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A Comprehensive Review on the Heavy Metal Toxicity and Sequestration in Plants

Riyazuddin Riyazuddin, Nisha Nisha, Bushra Ejaz and 4 more

Biomolecules · 2021 · Review · CC BY

doi:10.3390/biom12010043

Abstract

Heavy metal (HM) toxicity has become a global concern in recent years and is imposing a severe threat to the environment and human health. In the case of plants, a higher concentration of HMs, above a threshold, adversely affects cellular metabolism because of the generation of reactive oxygen species (ROS) which target the key biological molecules. Moreover, some of the HMs such as mercury and arsenic, among others, can directly alter the protein/enzyme activities by targeting their –SH group to further impede the cellular metabolism. Particularly, inhibition of photosynthesis has been reported under HM toxicity because HMs trigger the degradation of chlorophyll molecules by enhancing the chlorophyllase activity and by replacing the central Mg ion in the porphyrin ring which affects overall plant growth and yield. Consequently, plants utilize various strategies to mitigate the negative impact of HM toxicity by limiting the uptake of these HMs and their sequestration into the vacuoles with the help of various molecules including proteins such as phytochelatins, metallothionein, compatible solutes, and secondary metabolites. In this comprehensive review, we provided insights towards a wider aspect of HM toxicity, ranging from their negative impact on plant growth to the mechanisms employed by the plants to alleviate the HM toxicity and presented the molecular mechanism of HMs toxicity and sequestration in plants.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

Feeding an exponentially growing population in the era of global climate change is a serious challenge. Among different environmental factors, abiotic stressors are the major factors affecting crop yield and the livelihood of mankind. In particular, heavy metal (HM) toxicity has emerged as one of the most serious threats to the crop production that might become even more prevalent in the coming decades. HMs are a group of 52 metals including lead (Pb), manganese (Mn), copper (Cu), nickel (Ni), cobalt (Co), cadmium (Cd), mercury (Hg), and arsenic (As) which directly affect the plant performance in a concentration-dependent manner. When present in adequate amounts, both micro and macronutrients maintain the functionality of key enzymes and regulate the metabolic pathways including photosynthesis, DNA synthesis, protein modifications, sugar metabolism, and redox homeostasis. However, at higher concentrations, these exhibit toxicities and can be lethal for all the lifeforms including plants as well as animals.

Increased anthropogenic activities such as mining, modern agriculture practicing, fertilizer application, extensive use of groundwater for irrigation, sewage disposal, and industrialization have disturbed the distribution of these HMs, leading to their accumulation at specific sites. Accumulation of HMs consequently affects soil health and texture because of the alteration in soil pH and the ratio of essential/or nonessential elements, which is a global concern for agricultural production. Moreover, absorption of these HMs from the contaminated soil and their accumulation, especially in food crops, are a serious concern for human health. It has been reported that these HMs, following their absorption from the contaminated soil, can accumulate in the edible plant parts and thus enter the food chain with a potential health risk to humans and animals.

Plants growing in HM-contaminated soils show visible symptoms like stunted growth, chlorosis, root browning, and sometimes even death. Moreover, HM toxicity hinders the metabolic, cellular, and genetic potential of the plants required for normal growth and development. However, some of the plants can cope with a moderate concentration of HM(s) by reducing their uptake, their compartmentalization into vacuoles, their sequestration through phytochelatins (PC)/metallothioneins (MT), and activation of antioxidant defense. Since the accumulation of reactive oxygen species (ROS) is one of the most common effects of stress conditions in plants, activation of antioxidant defense mechanism is a major strategy to overcome the adverse effects of stress conditions. Nevertheless, the effectiveness and initiation of a particular defense response depend on the plant and type of HMs as well as their concentration and duration of exposure. Therefore, the need of the hour is to understand the effect of HM toxicity on crop plants in order to find a scientific way for improving crop yield in HMs contaminated soil, which is going to be more prevalent in near future. The present review was an upfront effort to integrate the recent understanding of morphological, physiological, and biochemical mechanisms of HMs-induced plant stress responses in order to present the molecular mechanism of HM toxicity and tolerance in plants.

2. HM Toxicity Induces Morphological, Anatomical, and Physiological Changes in Plants

Plants growing in HM contaminated soils show visible symptoms as the uptake and accumulation of HMs in plant tissues alter the morphology and overall health of the plants (Figure 1).

The effect of HM toxicity can be observed on almost all the plant tissues and at all the stages of plants’ life cycle starting from seed germination to senescence; however, these effects are more pronounced during seed germination and root growth. Since seed germination is sensitive to physicochemical conditions of the rhizosphere, decline in seed germination and vigor and subsequent seedling growth have been reported under HM toxicity in most cases. In particular, Pb-toxicity has been shown to induce adverse effects on seed morphology, physiology, germination, and early crop growth in a variety of crops including Raphanus sativus, Lens culinaris, Oryza sativa, Hordeum vulgare, Elsholtzia argyi, Spartina alterniflora, Vigna radiata, Medicago sativa, and Zea mays, as reviewed previously. In addition to Pb, exogenous application of other HMs also exhibits similar effects on seed morphology, physiology, and germination. For instance, a combined treatment of Cu and Cd to Solanum melongena severely reduced seed germination, seedling growth, and number of lateral roots. Although the exact molecular mechanism of this HM toxicity-induced changes in seed physiology is not well understood, a growing body of evidence suggests that HMs cause inhibition of various enzymes which results in these changes. For instance, Hg-mediated inhibition of seed germination and embryo growth was found to be because of the direct interaction of Hg with the –SH group(s) of the proteins, resulting in the formation of a S-Hg-S bridge causing uneven modification in protein structures and thus loss of enzymatic activities. Since the functions of certain enzymes such as amylases and proteases are crucial for seed germination, their inhibition affects the process of seed germination and subsequent hypocotyl and radical growth.

Apart from the seeds, changes in the root architecture have also been observed in the plants growing in the HM contaminated soils. In particular, decreased root elongation and increased lateral root formation have been reported in the presence of various HMs such as Cu, Pb, Cr, Zn, and Cd stress in several plants including Arabidopsis thaliana, Triticum aestivum, Sesbania rostrata, Sesbania cannabina, Pinus sylvestris, and Lupinus luteus, among others. In Vigna unguiculata, localized swelling was reported behind the root tips because of the initiation of the lateral roots and bending of some root tips along with the reduction in fresh biomass and decreased root growth under Pb-toxicity. It has been suggested that HMs, particularly Zn, accumulate in the endodermis and pericycle and trigger the formation of lateral roots. This formation of the lateral roots under HM toxicity is the initial symptom of HM toxicity, which subsequently impairs absorption and conduction of water which, in turn, results in lower transport of photosynthates to roots. Since roots receive lesser amounts of photosynthates during HM toxicity, the growth of primary and secondary roots are inhibited, resulting in a lower specific root length and a high root/shoot area ratio.

Subsequent research showed that these HM toxicity-induced changes in root architecture are partially remodeled by the action of indole acetic acid (IAA), and phenols produced in the presence of HMs. Genes involved in IAA biosynthesis were reported to be upregulated, leading to the increased content of auxin and auxin/cytokinin ratio under HM toxicity, which acted as key factors responsible for determining morphological changes in roots. Moreover, emerging evidence also highlights the role of Nitric oxide (NO) in inhibition of root meristem growth as observed under Cd stress in Arabidopsis. Cd-induced NO accumulation is involved in the inhibition of auxin transport to the root apex, leading to a reduction in the meristem size. Moreover, an auxin efflux carrier protein PINFORMED1 (PIN1), responsible for root meristem growth and elongation, was found to be downregulated under HM toxicity, further indicating the fine-tuning of auxin transport under HM toxicity. These observations were further supported by the results of, showing a similar NO-auxin cumulative root meristem inhibitory effect under Cu stress.

Along with the root inhibition, stunted growth of the plants has also been observed under HM toxicity. Transport of HMs from contaminated soils via roots to aerial parts and their accumulation in plants cells interfere directly with the cellular metabolism of shoot causing a reduction in the height as observed in a variety of crop and non-crop plants including mung bean, oats, Curcumas sativus, Lactuca sativa, Panicum miliaceum, wheat, Jatropha curcas, maize, rice, and poplar. Although the exact molecular mechanism of HM-induced growth inhibition is currently unknown, it has been reported that some of the HMs such as As and Hg induce loss of cell turgidity, a decline in mitotic activity, and inhibition of cell elongation as a result of their selective binding to the –SH group of proteins involved in the regulation of cell division and replacement of phosphate group of ATPs, and thus are involved in the reduction in plant growth under HM toxicity. Besides, As has also been shown to dismantle the chlorophyll molecules by interacting with the central atom (Mg) of the porphyrin ring, leading to the inhibition of photosynthesis which affects the overall growth as reported in the sunflower seedlings. Moreover, Cu toxicity mediated enhanced lignification in both shoots and roots has also been reported, which subsequently resulted in reduced biomass accumulation due to impairment in the cell development, leading to a greater formation of trichomes on the leaves and stems probably to sequester excess Cu.

In the case of leaves, HM toxicity affects the area, number, pigmentation, and thickness of leaves by impairing plant-water relations which, in turn, affects various physiological processes such as transpiration and photosynthesis. In general, a drop in leaf number, area, and biomass has also been reported in a number of plants including Albizia lebbeck, Arabidopsis thaliana, Spinacea oleracea, Brassica oleracea, Oryza sativa, Acacia holosericea, Leucaena leucocephala, Prosopis laevigata Arabidopsis thaliana, and Spinacea oleracea under HM toxicity. In the case of sugarcane, a lower concentration of Cr (40 ppm) induced leaf chlorosis while a higher concentration (80 ppm) caused necrosis. Moreover, browning of leaf tip of Phaseolus vulgaris due to Hg toxicity and small brittle purple leaves of Jatropha curcas in the presence of Pb have also been reported under HM-toxicity. Under Zn and Cd- Cu stress, a decrease in the stomatal index was observed in Beta vulgaris and Sorghum vulgaris. In some plants such as Helianthus annuus and Vigna radiata, an increased number of stomata has been reported in the presence of Pb and As at the earlier stages of HM toxicity, which was accompanied by the development of arrested, fused, and abnormal stomata in Vigna radiata. Similarly, Zn and Cd toxicity resulted in the development of anomalous and non-functional stomata in Zea mays. Further, HM toxicity also results in the reduction of parenchymatous tissues and xylem vessels along with the development of smaller mesophyll tissue as observed in Brachiaria decumbens under Cu stress. All these HM-toxicity-induced changes in the stomata, xylem vessels, parenchymatous and mesophyll cells subsequently alter the plant-water relation and thus are, at least partially, responsible for the decreased leaf growth.

3. HM Toxicity Negatively Influence the Photosynthesis

Since the accumulation of HMs in the plants leads to adverse changes in the primary photosynthetic organ leaves, a decline in the rate of photosynthesis can be presumed. Literature hints that the impact of HMs on photosynthetic machinery depends on the reactivity and concentration of HMs in leaves, which subsequently affects light capture, electron transport, and activities of photosynthetic enzymes including RuBisCO (Figure 2).

