plant growth. Toxic levels indicate concentrations at which plants exhibit growth inhibition, chlorosis, or other toxicity symptoms.
Table 2. Morphological, physiological, and biochemical responses of plants to heavy metal stresses.
Table 2. Morphological, physiological, and biochemical responses of plants to heavy metal stresses.
PlantsHM StressesMorphological, Physiological, and Biochemical ResponsesReferences
Rice (Oryza sativa)CdReduces catalase activity, which impairs H2O2 scavenging, resulting in higher lipid peroxide levels[84]
NiIncreases the level of H2O2 and TBARS[85]
PbIncreases lipid peroxidation[86]
HgDecreases canopy height, tillers number, panicle length, and yield[87]
Wheat (Triticum aestivum)NiIncreases electrolyte leakage and lipid peroxidation[88]
CdReduces shoot and root development[89]
Maize (Zea mays)Zn and NiIntensifies lipid peroxidation and decrease in permeability of cell membranes[90]
Sunflower (Helianthus annuus)CrIncreases lipid peroxidation by stimulating production of malondialdehyde and H2O2[91]
NiInhibits mobilization of stored proteins and amino acids; reduces α-amylase and protease activity[92]
Lentil (Lens culinaris)CuIncreases lipid peroxidation in roots[93]
Pigeon pea (Cajanus cajan)Cd and NiReduces photosynthetic activity[94]
Siris tree (Albizia lebbeck)Cd and PbCd impairs seedling development and elongation; Pb disrupts stored food material and reduces germination rate[95]
Indian mustard (Brassica juncea)CdReduces shoot and root biomass and decreases total chlorophyll content in the leaves[96]
Silene compecta and Thalpsi ochrolucumCuDamages the electron transport chain involved in photosynthesis[97]
Thale cress (Arabidopsis thaliana)CdIncreases lipid peroxidation[98]
Duckweed (Lemna minor)Cu[99]
Cd, cadmium; Cr, chromium; Cu, copper; HM, heavy metal; Hg, mercury; H2O2, hydrogen peroxide; Ni, nickel; Pb, lead; TBARS, thiobarbituric acid reactive substances; Zn, zinc.
Table 3. Responses of antioxidant enzymes in plants exposed to heavy metal stresses.
Table 3. Responses of antioxidant enzymes in plants exposed to heavy metal stresses.
Plants HM Antioxidant Enzymes ResponseReferences
Maize (Zea mays)CdIncreases APX and GPX activities[162]
ZnSOD and POD activities increase, while CAT activity decreases at higher Zn levels[163]
Barley (Hordeum vulgare)CdIncreases activities of APX and GPX[164]
Rice (Oryza sativa)PbElevates guaiacol peroxidase, SOD, and GR activities[86]
Mung bean (Vigna radiata)CrAPX activity increases, which helps reduce H2O2 accumulation[169]
Tomato (Lycopersicon esculentum)CuIncreases the activities of SOD, POD, and CAT[170]
Indian mustard (Brassica juncea)ZnIncreases CAT activity, which scavenges H2O2 and reduces oxidative stress[171]
Okra (Abelmoschus esculentus)HgIncreases SOD, APX, and GR activities and decreases CAT activity[172]
Peregrina (Jatropha integerrima)ZnPOD and CAT activities increase with Zn concentration[173]
Coffee (Coffea arabica)Increases GR activity, which supports GSH levels for PC biosynthesis[174]
Water hyacinth (Eichhornia crassipes)CAT activity increases with Ag, Cd, Cr, Pb, and Cu[175]
Camelthorn (Alhagi camelorum)CuInduces PC synthesis and depletes total GSH activity[176]
Ag, silver; APX, ascorbate peroxidase; CAT, catalase; Cd, cadmium; Cr, chromium; Cu, copper; GPX, glutathione peroxidase; GR, glutathione reductase; GSH, reduced glutathione; HM, heavy metal; Hg, mercury; H2O2, hydrogen peroxide; PC, phytochelatins; Pb, lead; POD, peroxidase; SOD, superoxide dismutase; Zn, zinc.
Table 4. Key signaling pathways and molecular components involved in heavy metal stress responses in plants.
Table 4. Key signaling pathways and molecular components involved in heavy metal stress responses in plants.
Signaling PathwaysKey ComponentsHeavy Metals ResponsesGenes InvolvedReferences
Calcium-dependent signalingCa2+ channels, calmodulins (CaMs), calmodulin-like proteins (CMLs), calcium-dependent protein kinases (CDPKs), calcineurin B-like proteins (CBLs)/CBL-interacting protein kinases (CIPKs)Cr, As, Pb, CuCalcium influx triggers antioxidant enzyme activation (e.g., SOD, APX); regulates redox homeostasis; CDPKs and CaMs modulate downstream responsesAtCBL1, CDPK-like kinases, CAMs[178,179,180]
MAPK cascade signaling MAPKKK → MAPKK → MAPK (MPKs)Cd, Cu, As, CrPhosphorylation of TFs (WRKY, DREB, bZIP, MYB); modulation of stress-responsive genes; interaction with HSPs for defenseOsMAPK2, ZmMPK3/6, WRKY, ERF, bZIP, MYB[177,181,182]
ROS signalingROS (O2–, H2O2, OH−), antioxidant enzymes (SOD, CAT, APX), thiol metabolism enzymesCd, Cr, As, PbLow ROS levels act as signaling molecules; high ROS induce PCD; upregulation of antioxidant genes maintains ROS balanceOsGSTL2, OsMATE1/2, DHAR, GR, SOD, CAT[178,183]
Hormonal SignalingABA, JA, ET, SA, EIN2/3, JAZ, AP2/ERF transcription factorsCd, Cr, AsPhytohormones regulate transcription and crosstalk with MAPK cascades; influence root development and HM detoxificationAP2/ERF, ACS, OsARM1, AtMYB, AB15, TGAL3[180,184]
Crosstalk and integrationInteractions among Ca2+, ROS, MAPKs, hormones, nitric oxide Cd, Pb, As, Cr, CuSynergistic and antagonistic interactions among signaling pathways coordinate stress responses; modulate TF networksMultigene families: WRKY, bZIP, HSF, MYB, ERF[177,178]
ABA, abscisic acid; AP2/ERF, APETALA2/ethylene-responsive factor; APX, ascorbate peroxidase; As, arsenic; Ca2+, calcium ion; CAT, catalase; Cd, cadmium; CBL, calcineurin B-like protein; CDPK, calcium-dependent protein kinase; CIPK, CBL-interacting protein kinase; Cr, chromium; Cu, copper; DHAR, dehydroascorbate reductase; ET, ethylene; GR, glutathione reductase; H2O2, hydrogen peroxide; HSP, heat shock protein; JA, jasmonic acid; MAPK, mitogen-activated protein kinase; MAPKK, MAPK kinase; MAPKKK, MAPK kinase kinase; OH−, hydroxyl radical; O2−, superoxide anion; PCD, programmed cell death; ROS, reactive oxygen species; SA, salicylic acid; SOD, superoxide dismutase; TF, transcription factor; Zn, zinc.
Table 5. Roles of transcription factors in plant adaptation to heavy metal stresses.
Table 5. Roles of transcription factors in plant adaptation to heavy metal stresses.
PlantsTFsGene(s)Key FindingsReferences
Wheat (Triticum aestivum)HSFTaHsfA4aUpregulates metallothionein genes under Cd stress[194]
Rice (Oryza sativa)MYBOsMYB45Downregulation increases Cd sensitivity; regulates antioxidant activity[182,195]
bZIP-Involved in auxin and HM signaling crosstalk
WRKY-Activated by MAPK pathways under HM stress
Sorghum (Sorghum bicolor)MYBSbMYB15Confers Cd and Ni stress tolerance[196]
Walnut (Juglans regia)MYBJrMYB2Improves tolerance to Cd stress[197]
Tomato (Solanum lycopersicum)HSFHSF1AInduces melatonin biosynthesis for Cd tolerance[198]
Rapeseed (Brassica napus)bZIPBnbZIP2, BnbZIP3Upregulated under drought and Cd; involved in stress signaling[199]
Arabidopsis (Arabidopsis thaliana)MYBAtMYB4Improves antioxidant defense under Cd stress[200]
WRKYAtWRKY12Downregulated under Cd; represses GSH1 to negatively regulate Cd tolerance[201]
WRKYAtWRKY13Upregulated under Cd; activates PDR8 to positively regulate Cd tolerance[202]
WRKYWRKY33Regulates HM uptake via IRT1 regulation under Cd stress[203]
bZIPAB15Interacts with MYB49 to reduce Cd uptake via IRT1 inactivation[204]
Cd, cadmium; Ni, nickel; GSH1, glutathione synthetase 1; HM, heavy metal; PDR8, pleiotropic drug resistance 8; IRT1, iron-regulated transporter 1; MAPK, mitogen-activated protein kinase; HSF, heat shock transcription factor; MYB, myeloblastosis transcription factor; TFs, transcription factors; WRKY, tryptophan-arginine-lysine-tyrosine transcription factor; bZIP, basic leucine zipper transcription factor.
Table 6. Nanoparticles for heavy metal stress mitigation in plants.
Table 6. Nanoparticles for heavy metal stress mitigation in plants.
NanoparticlesPlant SpeciesHMsReduction of HMs (%)Key FindingsReferences
Zinc oxide (ZnO)Rice, fenugreek, and Leucaena leucocephalaPb, Cd, Cr, CuPb: 79–85; Cd: 80–87; Cr: 38–81; Cu: 60Improves growth and Zn uptake; reduces HM accumulation[213,214]
Cerium oxide (CeO2)RiceCd8.4Reduces growth inhibition and oxidative stress[152]
Astaxanthin-functionalized gold (Ast-Au) NPs26–86Enhances chlorophyll content and amino acid metabolism; scavenges ROS[215]
Titanium dioxide (TiO2)Rice and cucumberPb, As, Al34–97Reduces HM contamination and toxicity[216]
Iron oxide (Fe3O4)WheatPb, Zn, Cd, CuRoots: 24–68; Shoots: 11–100Reduces oxidative stress and growth suppression[217,218]
Selenium NPs (Se, Bio-Se)Coriander and pak choiCd, Pb, HgCd: 21–31; Pb: 5–30; Hg: 3–23Enhances antioxidant defense; reduces HM uptake[219,220]
Graphene oxideLettuceCd-Reduces Cd toxicity; improves photosynthesis, chlorophyll content, antioxidant enzymes, and biomass[221]
Al, aluminum; As, arsenic; Bio-Se, biologically synthesized selenium; Cd, cadmium; Cr, chromium; Cu, copper; Fe, iron; HM, heavy metal; Hg, mercury; NPs, nanoparticles; Pb, lead; ROS, reactive oxygen species; Zn, zinc.
Table 7. Microbial and plant-based biosynthesis of nanoparticles and their role in mitigating heavy metal phytotoxicity.
Table 7. Microbial and plant-based biosynthesis of nanoparticles and their role in mitigating heavy metal phytotoxicity.
Nanoparticles Microorganisms/Plant Extracts UsedAlleviation of Phytotoxicity/Key FindingsReferences
Silver NPsEscherichia coliRapid reduction of Ag+ ions within minutes[230]
Pseudomonas stutzeriSilver-resistant; accumulates silver and reduces its toxicity[231]
Solanum xanthocarpum (berry extract)Enhances Ag+ ion reduction rate via phytochemicals[232]
Convolvulus arvensis (leaf extract)Achieves 98.99% Cu2+ ion removal via adsorption[233]
Gold NPsBacillus subtilisActs as a biocontrol agent with antifungal properties[234]
Aspergillus japonicusReduces Au(III) to Au(0); immobilized AuNPs[235]
Colletotrichum sp.Reduces and caps gold NPs[236]
ZnO NPsGreen algaeConverts metal ions into zero-valent metals via phytochemicals[237]
Citrus limon (leaf extract)Non-toxic synthesis; biomolecule-rich extract enhances safety[238]
Lead NPsClostridium pasteurianumReduces Cr(VI) to Cr(III); ~70% remediation efficiency[239]
Iron NPsChlorococcum (alga) Biosynthesized Fe NPs removed 92% Cr vs. 25% by bulk Fe[240]
Aspergillus oryzaeCost-effective and eco-friendly NP synthesis for remediation[241]
TiO2 NPsAspergillus nigerReduces Cr(VI) toxicity and DNA damage in Helianthus annuus by minimizing total Cr uptake[242]
Biogenic Fe–Mn oxides (BFMO)Pseudomonas sp.Converts As(III) to less mobile As(V); enhances arsenic remediation[243]
CdS NPsP. aeruginosaEPS-enriched CdS NPs enhance cadmium ion adsorption and stabilization[244]
Ag+, silver ions; As, arsenic; As(III), arsenite; As(V), arsenate; AuNPs, gold nanoparticles; CdS, cadmium sulfide; Cr, chromium; Cr(III), trivalent chromium; Cr(VI), hexavalent chromium; EPS, extracellular polymeric substances; Fe–Mn, iron–manganese; NPs, nanoparticles; TiO2, titanium dioxide.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Jarin, A.S.; Khan, M.A.R.; Apon, T.A.; Islam, M.A.; Rahat, A.; Akter, M.; Anik, T.R.; Nguyen, H.M.; Nguyen, T.T.; Ha, C.V.; et al. Plant Responses to Heavy Metal Stresses: Mechanisms, Defense Strategies, and Nanoparticle-Assisted Remediation. Plants 2025, 14, 3834. https://doi.org/10.3390/plants14243834