For instance, a reduction in maximal photochemical efficiency (Fv/Fm), effective quantum yield of photosystem II (φPSII), and photosynthetic electron transport rate (ETR) values were reported during Cd stress in lettuce plants, indicating inhibition of photosynthesis, while in wheat, Cd toxicity was manifested by the inhibition of the oxygen evolution, the decline in PSI activity, and chlorophyll fluorescence. Likewise, Mazur et al. (2016) reported that Tl toxicity resulted in a decrease in the plant and leaf size, the number of discolored and necrotic leaves, changes in the mesophyll structure, and a 50% decline in the PSI and PSII activities in white mustard (Sinapis alba L.). A similar result was also reported under Cr toxicity, where a reduced number of active reactions centers of photosystem II together with the loss of starch grains and appearance of plastoglobuli in the chloroplast of Spirodela polyrhiza were reported. Other plants experiencing toxicity of a variety of HMs also showed a similar drop in the photosynthesis and all of these studies collectively suggested that the decline in photosynthesis is majorly because of the decrease in the chlorophyll concentrations. Based on the literature evidence, it can be concluded that HMs can target chlorophyll in any of three ways: (1) by enhancing the activity of chlorophyllase enzyme; (2) by causing oxidation/reduction of chlorophyll molecules by the HM toxicity induced ROS; and (3) inhibition of chlorophyll biosynthesis as some of the HMs such as Hg, Cu, Pb, Ni, Cd, and Zn are able to replace the Mg in the porphyrin ring of the chlorophyll molecules. Besides, phaeophytization of chlorophyll molecules because of the replacement of Mg2+ ions by H+ ions has also been reported in Eudorina unicocca and Chlorella kessleri under Cr-toxicity.

In addition to targeting the chlorophyll molecules, changes in chloroplast and thylakoid membranes have also been reported in presence of several HMs because of the HM-stress-induced ROS production (Figure 2). For instance, swelling of thylakoids, degradation of internal chloroplast membranes, and loss of chloroplast membrane integrity were observed during Pb/Cd toxicity in barley and Lemna minor. Likewise, the poor lamellar arrangements with few grana with widely placed thylakoids were reported in Limnanthemum cristatum under Cr toxicity. In addition to causing the peroxidation of chloroplast membranes, HM-stress-induced ROS production also minimizes the uptake of crucial elements required for the synthesis of photosynthetic pigments such as Mg, K, Ca, and Fe as reported under various HM stresses such as in Pb, Cd, and Cr in Brassica napus, Cu, Pb and Cd stress in wheat, and Al, Pb, Cr, Cd and Zn toxicity in sorghum. Moreover, the inactivation of photosynthetic enzymes such as RuBisCO and other Calvin cycle enzymes has also been reported under HM toxicity (Figure 2). In barley, it was shown that Pb/Cd-induced ROS interacted with the thiol group of enzymes and ultimately hindered the functions of chloroplast, including photosynthesis. A similar observation was also reported during Cd toxicity where Cd altered the protein structure via ROS induction and inhibited enzyme activity by interacting with the sulfhydryl and carbonyl groups of the proteins and replacing essential co-factors of enzymes.

Taken together, it can be concluded that HM toxicity reduces the net photosynthesis rate by inhibiting both light and dark reactions of photosynthesis. It is quite evident that inhibition of light reactions during HM toxicity is because of the decreased efficiencies of PS I and PSII, which is a combined effect of reduced chlorophyll concentration and destabilized chloroplast and thylakoid membranes. On the other hand, inhibition of dark reactions is majorly because of the decreased activities of enzyme associated with the Calvin cycle.

4. Antioxidant Enzymes Alleviate the HM Toxicity Induced Oxidative Stress

HM toxicity induces the production of excessive ROS, which interact with macromolecules such as DNA, proteins, and lipids, leading to a series of vicious processes together termed as “oxidative stress”. A substantial number of investigations suggests that HMs alter cellular redox equilibrium in the five conceivable succeeding ways: (1) by shifting redox potential to more oxidized values; (2) by directly producing ROS through Fenton-like reactions and the Haber-Weiss cycle; (3) by consuming GSH, which is involved in the synthesis of PCs required for the chelation and sequestration of HMs into vacuoles via ABC transporters; (4) by directly inhibiting the activities antioxidant enzymes by exchanging essential cations from the specific binding sites and targeting their -SH groups; and (5) by inducing the activity of NADPH oxidases.

Redox homeostasis is largely dependent on the balance of reduced glutathione (GSH)-oxidized glutathione (GSSG), which is majorly maintained by the activity glutathione reductase (GR). Under normal conditions, glutathione and ascorbate are majorly available in the reduced form and are involved in the detoxification of oxidants at different cellular compartments including cytoplasm, endoplasmic reticulum, vacuoles, mitochondria, chloroplast, and peroxisome. At first, it was reported that Al toxicity elevated the level of GSH as an earlier response and provided HM-stress tolerance in Pisum sativum, which indicated the changes in cellular redox levels in response to HM toxicity and subsequent accumulation of antioxidants to maintain the redox homeostasis. Further, transcript levels of GR were found to be elevated in Cr treated Brassica juncea and maize seedlings. However, this increased GR expression with high GSH/GSSG was not sufficient to protect the cell from Cr-induced oxidative damage in maize. Yet, increased GR activity has been reported under moderate HM-stress conditions in a variety of plants including pea, wheat, alfalfa, S. vulgaris, and Arabidopsis. In addition to the GR, a substantial number of investigations suggest that GRXs also play a key role in HM toxicity tolerance in plants (Figure 2). GRXs are GSH-dependent disulfide oxidoreductases that catalyze the reduction of disulfide bonds of their substrate proteins and participate in oxidative stress responses in plants. It was reported that the ectopic expression of chickpea (Cicer arietinum L.) glutaredoxin (CaGrx) gene in A. thaliana elevated GSH levels and maintained the redox homeostasis under the toxicities of various HMs including AsIII, AsV, Cr(VI), and Cd. Likewise, OsGrx genes were also found to be involved in detoxification of As and provided HM stress tolerance by regulating/maintaining GSH level and/or GSH recycling. Transgenic A. thaliana plants overexpressing OsGrx_C7 and OsGrx_C2.1 genes showed elevated Grx activity and a higher intracellular GSH content under As stress as compared with wild-type (WT). These results altogether indicate that GRXs are able to maintain ROS homeostasis by increasing the production and recycling of GSH.

In addition to GR and GRX, functions of other enzymatic antioxidants in HM-stress tolerance have also been highlighted. For instance, Chowardhara et al. (2020) reported an accumulation of non-enzymatic antioxidants such as proline, ascorbate, and glutathione and increased activities of enzymatic antioxidants including SOD, CAT, GST, GR, APX, and POX under Cd toxicity in the three cultivars of B. juncea, indicating a pivotal role of these antioxidants in the HM-stress tolerance. Further, overexpression of Triticum aestivum catalase (TaCAT3) gene provided As stress tolerance via enhancing the catalase activity. Interestingly, overexpression of TaCAT3-B genes in E. coli also resulted in higher tolerance towards AsIII and AsV toxicity in the transgenic lines. Moreover, while comparing different flax (Linum usitatissimum L.) genotypes for their Pb-stress tolerance, Pan and co-workers observed that the Milas genotype, showing increased expression of various genes encoding for antioxidants such as LuSOD1, LuPOD1, and LuPOD2, was more tolerant to Pb-toxicity than others.

5. Tolerance to HM Toxicity Is Mediated by a Complex Signaling Network

Plants under HM toxicity exhibit biochemical, physiological, and molecular changes as a part of their tolerance response, and understanding these responses is crucial to induce HM tolerance in sensitive crop plants (Figure 3).

A growing body of evidence suggests a crucial role of various signaling molecules including H2S and Cys in HM stress tolerance. Both H2S and Cys are essential sulfur metabolism products that have emerged as novel gasotransmitters and redox signal molecules. At first, an upregulation of H2S biosynthesis genes such as L-Cysteine desulfhydrase (LCD) and L-Cysteine desulfhydrase 1 (DES1) was observed under Cd toxicity, suggesting a release of endogenous H2S under HM-toxicity. Therefore, to confirm the roles of these two signaling molecules, mutants of H2S (lcddes1-1) and Cys (oasa1, O-acetylserine(thiol)lyase isoform A1) biosynthesis genes were developed in Arabidopsis which were defective in the production of H2S and Cys. Interestingly, these mutants showed decreased Cd stress tolerance as compared with the WT, which confirmed the pivotal roles of these two molecules in HM-stress tolerance. Similarly, Arabidopsis oasa1-1 and oasa1-2 mutants, which are defective in Cys production, showed significantly reduced Cd tolerance. Altogether, it has been proposed that H2S and Cys participate in suppressing HM stress in plants via inhibiting ROS burst by inducing the expression level of MT genes, alternative respiration capacity, antioxidant activity, and GSH accumulation following the enhancement of the level of PCs genes (Figure 2). In addition to PCs, several other genes have been shown to play a positive role in mitigating HM toxicity (Table 1).

For instance, upregulation of acyl-CoA-binding proteins ACBP1 and ACBP4 was reported under Pb2+ stress and the overexpression of ACBP1 gene improved tolerance to Pb2+ in Arabidopsis. Moreover, transgenic tobacco overexpressing a truncated NtCBP4 was more tolerant to Pb2+ as compared with plants overexpressing the full-length NtCBP4 gene. Moreover, the disruption of the homologous Arabidopsis CNGC1 gene (cyclic nucleotide-gated ion channel) conferred tolerance to Pb toxicity. NtCBP4 and AtCNGC1 are both components of a transport pathway that facilitates the entry of Pb2+ into plant cells and thus disruption of these genes could be an important strategy for inducing the HM-stress tolerance in plants by limiting the uptake of these HMs inside the plant cells.

Transcription factors such as GRAS (GRAS domain family), myeloblastosis protein (MYB), C2H2, bHLH, NAC, basic leucine zipper (bZIP), ethylene-responsive (ERF), and WRKY, among others, are emerging out to be the regulators of HM-stress tolerance in plants. For instance, transcriptome analysis of kenaf (Hibiscus cannabinus L.) showed enhanced expression of various transcription factors, including WRKY, GRAS, MYB, bHLH, ZFP, ERF, and NAC under Cd stress. Similarly, activation of a large number of WRKY genes along with C2H2 zinc finger protein, AP2 domain-containing protein, MYB, and HSF have been reported in Arabidopsis under Pb and Cd toxicities and in rice under Cd-stress conditions. In Arabidopsis, several transcription factors including a Zinc-Finger protein ZAT6 were found to be induced during Cd stress and provided tolerance via the glutathione-dependent PC pathway.

6. Sequestration and Compartmentalization: Plants’ Way to Alleviate the HM Toxicity

During their growth and development, plants absorb essential elements such as carbon (C), nitrogen (N), potassium (K), zinc (Zn) as well as non-essential elements such as Cd, Hg, and Pb, among several others. Although trace quantities of non-essential elements are beneficial for plant growth, excessive accumulation of these elements adversely affects various physiological and metabolic processes and deteriorates plant growth and development. Metal accumulation in plants is majorly governed by the two processes including their uptake inside the plant cells and their translocation from roots to other parts. In most of the cases, the major percentage of the HMs in plants is transported from root to stem and thus the concentration of HMs in the aboveground parts is higher than the roots; however, the most toxic HMs are commonly not transported in non-hyperaccumulating plants and the highest concentration is usually found in the roots. For instance, in tomato plants, the highest concentrations for Cu, Ni, Cr, Mn, and Pb were reported in order of root > leaf > stem > fruit.

HM stress-tolerant and hyperaccumulator plants get rid of the unused and extra amount of metal ions by effluxing and/or compartmentalization majorly in the vacuole with the help of two vacuolar proton pumps, including an ATPase and a Ppas (Figure 2). For instance, sequestration of Zn in the hyperaccumulator plants has been majorly observed in the vacuoles of epidermal cells and trichomes of mesophyll cells, as shown in Thlaspi caerulescens and in Arabidopsis helleri respectively. In addition, Zn can also be accumulated, although to a lesser extent, in the cell wall and cytosol in leaves of another hyperaccumulator plant P. griffithii. Apart from the Zn, Ni was also found to be accumulated in the vacuoles of a Ni hyperaccumulator plant Alyssum serpytllifolium. Similar findings were also reported in the case of tolerant plants such as B. juncea, Silene vulgaris, and Brassica napus where an accumulation of Cd has been reported majorly in the epidermal and mesophyll cells.

Apart from sequestration, plants minimize the HM toxicity by limiting the absorption of HMs from the soil through secretion of chelating compounds in the root hairs. Plants synthesize cystine-rich metal-binding peptides known as PCs and MTs to chelate the HMs. Among different HMs, Cd has been identified as the most potent inducer of PC synthesis in plants. These PCs bind to the HMs and sequester them into the vacuoles; however, PCs accumulation does not always have a beneficial effect on plants. For instance, rice plants expressing TaPCS1 from Triticum aestivum were found to be Cd sensitive and showed enhanced Cd accumulation in shoots. Similar to the PCs, MTs also act as biochelators and can directly bind to various HMs such as Zn, Cu, Cd, and Ni, among others. These MTs are localized in the membrane of the Golgi apparatus and growing evidence also indicates their role in maintenance of ROS homeostasis during HM toxicity. For instance, ectopic expression of different MT genes including type 1, type 2, and type 3 genes from a variety of plants such as rice, B. juncea, and Elsholtzia haichowensis has been shown to enhance the tolerance to Cu and/or Cd stress in transgenic plants. This MT-induced enhanced HM-toxicity tolerance was because of the increased SOD and POD activities and decreased production of hydrogen peroxide (H2O2) that protected the transgenic plants from the HM-toxicity-induced oxidative stress. Similar to the MTs, some of the beneficial elements such as silicon (Si) and selenium (Se) also participate in the HM-stress tolerance by limiting the uptake of HMs and enhancing the activities of antioxidant enzymes. There are now ample reports which have shown that the exogenous application of either of these two metals enhances plants’ tolerance to HM toxicity. For instance, exogenous treatment of Si has been shown to decrease the uptake, transport, and accumulation of Cd in various plants such as peanut, Cucumis sativus, cotton, and Brassica chinensis and mitigate the toxic effects of Cd toxicity by reducing the electrolyte leakage, MDA and H2O2 contents and improving the activities of antioxidant enzymes such as CAT, SOD, and POD.

Apart from these proteins and metals, various secondary metabolites also act as metal chelators and are involved in the sequestration of HMs to vacuole to provide HM-stress tolerance (Figure 2). Su et al. (2020) investigated the role of lignin in HM-stress tolerance and found that two lignin-defective mutants (ldm1 and ldm2) of rice showed dwarf shoots and roots due to higher levels of Cu accumulation in the roots and leaf sheaths tissues, suggesting that the promotion of lignin synthesis in plants may be an adaptive strategy for Cu adaptation. Interestingly, a higher accumulation of phenolics and amino acids was found to be associated with Co and Cu stress tolerance. It was observed that exposure of Co and/or Cu significantly reduced chlorophyll content and photosynthetic and transpiration rates of the two barley genotypes. In the comparison of a single treatment of Co or Cu, their co-application significantly attributed the higher accumulation of phenolics, including cinnamic acid and benzoic acid derivatives, together with free amino acids in tolerant genotypes (Yan66) than in susceptible genotype (Ea52). Moreover, phenolic compounds also participated in the vacuolar sequestration of Cd which enhanced Cd tolerance in Thlaspi caerulescens. In Jatropha curcas, phenylalanine ammonia-lyase (JcPAL) genes were identified in the metal detoxification mechanism along with the metallothioneins (JcMT2a). Interestingly, the transcript levels of JcPAL-R and JcPAL-L were upregulated with increasing Pb dose in a dose-dependent manner. Overall, their results suggested that along with the steadiness of growth traits, upregulation of metal transporter, and antioxidant defense system and higher accumulation of antioxidants including flavonoids and phenolics also participate in alleviating the HM-toxicity. Similarly, the phenylalanine ammonium lyase-related gene (HvPAL) was found to be highly upregulated along with the genes (HvMDH and HvCSY), involved in the biosynthesis of malate and citrate, under the combined treatment of Co and Cu in barley. Some organic acids such as citrate and malate are known to participate in HM tolerance directly or indirectly. The increase of these organic acids might be responsible for energy production under the combined treatment to fulfill the higher energy demand by metal transporters to improve Co and Cu tolerance. These metal transporters, including ABC type transporters, are a group of organic solute transporters that help in vacuolar sequestration of “PC-metal complexes” and play an important role in metal ion homeostasis and tolerance. For instance, it was shown that “PC-metal complexes” of metal ions such as Zn2+, Cu2+, and Mn2+ can be transported into the vacuole through the putative ABC transporter(s). A recent study has highlighted that H2S functions by regulating the expression levels of genes of the ATP-binding cassette (ABC) superfamily to provide HM-stress tolerance. In rice, H2S was found to alleviate the Al3+ toxicity by enhancing the expression levels of ABC transporters, including OsSTAR1 and OsSTAR2 genes which prevent entering of Al into the cytoplasm. Besides, some other studies have also highlighted the pivotal roles of ABC and other transporters in HM-stress tolerance. For instance, upregulation of wheat ABCC transporters including TaABCC3, TaABCC4, TaABCC11, and TaABCC14 was observed under Cd toxicity. In Brassica napus, ABCC transporters BnaABCC3 and BnaABCC4 were upregulated under Cd stress and enhanced Cd tolerance by limiting the entry of Cd inside the cells and their phytochelatin-mediated detoxification. Similar observations have been observed in Arabidopsis where ABCC transporters AtABCC3 and AtABCC6 were found to be involved in phytochelatin-mediated Cd tolerance during seedling development. In addition to these expression studies, overexpression studies have further supported the role of ABC transporters in HM-stress tolerance. For instance, overexpression of FvABCC11 gene increased Cd tolerance in strawberry and AtABCC1 and AtABCC2 conferred tolerance to Cd and Hg in Arabidopsis through the vacuolar sequestration of these HMs. It was determined that OsABCC1 regulated As-stress tolerance by sequestering As in vacuoles of the phloem companion cells of the nodes in rice grains. Similarly, a heavy metal transporter gene AtPDR8 (an ABC transporter) was identified as a cadmium-extrusion pump in Arabidopsis to mediate resistance against Cd and Pb toxicity.

Along with the ABC transporters, involvement of other transporters including multidrug and toxic compound extrusion (MATE) family proteins, zinc-iron permease (ZIP), iron-regulated transporters (IRT1), natural resistance-associated macrophage proteins (NRAMP), copper transporters (Ctr/COPT), and heavy metal ATPase (HMA) transporters has also been highlighted in tolerance to HM toxicity. These metal transporters are involved in mediating metal intake and translocation in plants. For instance, IRT1 (a Fe transporter gene) that belongs to the ZIP family has been identified in Arabidopsis that leads to high-affinity Fe uptake under Fe-deficient conditions along with uptake of other heavy metals such as Cd and Zn. Other ZIP metal transporters such as ZIP1 and ZIP2 were identified as Zn and Mn transporters in roots that mediate remobilization of Zn and/or Mn from the vacuole to root stele.

Metal transporters such as cation diffusion facilitator (CDF) transporters, ferroportins, VIT1/CCC1 also play a crucial role in the detoxification of HMs in plants and prominently remove transition metals out of the cytoplasm in the plant cell. ZAT transporters (a CDF transporter) in Arabidopsis such as ZAT1 showed a significant role in Zn metal sequestration as transgenic lines with overexpression of ZAT1 exhibited increased Zn resistance. It was hypothesized that ZAT is involved in vesicular or vacuolar sequestration of HMs such as Zn and thus is involved in enhancing Zn tolerance in plants. The expression of ZTP1 (a ZAT gene) in the Zn hyperaccumulators such as Thlaspi caerulescens in response to calamine (source of Zn, Pb, and Cd) and serpentine (rich in Ni) suggests the alleviatory role of ZTP1 in plants during HM toxicity. ShMTP1, a CDF transporter, confers Mn tolerance in Arabidopsis by sequestering metal to internal organelles and may function as an antiporter of Mn to enhance tolerance. Several P1B-ATPases in Arabidopsis have been identified that majorly alleviate metal accumulation. For instance, ectopic overexpression of AtHMA4 in Arabidopsis mediated plant growth and development by enhancing the root growth and root-to-shoot metal translocation in the presence of toxic heavy metals (Zn, Co, and Cd). The expression of P-type ATPase transporters enhanced under Pb stress in Brassica juncea plants and tomato seedlings. The metal transporters including ABC, ZIP, NRAMP, Ctr/COPT, and HMA maintain metal homeostasis via activating different signaling components such as MAPK signaling and hormone and calcium signaling. Metal tolerance proteins (MTP) are also considered to be the potential efflux transporters that extrude mainly Zn out of cytoplasm along with other metals (Mn, Fe, Cd, Co, and Ni). MTP1 confers to Zn hypertolerance in plants during high Zn concentration. Identification of undiscovered transporter genes, their functional characterization, and their manipulation can further aid in the production of hyperaccumulators as well as plants with enhanced phytoremedial potential. The HM-stress detoxifying transporters can be employed in growing applications of molecular-genetic technologies for a better understanding of heavy metal accumulation and tolerance in plants. These transporters either limit the entry of HMs into the cells or are involved in the vacuole sequestration of these HMs to improve HM-stress tolerance.

7. Plants Retaliate against HM Toxicity by Elevating the Levels of Compatible Solutes

HM toxicity obstructs the plant metabolic, cellular, and genetic potential required for normal growth and development. Cellular toxicity associated with the overproduction of reactive oxygen species (ROS) leads to induction of oxidative stress. At the metabolic level, HMs interfere with various proteins, causing their inactivation, resulting in the repression of key physiological processes such as photosynthesis and respiration. Metal toxicity provokes oxidative stress in plants which eventually leads to acceleration of the antioxidant system and osmoregulation via accumulation of osmolytes or compatible solutes which maintains the osmoticum of the cells. In response to stress, plants produce various types of compatible solutes including proline, polyols, soluble sugars, and quaternary ammonium compounds (QACs) such as glycine betaine, proline betaine, alanine betaine, and polyamines, which participate in osmotic adjustment, stabilization of macromolecules, metal chelation, and ROS detoxification. In addition, a direct role of some of these compatible solutes, including polyamines, organic acids, and amino acids, in the HM chelation has also been reported. For instance, exogenous application of polyamine spermidine (Spd) induced the activities of SOD and GPX and thus maintained the lower levels of superoxide anion (O2−) and MDA in leaves of Malus hupehensis under Cd toxicity. Similar observations were also reported in rice where a protective role of Spd and spermine (Spm) were reported under Cd stress. It was reported that exogenous treatment of these polyamines reduced the CdCl2-induced oxidative stress in plants by lowering the MDA and H2O2 level due to augmented levels of SOD, GR, and APX. In wheat, priming of seed with polyamines protected the seedlings from Pb stress and improved the growth and yield traits by improving the membrane stability index (MSI), relative water content (RWC), contents of photosynthetic pigments, osmoprotectants, nutrients, ascorbic acid, total glutathione, and activities of SOD and CAT. Spd also improved the length of roots, shoots, and fresh weight of Cr-stressed seedlings of Raphanus sativus by increasing GSH, ascorbic acid, proline, glycine betaine total phenol, and antioxidant enzyme activities such as guaiacol peroxidase, CAT, SOD, and GR. In addition, polyamines also function as signaling molecules and regulate plant stress responses under HM toxicity through ion homeostasis and transportation. It was shown that pre-treatment of Spm reversed the Cu and Cd-induced ROS production and subsequent lipid peroxidation. Similarly, pre-treatment or exogenous applications of Spm and Spd were found to be effective in alleviating the toxic effects of HMs as observed in a variety of plants including Nymphoides peltatum, Typha latifolia, Raphanus sativus, Boehmeria nivea, Triticum aestivum, Vigna radiata, Salix matsudana, Vigna angularis, and Zea mays.

Similar to the polyamines, organic acids such as tartrate, citrate, oxalate, malonate, aconitate, and malate have also been shown to bind with the ions of HMs via the chelation with carboxyl groups that act as oxygen donors in metal ligands events. However, many studies revealed the involvement of OAs in the regulation of transport and internal chelation of HMs in plants. In the root tip of wheat plants, membrane-localized malate transport channels (ALMT) were found to be activated in response to a high concentration of Al3+, which resulted in the excretion of malate to limit the entry of Al3+ into roots via their chelation. Moreover, secretion of oxalic acid was observed in the root apex of tomato plants which resulted in the formation of a Cd-oxalate complex and thus decreased the uptake of Cd. A similar complex formation has also been observed between oxalate and Pb, which lowered the bioavailability of Pb in the roots of rice plants to provide Pb-stress tolerance. In the Zn-hyperaccumulator plant Thlaspi alpestre, the accumulation of a higher concentration of Zn was correlated with the amount of malate. Moreover, aerial parts of A. helleri showed sequestration of Zn via the formation of the Zn-malate complex. Likewise, malate was also shown to be involved in the chelation and transfer of Cd into the vacuoles of Solanum nigrum leaves.

Amino acids, histidine, in particular, exhibit a strong affinity for metal ions such as Zn2+, Co2+, Ni2+, and Cu2+ and thus are involved in the direct chelation of these HMs. The capacity of Alyssum (Brassicaceae) plants to produce a high amount of histidine was reported to be directly correlated to the Ni-hyperaccumulation. Moreover, the formation of the Zn-histidine complex has been observed in the roots of a Zn hyperaccumulator plant Thlaspi caerulescens, which allowed the plants to withstand a higher concentration of Zn. Moreover, transgenic Arabidopsis plants with a 2-fold higher concentration of histidine showed improved Ni tolerance as compared with the wild type, further confirming a role of histidine in HM-stress tolerance.

In addition to these polyamines, organic acids, and amino acids, which are directly involved in the chelation of HMs, a rise in proline content has also been observed in many plant species including Brassica juncea, Solanum melongena, Malva parviflora, Arachis hypogsea, hybrid poplar (Populus trichocarpa × deltoides), and Groenlandia densa under HM toxicity. The proline thus produced is involved in providing stability and maintaining activities of various enzymes viz. nitrate reductase, protease, and ribonuclease as reported in rice. Further, it was shown that exogenous applications of L-proline and betaine restored the membrane integrity and growth inhibition under Cd toxicity in cultured tobacco Bright Yellow (BY-2) cells. Transgenic Swingle citrumelo plants carrying pyrroline-5-carboxylate synthetase (P5CS112A) genes showed higher production of endogenous L-proline which led to the enhanced expression of chloroplastic GR, cytosolic APX, and Cu/Zn SOD isoforms, indicating an intricate relationship between L-proline and enzymatic antioxidants. Similarly, the role of glycinebetaine in tolerance to HM toxicity has also been highlighted. It was shown that foliar application of glycinebetain during Cr toxicity alleviated the toxic effects by reducing the Cr uptake and enhancing the antioxidants activity in different parts of mung bean enhances. Moreover, the synthesis of osmoprotectants utilizes the excess reductants which provide NAD+ and NADP+ required for the regulation of respiration and photosynthesis, resulting in enhancement of biomass production, photosynthesis, promoted osmotic adjustment, and ROS scavenging systems in response to metals exposure.

Mannitol is a sugar alcohol that is capable of ROS scavenging activity, thus protecting the plants against oxidative stress induced by ·OH radicals. reported that Cd-tolerant lines of Medicago truncatula showed higher mobilization of total soluble sugars (glucose, fructose, and sucrose) than the Cd- susceptible lines, thus highlighting the role of mannitol in HM-stress tolerance. Similarly, the accumulation of mannitol along with other osmolytes including sucrose and glycinebetain has been observed in Salvinia natans plants exposed to a variety of HMs. Further, exogenous application of mannitol was able to negate the toxic effects of Cr toxicity as reported in wheat and maize, confirming a positive role of mannitol in HM-stress tolerance.

8. HM-Stress Tolerance Is Mediated by the Phytohormones Signaling

Phytohormones play a decisive role in stress tolerance of plants grown in metal-polluted via activation of a signaling cascade and antioxidant defense mechanism (Figure 3). For instance, Indole-3-butyric acid (IBA), IAA precursor, induced the antioxidant defense mechanism via NO signaling and decrease the ROS level by activating the GPX activity in barley roots as well as in tomato plants under Cd stress. In Oryza sativa, the application of epibrassinolide (EBL) helps to plant combat Cr-induced oxidative stress following the upregulation of the antioxidant mechanism at the molecular level. Nevertheless, GR activity was found to be elevated when Cr-treated seedlings were exposed to EBL, resulting in the improvement of the growth of seedlings. From the study, it was revealed that the Cr metal uptake and bioconcentration factor (BCF) content was significantly reduced under the influence of BR treatments. Hence, it is well known that phytohormones in metal tolerance such as brassinosteroids (BRs) play a key role in the mitigation of various stresses via inducing antioxidant defense system and confer tolerance against HMs toxicity in various plants like rice, maize, tomato, wheat, Arabidopsis, radish, and mustard. Their findings showed that treatment with EBL significantly decreased the amount of oxidative indicator MDA and H2O2 via elevating low molecular weight antioxidant ascorbic acid levels in Cr-treated seedlings. Similarly, a recent study revealed that melatonin plays a protective role in melon root development in response to Cu toxicity by inhibiting the formation of jasmonic acid (JA). Pre-treatment of melatonin to melon seeds promoted excess Cu2+ chelation, reversed Cu-toxicity-induced root growth inhibition and the expression of genes related to the ROS-detoxification and cell wall modifications. Moreover, the expression level of genes and metabolites were altered under melatonin treatment and involved in JA biosynthesis, suggesting a negative regulation of JA in HM-stress tolerance. Further, the involvement of different phytohormones in HM-stress tolerance in plants has been excellently reviewed recently (Figure 3).

9. Conclusions

HM toxicity is emerging as one of the most serious concerns across the globe. The toxic effects of HMs on plants depend on a variety of factors including type and concentration of HMs and plant species, plant growth stage, and exposure time. The negative effects of the HMs on the growth of the plants are the combined outcome of the changes in their anatomy and physiology. Tolerant plants retaliate to HM toxicity by activating a complex signaling network which often culminates into activation of a defense response that includes accumulation of (1) antioxidants for detoxification of excess ROS, (2) secondary metabolites for sequestration of HMs to vacuoles, and (3) compatible solutes for the osmoregulation along with regulation of metal transporters, among others. The information derived from the HM accumulator/hyperaccumulator plants can be used in the future to improve the ability of non-food plants to accumulate higher amounts of HMs in order to be used to mitigate the HM contamination in environmental matrices. Moreover, the information derived from the HM tolerant plants can be used to induce the mechanisms that result in reduced uptake and accumulation of HMs in food plants and thus their negative consequences for human health.

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    Sharma J., Shrivastava S. Physiological and morphological responses of Phaseolus vulgaris caused by mercury stress under lab conditions. Recent Adv. Biol Med. 2014;1:136.

    Not in our library10.18639/rabm.2014.01.66172

  65. 65.

    Sagardoy R., Vázquez S., Florez-Sarasa I.D., Albacete A., Ribas-Carbó M., Flexas J., Abadía J., Morales F. Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol. 2010;187:145-158.

    Not in our library10.1111/j.1469-8137.2010.03241.x

  66. 66.

    Kasim W.A. Changes induced by copper and cadmium stress in the anatomy and grain yield of Sorghum bicolor (L.) Moench. Int. J. Agric. Biol. 2006;8:123-128.

    Not in our library

  67. 67.

    Kastori R., Petrović M., Petrović N. Effect of excess lead, cadmium, copper, and zinc on water relations in sunflower. J. Plant Nutr. 1992;15:2427-2439.

    Not in our library10.1080/01904169209364485

  68. 68.

    Gupta P., Bhatnagar A.K. Spatial distribution of arsenic in different leaf tissues and its effect on structure and development of stomata and trichomes in mung bean, Vigna radiata (L.) Wilczek. Environ. Exp. Bot. 2015;109:12-22.

    Not in our library10.1016/j.envexpbot.2014.08.001

  69. 69.

    Souza J.F., Dolder H., Cortelazzo A.L. Effect of excess cadmium and zinc ions on roots and shoots of maize seedlings. J. Plant Nutr. 2005;28:1923-1931.

    Not in our library10.1080/01904160500310435

  70. 70.

    Gomes M.P., de Sá e Melo Marques T.C.L.L., de Oliveira Gonçalves Nogueira M., de Castro E.M., Soares Â.M. Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Sci. Agric. 2011;68:566-573.

    Not in our library10.1590/s0103-90162011000500009

  71. 71.
    Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)] · 2014
    No notice
  72. 72.
    Effects of Different Metals on Photosynthesis: Cadmium and Zinc Affect Chlorophyll Fluorescence in Durum Wheat · 2018
    No notice
  73. 73.

    Latif U., Farid M., Rizwan M., Ishaq H.K., Farid S., Ali S., El-Sheikh M.A., Alyemeni M.N., Wijaya L. Physiological and Biochemical Response of Alternanthera bettzickiana (Regel) G. Nicholson under Acetic Acid Assisted Phytoextraction of Lead. Plants. 2020;9:1084.

    Not in our library10.3390/plants9091084

  74. 74.

    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.

    Not in our library10.1016/j.plaphy.2020.06.021

  75. 75.

    Yotsova E., Dobrikova A., Stefanov M., Misheva S., Bardáčová M., Matušíková I., Žideková L., Blehová A., Apostolova E. Effects of cadmium on two wheat cultivars depending on different nitrogen supply. Plant Physiol. Biochem. 2020;155:789-799.

    Not in our library10.1016/j.plaphy.2020.06.042

  76. 76.

    Mazur R., Sadowska M., Kowalewska Ł., Abratowska A., Kalaji H.M., Mostowska A., Garstka M., Krasnodębska-Ostręga B. Overlapping toxic effect of long term thallium exposure on white mustard (Sinapis alba L.) photosynthetic activity. BMC Plant Biol. 2016;16:191.

    Not in our library10.1186/s12870-016-0883-4

  77. 77.

    Appenroth K.-J., Keresztes A., Sárvári É., Jaglarz A., Fischer W. Multiple effects of chromate on Spirodela polyrhiza: Electron microscopy and biochemical investigations. Plant Biol. 2003;5:315-323.

    Not in our library10.1055/s-2003-40801

  78. 78.

    Hegedüs A., Erdei S., Horváth G. Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci. 2001;160:1085-1093.

    Not in our library10.1016/s0168-9452(01)00330-2

  79. 79.

    Gill S.S., Anjum N.A., Ahmad I., Thangavel P., Sridevi G., Pacheco M., Duarte A.C., Umar S., Khan N.A., Pereira M.E. Metal hyperaccumulation and tolerance in Alyssum, Arabidopsis and Thlaspi: An overview. Plant Fam. Brassicaceae. 2012;21:99-137.

    Not in our library

  80. 80.

    Moradi L., Ehsanzadeh P. Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. Photosynthetica. 2015;53:506-518.

    Not in our library10.1007/s11099-015-0150-1

  81. 81.

    Sela M., Garty J., TEL-OR E. The accumulation and the effect of heavy metals on the water fern Azolla filiculoides. New Phytol. 1989;112:7-12.

    Not in our library10.1111/j.1469-8137.1989.tb00302.x

  82. 82.

    Bertrand M., Poirier I. Photosynthetic organisms and excess of metals. Photosynthetica. 2005;43:345-353.

    Not in our library10.1007/s11099-005-0058-2

  83. 83.

    Singh H.P., Mahajan P., Kaur S., Batish D.R., Kohli R.K. Chromium toxicity and tolerance in plants. Environ. Chem. Lett. 2013;11:229-254.

    Not in our library10.1007/s10311-013-0407-5

  84. 84.

    Shahzad B., Tanveer M., Rehman A., Cheema S.A., Fahad S., Rehman S., Sharma A. Nickel; whether toxic or essential for plants and environment-A review. Plant Physiol. Biochem. 2018;132:641-651.

    Not in our library10.1016/j.plaphy.2018.10.014

  85. 85.

    Sharma A., Kumar V., Shahzad B., Ramakrishnan M., Sidhu G.P.S., Bali A.S., Handa N., Kapoor D., Yadav P., Khanna K. Photosynthetic response of plants under different abiotic stresses: A review. J. Plant Growth Regul. 2019;1-23.

    Not in our library10.1007/s00344-019-10018-x

  86. 86.

    Juarez A.B., Barsanti L., Passarelli V., Evangelista V., Vesentini N., Conforti V., Gualtieri P. In vivo microspectroscopy monitoring of chromium effects on the photosynthetic and photoreceptive apparatus of Eudorina unicocca and Chlorella kessleri. J. Environ. Monit. 2008;10:1313-1318.

    Not in our library10.1039/b809566c

  87. 87.

    Wang X., Ma R., Cui D., Cao Q., Shan Z., Jiao Z. Physio-biochemical and molecular mechanism underlying the enhanced heavy metal tolerance in highland barley seedlings pre-treated with low-dose gamma irradiation. Sci. Rep. 2017;7:14233.

    Not in our library10.1038/s41598-017-14601-8

  88. 88.

    Hou W., Chen X., Song G., Wang Q., Chang C.C. Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiol. Biochem. 2007;45:62-69.

    Not in our library10.1016/j.plaphy.2006.12.005

  89. 89.

    Garg P., Chandra P., Devi S. Chromium (VI) induced morphological changes in Limnanthemum cristatum Griseb.: A possible bioindicator. Phytomorphology. 1994;44:201-206.

    Not in our library

  90. 90.

    Piotrowska A., Bajguz A., Godlewska-Żyłkiewicz B., Czerpak R., Kamińska M. Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ. Exp. Bot. 2009;66:507-513.

    Not in our library10.1016/j.envexpbot.2009.03.019

  91. 91.

    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.

    Not in our library10.1155/2012/217037

  92. 92.

    Ehsan S., Ali S., Noureen S., Mahmood K., Farid M., Ishaque W., Shakoor M.B., Rizwan M. Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol. Environ. Saf. 2014;106:164-172.

    Not in our library10.1016/j.ecoenv.2014.03.007

  93. 93.

    Afshan S., Ali S., Bharwana S.A., Rizwan M., Farid M., Abbas F., Ibrahim M., Mehmood M.A., Abbasi G.H. Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ. Sci. Pollut. Res. 2015;22:11679-11689.

    Not in our library10.1007/s11356-015-4396-8

  94. 94.

    Rizwan M., Meunier J.-D., Davidian J.-C., Pokrovsky O.S., Bovet N., Keller C. Silicon alleviates Cd stress of wheat seedlings (Triticum turgidum L. cv. Claudio) grown in hydroponics. Environ. Sci. Pollut. Res. 2016;23:1414-1427.

    Not in our library10.1007/s11356-015-5351-4

  95. 95.

    Keller C., Rizwan M., Davidian J.-C., Pokrovsky O.S., Bovet N., Chaurand P., Meunier J.-D. Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 µM Cu. Planta. 2015;241:847-860.

    Not in our library10.1007/s00425-014-2220-1

  96. 96.

    Kuriakose S.V., Prasad M.N. V Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul. 2008;54:143-156.

    Not in our library10.1007/s10725-007-9237-4

  97. 97.

    Soudek P., Petrová Š., Vaňková R., Song J., Vaněk T. Accumulation of heavy metals using Sorghum sp. Chemosphere. 2014;104:15-24.

    Not in our library10.1016/j.chemosphere.2013.09.079

  98. 98.

    Qin W., Bazeille N., Henry E., Zhang B., Deprez E., Xi X.-G. Mechanistic insight into cadmium-induced inactivation of the Bloom protein. Sci. Rep. 2016;6:26225.

    Not in our library10.1038/srep26225

  99. 99.

    Jia H., Wang X., Shi C., Guo J., Ma P., Ren X., Wei T., Liu H., Li J. Hydrogen sulfide decreases Cd translocation from root to shoot through increasing Cd accumulation in cell wall and decreasing Cd2+ influx in Isatis indigotica. Plant Physiol. Biochem. 2020;155:605-612.

    Not in our library10.1016/j.plaphy.2020.08.033

  100. 100.

    Ekmekçi Y., Tanyolaç D., Ayhan B. A crop tolerating oxidative stress induced by excess lead: Maize. Acta Physiol. Plant. 2009;31:319-330.

    Not in our library10.1007/s11738-008-0238-3

  101. 101.

    Souri Z., Cardoso A.A., da-Silva C.J., de Oliveira L.M., Dari B., Sihi D., Karimi N. Heavy metals and photosynthesis: Recent developments. Photosynthesis, Productivity, and Environmental Stress. 2019;107-134.

    Not in our library

  102. 102.

    Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7:405-410.

    Not in our library10.1016/s1360-1385(02)02312-9

  103. 103.

    Sharma S.S., Dietz K.-J. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009;14:43-50.

    Not in our library10.1016/j.tplants.2008.10.007

  104. 104.

    Hossain M.A., Piyatida P., da Silva J.A.T., Fujita M. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012;2012:872875.

    Not in our library10.1155/2012/872875

  105. 105.

    Foyer C.H., Noctor G. Stress-triggered redox signalling: What’s in pROSpect? Plant Cell Environ. 2016;39:951-964.

    Not in our library10.1111/pce.12621

  106. 106.

    Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995;18:321-336.

    Not in our library10.1016/0891-5849(94)00159-h

  107. 107.

    SONG W., MENDOZA-CÓZATL D.G., Lee Y., Schroeder J.I., AHN S., LEE H., Wicker T., Martinoia E. Phytochelatin–metal (loid) transport into vacuoles shows different substrate preferences in barley and A rabidopsis. Plant Cell Environ. 2014;37:1192-1201.

    Not in our library10.1111/pce.12227

  108. 108.

    Shahid M., Pourrut B., Dumat C., Nadeem M., Aslam M., Pinelli E. Heavy-metal-induced reactive oxygen species: Phytotoxicity and physicochemical changes in plants. Rev. Environ. Contam. Toxicol. 2014;232:1-44.

    Not in our library10.1007/978-3-319-06746-9_1

  109. 109.

    Noctor G., Mhamdi A., Chaouch S., Han Y.I., Neukermans J., Marquez-Garcia B., Queval G., Foyer C.H. Glutathione in plants: An integrated overview. Plant Cell Environ. 2012;35:454-484.

    Not in our library10.1111/j.1365-3040.2011.02400.x

  110. 110.

    Mittler R., Zilinskas B.A. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem. 1992;267:21802-21807.

    Not in our library10.1016/s0021-9258(19)36683-9

  111. 111.

    Jiménez A., Hernández J.A., Pastori G., del Rıo L.A., Sevilla F. Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol. 1998;118:1327-1335.

    Not in our library10.1104/pp.118.4.1327

  112. 112.

    Panda S.K., Matsumoto H. Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. Biometals. 2010;23:753-762.

    Not in our library10.1007/s10534-010-9342-0

  113. 113.

    Pandey V., Dixit V., Shyam R. Antioxidative responses in relation to growth of mustard (Brassica juncea cv. Pusa Jaikisan) plants exposed to hexavalent chromium. Chemosphere. 2005;61:40-47.

    Not in our library10.1016/j.chemosphere.2005.03.026

  114. 114.

    Adhikari A., Adhikari S., Ghosh S., Azahar I., Shaw A.K., Roy D., Roy S., Saha S., Hossain Z. Imbalance of redox homeostasis and antioxidant defense status in maize under chromium (VI) stress. Environ. Exp. Bot. 2020;169:103873.

    Not in our library10.1016/j.envexpbot.2019.103873

  115. 115.

    Dixit V., Pandey V., Shyam R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J. Exp. Bot. 2001;52:1101-1109.

    Not in our library10.1093/jexbot/52.358.1101

  116. 116.

    Yannarelli G.G., Fernández-Alvarez A.J., Santa-Cruz D.M., Tomaro M.L. Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry. 2007;68:505-512.

    Not in our library10.1016/j.phytochem.2006.11.016

  117. 117.

    Sobrino-Plata J., Ortega-Villasante C., Flores-Cáceres M.L., Escobar C., Del Campo F.F., Hernández L.E. Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere. 2009;77:946-954.

    Not in our library10.1016/j.chemosphere.2009.08.007

  118. 118.

    Wang X., Wei Z., Liu D., Zhao G. Effects of NaCl and silicon on activities of antioxidative enzymes in roots, shoots and leaves of alfalfa. Afr. J. Biotechnol. 2011;10:545-549.

    Not in our library

  119. 119.

    Sobrino-Plata J., Herrero J., Carrasco-Gil S., Pérez-Sanz A., Lobo C., Escobar C., Millán R., Hernández L.E. Specific stress responses to cadmium, arsenic and mercury appear in the metallophyte Silene vulgaris when grown hydroponically. RSC Adv. 2013;3:4736-4744.

    Not in our library10.1039/c3ra40357b

  120. 120.

    Sobrino-Plata J., Carrasco-Gil S., Abadía J., Escobar C., Álvarez-Fernández A., Hernández L.E. The role of glutathione in mercury tolerance resembles its function under cadmium stress in Arabidopsis. Metallomics. 2014;6:356-366.

    Not in our library10.1039/c3mt00329a

  121. 121.

    Rouhier N., San Koh C., Gelhaye E., Corbier C., Favier F., Didierjean C., Jacquot J.-P. Redox based anti-oxidant systems in plants: Biochemical and structural analyses. Biochim. Biophys. Acta (BBA)-General Subj. 2008;1780:1249-1260.

    Not in our library10.1016/j.bbagen.2007.12.007

  122. 122.

    El-Kereamy A., Bi Y.-M., Mahmood K., Ranathunge K., Yaish M.W., Nambara E., Rothstein S.J. Overexpression of the CC-type glutaredoxin, OsGRX6 affects hormone and nitrogen status in rice plants. Front. Plant Sci. 2015;6:934.

    Not in our library10.3389/fpls.2015.00934

  123. 123.

    Kumar A., Dubey A.K., Kumar V., Ansari M.A., Narayan S., Kumar S., Pandey V., Shirke P.A., Pande V., Sanyal I. Over-expression of chickpea glutaredoxin (CaGrx) provides tolerance to heavy metals by reducing metal accumulation and improved physiological and antioxidant defence system. Ecotoxicol. Environ. Saf. 2020;192:110252.

    Not in our library10.1016/j.ecoenv.2020.110252

  124. 124.

    Verma P.K., Verma S., Pande V., Mallick S., Deo Tripathi R., Dhankher O.P., Chakrabarty D. Overexpression of rice glutaredoxin OsGrx_C7 and OsGrx_C2. 1 reduces intracellular arsenic accumulation and increases tolerance in Arabidopsis thaliana. Front. Plant Sci. 2016;7:740.

    Not in our library10.3389/fpls.2016.00740

  125. 125.

    Chowardhara B., Borgohain P., Saha B., Awasthi J.P., Panda S.K. Differential oxidative stress responses in Brassica juncea (L.) Czern and Coss cultivars induced by cadmium at germination and early seedling stage. Acta Physiol. Plant. 2020;42:105.

    Not in our library10.1007/s11738-020-03094-0

  126. 126.

    Tyagi S., Singh K., Upadhyay S.K. Molecular characterization revealed the role of catalases under abiotic and arsenic stress in bread wheat (Triticum aestivum L.). J. Hazard. Mater. 2021;403:123585.

    Not in our library10.1016/j.jhazmat.2020.123585

  127. 127.

    Pan G., Zhao L., Li J., Huang S., Tang H., Chang L., Dai Z., Chen A., Li D., Li Z. Physiological responses and tolerance of flax (Linum usitatissimum L.) to lead stress. Acta Physiol. Plant. 2020;42:113.

    Not in our library10.1007/s11738-020-03103-2

  128. 128.

    Jia H., Wang X., Dou Y., Liu D., Si W., Fang H., Zhao C., Chen S., Xi J., Li J. Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci. Rep. 2016;6:39702.

    Not in our library10.1038/srep39702

  129. 129.

    López-Martín M.C., Becana M., Romero L.C., Gotor C. Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol. 2008;147:562-572.

    Not in our library10.1104/pp.108.117408

  130. 130.

    Xiao S., Gao W., Chen Q., Ramalingam S., Chye M. Overexpression of membrane-associated acyl-CoA-binding protein ACBP1 enhances lead tolerance in Arabidopsis. Plant J. 2008;54:141-151.

    Not in our library10.1111/j.1365-313x.2008.03402.x

  131. 131.

    DU Z., CHEN M., CHEN Q., GU J., CHYE M. Expression of A rabidopsis acyl-CoA-binding proteins AtACBP 1 and AtACBP 4 confers P b (II) accumulation in B rassica juncea roots. Plant Cell Environ. 2015;38:101-117.

    Not in our library10.1111/pce.12382

  132. 132.

    Sunkar R., Kaplan B., Bouché N., Arazi T., Dolev D., Talke I.N., Maathuis F.J.M., Sanders D., Bouchez D., Fromm H. Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J. 2000;24:533-542.

    Not in our library10.1046/j.1365-313x.2000.00901.x

  133. 133.

    Ogawa I., Nakanishi H., Mori S., Nishizawa N.K. Time course analysis of gene regulation under cadmium stress in rice. Plant Soil. 2009;325:97-108.

    Not in our library10.1007/s11104-009-0116-9

  134. 134.

    He F., Liu Q., Zheng L., Cui Y., Shen Z., Zheng L. RNA-Seq analysis of rice roots reveals the involvement of post-transcriptional regulation in response to cadmium stress. Front. Plant Sci. 2015;6:1136.

    Not in our library10.3389/fpls.2015.01136

  135. 135.

    Liu Z., Fang H., Pei Y., Jin Z., Zhang L., Liu D. WRKY transcription factors down-regulate the expression of H 2 S-generating genes, LCD and DES in Arabidopsis thaliana. Sci. Bull. 2015;60:995-1001.

    Not in our library10.1007/s11434-015-0787-y

  136. 136.

    Rui H., Zhang X., Shinwari K.I., Zheng L., Shen Z. Comparative transcriptomic analysis of two Vicia sativa L. varieties with contrasting responses to cadmium stress reveals the important role of metal transporters in cadmium tolerance. Plant Soil. 2018;423:241-255.

    Not in our library10.1007/s11104-017-3501-9

  137. 137.

    Chen P., Chen T., Li Z., Jia R., Luo D., Tang M., Lu H., Hu Y., Yue J., Huang Z. Transcriptome analysis revealed key genes and pathways related to cadmium-stress tolerance in Kenaf (Hibiscus cannabinus L.). Ind. Crops Prod. 2020;158:112970.

    Not in our library10.1016/j.indcrop.2020.112970

  138. 138.

    Weber M., Trampczynska A., Clemens S. Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+−hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ. 2006;29:950-963.

    Not in our library10.1111/j.1365-3040.2005.01479.x

  139. 139.

    Liu T., Liu S., Guan H., Ma L., Chen Z., Gu H., Qu L.-J. Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ. Exp. Bot. 2009;67:377-386.

    Not in our library10.1016/j.envexpbot.2009.03.016

  140. 140.

    Chen J., Yang L., Yan X., Liu Y., Wang R., Fan T., Ren Y., Tang X., Xiao F., Liu Y. Zinc-finger transcription factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol. 2016;171:707-719.

    Not in our library10.1104/pp.15.01882

  141. 141.

    He G., Qin L., Tian W., Meng L., He T., Zhao D. Heavy metal Transporters-Associated proteins in Solanum tuberosum: Genome-wide identification, comprehensive gene feature, evolution and expression analysis. Genes. 2020;11:1269.

    Not in our library10.3390/genes11111269

  142. 142.

    Clemens S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie. 2006;88:1707-1719.

    Not in our library10.1016/j.biochi.2006.07.003

  143. 143.

    Arslan Topal E.I., Topal M., Öbek E. Assessment of heavy metal accumulations and health risk potentials in tomatoes grown in the discharge area of a municipal wastewater treatment plant. Int. J. Environ. Health Res. 2020;1-13.

    Not in our library10.1080/09603123.2020.1762071

  144. 144.

    Clemens S. Molecular mechanisms of plant metal tolerance and homeostasis. Planta. 2001;212:475-486.

    Not in our library10.1007/s004250000458

  145. 145.

    Cobbett C., Goldsbrough P. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 2002;53:159-182.

    Not in our library10.1146/annurev.arplant.53.100301.135154

  146. 146.

    Anjum N.A., Hasanuzzaman M., Hossain M.A., Thangavel P., Roychoudhury A., Gill S.S., Rodrigo M.A.M., Adam V., Fujita M., Kizek R. Jacks of metal/metalloid chelation trade in plants—An overview. Front. Plant Sci. 2015;6:192.

    Not in our library10.3389/fpls.2015.00192

  147. 147.

    Frey B., Keller C., Zierold K. Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 2000;23:675-687.

    Not in our library10.1046/j.1365-3040.2000.00590.x

  148. 148.

    Zhao F.J., Lombi E., Breedon T. Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ. 2000;23:507-514.

    Not in our library10.1046/j.1365-3040.2000.00569.x

  149. 149.

    Küpper H., Lombi E., Zhao F.-J., McGrath S.P. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta. 2000;212:75-84.

    Not in our library10.1007/s004250000366

  150. 150.

    Hu P.-J., Qiu R.-L., Senthilkumar P., Jiang D., Chen Z.-W., Tang Y.-T., Liu F.-J. Tolerance, accumulation and distribution of zinc and cadmium in hyperaccumulator Potentilla griffithii. Environ. Exp. Bot. 2009;66:317-325.

    Not in our library10.1016/j.envexpbot.2009.02.014

  151. 151.

    Brooks R.R., Reeves R.D., Morrison R.S., Malaisse F. Hyperaccumulation of copper and cobalt—A review. Bull. la Société R. Bot. Belgique/Bulletin van K. Belgische Bot. Ver. 1980;113:166-172.

    Not in our library

  152. 152.

    Salt D.E., Prince R.C., Pickering I.J., Raskin I. Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 1995;109:1427-1433.

    Not in our library10.1104/pp.109.4.1427

  153. 153.

    Chardonnens A.N., Ten Bookum W.M., Kuijper L.D.J., Verkleij J.A.C., Ernst W.H.O. Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. Physiol. Plant. 1998;104:75-80.

    Not in our library10.1034/j.1399-3054.1998.1040110.x

  154. 154.

    Masood A., Iqbal N., Khan N.A. Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ. 2012;35:524-533.

    Not in our library10.1111/j.1365-3040.2011.02432.x

  155. 155.

    Carrier P., Baryla A., Havaux M. Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta. 2003;216:939-950.

    Not in our library10.1007/s00425-002-0947-6

  156. 156.
    Phytoremediation: A Promising Approach for Revegetation of Heavy Metal-Polluted Land · 2020
    No notice
  157. 157.

    Thangavel P., Long S., Minocha R. Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell. Tissue Organ Cult. 2007;88:201-216.

    Not in our library10.1007/s11240-006-9192-1

  158. 158.

    Dago À., González I., Ariño C., Díaz-Cruz J.M., Esteban M. Chemometrics applied to the analysis of induced phytochelatins in Hordeum vulgare plants stressed with various toxic non-essential metals and metalloids. Talanta. 2014;118:201-209.

    Not in our library10.1016/j.talanta.2013.09.058

  159. 159.

    Wang F., Wang Z., Zhu C. Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity. Acta Biochim. Biophys. Sin. 2012;44:886-893.

    Not in our library10.1093/abbs/gms073

  160. 160.

    Zhigang A., Cuijie L., Yuangang Z., Yejie D., Wachter A., Gromes R., Rausch T. Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. J. Exp. Bot. 2006;57:3575-3582.

    Not in our library10.1093/jxb/erl102

  161. 161.

    Kumar G., Kushwaha H.R., Panjabi-Sabharwal V., Kumari S., Joshi R., Karan R., Mittal S., Pareek S.L.S., Pareek A. Clustered metallothionein genes are co-regulated in rice and ectopic expression of OsMT1e-P confers multiple abiotic stress tolerance in tobacco via ROS scavenging. BMC Plant Biol. 2012;12:107.

    Not in our library10.1186/1471-2229-12-107

  162. 162.
    Heavy Metal Stress and Some Mechanisms of Plant Defense Response · 2015
    No notice
  163. 163.

    Zhou B., Yao W., Wang S., Wang X., Jiang T. The metallothionein gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in tobacco. Int. J. Mol. Sci. 2014;15:10398-10409.

    Not in our library10.3390/ijms150610398

  164. 164.

    Xia Y., Qi Y., Yuan Y., Wang G., Cui J., Chen Y., Zhang H., Shen Z. Overexpression of Elsholtzia haichowensis metallothionein 1 (EhMT1) in tobacco plants enhances copper tolerance and accumulation in root cytoplasm and decreases hydrogen peroxide production. J. Hazard. Mater. 2012;233:65-71.

    Not in our library10.1016/j.jhazmat.2012.06.047

  165. 165.

    Emamverdian A., Ding Y., Xie Y., Sangari S. Silicon mechanisms to ameliorate heavy metal stress in plants. Biomed. Res. Int. 2018;2018:8492898.

    Not in our library10.1155/2018/8492898

  166. 166.
    Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics · 2016
    No notice
  167. 167.

    Shi G., Cai Q., Liu C., Wu L. Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul. 2010;61:45-52.

    Not in our library10.1007/s10725-010-9447-z

  168. 168.

    Song A., Li Z., Zhang J., Xue G., Fan F., Liang Y. Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J. Hazard. Mater. 2009;172:74-83.

    Not in our library10.1016/j.jhazmat.2009.06.143

  169. 169.

    Feng J., Shi Q., Wang X., Wei M., Yang F., Xu H. Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci. Hortic. 2010;123:521-530.

    Not in our library10.1016/j.scienta.2009.10.013

  170. 170.

    Farooq M.A., Ali S., Hameed A., Ishaque W., Mahmood K., Iqbal Z. Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol. Environ. Saf. 2013;96:242-249.

    Not in our library10.1016/j.ecoenv.2013.07.006

  171. 171.

    Su N., Ling F., Xing A., Zhao H., Zhu Y., Wang Y., Deng X., Wang C., Xu X., Hu Z. Lignin synthesis mediated by CCoAOMT enzymes is required for the tolerance against excess Cu in Oryza sativa. Environ. Exp. Bot. 2020;175:104059.

    Not in our library10.1016/j.envexpbot.2020.104059

  172. 172.

    Kupper H., Mijovilovich A., Meyer-Klaucke W., Kroneck P.M.H. Tissue-and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol. 2004;134:748-757.

    Not in our library10.1104/pp.103.032953

  173. 173.

    Mohamed A.A.A., Dardiry M.H.O., Samad A., Abdelrady E. Exposure to Lead (Pb) Induced Changes in the Metabolite Content, Antioxidant Activity and Growth of Jatropha curcas (L.). Trop. Plant Biol. 2020;13:150-161.

    Not in our library10.1007/s12042-019-09244-0

  174. 174.

    Xu J., Zhu Y., Ge Q., Li Y., Sun J., Zhang Y., Liu X. Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. New Phytol. 2012;196:125-138.

    Not in our library10.1111/j.1469-8137.2012.04236.x

  175. 175.

    Lwalaba J.L.W., Zvobgo G., Mwamba T.M., Louis L.T., Fu L., Kirika B.A., Tshibangu A.K., Adil M.F., Sehar S., Mukobo R.P. High accumulation of phenolics and amino acids confers tolerance to the combined stress of cobalt and copper in barley (Hordeum vulagare). Plant Physiol. Biochem. 2020;155:927-937.

    Not in our library10.1016/j.plaphy.2020.08.038

  176. 176.

    Verbruggen N., Hermans C., Schat H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. 2009;181:759-776.

    Not in our library10.1111/j.1469-8137.2008.02748.x

  177. 177.

    Solanki R., Dhankhar R. Biochemical changes and adaptive strategies of plants under heavy metal stress. Biologia. 2011;66:195-204.

    Not in our library10.2478/s11756-011-0005-6

  178. 178.

    Song W.-Y., Yamaki T., Yamaji N., Ko D., Jung K.-H., Fujii-Kashino M., An G., Martinoia E., Lee Y., Ma J.F. A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc. Natl. Acad. Sci. USA. 2014;111:15699-15704.

    Not in our library10.1073/pnas.1414968111

  179. 179.

    Rea P.A. MRP subfamily ABC transporters from plants and yeast. J. Exp. Bot. 1999;50:895-913.

    Not in our library10.1093/jxb/50.special_issue.895

  180. 180.

    Martinoia E., Klein M., Geisler M., Bovet L., Forestier C., Kolukisaoglu U., MuÈller-RoÈber B., Schulz B. Multifunctionality of plant ABC transporters–more than just detoxifiers. Planta. 2002;214:345-355.

    Not in our library10.1007/s004250100661

  181. 181.

    Huang D., Huo J., Liao W. Hydrogen sulfide: Roles in plant abiotic stress response and crosstalk with other signals. Plant Sci. 2020;302:110733.

    Not in our library10.1016/j.plantsci.2020.110733

  182. 182.

    Bhati K.K., Sharma S., Aggarwal S., Kaur M., Shukla V., Kaur J., Mantri S., Pandey A.K. Genome-wide identification and expression characterization of ABCC-MRP transporters in hexaploid wheat. Front. Plant Sci. 2015;6:488.

    Not in our library10.3389/fpls.2015.00488

  183. 183.

    Zhang X.D., Zhao K.X., Yang Z.M. Identification of genomic ATP binding cassette (ABC) transporter genes and Cd-responsive ABCs in Brassica napus. Gene. 2018;664:139-151.

    Not in our library10.1016/j.gene.2018.04.060

  184. 184.

    Gaillard S., Jacquet H., Vavasseur A., Leonhardt N., Forestier C. AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol. 2008;8:22.

    Not in our library10.1186/1471-2229-8-22

  185. 185.
    Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis · 2015
    No notice
  186. 186.

    Shi M., Wang S., Zhang Y., Wang S., Zhao J., Feng H., Sun P., Fang C., Xie X. Genome-wide characterization and expression analysis of ATP-binding cassette (ABC) transporters in strawberry reveal the role of FvABCC11 in cadmium tolerance. Sci. Hortic. 2020;271:109464.

    Not in our library10.1016/j.scienta.2020.109464

  187. 187.

    Park J., Song W., Ko D., Eom Y., Hansen T.H., Schiller M., Lee T.G., Martinoia E., Lee Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012;69:278-288.

    Not in our library10.1111/j.1365-313x.2011.04789.x

  188. 188.

    Kim D., Bovet L., Maeshima M., Martinoia E., Lee Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007;50:207-218.

    Not in our library10.1111/j.1365-313x.2007.03044.x

  189. 189.

    Qiao C., Yang J., Wan Y., Xiang S., Guan M., Du H., Tang Z., Lu K., Li J., Qu C. A Genome-Wide Survey of MATE Transporters in Brassicaceae and Unveiling Their Expression Profiles under Abiotic Stress in Rapeseed. Plants. 2020;9:1072.

    Not in our library10.3390/plants9091072

  190. 190.

    Yao J., Sun J., Chen Y., Shi L., Yang L., Wang Y. The molecular mechanism underlying cadmium resistance in NHX1 transgenic Lemna turonifera was studied by comparative transcriptome analysis. Plant Cell Tissue Organ Cult. 2020;143:189-200.

    Not in our library10.1007/s11240-020-01909-z

  191. 191.

    Zhang X.D., Meng J.G., Zhao K.X., Chen X., Yang Z.M. Annotation and characterization of Cd-responsive metal transporter genes in rapeseed (Brassica napus). Biometals. 2018;31:107-121.

    Not in our library10.1007/s10534-017-0072-4

  192. 192.

    Komal T., Mustafa M., Ali Z., Kazi A.G. Heavy metal uptake and transport in plants. Heavy Metal Contamination of Soils. 2015;181-194.

    Not in our library

  193. 193.

    Vert G., Grotz N., Dédaldéchamp F., Gaymard F., Guerinot M.L., Briat J.-F., Curie C. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell. 2002;14:1223-1233.

    Not in our library10.1105/tpc.001388

  194. 194.

    Connolly E.L., Fett J.P., Guerinot M. Lou Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell. 2002;14:1347-1357.

    Not in our library10.1105/tpc.001263

  195. 195.

    Milner M.J., Seamon J., Craft E., Kochian L.V. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J. Exp. Bot. 2013;64:369-381.

    Not in our library10.1093/jxb/ers315

  196. 196.

    González-Guerrero M., Escudero V., Saéz Á., Tejada-Jiménez M. Transition metal transport in plants and associated endosymbionts: Arbuscular mycorrhizal fungi and rhizobia. Front. Plant Sci. 2016;7:1088.

    Not in our library10.3389/fpls.2016.01088

  197. 197.

    Van der Zaal B.J., Neuteboom L.W., Pinas J.E., Chardonnens A.N., Schat H., Verkleij J.A.C., Hooykaas P.J.J. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 1999;119:1047-1056.

    Not in our library10.1104/pp.119.3.1047

  198. 198.

    Assunção A.G.L., Martins P.D.C., De Folter S., Vooijs R., Schat H., Aarts M.G.M. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 2001;24:217-226.

    Not in our library10.1111/j.1365-3040.2001.00666.x

  199. 199.

    Delhaize E., Kataoka T., Hebb D.M., White R.G., Ryan P.R. Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell. 2003;15:1131-1142.

    Not in our library10.1105/tpc.009134

  200. 200.

    Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., Vavasseur A., Richaud P. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 2004;576:306-312.

    Not in our library10.1016/j.febslet.2004.09.023

  201. 201.

    Kohli S.K., Handa N., Bali S., Arora S., Sharma A., Kaur R., Bhardwaj R. Modulation of antioxidative defense expression and osmolyte content by co-application of 24-epibrassinolide and salicylic acid in Pb exposed Indian mustard plants. Ecotoxicol. Environ. Saf. 2018;147:382-393.

    Not in our library10.1016/j.ecoenv.2017.08.051

  202. 202.

    Bali S., Jamwal V.L., Kaur P., Kohli S.K., Ohri P., Gandhi S.G., Bhardwaj R., Al-Huqail A.A., Siddiqui M.H., Ahmad P. Role of P-type ATPase metal transporters and plant immunity induced by jasmonic acid against Lead (Pb) toxicity in tomato. Ecotoxicol. Environ. Saf. 2019;174:283-294.

    Not in our library10.1016/j.ecoenv.2019.02.084

  203. 203.
    Traversing the Links between Heavy Metal Stress and Plant Signaling · 2018
    No notice
  204. 204.

    Chaturvedi R., Varun M., Paul M.S. Phytoremediation: Uptake and role of metal transporters in some members of Brassicaceae. Phytoremediation. 2016;453-468.

    Not in our library

  205. 205.

    Ricachenevsky F.K., Menguer P.K., Sperotto R.A., Williams L.E., Fett J.P. Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front. Plant Sci. 2013;4:144.

    Not in our library10.3389/fpls.2013.00144

  206. 206.
    Glutathione Is a Key Player in Metal-Induced Oxidative Stress Defenses · 2012
    No notice
  207. 207.

    Rui H., Chen C., Zhang X., Shen Z., Zhang F. Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances. J. Hazard. Mater. 2016;301:304-313.

    Not in our library10.1016/j.jhazmat.2015.08.052

  208. 208.

    Anjum S.A., Tanveer M., Hussain S., Shahzad B., Ashraf U., Fahad S., Hassan W., Jan S., Khan I., Saleem M.F. Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ. Sci. Pollut. Res. 2016;23:11864-11875.

    Not in our library10.1007/s11356-016-6382-1

  209. 209.

    Chen T.H.H., Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 2002;5:250-257.

    Not in our library10.1016/s1369-5266(02)00255-8

  210. 210.
    Ethylene: A Master Regulator of Salinity Stress Tolerance in Plants · 2020
    No notice
  211. 211.
    Phytohormones Regulate Accumulation of Osmolytes Under Abiotic Stress · 2019
    No notice
  212. 212.

    Liang X., Zhang L., Natarajan S.K., Becker D.F. Proline mechanisms of stress survival. Antioxid. Redox Signal. 2013;19:998-1011.

    Not in our library10.1089/ars.2012.5074

  213. 213.

    Zhao H., Yang H. Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci. Hortic. 2008;116:442-447.

    Not in our library10.1016/j.scienta.2008.02.017

  214. 214.

    Hsu Y.T., Kao C.H. Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil. 2007;291:27-37.

    Not in our library10.1007/s11104-006-9171-7

  215. 215.

    Rady M.M., Hemida K.A. Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicol. Environ. Saf. 2015;119:178-185.

    Not in our library10.1016/j.ecoenv.2015.05.008

  216. 216.

    Rady M.M., El-Yazal M.A.S., Taie H.A.A., Ahmed S.M.A. Response of wheat growth and productivity to exogenous polyamines under lead stress. J. Crop Sci. Biotechnol. 2016;19:363-371.

    Not in our library10.1007/s12892-016-0041-4

  217. 217.
    Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. · 2012
    Not checked
  218. 218.

    Podlešáková K., Ugena L., Spíchal L., Doležal K., De Diego N. Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. N. Biotechnol. 2019;48:53-65.

    Not in our library10.1016/j.nbt.2018.07.003

  219. 219.

    Groppa M.D., Tomaro M.L., Benavides M.P. Polyamines and heavy metal stress: The antioxidant behavior of spermine in cadmium-and copper-treated wheat leaves. Biometals. 2007;20:185-195.

    Not in our library10.1007/s10534-006-9026-y

  220. 220.

    Wang X., Shi G., Xu Q., Hu J. Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J. Plant Physiol. 2007;164:1062-1070.

    Not in our library10.1016/j.jplph.2006.06.003

  221. 221.

    Tang C.F., Zhang R.Q., Wen S.Z., Li C.F., Guo X.F., Liu Y.G. Effects of exogenous spermidine on subcellular distribution and chemical forms of cadmium in Typha latifolia L. under cadmium stress. Water Sci. Technol. 2009;59:1487-1493.

    Not in our library10.2166/wst.2009.170

  222. 222.

    Choudhary S.P., Oral H.V., Bhardwaj R., Yu J.-Q., Tran L.-S.P. Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J. Exp. Bot. 2012;63:5659-5675.

    Not in our library10.1093/jxb/ers219

  223. 223.

    Gong X., Liu Y., Huang D., Zeng G., Liu S., Tang H., Zhou L., Hu X., Zhou Y., Tan X. Effects of exogenous calcium and spermidine on cadmium stress moderation and metal accumulation in Boehmeria nivea (L.) Gaudich. Environ. Sci. Pollut. Res. 2016;23:8699-8708.

    Not in our library10.1007/s11356-016-6122-6

  224. 224.

    Nahar K., Hasanuzzaman M., Rahman A., Alam M., Mahmud J.-A., Suzuki T., Fujita M. Polyamines confer salt tolerance in mung bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Front. Plant Sci. 2016;7:1104.

    Not in our library10.3389/fpls.2016.01104

  225. 225.

    Tang C., Zhang R., Hu X., Song J., Li B., Ou D., Hu X., Zhao Y. Exogenous spermidine elevating cadmium tolerance in Salix matsudana involves cadmium detoxification and antioxidant defense. Int. J. Phytoremediation. 2019;21:305-315.

    Not in our library10.1080/15226514.2018.1524829

  226. 226.

    Ahanger M.A., Aziz U., Alsahli A., Alyemeni M.N., Ahmad P. Combined kinetin and spermidine treatments ameliorate growth and photosynthetic inhibition in vigna angularis by up-regulating antioxidant and nitrogen metabolism under cadmium stress. Biomolecules. 2020;10:147.

    Not in our library10.3390/biom10010147

  227. 227.

    Naz R., Sarfraz A., Anwar Z., Yasmin H., Nosheen A., Keyani R., Roberts T.H. Combined ability of salicylic acid and spermidine to mitigate the individual and interactive effects of drought and chromium stress in maize (Zea mays L.). Plant Physiol. Biochem. 2021;159:285-300.

    Not in our library10.1016/j.plaphy.2020.12.022

  228. 228.

    Anjum N.A., Singh H.P., Khan M.I.R., Masood A., Per T.S., Negi A., Batish D.R., Khan N.A., Duarte A.C., Pereira E. Too much is bad—An appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environ. Sci. Pollut. Res. 2015;22:3361-3382.

    Not in our library10.1007/s11356-014-3849-9

  229. 229.

    Yang L.-T., Qi Y.-P., Jiang H.-X., Chen L.-S. Roles of organic acid anion secretion in aluminium tolerance of higher plants. Biomed. Res. Int. 2013;2013:173682.

    Not in our library10.1155/2013/173682

  230. 230.

    Zhu X.F., Zheng C., Hu Y.T., Jiang T.A.O., Liu Y.U., Dong N.Y., Yang J.L., Zheng S.J. Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ. 2011;34:1055-1064.

    Not in our library10.1111/j.1365-3040.2011.02304.x

  231. 231.

    Yang Y.-Y., Jung J.-Y., Song W.-Y., Suh H.-S., Lee Y. Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol. 2000;124:1019-1026.

    Not in our library10.1104/pp.124.3.1019

  232. 232.

    Nriagu J.O. Zinc in the Environment. Part II: Health Effects. 1980;10016.

    Not in our library

  233. 233.

    Tolrà R.P., Poschenrieder C., Barceló J. Zinc hyperaccumulation in Thlaspi caerulescens. II. Influence on organic acids. J. Plant Nutr. 1996;19:1541-1550.

    Not in our library10.1080/01904169609365220

  234. 234.

    Sun R., Zhou Q., Jin C. Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Plant Soil. 2006;285:125-134.

    Not in our library10.1007/s11104-006-0064-6

  235. 235.

    Krämer U., Cotter-Howells J.D., Charnock J.M., Baker A.J.M., Smith J.A.C. Free histidine as a metal chelator in plants that accumulate nickel. Nature. 1996;379:635-638.

    Not in our library10.1038/379635a0

  236. 236.

    Salt D.E., Prince R.C., Baker A.J.M., Raskin I., Pickering I.J. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ. Sci. Technol. 1999;33:713-717.

    Not in our library10.1021/es980825x

  237. 237.

    Wycisk K., Kim E.J., Schroeder J.I., Krämer U. Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett. 2004;578:128-134.

    Not in our library10.1016/j.febslet.2004.10.086

  238. 238.

    Sun R.-L., Zhou Q.-X., Sun F.-H., Jin C.-X. Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ. Exp. Bot. 2007;60:468-476.

    Not in our library10.1016/j.envexpbot.2007.01.004

  239. 239.

    Zoufan P., Jalali R., Hassibi P., Neisi E., Rastegarzadeh S. Evaluation of antioxidant bioindicators and growth responses in Malva parviflora L. exposed to cadmium. Physiol. Mol. Biol. Plants. 2018;24:1005-1016.

    Not in our library10.1007/s12298-018-0596-2

  240. 240.

    Dinakar N., Nagajyothi P.C., Suresh S., Damodharam T., Suresh C. Cadmium induced changes on proline, antioxidant enzymes, nitrate and nitrite reductases in Arachis hypogaea L. J. Environ. Biol. 2009;30:289-294.

    Not in our library

  241. 241.

    Nikolic N., Kojic D., Pilipovic A., Pajevic S., Krstic B., Borisev M., Orlovic S. Responses of hybrid poplar to cadmium stress: Photosynthetic characteristics, cadmium and proline accumulation, and antioxidant enzyme activity. Acta Biol. Cracoviensia Ser. Bot. 2008;50:95-103.

    Not in our library

  242. 242.

    Yılmaz D.D., Parlak K.U. Changes in proline accumulation and antioxidative enzyme activities in Groenlandia densa under cadmium stress. Ecol. Indic. 2011;11:417-423.

    Not in our library10.1016/j.ecolind.2010.06.012

  243. 243.

    Mishra S., Dubey R.S. Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: Role of proline as enzyme protectant. J. Plant Physiol. 2006;163:927-936.

    Not in our library10.1016/j.jplph.2005.08.003

  244. 244.

    Islam M.M., Hoque M.A., Okuma E., Jannat R., Banu M.N.A., Jahan M.S., Nakamura Y., Murata Y. Proline and glycinebetaine confer cadmium tolerance on tobacco bright yellow-2 cells by increasing ascorbate-glutathione cycle enzyme activities. Biosci. Biotechnol. Biochem. 2009;909031637.

    Not in our library10.1271/bbb.90305

  245. 245.

    De Carvalho K., de Campos M.K.F., Domingues D.S., Pereira L.F.P., Vieira L.G.E. The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol. Biol. Rep. 2013;40:3269-3279.

    Not in our library10.1007/s11033-012-2402-5

  246. 246.

    Jabeen N., Abbas Z., Iqbal M., Rizwan M., Jabbar A., Farid M., Ali S., Ibrahim M., Abbas F. Glycinebetaine mediates chromium tolerance in mung bean through lowering of Cr uptake and improved antioxidant system. Arch. Agron. Soil Sci. 2016;62:648-662.

    Not in our library10.1080/03650340.2015.1082032

  247. 247.

    Bhatti K.H., Anwar S., Nawaz K., Hussain K., Siddiqi E.H., Sharif R.U., Talat A., Khalid A. Effect of exogenous application of glycinebetaine on wheat (Triticum aestivum L.) under heavy metal stress. Middle East J. Sci. Res. 2013;14:130-137.

    Not in our library

  248. 248.

    Stoyanova S., Geuns J., Hideg E., Van den Ende W. The food additives inulin and stevioside counteract oxidative stress. Int. J. Food Sci. Nutr. 2011;62:207-214.

    Not in our library10.3109/09637486.2010.523416

  249. 249.

    Rahoui S., Chaoui A., Ben C., Rickauer M., Gentzbittel L., El Ferjani E. Effect of cadmium pollution on mobilization of embryo reserves in seedlings of six contrasted Medicago truncatula lines. Phytochemistry. 2015;111:98-106.

    Not in our library10.1016/j.phytochem.2014.12.002

  250. 250.

    Dhir B., Nasim S.A., Samantary S., Srivastava S. Assessment of osmolyte accumulation in heavy metal exposed Salvinia natans. Int. J. Bot. 2012;8:153-158.

    Not in our library10.3923/ijb.2012.153.158

  251. 251.

    Adrees M., Ali S., Iqbal M., Bharwana S.A., Siddiqi Z., Farid M., Ali Q., Saeed R., Rizwan M. Mannitol alleviates chromium toxicity in wheat plants in relation to growth, yield, stimulation of anti-oxidative enzymes, oxidative stress and Cr uptake in sand and soil media. Ecotoxicol. Environ. Saf. 2015;122:1-8.

    Not in our library10.1016/j.ecoenv.2015.07.003

  252. 252.

    Habiba U., Ali S., Rizwan M., Ibrahim M., Hussain A., Shahid M.R., Alamri S.A., Alyemeni M.N., Ahmad P. Alleviative role of exogenously applied mannitol in maize cultivars differing in chromium stress tolerance. Environ. Sci. Pollut. Res. 2019;26:5111-5121.

    Not in our library10.1007/s11356-018-3970-2

  253. 253.

    Demecsová L., Zelinová V., Liptáková Ľ., Tamás L. Mild cadmium stress induces auxin synthesis and accumulation, while severe cadmium stress causes its rapid depletion in barley root tip. Environ. Exp. Bot. 2020;175:104038.

    Not in our library10.1016/j.envexpbot.2020.104038

  254. 254.

    Sharma P., Kumar A., Bhardwaj R. Plant steroidal hormone epibrassinolide regulate–Heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environ. Exp. Bot. 2016;122:1-9.

    Not in our library10.1016/j.envexpbot.2015.08.005

  255. 255.

    Mazorra L.M., Nunez M., Hechavarria M., Coll F., Sánchez-Blanco M.J. Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Biol. Plant. 2002;45:593-596.

    Not in our library10.1023/a:1022390917656

  256. 256.

    Özdemir F., Bor M., Demiral T., Türkan İ. Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regul. 2004;42:203-211.

    Not in our library10.1023/b:grow.0000026509.25995.13

  257. 257.

    Bajguz A., Hayat S. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 2009;47:1-8.

    Not in our library10.1016/j.plaphy.2008.10.002

  258. 258.

    Liu Y., Zhao Z., Si J., Di C., Han J., An L. Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul. 2009;59:207-214.

    Not in our library10.1007/s10725-009-9405-9

  259. 259.

    Alam M.M., Hayat S., Ali B., Ahmad A. Effect of 28-homobrassinolide on nickel induced changes in Brassica juncea. Photosynthetica. 2007;45:139.

    Not in our library10.1007/s11099-007-0022-4

  260. 260.

    Anuradha S., Rao S.S.R. The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ. 2007;53:465.

    Not in our library10.17221/2307-pse

  261. 261.

    Kagale S., Divi U.K., Krochko J.E., Keller W.A., Krishna P. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta. 2007;225:353-364.

    Not in our library10.1007/s00425-006-0361-6

  262. 262.

    Sharma P., Bhardwaj R. Effects of 24-epibrassinolide on growth and metal uptake in Brassica juncea L. under copper metal stress. Acta Physiol. Plant. 2007;29:259-263.

    Not in our library10.1007/s11738-007-0032-7

  263. 263.

    Hu Z., Fu Q., Zheng J., Zhang A., Wang H. Transcriptomic and metabolomic analyses reveal that melatonin promotes melon root development under copper stress by inhibiting jasmonic acid biosynthesis. Hortic. Res. 2020;7:79.

    Not in our library10.1038/s41438-020-0293-5

  264. 264.

    Khan M.I.R., Chopra P., Chhillar H., Ahanger M.A., Hussain S.J., Maheshwari C. Regulatory hubs and strategies for improving heavy metal tolerance in plants: Chemical messengers, omics and genetic engineering. Plant Physiol. Biochem. 2021;164:260-278.

    Not in our library10.1016/j.plaphy.2021.05.006

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