AMA Style

Jarin AS, Khan MAR, Apon TA, Islam MA, Rahat A, Akter M, Anik TR, Nguyen HM, Nguyen TT, Ha CV, et al. Plant Responses to Heavy Metal Stresses: Mechanisms, Defense Strategies, and Nanoparticle-Assisted Remediation. Plants. 2025; 14(24):3834. https://doi.org/10.3390/plants14243834

Chicago/Turabian Style

Jarin, Aysha Siddika, Md Arifur Rahman Khan, Tasfiqure Amin Apon, Md Ashraful Islam, Al Rahat, Munny Akter, Touhidur Rahman Anik, Huong Mai Nguyen, Thuong Thi Nguyen, Chien Van Ha, and et al. 2025. "Plant Responses to Heavy Metal Stresses: Mechanisms, Defense Strategies, and Nanoparticle-Assisted Remediation" Plants 14, no. 24: 3834. https://doi.org/10.3390/plants14243834

APA Style

Jarin, A. S., Khan, M. A. R., Apon, T. A., Islam, M. A., Rahat, A., Akter, M., Anik, T. R., Nguyen, H. M., Nguyen, T. T., Ha, C. V., & Tran, L.-S. P. (2025). Plant Responses to Heavy Metal Stresses: Mechanisms, Defense Strategies, and Nanoparticle-Assisted Remediation. Plants, 14(24), 3834. https://doi.org/10.3390/plants14243834

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop