REVIEW article

Front. Plant Sci., 09 March 2022

Sec. Plant Abiotic Stress

Volume 13 - 2022 | https://doi.org/10.3389/fpls.2022.773815

Cadmium Phytotoxicity, Tolerance, and Advanced Remediation Approaches in Agricultural Soils; A Comprehensive Review

  • 1. Department of Agronomy, University of Agriculture Faisalabad, Faisalabad, Pakistan

  • 2. College of Life Sciences, Yan’an University, Yan’an, China

  • 3. Department of Botany, University of Agriculture Faisalabad, Faisalabad, Pakistan

  • 4. Agronomic Research Institute, Ayub Agricultural Research Institute, Faisalabad, Pakistan

  • 5. College of Resources and Environmental Sciences, Gansu Agricultural University, Lanzhou, China

  • 6. Department of Soil and Environmental Science, College of Agriculture, University of Sargodha, Sargodha, Pakistan

  • 7. Institute of Soil and Environmental Science, University of Agriculture Faisalabad, Faisalabad, Pakistan

  • 8. Institute of Chemistry and Technology of Environmental Protection, Faculty of Chemistry, Brno University of Technology, Brno, Czechia

  • 9. Department of Agrochemistry, Soil Science, Microbiology and Plant Nutrition, Faculty of AgriSciences, Mendel University in Brno, Brno, Czechia

  • 10. Institute for Environmental Studies, Faculty of Science, Charles University in Prague, Prague, Czechia

Article metrics

View details

230

Citations

28,2k

Views

7,7k

Downloads

Abstract

Cadmium (Cd) is a major environmental contaminant due to its widespread industrial use. Cd contamination of soil and water is rather classical but has emerged as a recent problem. Cd toxicity causes a range of damages to plants ranging from germination to yield suppression. Plant physiological functions, i.e., water interactions, essential mineral uptake, and photosynthesis, are also harmed by Cd. Plants have also shown metabolic changes because of Cd exposure either as direct impact on enzymes or other metabolites, or because of its propensity to produce reactive oxygen species, which can induce oxidative stress. In recent years, there has been increased interest in the potential of plants with ability to accumulate or stabilize Cd compounds for bioremediation of Cd pollution. Here, we critically review the chemistry of Cd and its dynamics in soil and the rhizosphere, toxic effects on plant growth, and yield formation. To conserve the environment and resources, chemical/biological remediation processes for Cd and their efficacy have been summarized in this review. Modulation of plant growth regulators such as cytokinins, ethylene, gibberellins, auxins, abscisic acid, polyamines, jasmonic acid, brassinosteroids, and nitric oxide has been highlighted. Development of plant genotypes with restricted Cd uptake and reduced accumulation in edible portions by conventional and marker-assisted breeding are also presented. In this regard, use of molecular techniques including identification of QTLs, CRISPR/Cas9, and functional genomics to enhance the adverse impacts of Cd in plants may be quite helpful. The review’s results should aid in the development of novel and suitable solutions for limiting Cd bioavailability and toxicity, as well as the long-term management of Cd-polluted soils, therefore reducing environmental and human health hazards.

Introduction

The presence of organic and inorganic pollutants in the environment leads to its deterioration, which has become a grave issue and is threatening the global ecosystem (Zulfiqar et al., 2019; Zeeshan et al., 2021). Enrichment of soil with toxic heavy metals such as cadmium (Cd), lead (Pb), arsenic (As), nickel (Ni), mercury (Hg), and chromium (Cr) causes serious hazards to plant life and human health. These potentially toxic elements are present at low concentrations in the environment (Palansooriya et al., 2020). High levels of these toxic metals are harmful to humans, plants, and animals (but not exceptionally) because of their persistent nature in the environment (Afzal et al., 2019). Cd is one of the most toxic heavy metals to living organisms (Chellaiah, 2018; Zulfiqar et al., 2021). Cd is an element ranked 7th in the list of 20 most toxic metals and classified as group 1 carcinogen (Jaishankar et al., 2014). It is one of the most perilous metals owing to its high toxicity and serious extent of bioaccumulation (Singh et al., 2020; Qianqian et al., 2022). Cd toxicity adversely affects the human body, and it accumulates in the kidneys and causes emphysema, renal tubular damage, and kidney stones (Mahajan and Kaushal, 2018). In minerals, it replaces calcium owing to similar charge, ionic radius, and chemical behavior (Kubier et al., 2019). Therefore, it can easily be transferred and stored in the human body (Hajeb et al., 2014). Cd toxicity causes severe liver damage and reduces the supply of calcium in the body (Lata et al., 2019). Moreover, Cd directly influences the regulation of Zn and Fe via ZIP, and NRAMP (Tanveer and Shabala, 2022). It is released to the environment through natural as well as anthropogenic systems. Among natural systems, weathering of Cd-containing rocks, forest fires, volcanic eruptions, and wastewater are the principal means (Liu et al., 2013; Manzoor et al., 2019). Anthropogenic activities are a source of Cd contamination, mainly including metallurgical works, mining, electroplating, paints, combustion emissions, and excessive use of fertilizers and pesticides (Singh et al., 2020; Haider et al., 2021a; Figure 1). It is readily soluble, and it is mobile compared to other metals; therefore, it is quickly taken by plants (Song et al., 2015). After uptake, Cd is translocated and accumulated in edible parts of plants (Adil et al., 2020).

FIGURE 1

FIGURE 1

Sources of cadmium (Cd) contamination in the environment.

Cadmium toxicity adversely affects plants by inhibiting carbon fixation and reducing chlorophyll synthesis and photosynthetic activity (Liu et al., 2018). Exposure to Cd causes physiochemical, morphological, and structural changes in plants such as chlorosis and inhibition of lateral root formation and stomatal density (Bari et al., 2019; Huybrechts et al., 2020). It induces osmotic stress in plants by reducing leaf relative water content, stomatal conductance, and transpiration (Rizwan et al., 2016). It also has harmful effects on uptake and transportation of mineral elements, resulting in yield decline (Chen et al., 2018a,b,c). Cd toxicity causes overproduction of reactive oxygen species (ROS) and results in damage to plant membranes and destruction of cell organelles (Abbas et al., 2017). Cd is a very toxic heavy metal that adversely affects a variety of physiological functions leading to stunted growth with ultimate yield penalty on field crops.

The bioavailability and toxicity of Cd depend on physical and chemical properties of soil (Violante et al., 2010). With decrease in soil pH, Cd is transformed from a fixed form to a readily mobile form that enhances its availability for plant uptake (Mondal et al., 2020). Therefore, understanding the physical and chemical properties of soil and the dynamics of Cd in soil is essential for reducing the toxicity caused by Cd. This review presents an overview of the adverse effects of Cd toxicity on plants, ultrastructural and oxidative damage, carbon metabolism, and yield formation. The dynamics of Cd in the rhizosphere, and soil factors affecting soil uptake are also discussed. Moreover, potential remediation strategies such as physical, chemical, and biological methods to decontaminate Cd from polluted soils are also highlighted. Furthermore, the use of different forms of organic materials and molecular techniques to reduce Cd uptake and accumulation are described.

Cadmium Dynamics in Soil and the Rhizosphere

Biologically, Cd is not important for plants; however, it is easily acquired by plants because of micronutrients from the rhizosphere of soils (the soil-root interface) (Shahid et al., 2016). The presence of Cd has been observed in soils ranging between 0.07 to 1.1 mg kg–1 soil (World Health Organization [WHO], 2007). However, threshold level is approximately 100 mg kg–1 in agricultural soils (Asgher et al., 2015).

Cadmium (Cd) is primarily present as Cd ions or forming complexes, i.e., organic and inorganic in the soil solution. Both anionic and cationic forms of Cd exist in soils (Kabata-Pendias and Sadurski, 2004). Anionic forms are CdCl3, Cd(OH)3, Cd(OH)42–, and Cd(HS)42–, while cationic forms are CdCl+, CdOH+, CdHS+, and CdHCO3+. It has been found that 99% Cd is present in the soil solution as a free ionic form (Kabata-Pendias, 1993).

Several chemical reactions, namely, dissolution/precipitation, desorption/adsorption, and Cd ligand formation, affect the partitioning of Cd in soils. These processes are mainly influenced by ligands (organic and inorganic) (Shahid et al., 2014), redox conditions (Zhang et al., 2012), soil pH (Saeki and Kunito, 2012), metal contents, and temperature (Silber et al., 2012). Partitioning of Cd is vital in soil systems for regulation of Cd toxicity (Rizwan et al., 2017). Cd biogeochemical behavior depends on the concentration of free Cd ions in a soil medium (Shahid et al., 2016). Accumulation of Cd in plant root varies with Cd contents in the rhizosphere and plant type. Maize (Zea mays L.) showed more Cd accumulation in cell wall fraction than broad bean (Vicia faba L.) seedlings (Lozano-Rodriguez et al., 1997).

Factors Affecting Cadmium Dynamics

Several factors like soil pH, cation exchange capacity (CEC), organic matter, microbial activities in the soil, and root exudates influence the bioavailability of Cd (Jung, 2008; Shahid et al., 2016). One of the crucial factors in the regulation of Cd partitioning and its bioavailability is soil pH (Yu et al., 2016). Cd exists in various chemical forms at varying soil pH levels. It has been observed that Cd solubility in the soil solution is primarily affected by acidic soil conditions. A change in Cd from immobile forms like carbonates and Mn and Fe oxides to better exchangeable forms allow free Cd phytoavailability and mobility (Qi et al., 2018). For the solubility of Cd in soil, pH 6 acts as a threshold point because of complex formation with organic matter and its adsorption on mineral surfaces (Sullivan et al., 2013). On the other hand, rise in pH increases its alkalinity, affecting Cd adsorption into soil particles. Yu et al. (2016) described that soil pH played a key role in acclimatization of Cd in rice grains. Enhanced soil pH imparts a negative influence on phytoavailability, as adsorption and precipitation of Cd decrease free Cd availability in the soil solution (Meng et al., 2018).

The bioavailability of Cd is influenced by soil organic matter (SOM) because of formation of various complexes with Cd in the soil solution. The bioavailability of Cd depends on SOM source, concentration, and chemical forms. In addition, SOM has a direct influence on Cd binding and its acclimatization. Kirkham (2006) reported that higher SOM causes more sorption potential, which is 30 times more than mineral soil. Biochar application greater than 10% reduces the bioavailability of Cd in plants through its immobilization in soil (Xiao et al., 2019). In another study, the application of biochar decreased Cd stress in wheat (Triticum aestivum L.) by reducing its bioavailability (Abbas et al., 2018). On the contrary, Yousaf et al. (2016) depicted that SOM content and uptake of Cd increased in wheat predominantly because of application of poultry manure, sewage sludge, and farmyard manure.

Cation exchange capacity of the soil strongly influences the mobility and bioavailability of Cd. In a study, binding of Cd to exchangeable and acid-soluble fractions occurred in loamy and loamy sand soils having small Cd contents, and was found to be related to SOM. However, Cd was bound to a reducible fraction followed by an exchangeable acid-soluble fraction in silt-clay soil (Gusiatin and Klimiuk, 2012). Hong et al. (2002) reported less Cd mobility due to its strong affinity with clay mineral surface, Fe–Al oxides, and humus in clayey soils. The bioavailability Cd is directly influenced by the occurrence of mineral ions in the soil solution. This is directly related to ionic strength, competition, and complexation for root or soil exchange sites. Additionally, there is an inverse relationship between ionic strength and bioavailability, as Cd extraction by plants is enhanced because of less ionic strength in growth media (Gothberg et al., 2004).

Soil microbial activity is found to enhance the availability of Cd through organic acid secretion and succeeding solubilization of Cd-bearing minerals (Ahmad et al., 2015). Soil amendments having Cd-solubilizing microbes like plant growth-promoting rhizobacteria (PGPRs) play an essential role in enhancing the bioavailability of Cd (Wu et al., 2020). In a study, Sangthong et al. (2016) depicted the ability of Micrococcus sp. TISTR2221 to modulate more uptake of Cd in the root and stem parts of maize plant under Cd stress. On the other hand, to reduce the toxicity of Cd in plants, microbes like PGPRs and arbuscular mycorrhizal fungi play a crucial role in restricting the uptake of Cd in roots. Reduction in Cd phytoavailability was found by soil bioaugmentation, causing immobilized and free Cd-resistant bacteria and fungi in the rhizosphere (Sharma and Archana, 2016).

Root exudates also impart a role in sequestration and binding of Cd in soils and protect plant roots from Cd toxicity in soils (Liao and Xie, 2004). Furthermore, Cd uptake is minimized by root exudates in plants (Sarwar et al., 2010). Factors affecting Cd dynamics are presented in Figure 2.

FIGURE 2

FIGURE 2

Factors affecting Cd dynamics in soils (conceived from Shahid et al., 2016).

Toxic Impacts of Cadmium on Plants

Impact of Cadmium Toxicity on Plant Growth and Yield Formation

Cadmium accumulation in agricultural soils has become a primary concern of scientific factions because of Cd’s increasing concentration, which substantially reduces plant growth and yield (Romero-Puertas et al., 2004; Goix et al., 2014; Zhang et al., 2014). Cd toxicity in soils causes several harmful impacts on plants, i.e., overproduction of oxidative markers like ROS, free radicals, and lipid peroxidation which induces oxidative stress and ultimately causes reduction in the yield of crops (Qayyum et al., 2017; Hussain et al., 2018). Therefore, it is a necessity for the current era to overcome Cd toxicity for better health of humans and plants. To overcome the toxic impacts of Cd, following strategies could be useful such as introduction of plant species that can phytoremediate heavy metals by sequestration of the metals in their vegetative parts and avoidance of the introduction of these heavy metals to plants by control of anthropogenic activities and implementation of lawful strategies of countries and governments.

Ultrastructural Changes Due to Cadmium Toxicity

Plants exhibit a different response when exposed to varying concentrations of Cd. Anatomical abnormalities mainly depend on plant species, exposure duration, uptake amount, sequestration, and localization in different parts (Shah et al., 2019). Cadmium is phloem-mobile and localized in any part of plants; it leads to reduction in biomass and yield; it causes chlorosis and even leaf fall that contradicts normal plant movements (Gallego et al., 2012).

Cadmium exposure causes considerable anatomical alterations in roots, stems, and leaves of Ceratopteris pteridoides. These alterations include closure of abaxial stomata, stomatal size reduction in leaves, scarification in tracheid walls, narrow xylem vessels, and disorganization in vascular bundles in roots and stems (Bora and Sarma, 2021). Trichome length, abaxial and adaxial density of stomata, and proportion of cortex were decreased in Trigonella foenum under Cd stress (Ahmad et al., 2005). Heterogeneity in vascular tissues of stems and leaves occurs in Arundo donax L. when exposed to Cd stress (Guo and Miao, 2010). Plants exposed to Cd cause severe impacts by reducing the size of parenchyma in leaves, disrupting the ultrastructure of chloroplasts, disorganizing vascular s organization, reducing epidermal tissue thickness, and exhibiting narrow xylem and phloem vessels. Heavy metal-tolerant plants can induce a plethora of mechanisms to reduce the noxious impacts of heavy metals by modification of microstructures. These modifications include an efficient vascular system by increasing a vascular bundle area for better translocation of water and food. These plants also develop a thick epidermis to conserve plenty of water in their bodies, which is covered with a waxy cuticle layer, and sequester a large amount of water in roots and shoots to prevent from translocation into the leaves. This prevention in uptake could modify the photosynthetic apparatus of plants. Some heavy metal-tolerant species also exhibit various avoidance mechanisms to prevent the entrance of heavy metals into roots. Effects of Cd on the ultrastructure of roots, stems, and leaves of different plant species are illustrated in Table 1.

TABLE 1

Plant speciesCd levelsUltrastructural changes/damagesReferences
At root level
Gossypium hirsurum L.20.26 μMCd deposit between intercellular spaces of secondary phloem, and root periderm indicated adsorption and localization of Cd.Chen et al., 2015
Solanum tuberosum L.25 μMAccumulation of Cd in root cells was higher than in the stem.Xu et al., 2013
Hordeum vulgare L.30 μMHyper accumulation of the Cd in root tissues as compared to its counterparts. Cd cause reduction of passage cells in the endodermis, thickened pericycle cell walls was assessed.Alle et al., 2016
Pteris vittata L.100 μMFewer numbers of root hairs, reduce apical meristem, reddish colored precipitates formed in root vacuoles.Balestri et al., 2014
Oryza sativa L.100 μMDisintegration occurs in root cell walls and vascular tissues, brown granular deposits in the root exodermal cells, and prominence of root nucleoli.Shah et al., 2013
Miscanthus floridulus L.10 μMHyper accumulation of Cd in root cells.Guo et al., 2016
Zea mays L.0.1 mMExtensive root area, large parenchyma, and cortical cells of roots.Maksimović et al., 2007
Aegiceras corniculatum L.4 g L–1Root tissues decreased in the following order: endodermis > pith > xylem > epidermis and exodermis > phloem > cortex.Li J. et al. (2019)

At stem level
Ceratopteris pteridoides L.60 μM L–1Tracheids consist of pits in later walls, narrowing occur in the xylem and phloem vessels, vascular bundles disrupted in the form of aggregation, grana were dissolved and chloroplast form ellipsoidal shape.Bora and Sarma, 2021
Trigonella foenum L.50 μg g–1Proportion of cortex and vasculature decreased, prominent alteration occur in the xylem and phloem.Ahmad et al., 2005
Arundo donax L.101 mg kg–1Lower proportion of xylem, thin epidermal tissues, sclerification occurs in epidermis.Guo and Miao, 2010

At leaf level
Pistia stratiotes L.12.8 mg L–1Reduce proportion of aerenchyma in leaves.Silva et al., 2013
Avicennia schaueriana L.64 mg L–1Disruption occurs in nuclear membranes, dense material deposit in the vascular bundles of parenchyma cells.Mizushima et al., 2019
Eucalyptus urophylla L.450 μMDecline occurs in adaxial and abaxial epidermal thickness, palisade, and spongy parenchyma thickness.da Silva Cunha et al., 2020
Cicer arietinum L.0.1 mMReduce leaf thickness, abaxial and adaxial stomata closedLiza et al., 2020
Ceratopteris pteridoides L.60 μM L–1Cause stomatal closure, narrow xylem vessels, disorganized chloroplast, and chloroplast components, excessive plastoglobules and large starch grains.Bora and Sarma, 2021
Populus deltoides L.8.14 mg kg–1Size of palisade tissues decreased, adaxial epidermal cell size decreased.Nikolić et al., 2017
Salvia sclarea L.100 μMDecline in epidermal cell size, osmiophilic granules embedded in cell vacuoles, loss of intercellular spaces, dense mesophyll cells seemed.Dobrikova et al., 2021

Ultrastructural/anatomical damages in different plant species due to cadmium (Cd) toxicity.

Oxidative Damages Due to Cadmium Toxicity

Cadmium, like other HMs, induces oxidative damages by producing excessive H2O2 and lipid peroxidation in plants (Rizwan et al., 2019a; Shiyu et al., 2020; Yang et al., 2020; Figure 3). It is well-documented that Cd regimes induce the production of ROS (H2O2, O–2); these scavenge antioxidant enzymes (Kapoor et al., 2019; Hasanuzzaman et al., 2020; Unsal et al., 2020). Several studies suggest that Cd does not directly participate in ROS production but induces temporal oxidative damage to plants (Cuypers et al., 2010, 2016). Cellular ROS mainly comprise both free radicals and non-radicals (Hasanuzzaman et al., 2020). Free radicals include O2 •−, •OH, RO•, peroxyl radical (ROO•) and non-radicals, H2O2, 1O2, and ozone (O3) (Farooq et al., 2019; Maurya, 2020), while other non-radicals that exist in plants are excited carbonyls, hypochlorous acid (HOCl) and hydroperoxides (ROOH) (Kapoor et al., 2015). Because of oxidative damage, accumulation of thiobarbituric acid reactive substances (TBARSs) and malondialdehyde (MDA) occurs in, and results in electrolyte leakage under Cd stress (Younis et al., 2016).

FIGURE 3

FIGURE 3

Cd-induced oxidative stress and damages in plants (conceived from Genchi et al., 2020; Shiyu et al., 2020). 1O2, singlet oxygen; ROS, reactive oxygen species; O2•–, superoxide anion; H2O2, hydrogen peroxide; OH, hydroxyl radical; APX, ascorbate peroxidase; GR, glutathione reductase; POD, peroxidase; CAT, catalase; SOD, superoxide dismutase; DHAR, dehydro-ascorbate reductase.

Accumulation of Cd in plants occurs because of some significant mechanisms like (i) structural similarity with nutrients taken by roots (phosphorous and zinc), (ii) direct Cd influence on the sulfhydryl (–SH) group, which impairs protein structure, (iii) dislocation of essential cations from binding sites, (iv) disturbance of normal level of ROS and antioxidants, which consequently damage nucleic acids, lipids, proteins, cellular pigments, and essential nutrients (Hossain et al., 2012; Choppala et al., 2014; Singh et al., 2016). Cd induces oxidative stress in several plant species, i.e., Phyllostachys pubescens (Li S. et al., 2016), Phoenix dactylifera L. (Zouari et al., 2016), Solanum lycopersicum (Medyńska-Juraszek et al., 2020), Triticum aestivum L. (Lin et al., 2007), Salvinia auriculata (Vestena et al., 2011), Spartina densiflora (Martínez Domínguez et al., 2010), and Phyllostachys pubescens (Li S. et al., 2016). Cd, in bivalent form, is unable to produce free radicals directly; however, after exposure to Cd, there is a significant increase in production of ROS (super oxide radicals, H2O2, and hydroxyl radicals). Cd induces oxidative stress by counteracting normal antioxidants, i.e., peroxidase (POD), dehydro-ascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), ascorbate peroxidase (APX), catalase (CAT), and superoxide dismutase (SOD), and non-enzymatic antioxidants, i.e., vitamins C and E, tocopherols, carotenoids, ascorbic acid (ASA), and glutathione reductase (GR), which results in overproduction of ROS and causes damage to the biosynthetic machinery of cells. This xenobiotic-induced oxidative stress results in damage of biological membranes, macromolecules (proteins, lipids, and phospholipids), and biological membranes of cells. Cd also negatively influences the mitochondrial matrix by disrupting oxidative phosphorylation and ATP synthesis. Exposure to Cd also causes negative impacts on the cell repairing process of enzymatic proteins and damage to DNA and RNA, and reduces the proliferation and differentiation of cells (Akhter et al., 2021).

Carbon Metabolism and Yield Formation

Plants face toxic environmental constraints and mitigate these by dealing with carbon metabolism, constant supply of CO2, maintaining electron transport chain, and assimilation of CO2 at certain levels (Leegood, 1993). Disturbance in carbon metabolism occurs because of Cd toxicity and leads to decrease in photosynthetic efficiency (Gouia et al., 2003). Cd effectively causes alteration in photosynthesis by negative influence on its all aspects, including electron transport chain (ETC), photosystems (PSI and PSII), chl-proteins complexes, and CO2 reduction pathways in the stroma (Parmar et al., 2013). Cd-induced toxicity also convincingly results in alteration of chloroplast ultrastructure with inflated and disrupted thylakoids (Najeeb et al., 2011). Alteration in chloroplast ultrastructure was manifested by reduction in number of chloroplasts and size and number of grana, accumulation of plastoglobules, and excessive starch in leaves of Hordeum vulgare, Picris divarticata, and Brassica spp. (Ying et al., 2010; Wang et al., 2011; Elhiti et al., 2012). Moreover, the Willow plant showed aggregation of grana, disrupted thylakoids, and swallowed intrathylakoidal spaces owing to lipid peroxidation (LPX) (Hakmaoui et al., 2007). LPX is ensued by the activity of lipoxygenase (LOX) enzyme (Remans et al., 2010). This enzyme mediates the peroxidation of membrane fatty acids such as phosphatide glycerol (PG) and mono- and digalactosyldiacyl glycerol (MGDG, and DGDG. For instance, more accumulation of the activation of MGDG, DGDG, and PG results in the production of ROS and free radicals. Correlation of LOX with LPX reported in many plants like Lupine, Barely, Phaseolus, and Arabidopsis thaliana in response to Cd exposure (Maksymiec and Krupa, 2006; Tamás et al., 2009). In general, Cd causes a significant reduction in carbon metabolism, this reduction causes change in photosynthesis because of low supply of CO2, and low carbon levels counteract ETC and thylakoid membranes and photosynthetic enzymes. Ultrastructural changes in cell components like chloroplasts are also a major cause of reduction in photosynthesis efficiency of cells in leaves.

Disruption of photosynthetic pigments and biosynthetic inhibition in old and young leaves of plants have been reported as a primary cause of Cd toxicity (Xue et al., 2013; Anjum et al., 2016). Chlorophyll biosynthesis mainly depends on the aminolevulinate (ALA) compound, and Cd inhibits ALA at the site of glutamate availability and contradicts with the SH functional group of enzyme-like porphobilinogen deaminase and δ-aminolevulinic acid (Myśliwa-Kurdziel and Strzałka, 2002; Skrebsky et al., 2008). However, excessive concentration of ALA is responsible for the production of ROS, which can alter the redox potential of cells and alter cellular homeostatic functions, as reported in Cucumis sativus (Goncalves et al., 2009) and soybean (Noriega et al., 2007).

Cadmium toxicity alters the function of photosystems (PSI and PSII), interacts with PSII core complex and PSII supramolecular entities, and retards photoactivation (Quartacci et al., 2000; Sigfridsson et al., 2004). In contrast, PSI is considered more susceptible to Cd toxicity, and it might be because of Cd-induced Fe deficiency, which causes more damage to PSI (Timperio et al., 2007). Iron-deficit damage to PSI has been reported in Cucumis sativus L. under 10-μM Cd stress (Sárvári, 2008). In comparison to PSII, PSI is less explored in terms of Cd toxicity; however, photosynthetic yield was severely hindered because of Cd in Thlaspi caerulescens and Pisum sativum (Küpper et al., 2007; Wodala et al., 2012). Cd toxicity also hampers the Calvin cycle and shows inhibitory effects on various enzyme activities (Ying et al., 2010). Enzymes RUBP and PEP play a vital role during photosynthesis and are involved in CO2 fixation (Zhang et al., 2007). Excessive Cd ions decrease the activity of RUBP and PEP by causing alteration in their structures, and replace essential cofactors, such as Mg2+, which are involved in the process of carboxylation and shift to oxygenation reactions (Tran and Popova, 2013). Cd stress leads to disruption of photosynthetic traits, which results in damage of chloroplast components and hindrance in vital photosynthetic enzymes (Singh and Prasad, 2017).

Cadmium stress severely hinders plant growth, photosynthesis, and grain yield (Rizwan et al., 2016; Abbas et al., 2018). Several studies reported that Cd translocates to rice grains because of significant decline in grain yield and uptake of nutrients by roots (He et al., 2006; Liu et al., 2007; Rodda et al., 2011; Li and Zhou, 2012). However, in rice, the amplitude of yield reduction depends on genotype, concentration of Cd treatment, and duration of exposure (Song et al., 2017). Cadmium toxicity also severely reduces yield traits like number of spikelets per plant, grain number per ear, ear length, and weight in wheat crop (Khan et al., 2007). For instance, the threshold of Cd toxicity varies from genotype to genotype, exposure duration, and concentration of dose (Rizwan et al., 2016). Reduction in yield of crops has been reported previously on several plant species such as barley (Lentini et al., 2018), pea (Januškaitienė, 2010), tomato (Hayat et al., 2012), Phaseolus vulgaris (Rady, 2011), Zea mays L. (Anjum et al., 2015), and Cicer arietinum L. (Hayat et al., 2013; Liza et al., 2020). Cd toxicity severely reduces the growth and yield traits of plants; however, severity depends on plant species, Cd level, and exposure period. The impact of Cd on different plant crop yields is documented in Table 2.

TABLE 2

Crop speciesLevel of CdYield reduction (%)References
Radish (Raphanus sativus)200 mg kg–129.55–53.48Varalakshmi and Ganeshamurthy, 2013
Radish (Raphanus sativus)10 mg L–110.0Amirabad et al., 2020
Wheat (Triticum aestivum L.)1 mg L–15.0–9.0Zhang et al., 2002
Wheat (Triticum aestivum L.)100 mg kg–126–53Khan et al., 2007
Rice (Oryza sativa L.)150 mg kg–138.3–47.1Huang et al., 2008
Rice (Oryza sativa L.)100 mg kg–122.16–32Lin et al., 2016
Rice (Oryza sativa L.)100 mg kg–115–38Cao et al., 2015
Cotton (Gossypium hirsutum L.)600 μM60.6Li et al., 2012
Mustard (Brassica juncea L.)150 mg kg–133–79–60Gill et al., 2011
Canola (Brassica napus L.)12 mg kg–165.39Ghani, 2011
Mungbean (Vigna radiata L.)25 mg kg–126–37Wahid and Ghani, 2008
Tomato (Solanum lycopersicum)50 μM25.5Kumar et al., 2015
Tomato (Solanum lycopersicum)50 μM10.31–25.50Xie et al., 2021
Barley (Hordeum vulgare L.)5 μM10.7–55.8Wu et al., 2007

Impact of Cd toxicity on yield of some representative crops.

Remediation of Cadmium-Polluted Soils

Physicochemical Remediation Methods

Remediation of Cd-contaminated soils could be achieved via organic chelate and surfactant application, and it is known as chelate-assisted phytoextraction or chelate-induced phytoextraction (Habiba et al., 2015; Sakouhi et al., 2016). Compared to traditional phytoremediation, chelate-induced phytoextraction is more beneficial, convenient, and environment frindly, because chelate-induced phytoextraction augments the extraction aptitude of hyperaccumulators (Clabeaux et al., 2011; Zhao et al., 2015; Wang et al., 2019). In chelate application strategy, different types of amino polycarboxylic acid chelates like S,S-ethylenediamine disuccinic acid (EDDS), iminodisuccinic acid (IDSA), [N, N]-bis glutamic acid (GLDA), ethylenediaminetetraacetate (EDTA), nitrilotriacetic acid (NTA), diethylenetriaminepentaacetic acid (DTPA), methylglycinediacetic acid (MGDA), ethylenebis (oxyethylenenitrilo) (EGTA) tetraacetic acid, and trans-1,2-diaminocyclohexane-N, N, N0, N0 -tetraacetic acid diethylenetriaminepentaacetic acid (CDTA) are applied in a Cd-contaminated growth medium to escalate Cd mobilization as well as phytoextraction capacity (Table 3; Zaheer et al., 2015; Hasan et al., 2019). Similarly, organic acids having low molecular weight, like oxalic acid (OA), citric acid CA), and tartaric acid (TA), have also been used as chelating agents. Having multi-ligand structures, these chelating agents form stable compounds with HMs and, resultantly, increase the mobility of soil HMs (Guo et al., 2019). According to Bian et al. (2016) and Moslehi et al. (2019), these chelating agents not only enhance the mobility of Cd in the soil solution but also change the form of Cd in soils, boost the availability of Cd for uptake and translocation, and, ultimately, upsurge Cd accumulation in aboveground biomass of plants grown in Cd-contaminated soils.

TABLE 3

CropCd concentration in soilChelate appliedDoseCd uptake
References
ControlChelate treated
Cicer arietinum L.200 μM CdCl2.EGTA100 μM300 μg g–1195 μg g–1Sakouhi et al., 2016
Brassica napus0.37 mg kg–1100 kg ha–10.44 mg kg–10.33 mg kg–1Bloem et al., 2016
0.37 mg kg–1500 kg ha–10.44 mg kg–10.25 mg kg–1
0.37 mg kg–11000 kg ha–10.44 mg kg–10.24 mg kg–1
Neyraudia reynaudianaEDTA2.5 m mol kg–198 mg kg–1184 mg kg–1Li Z. et al., 2018
Neyraudia reynaudianaEDTA5 m mol kg–198 mg kg–186 mg kg–1Li Z. et al., 2018
Amaranthus hybridus L.30.15 mg kg–1EDDS5.0 mmol kg–199 mg kg–1146 mg kg–1Li Z. et al., 2018
Amaranthus hypochondriacus L.2.12 mg/kgGLDA3 mM15 mg kg–144 mg kg–1Wang et al., 2019
2.12 mg/kgGLDA5 mM15 mg kg–149 mg kg–1
2.12 mg/kgNTA3 mM15 mg kg–151.5 mg kg–1
2.12 mg/kgNTA5 mM15 mg kg–137.5 mg kg–1
2.12 mg/kgCA3 mM15 mg kg–123 mg kg–1
2.12 mg/kgCA5 mM15 mg kg–127 mg kg–1
2.12 mg/kgEDDS3 mM15 mg kg–144 mg kg–1
2.12 mg/kgEDDS5 mM15 mg kg–135 mg kg–1
Amaranthus hypochondriacus L.2.89 mg/kgGLDA3 mM18 mg kg–136.5 mg kg–1
2.89 mg/kgGLDA5 mM18 mg kg–139 mg kg–1
2.89 mg/kgNTA3 mM18 mg kg–137.5 mg kg–1
2.89 mg/kgNTA5 mM18 mg kg–132.5 mg kg–1
2.89 mg/kgCA3 mM18 mg kg–124.5 mg kg–1
2.89 mg/kgCA5 mM18 mg kg–126 mg kg–1
2.89 mg/kgEDDS3 mM18 mg kg–137 mg kg–1
2.89 mg/kgEDDS5 mM18 mg kg–130 mg kg–1
Helianthus annuus L.50 mg kg_1EDDS5 mmol kg–11.7 mg pot–11.6 mg pot–1Moslehi et al., 2019
100 mg kg_1EDDS5 mmol kg–12.9 mg pot–12.4 mg pot–1
Tagetes patula L.2.44 mg kg–1EDDS1 mM832.11 μg/pot1081.2 μg/pot
2.44 mg kg–1EDDS3 mM832.11 μg/pot1088.9 μg/pot
2.44 mg kg–1EDDS5 mM832.11 μg/pot619.5 μg/pot
Phytolacca americana L.2.44 mg kg–1EDDS1 mM16.42 μg/pot72.3 μg/pot
2.44 mg kg–1EDDS3 mM16.42 μg/pot144.8 μg/pot
2.44 mg kg–1EDDS5 mM16.42 μg/pot64.3 μg/pot

Chemical remediation of Cd-contaminated soil.

Among these chelating agents, EDTA has been most widely used because of its slower biodegradability and strong binding affinity toward Cd ions (Chen et al., 2004; Saifullah et al., 2009; Jiang et al., 2019). Structural characteristics of EDTA enable it to form a strong bond with Cd and increase Cd solubilization, translocation, and phytoextraction capacity of phytoremediation (Nowack, 2002; Hasan et al., 2019). However, remediation of Cd-polluted soils varies with different EDTA application rates, plant species, and soil types (Evangelou et al., 2007).

After EDTA, another widely used chelating agent for successful phytoextraction of Cd is EGTA (Pereira et al., 2010). Cheating agent EGTA enhances the uptake of Cd by plants efficiently (Hasan et al., 2019). Previous research studies have highlighted that application of EGTA increased the phytoextraction of Cd by 72% in Althaea rosea (Liu et al., 2008) by 43% in Mirabilis jalapa (Wang and Liu, 2014), and by 217% in Calendula officinalis (Jianv et al., 2010). Similarly, a surfactant named SDS is also being used to remediate organic and metal contaminations in soils (Pierattini et al., 2017). It was concluded that application of SDS not only increased the biomass but also increased Cd accumulation in roots and shoots of Althaea rosea (Liu et al., 2009, 2008) and Calendula officinalis (Jianv et al., 2010). GLDA is known as a green chelating agent, and it has better Cd extraction efficiency (Wu et al., 2015).

In terms of degradation, EDTA biodegrades slowly, while EDDS is a quick biodegradable chelating agent that can augment the mobility of HMs and their uptake, and translocation and accumulation of HMs in plant shoots in HM-contaminated soils (Li et al., 2013; Attinti et al., 2017; Zhu et al., 2017). However, EDDS phytoextraction efficacy depends on time of application, method of application, dose, and level of Cd contamination in soils.

Similar to EDDS and GLDA, NTA is also a quick biodegradable (approximately 7 days) and highly effective chelate for remediation of Cd-polluted soils (Hu X. et al., 2017). Similarly, application of some other chelating agents like DTPA and IDSA proved to be useful in Cd complexation, enhancing Cd solubility and its uptake by plants, e.g., hydroponically grown maize (Zhao et al., 2010). Saifullah et al. (2009) and Wang et al. (2019) highlighted that besides application of single chelating agents, when chelator complexes (a combination of two different chelates), e.g., GLDA + NTA and GLDA + CA were applied on Cd-contaminated soils, biomass production and Cd uptake by plants increased significantly.

Contrarily, where chemical amendments using chelating agents are conducted to phytoextract Cd from soil (Lambrechts et al., 2011), at the same time, these chemical amendments have a limitation of stunted plant growth, e.g., Pseudomonas brassicacearum (Krujatz, 2012), Lolium perenne, Brassica juncea, and Typha angustifolia (Muhammad et al., 2009; Goel and Gautam, 2010; Xu et al., 2010). Under such circumstances where the application of a single chelating agent resulted in stunted growth, application of a quick biodegradable chelate complex is a potential option for enhancing Cd phytoextraction (Wang et al., 2019). Similarly, combined application of chelating agents and plant growth regulators increased Cd uptake and biomass accumulation (Li Z. et al., 2018). Hence, in crux use of chelating agents is a viable option for remediation of Cd polluted soils. The application of chelating agents significantly enriched Cd uptake in plant biomass of many important plants (Table 3). Studies propose that application of chelates is a viable strategy for remediation of Cd-polluted soils. Soil contamination with heavy metals is a widespread environmental constraint. Therefore, it is very important to reduce the toxic impacts of HMs and their associated risks to plants and restoration of soils. The phytoremediation process includes phytostimulation, phytofiltration, phytotransformation, and phytoaccumulation, which extensively reduced the noxious effects of HMs in soils. The soil physicochemical remediation process includes soil washing, vitrification, solidification, stabilization, and use of metallophytes for phytoextraction. The process of phytoremediation of HM-contaminated soils is a reliable tool and necessary to make land resources accessible for crop production.

Plant Growth Regulators Assisted Remediation

Modulation of phytohormones or plant growth regulators (PGRs) not only mitigates the toxic effect of Cd stress on plants (Li Y. et al., 2018) but also enhances the tolerance of plants to Cd stress (Asgher et al., 2015) and efficacy of phytoextraction of Cd by plants in Cd-polluted soils (Sun et al., 2020). Research studies suggested the positive effect of PGRs on Cd translocation and accumulation, promotion of plant growth and nutritive value, and biomass accumulation under Cd stress (Asgher et al., 2015; Aderholt et al., 2017; Chen et al., 2019). Among key PGRs, cytokinins (CKs), ethylene, gibberellins (GAs), auxins, abscisic acid (ABA), polyamines (Pas), jasmonic acid (JA), brassinosteroids (BRs), and nitric oxide (NO) play substantial roles specifically in plant growth and developmental processes (Asgher et al., 2015). According to Piotrowska-Niczyporuk et al. (2012) and Sun et al. (2020), exogenous application of PGRs acts in diverse modes and enhances plant adaptability and tolerance to Cd stress in different ways. In addition, the role of CKs, indole-3-acetic acid (IAA), indole-3-butyric acid (IBA), and 1-naphthaleanecetic acid (NAA) in phytoextraction of Cd from Cd-polluted soils has been documented in many studies (Table 4; Bulak et al., 2014; Okem et al., 2015).

TABLE 4

CropCd concentration in soilPGRDoseEffect
References
ControlPGR treated
Vicia faba150 mg L–1Jasmonic acid0.01 mM43.2 μmol g–117.3 μmol g–1Ahmad et al., 2017
Mentha piperita L.30 mg kg–1Salicylic acid10 μM6 μmol g–17 μmol g–1Ahmad et al., 2018
Mentha piperita L.60 mg kg–1Salicylic acid10 μM6 μmol g–114 μmol g–1
Mentha piperita L.120 mg kg–1Salicylic acid10 μM6 μmol g–134 μmol g–1
Zea mays L.0.5 mMSalicylic acid0.5 mM46.3 μmol g–114.7 μmol g–1Gondor et al., 2016
Oryza sativa50 μMSalicylic acid50 μM166.7 μg g–190.6 μg g–1Singh et al., 2018
Brassica napus (Zheshuang-72)75.12 mg kg–1Salicylic acid50 μM125 mg g–180 mg g–1Ali et al., 2015
150.12 mg kg–1Salicylic acid50 μM185 mg g–1125 mg g–1
300.12 mg kg–1Salicylic acid50 μM240 mg g–1175 mg g–1
Brassica juncea L.15.31 mg kg_1Indole acetic acid100 mg L–198.1 mg g–195.3 mg g–1Chen et al., 2020
15.31 mg kg_1250 mg L–198.1 mg g–1107.8 mg g–1
15.31 mg kg_1500 mg L–198.1 mg g–1138.5 mg g–1
Brassica juncea L.15.31 mg kg_1Gibberellic acid100 mg L–198.1 mg g–199.8 mg g–1Chen et al., 2020
15.31 mg kg_1250 mg L–198.1 mg g–1115.2 mg g–1
15.31 mg kg_1500 mg L–198.1 mg g–195.3 mg g–1
Brassica juncea L.15.31 mg kg_124-Epibrassinolide5 mg L–198.1 mg g–196.3 mg g–1Chen et al., 2020
15.31 mg kg_110 mg L–198.1 mg g–1120.5 mg g–1
15.31 mg kg_150 mg L–198.1 mg g–1132.5 mg g–1
Amaranthus hybridus L.30.15 mg kg–1Diethyl aminoethyl hexanoate10 μM99 mg kg–1125.7 mg kg–1Li Y. et al., 2018
30.15 mg kg–1100 μM99 mg kg–1113.5 mg kg–1
Amaranthus hybridus L.30.15 mg kg–16-Benzylaminopurine10 μM99 mg kg–1110 mg kg–1Li Y. et al., 2018
30.15 mg kg–1100 μM99 mg kg–1100 mg kg–1

Plant growth regulators assisted remediation of Cd-polluted soils.

Gibberellins

Gibberellins (GA) can also protect plants from negative impacts of trace metals by reducing oxidative stress and increasing antioxidant mechanisms (Nguyen et al., 2020). GAs enhance sulfate assimilation, which promotes GSH/phytochelatin production, as S-containing metabolites are important for plant defense mechanisms. Application of GAs increased biomass accumulation, Cd uptake efficacy of Lolium perenne L. (He et al., 2014) and Helianthus annuus L. (Long et al., 2017), hampered MDA contents and oxidative stress of B. juncea under Cd toxicity (Meng et al., 2019), and in lupin plants and broad beans, it mitigated Cd toxicity by increasing soluble proteins under Cd stress (Sharaf et al., 2009). GAST1, a GA-stimulated transcript implicated in the control of ROS buildup, was also upregulated after an exogenous gibberellin was applied and subsequent transcriptomic techniques were employed (Sun et al., 2013). GA signaling boosted the expression of adenosine 50-phosphosulfate reductase, an enzyme crucial in sulfate assimilation, in A. thaliana under stress (Koprivova et al., 2008).

Abscisic Acid

Abscisic acid (ABA) is a plant hormone that regulates many aspects of plant development, growth, and stress responses (Nian et al., 2021). Reduced seed dormancy and wilty phenotypes are seen in ABA-deficient mutants from a variety of plant species, indicating that these important ABA activities are maintained across the plant kingdom (Haider et al., 2021b). In Bidens pilosa, the application of a stress hormone, e.g., ABA, enhanced plant tolerance to Cd stress and Cd extraction from Cd polluted-soil (Liu et al., 2017; Pompeu et al., 2017). Li et al. (2014) concluded that pretreatment of ABA decreased the activities of ascorbic acid, CAT, SOD, APX, POD, and GSH in roots of Vigna radiate L. under Cd stress. ABA, when used as a pretreatment before Cd treatment, did not result in increased contents of cysteine (CYS) and phytochelation (PC). This suggests the role of ABA in the regulation of PCS (Stroiński et al., 2013). The protective role of ABA against Cd stress has also been demonstrated by experiments comparing wild-type Arabidopsis plants and ABA-deficient plants, in which the mutants proved to be more sensitive to Cd metal stress (Sharma and Kumar, 2002). These findings strongly suggest that ABA may be involved in signal pathways during Cd stress.

Nitric Oxide

Nitric oxide is a free radical that reacts with oxygen molecules and controls the deposition of oxygen in plant tissues (Tran et al., 2011). NO is a signal molecule that activates cell defense mechanisms in response to a variety of stressors (Tran and Popova, 2013). Tran and Popova (2013) and Xu et al. (2015) documented that NO application diminished the structural modification of leaves, increased nutritional value, and improved antioxidant enzyme activities under Cd Stress. In other studies, application of NO on Cucumis sativus L. under Cd stress augmented chlorophyll contents and biomass accumulation, and decreased chlorosis symptoms and oxidative stress in plants (Yu et al., 2013).

Salicylic Acid

An endogenous phenolic PGR such as salicylic acid (SA) governs an imperative role in plant physiological processes (photosynthesis, growth, and development), specifically under abiotic stresses, including Cd toxicity (Tran and Popova, 2013; Gruznova et al., 2018). Ahmad et al. (2011) highlighted that SA in initial growth stages assisted plants in mitigating increased damage caused by Cd toxicity by expressing specific proteins and defense-related enzymes (Çanakci and Dursun, 2012; Roychoudhury et al., 2016). Pretreatment of SA abridged Cd accumulation, electrolyte leakage, and level of MDA in wheat shoots under Cd stress (Shakirova et al., 2016), enriched the level of lipids, upregulated the antioxidant system, and caused variations in fatty acid composition of vegetable seedlings (Tran and Popova, 2013; Semida et al., 2015; Rizwan et al., 2017). Increased levels of SA, in response to Cd stress, are reported in pea (Rodríguez-Serrano et al., 2006), maize (Krantev et al., 2008), Arabidopsis (Zawoznik et al., 2007), and halophyte Kosteletzkya virginica (Han et al., 2013). The role of SA in modulating the oxidative stress caused by Cd toxicity is evident by comparing the SA accumulating and deficient lines of Arabidopsis (Zawoznik et al., 2007; Tao et al., 2013). Mutants showed variable levels of H2O2 contents, lipid peroxidation, and antioxidant enzymes in comparison with wild plants. Increased levels of endogenous SA led to growth retardation while mutants having decreased endogenous SA showed least retardation in growth because of Cd stress. However, majority of studies disclose the protective role of SA in reduction of oxidative stress caused by Cd.

Jasmonic Acid

Jasmonates are oxylipins, which are oxygenated fatty acid derivatives (Ahmad et al., 2017). Methyl JA (MeJA) is a volatile molecule that may have a role in plant-to-plant communication. Exogenous application jasmonic acid (JA) resulted in reduced Cd, H2O2, and malondialdehyde accumulation in Vicia faba L. (Ahmad et al., 2017). Similarly, exogenous application of GB reduced the oxidative stress caused by Cd stress and increased the biomass of wheat (Rasheed et al., 2014). Application of ethylene on Arabidopsis thaliana under Cd stress increased root proliferation by modulating superoxide anion (Abozeid et al., 2017). At low levels (10−4 mol/L), it may incur a protective role in mitigation of Cd stress, but at high concentrations, JA might induce retardation in growth by degrading chlorophyll and photosynthetic enzymes (Maksymiec and Krupa, 2002).

Auxins

The auxin IAA is a well characterized hormone and is involved in growth regulation and physiological development of plant; however, it is still a less studied and less understood mystery in terms of response to Cd stress (Farooq et al., 2015; Teiri et al., 2018). Exogenous application of IAA on B. Juncea promoted uptake and accumulation of Cd that might be attributed to increased cell division, formation of vascular tissue and development of a broader root system that as a result, reduces the toxic effect of Cd (Teiri et al., 2018; Rostami and Azhdarpoor, 2019). Farooq et al. (2015) opined augmented growth and yield of rice when a precursor of an auxin was applied in Cd-contaminated soil. Elobeid et al. (2012), in their experiment, reported disturbed homeostasis of auxin in response to exogenously applied Cd. Yu et al. (2017) stated that an auxin transporter (OsAUX1) induced the extension of root hair and primary roots of rice under Cd stress. Ostrowski et al. (2016) reported that the application of an auxin conjugate (IAA-Asp) induced reduction of H2O2, and upregulated POD and CAT activity under Cd stress.

Cytokinins

Cytokinins (CKs) are a kind of plant hormone that promotes cytokinesis (cell division) in plant roots and shoots (Singh and Prasad, 2016). They have a role in cell proliferation and differentiation, as well as apical dominance, axillary bud development, and leaf senescence. Exogenous application of CKs inhibited Cd biosorption and augmented the activities of antioxidant enzymes in Chlorella vulgaris (Piotrowska-Niczyporuk et al., 2012) and tomato under Cd-contaminated soil conditions (Singh and Prasad, 2016).

Brassinosteroids

Brassinosteroids (BRs) are endogenous plant hormones that regulate a variety of physiological processes that are necessary for appropriate plant growth and development (Rehman et al., 2022a,b). Application of 28-homobrassinolide (homoBL) on the foliage of Brassica juncea improved Cd tolerance because of enhanced activity of antioxidant enzymes (CAT, POD, and SOD) (Hayat et al., 2007). The effect of 24-epibrassinolide (24-epiBL) was examined on Phaseolus vulgaris in response to Cd stress (Shahzad et al., 2018). 24-epiBL improved membrane stability index, proline content, and antioxidant system (Rady, 2011). Plants exposed to Cd stress have impaired electron transport (ETC) because of demolished photochemical reaction centers, whereas epi-brassinolide (EBL) reduced Cd toxicity and impaired the reaction centers of photosystems and ETC (Janeczko et al., 2005). Moreover, Cd stress helped older tissues more effectively and EBL improved the photosynthetic activity in radish leaves (Anuradha and Rao, 2009). Similarly, in tomatoes, BR application reduced the phytotoxic effects of Cd and improved fruit quality and yield (Hayat et al., 2012). Application of EBL in bean plants subjected to Cd stress increased the levels of antioxidant enzymes. Rise in an antioxidant system (superoxide dismutase, catalase, peroxidase and glutathione reductase, and proline) leads to increased tolerance, enhanced photosynthetic machinery, and growth. Similar kind of results were reported on other crops, i.e., mustard (Hayat et al., 2007) and chickpea (Rady, 2011), by exogenous application of EBL and HBL, respectively. The application of BRs as a shotgun approach (EBL and HBL) improved the chlorophyll content and photosynthesis efficiency of Cd- stressed tomato plants (Hayat et al., 2010). Besides this, BR treatment significantly increased the number of fruits, fruit yield, lycopene, and β-carotene contents in fruits of plants grown under Cd stress.

Polyamines

Polyamines are necessary for cell growth. Polyamine content is greater in quickly expanding tissues, and growth-promoting and regenerative hormone cues boost polyamine production and content (Hasanuzzaman et al., 2019). Rady and Hemida (2015) discussed that presoaking wheat seeds with polyamines, spermine or spermidine resulted in enhanced seedling growth, relative water contents, starch, ascorbic acid, membrane stability index, total glutathione, and concentration of protein, and that H2O2, total soluble sugars, concentration of proline, electrolyte leakage and MDA were decreased under Cd stress.

Some other compounds (paclobutrazol, daminozide, humic acid, and melatonin) are extensively used worldwide to decrease the devastating effects of Cd stress in cultivable plants (Khan et al., 2017; Hasan et al., 2019). In conclusion, the use of the above-mentioned PGRs might be an effective, eco-friendly strategy to enhance the growth and development of plants cultivated in a Cd-stressed environment.

Microbe-Assisted Remediation of Cadmium Stress

Soil microorganisms may not destroy or degrade HMs; however, they can affect physical and chemical characteristics that might help to migrate and transform them from highly toxic to less toxic forms and restrict their uptake by plants through a number of mechanisms including extracellular complexation, intracellular accumulation, and oxidation–reduction reaction. Furthermore, soil microorganisms could improve plant health by improving the uptake of nutrients that could upregulate plant growth and biomass production (Nejad et al., 2017; Rizwan et al., 2017). Thus, microbial symbioses have imperative ecological roles and can be used to increase the resilience and sustainability of ecosystems (French, 2017), especially in Cd-contaminated areas. Cd-induced polluted soil remediation can be mediated by two common types of mycorrhizae: (1) Ecto-mycorrhiza (ECM) and (2) Arbuscular mycorrhiza (AM).

In all ecosystems, AM and the other fungus, ECM, have made associations with almost all plant species (Lehmann et al., 2017). AM is a unique one, as it colonizes almost all types of plants to remediate HMs; however, unlike AM, ECM mostly colonizes woody plants. Phytoextraction of Cd mediated by Phragmites australis was observed under low Cd stress, and immobilization of Cd has in roots under high Cd stress has been reported (Huang et al., 2017). Sell et al. (2005) inoculated Populus canadensis and Salix viminalis with ECM strains including Hebeloma crustuliniforme, Pisolithus tinctorius, and Paxillus involutus, and observed an increase in Cd uptake and translocation from a sterilized Cd-contaminated soil. Hence, it can be stated that along with ECM inoculation, choice of the host plant is a determinant of better results. Arbuscular mycorrhizal fungi (AMFs) form a mycorrhizal symbiosis with almost 80% of higher plants and may increase the remediation of Cd-contaminated soils (Abdel-Latef et al., 2016; Table 5). The increasing attention on AMFs’ aptitude to retain HMs in the mycelium is due to a process known as “mycorrhizal-remediation,” which decreases the translocation of metals to other plant parts such as shoots and subsequently increases plant tolerance under such conditions (Moreira et al., 2015).

TABLE 5

MycorrhizaePlantMechanisms of heavy metals alleviationReferences
Aspergillus aculeatusCynodondactylon (L.)Alteration of metabolites, IAA production, and Higher relative growth rate (RGR) and normalized relative transpiration rate (NRT).Li et al., 2017a
Alternaria alternataSolanum nigrumHigh antioxidant activity, Improvement in plant photosynthetic efficiency, Attenuated lipid peroxidationLi et al., 2017b
Glomus versiforme, Funneliformis mosseae, Rhizophagus intraradicesZea mays L.This study demonstrated a synergistic effect between AMF and biochar on improving maize growth and decreasing Cd/Pb accumulation in maizeZhuo et al., 2020
Glomus intraradicesZea mays L. Zea mays L.Decreasing Cd phyto-toxicity due to the synergistic effect of microbes and biochar
Rhizophagus intraradices, Glomus versiformeLonicera japonicaMicrobial symbiosis ameliorated the Cd toxicity by reducing Cd content in shoot and improved of P uptakeLiu et al., 2018
Glomus versiforme Glomus elunicatum, Glomus aggregatum, Glomus intraradices,Medicago sativaReduced Cd content
Rhizophagus irregularisGlycine maxArbuscular mycorrhizal colonization had no impact on Cd concentration and translocation in HN89 and HX3 plantsJiang et al., 2016
Glomus aggregatum Rhizophagus fasciculatus, Funneliformis mosseae, Rhizophagus intraradicesZea maysPhytoextraction
Glomus geosporum Glomus mosseae Glomus intraradices Glomus claroideumNicotiana tabacumReduced the Cd mobility in the soil (Phytostabilization)Zhang et al., 2019
Glomus intraradicesZea maysCd concentration was reduced by improving the growth of maize; Sequestered Cd toxicity by upregulating the activities of SOD, POD, and CAT
Scutellospora sp. Gigaspora sp. Acaulospora sp. Glomus sp.Fabaceae, Asteraceae, PoaceaeImproved glomalin protein to sequester Cd contentCui et al., 2019
Glomus sp.Triticum aestivumPhytostabilization potential to sequester Cd; Cd immobilization
Rhizophagus irregularisPhragmites australisCd toxicity ameliorated by improving photosynthesis rate, root biomass, micro- and macro-element concentrations in plants and decreased the malonaldehyde (MDA) and proline content; Reduced stomatal conductance and transpiration rate to alleviate Cd toxicitySingh et al., 2019
Rhizophagus intraradices G. versiformeLonicera japonicaDecreased MDA by improving P acquisition, antioxidant activity (CAT, APX, and GR)
G. mosseaeApium graveolensIncreased chlorophyll content, P accumulation, and plant growth by increasing phytoextraction in Cd stressJanoušková et al., 2006
G. mosseae, G. intraradices, G. etunicatumCassia italic MillCd stress mitigated by the enhanced production of antioxidants, chlorophyll, and protein content, and osmoprotectants including proline and phenol content

Bioremediation potential of arbuscular mycorrhizae fungi (AMF) against Cd toxicity.

Inoculation of AMF improved the metal content in organic matter, electrical conductivity, soil pH, and the proportion of bioavailable Cd in a post-harvest soil (Wu et al., 2016). Nevertheless, Glomus versiforme significantly increased the translocation of Cd from roots to shoots relative to Fusarium caledonium. Furthermore, HMs cause oxidative stress in plants because of overproduction of ROS normally occurring during plant metabolism. There is always a balance between production and utilization of ROS in plant cells (Riaz et al., 2018; Yan et al., 2018; Kamran et al., 2019). AMF (Rhizoglomus intraradices, Glomus etunicatum, and Glomus versiforme) inoculation upregulated the activity of antioxidant enzymes in Cd-stressed plants that helped to increase plant growth and biomass (Tanwar et al., 2015; Sharma et al., 2017; Liu et al., 2018; Molina et al., 2020). Synthesis of sulfur-rich compounds such as phytochelatins and glutathione is important to mediate plant tolerance among numerous stress-induced detoxification pathways activated in plants (Mishra et al., 2009). AM’s role in regulation of thiol metabolism has recently been associated with Cd stress (Garg and Chandel, 2015). Thus, the defensive effect of AM is embodied in the mediation of the antioxidant enzyme system, alleviating the index of the lipid peroxidation process (Zhan et al., 2018; Janeeshma and Puthur, 2020; Luo et al., 2020), and AM inoculation improved phenol contents and proline and reduced H2O2 and lipid peroxidation (Hashem et al., 2016). Mycorrhizal plants show greater tolerance against metal stress through mechanisms such as chelation of metals in hyphae, immobilization, glomalin, root colonization, and compartmentalization in fungal cells (Yang et al., 2017). Inoculation of Anaerolineaceae in bioremediation of Cd stress is another possible method, because this regulates the shaping of microbial communities and mediates Cd solubility. AM (Rhodobacter sphaeroides) helped in P solubilization (Chen et al., 2019), Fe nutrition (Lehmann and Rillig, 2015), P and N uptake under different irrigation regimes (Liu et al., 2018), and enhanced the levels of K, P, and Ca in Euonymus japonica, and prominent levels of Zn, Mn, P, and K were sustained under stress (Bagheri et al., 2012). Chang et al. (2018) studied the putative role of Claroideoglomus etunicatum fungus that improved the uptake of N, P, and K by 20.1–76.8%, and by decreasing Cd uptake. AMF-induced glomalin accumulation acts as a defense system in plants against Cd-mediated oxidative stress in soils and plant tissues (Babadi et al., 2019). Bioaugmentation is a method that could be beneficial under low native AMF inoculum potential and involves the addition of microbial population for remediation of contaminated areas (Mongkhonsin et al., 2019). New stimulant formulations and techniques aimed at producing AMF inoculants might instigate the prevalent practice of AMF inoculation in the near future. Microbial flora such as fungi, algae, and photosynthetic flora effectively reduce HM contamination. Microbes showed various possible mechanisms to eliminate Cd toxicity including sequestering or accumulating metals in their cell walls and altering the composition of toxic compounds. Cadmium can be introduced to bacterial cells in the form of divalent cations by gene amplification, active efflux, and active influence on metallothionein genes. The major potential of remediation of metals by microbes is low operating costs, high capacity, metal recovery potential, and effective biosorbent regeneration.

Plant Growth-Promoting Rhizobacteria

Plant growth-promoting rhizobacteria (PGPRs) are rhizosphere inhabitants that enhance plant growth by improving plant nutrient availability, water relationship, and antioxidant activity to improve abiotic stress tolerance (Saeed et al., 2021). They are categorized based on (a) inherent characters (Kloepper, 1994): they (i) enhance root colonization, (ii) improve plant growth, (iii) acclimatize, survive, reproduce, and compete until expression of their potential in plant growth promotion/protection; (b) functional properties (Ahemad, 2014): (i) phytostimulators (phytohormones improve growth), (ii) biofertilizers (regulate nutrient uptake), (iii) rhizoremediators (solubilization of metals), and (iv) biopesticides (regulate plant diseases and pathogens by producing metabolic compounds and lytic enzymes). PGPRs help in phytoremediation; production of soluble minerals, siderophore, phytohormones, rhamnolipid, extracellular polymeric substances, osmo-protectants, 1-aminocyclopropane-1-carboxylate deaminase (ACCD), immobilization of metals (Mahajan and Kaushal, 2018), bioremediation; accumulation or transformation of contaminants, rhizoremediation; and remediation of contaminated soils by symbiotic relationship between plant roots and suitable microbial species. Inoculation of PGPRs has been reported to decrease Cd uptake and alleviate Cd-induced oxidative stress by producing phytohormones (Glick, 2014; Wang et al., 2015), ammonia, and siderophores that mediate nutrient availability, plant biomass accumulation, and plant water status (Ahmad et al., 2015; Hassan et al., 2015; Figure 4). However, Cd uptake may be improved by inoculation of Cd-tolerant bacteria in plants (Bojorquez et al., 2016; Sharma and Archana, 2016), which depicts the specificity of PGPRs and aim of experiment, i.e., phytostabilization vs. phytoextraction. Under heavy metal stress conditions, PGPR-induced IAA acts as a phytohormone to improve cell division and elongation to stimulate root growth, and enhances root nodulation, vascular bundle development, and plant growth (Goswami et al., 2016; Chen et al., 2017). Pseudomonas aeruginosa strains ZGKD5 and ZGKD2 augment to synthesize IAA in Solanum nigrum to improve tolerance against Cd stress (Shi et al., 2016). Huang et al. (2016) observed that Pse-w-MT induces Cd tolerance in Pisum sativum L. by improving the production of IAA. A Bacillus megaterium strain regulated cytokinin production by mediating the transcriptional level of the roots and shoots s receptor (AHK3/AHK4) that induced root morphogenesis in Arabidopsis thaliana (Jianfeng et al., 2017). Cd toxicity and uptake have been decreased by inoculation of Cd-resistant Micrococcus sp. TISTR2221 in maize (Suksabye et al., 2016) and Pseudomonas aeruginosa and Bacillus subtilis in rice (Sangthong et al., 2016).

FIGURE 4

FIGURE 4

Impact of plant growth-promoting rhizobacteria (PGPRs) on remediation of Cd-contaminated soils (conceived from Ullah et al., 2015; Sharma and Archana, 2016).

Extracellular polymeric substances (EPSs), mucopolysaccharides, and proteins are produced by different PGPRs that help to bind toxic HMs for thriving plant growth (Upadhyay et al., 2011; Rajkumar et al., 2012). PGPR strains have been identified that produce EPS to counter the toxic effect of Cd contamination by decreasing the uptake of Cd in wheat (Joshi and Juwarkar, 2009). Pseudomonas aeruginosa inoculation with a PGPR strain helps to detoxify Cd stress based on extracellular biosorption, bioaccumulation, controlled siderophore production, formation of biofilm, enhanced respiration, and modified protein profile (Zivkovic et al., 2018). Recent studies have also shown the detoxification of Cd stress by P. aeruginosa (Zivkovic et al., 2018) and its adapted cells (Tang et al., 2018). Cd stress involved in the uptake of different nutrients influences metal solubility, and P solubilization, and improves nutrient mobility (chelation, precipitation, and immobilization) (Rafique et al., 2017; Saeid et al., 2018). PGPRs could be a promising option to enhance phyto-stabilization efficiency and bioleaching of Cu and Cd in heavily polluted soils owing to biosorption or bioaccumulation (Yang et al., 2018; Ke et al., 2021). Plants produce ROS-scavenging enzymes to detoxify ROS, which are produced under HM stress (Zainab et al., 2020). Exogenous applications of PGPR a strain, Streptomyces strain IT25, decreased catalase (CAT),and it is reported that PGPRs upregulated SOD (superoxide dismutase), POD (peroxidase), and PPO (plant polyphenol oxidases) genes to sequester Cd stress (Khanna et al., 2019; Abbasi et al., 2020) (Table 6). Azospirillum brasilense may ameliorate the negative effects of Cd stress by upregulation of lower Na/K ratio, TaSOS1 transcript level, proline, higher pigments, and antioxidant activities to improve dry weight (Ghassemi and Mostajeran, 2018). PGPR-mediated remediation of HMs and promotion of plant growth depend on PGPR strains coded by several genes and must be understood to build a multidimensional PGPR strain to perform multidimensional functions. Nevertheless, use of genetically engineered PGPR strains with hyper-accumulator plants to remove HMs is less common (Ullah et al., 2015). Several studies have also documented that genetic engineering mediated the improvement in remediation of HM stress in plants (Verma et al., 2017). Qiu et al. (2014) incorporated a bifunctional glutathione synthase gene (gcsgs) into Enterobacter sp. CBSB1 improved the efficiency of HM removal in B. juncea.

TABLE 6

ConditionsPlantGenesPGPRMechanismsReferences
Hydroponic mediaTriticum aestivumTatm20Azospirillum brasilenseCd toleranceGhassemi and Mostajeran, 2018
HydroponicsSarcosphaera coronariaPCS, F-boxPGPR strainsImproved Cd tolerance and Cd transportJebara et al., 2018
HydroponicSedum alfrediiNRAMP, HMA family genes, ZIPEndophytic bacteriumImproved C uptake, Regulated plant acquisition of essential nutrientsPan et al., 2017
HydroponicSedum alfrediiNRAMP, HMA family genes, ZIPPseudomonas fluorescensCd uptakeChen et al., 2017
Growth chamberArabidopsis thalianaIRT1, FIT1, FRO2Bacillus amyloliquefaciensEnhancing uptakeZhou et al., 2017
Controlled conditionsLycopersicon esculentum6MT, MT3, 5, MT1, MT7Burkholderia gladioli and Pseudomonas aeruginosaEnhancing photosynthetic pigments and growthKhanna et al., 2019
Soil less pot s systemCucumis melo L.Fe (IRT1, FRO), NH4+ (AMT2), Pi (PHT1)Enterobacter asburiae, Pseudomonas koreensis, Pseudomonas liniEnhanced the yield of fruitMurgese et al., 2020
Green house experimentMedicago sativaNRAMP1Proteus sp., Pseudomonas sp., Ensifer melilotiRemediate metal-contaminated soilsRaklami et al., 2019

Influence of inoculation with plant growth-promoting rhizobacteria (PGPRs) on Cd chelator and transporter gene expression (MT: metal transporter 1).

Cadmium Remediation Through Organic Amendments

To minimize the noxious effects of Cd in plants, use of soil additives is a promising method to fix Cd in soils because of its in situ assistance, low cost, and low energy needs (Yao et al., 2021). However, immobilization of Cd in soils has been performed using different inorganic and organic amendments. Various chemical and biological reactions are involved in Cd immobilization through these amendments (He et al., 2019). Two major sources of organic amendments are plants and animals that can increase soil fertility, as they are saturated with carbon, hydrogen, and oxygen (Hamid et al., 2020a). Use of organic amendments in agricultural soils have many benefits, but their most promising role is immobilization (Hu W. et al., 2017). Biochar, compost, and manure have been used as chief organic amendments for remediation of soil Cd (Hamid et al., 2019) through chelation, adsorption, and precipitation (Hamid et al., 2020a; Mondal et al., 2020).

Biochar

To overcome the deleterious effects of HMs, biochar addition to soil is a practical approach (Yuan et al., 2019). Soil productivity and growth of plants have been increased with biochar (Qayyum et al., 2017). In the past years, biochar (BC) has been used in HM-contaminated soils because of its higher adsorption capacity and ability to lower HM contents in soils (Boostani et al., 2019). Use of biochar is an efficient approach to minimize HMs in soils, but it is expensive compared to other amendments in terms of production (Sohail et al., 2020). Biochar, an organic soil additive, has been very helpful in immobilizing the in soils (Hamid et al., 2020b; Haider et al., 2022). Its role in Cd immobilization is auspicious because of its basic nature, porous texture, energetic functional groups, and higher CEC (Medynska-Juraszek and Cwielag-Piasecka, 2020). Biochar-amended soils showed lower Cd transport and accumulation (Abbas et al., 2018). Biochar can easily adsorb Cd, Pb, and Cu by forming complexes and cation exchange mechanisms in soils (Farooq et al., 2020). Breakdown of natural organic material under controlled temperature and limited or no oxygen resulted in biochar production (Hussain et al., 2021). It is well-reported in the published literature that the use of biochar in pots and field tests has significantly improved growth, biomass, and economic productivity in Cd-contaminated soils (Table 7).

TABLE 7

Plant speciesFeed stockApplied rateExperiment typeSoil typeHeavy metalsEffectsReferences
Rice (Oryza sativa)Rice Straw (450°C)0, 3, and 5% (w/w)PotSandy clay loamCdBiochar application significantly decreased the Cd uptake (38%) along with a considerable increase in plant growth.Hafeez et al., 2019
Pak choi (Brassica chinensis)Rice straw (550°C)0, 2.5 and 5% (w/w)PotAlfisolCdApplication of biochar reduced the Cd uptake in root (29.23%) and shoot (42.49%), while increased the plant production together with enhanced enzymatic antioxidant activity.Kamran et al., 2019
Saffron (Crocus sativus)Beeswax waste (400°C)0, 1.5, 3 and 6% (w/w)PotCdThe Cd uptake was reduced up to 24% in corm and 33% in leaf coupled with increased plant biomass with biochar application.Moradi et al., 2019
Spinach (Spinacia oleracea)Cotton stalk, Rice straw (450°C)0, 2 and 5% (w/w)FieldCdBoth the biochar applications minimize the Cd uptake in plants up to 66% and enhanced the fresh biomass of spinach and phosphorous concentration in the soil.Qayyum et al., 2019
Spinach (Spinacia oleracea)Cotton stalk, Rice straw (450°C)0 and 2% (w/w)PotCdThe treatments of both rice and cotton biochar considerably increased the fresh mass and reduced the Cd uptake (61%).Qayyum et al., 2019
Maize (Zea mays)Common reed (550°C)0 and 1% (w/w)PotAlkaline soilCdApplication of biochar enhanced the plant biomass, root length, and root volume in addition to reduced Cd uptake (57%).Rafique et al., 2019
Pak choi (Brassica chinensis)Platanus orientalis branches (650°C)0, 0.5, 1, 2, and 4% (w/w)PotLoamy soilCdBiochar application reduced the Cd availability (80%) and malondialdehyde concentration in the shoot.Chen et al., 2019
Garden lettuce (Lactuca sativa)Rice husk (500°C)0 and 5% (w/w)PotCd, Pb, As, Ni, CrApplication of biochar reduced the bioavailability of Cd (31%), Pb (20%), and As (22%) in addition to increased P, total nitrogen, and total carbon contents in the soil.Ibrahim et al., 2019
Wild mint (Mentha arvensis)Mentha arvensis waste (450°C)0, 2, and 4% (w/w)PotSandy loam soilCd, PbBiochar enhanced the Cd and Pb tolerance by decreasing Cd (50%) and Pb (25%) uptake in mint along with an increase in photosynthetic pigments and stomatal activity.Nigam et al., 2019
White willow (Salix alba)Carpinus betulus waste biomass (400°C)0, 2.5, and 5% (w/w)PotSandCd, Cu, PbBiochar treatment increased the plant height, root length, leaf area, photosynthetic pigments, CO2 assimilation rate, and intracellular CO2 concentration in addition to reduced cd, Pb, and Cu availability.Mokarram-Kashtiban et al., 2019
Lebbek tree (Albizia lebbeck)Farmyard manure (450°C)0, 3, and 6% (w/w)PotSandy loamCdApplication of biochar enhanced the growth and gas exchange characteristics by lowering the absorption rate of Cd in root, shoot, and leaves up to 34, 33, and 50% respectively.Yousaf et al., 2019
Rice (Oryza sativa)Rice straw (450°C)0 and 1% (w/w)PotCdBiochar treatment significantly decreased the Cd uptake in root (29%) and shoot (45%) along with a considerable increase in shoot and root dry weight of plant and chlorophyll-a concentration.Rizwan et al., 2019b
Rice (Oryza sativa)Sugarcane bagasse (500°C)0 and 3% (w/w)PotFragile sandy soilCdApplication of biochar alleviates the ROS and decreased the bioavailability of Cd in fragile soil along with an increase in growth of plant root and photosynthetic pigments.García et al., 2020
Wheat (Triticum aestivum)Farm yard (500°C)0, 2.5, and 5 g/kg of soilPotAlkaline soilCdBiochar application reduced the Cd concentration in plant root (71–92%), shoot (82–92%), and grain (90–96%) in addition to enhanced wheat yield.Ijaz et al., 2020
Rapeseed (Brassica napus)Woodchip (300°C)0, 1, and 2% (w/w)PotCd, Pb, Ni, CuThe concentration of Cd (44%), Pb (51%), Ni (59%), and Cu (45%) were decreased along with an increase in fresh root and shot biomass, total chlorophyll, and enzymatic antioxidant activity under biochar application.Kamran et al., 2020
Quinoa (Chenopodium quinoa)Wheat straw (350°C)0, 1, and 2% (w/w)PotCdThe treatment with biochar enhanced the overall growth, pigments, and gas exchange parameters by limiting the Cd accumulation in root (30%), shoot (25%), and grain (45%) of quinoa.Naeem et al., 2020
Wheat (Triticum aestivum)Rice husk (400–500°C)0.4, 3 and 5%PotCd, PbBiochar application showed a promising decrease in shoot Cd (77%) and Pb (50%) availability in the soil and increased the plant growth and grain yield.Zhang S. et al., 2020
Cotton (Gossypium hirsutum)Cotton straw (550°C)0 and 3% (w/w)PotCdApplication of biochar considerably enhanced the chlorophyll contents, gas exchange parameters, and the activities of SOD and POD by decreasing the Cd uptake in both root (17.8%) and stem (15%).Zhu et al., 2020
Radish (Raphanus sativus)Wheat feedstock (500°C)0 and 0.5% (w/w)PotPaddy soilCdBiochar application showed a prominent increase in the activity of antioxidant enzymes and mineral contents along with a clear reduction of 92% in Cd uptake through roots.Dad et al., 2020
Rice (Oryza sativa)Platanus orientalis branches (650°C)0 and 3% (w/w)PotSilty clay loamCd, As, PbApplication of biochar reduced the bioavailability of Cd (37%) and Pb (23%) along with a considerable increase in catalase activity and grain yield.Wen et al., 2020
Oak (Quercus castaneifolia)Rice husk (500–550°C)1, 3, and 5% (w/w)PotLoamy soilCdBiochar treatment improved the oak growth and decreased the bioavailability of Cd up to 67%.Amirahmadi et al., 2020
Wheat (Triticum aestivum)Dry maize (700°C)0, 1.5, and 3% (w/w)PotCdPlant fresh and dry biomass, root length, and root surface area were increased along with reduced Cd uptake in root (51%) and shoot (48%).Jan et al., 2020
Tobacco (Nicotiana tabacum)Tobacco stem (450°C)0, 1, and 2% (w/w)PotCdApplication of biochar decreased the absorption, accumulation, and concentration of Cd in root (81%), stem (68%), and leaves (80%) along with increased plant biomass.Yao et al., 2021
Sweet basil (Ocimum ciliatum)Mulberry wood residues (530°C)0, 1, and 2% (w/w)PotSandy loamCdBiochar application reduced the Cd uptake in leaf up to 40% along with an increase in photosynthetic pigments, morphological traits, and catalase activity.Mehdizadeh et al., 2021
Tobacco (Nicotiana tabacum)Corn Cob (500°C)0 and 1% (w/w)PotClay loamCdBiochar treatment considerably reduced the Cd contents in shoot (32%) and improved the plant growth.Erdem, 2021
Wheat (Triticum aestivum)Bamboo biochar (750°C)0, 0.1, 1, and 5% (w/w)PotCdCd uptake was reduced in root (34.06%), straw (21.57%), and grain (23.33%).Ma et al., 2021
Tobacco (Nicotiana tabacum)Peanut-shell waste (400°C)0 and 1% (w/w)PotCinnamon soilCdPhotosynthetic pigments, gas exchange attributes, and activity of enzymatic antioxidants were increased along with a decrease of 14.8% in leaf Cd absorption.Ren et al., 2021

Effect of biochar on remediation of Cd-contaminated soils.

Moreover, application of biochar enhances soil pH, water holding capacity, and porosity (Yuan et al., 2019). The role of biochar in growth enhancement is due to the presence of essential nutrients available for plants (Sohail et al., 2019). Rizwan et al. (2018) reported that application of biochar has a positive influence on plant growth. With application of biochar, the exchange portion of Cd in soils is reduced by up to 28% because of increase in soil pH (Bashir et al., 2018). Application of rice straw considerably reduced the concentration of extractable Cd and Cd in soils (Elyamine et al., 2019). Zia-ur-Rehman et al. (2020) reported that various types of biochar showed significant increase in wheat grain in addition to reduced Cd bioavailability. Different low-cost amendments enhanced the photosynthetic pigments and activity of enzymatic antioxidants (SOD, POD, CAT, and ASP) in maize (Shahkolaie et al., 2020).

Compost

In contrast to various fertilizers, utilization of compost is a valuable practice to increase soil fertility and crop yield (Abbas et al., 2020). Being a saturated organic carbon, compost enhances the HM-holding capacity of soils along with increase in soil absorption capacity (Medyńska-Juraszek et al., 2020). The bioavailability of HMs in soils has been decreased with the application of compost because of the mechanism of chelation, degradation of microbes, co-precipitation, and de-methylation (Hussain et al., 2021). Naturally, the process of composting helps to stabilize HMs and solid wastes from agricultural and municipal sources by degradation of various microbes (Awasthi et al., 2015). Addition of compost modifies soil aggregation, soil moisture content, and percentage of organic matter, and different nutrients resulted in higher crop growth and yield (Abd El-Mageed et al., 2018). This improved aggregation of soil resulted in altered soil physical and chemical properties, which helps to improve seed germination and roots of seedlings (Abd-El-Mageed et al., 2019). Addition of compost to soils showed 20, 19, and 10% decrease in shoot Cd, Cu, and Zn, respectively (Eissa, 2019). Application of vegetable waste compost reduced Cd concentration by up to 50 and 46% in maize shoots and roots, respectively, along with significant increase in plant growth and NPK contents (Bashir et al., 2021). An increase of 39–85 and 29–63% was observed in shoot and root fresh weight of pak choi cabbage, respectively, along with decrease in the concentration of Cd both in roots and shoots by up to 21–44 and 26–53%, respectively, when green waste compost was applied to HM-contaminated soils (Li et al., 2021).

Manure

Manure is used as a replacement for fertilizers, as it is a proper organic fertilizer for plant production (Zhen et al., 2020). Being an organic soil amendment, manure has been extensively used to mobilize HM-contaminated soils (Huang et al., 2018). Its application increased soil pH because of mineralization of carbon and excessive addition of basic cations (Hussain et al., 2021). Application of manure increased the organic matter in soils that resulted in reduced Cd mobilization and phytotoxicity (Liu et al., 2015). Higher accumulation of organic matter in soils stops Cd mobilization by forming organic compounds or, more importantly, adsorption (Halim et al., 2015). Long-term use of manure in uncontaminated soils introduced the availability of HMs as there is little or no information regarding the available or total HMs in the soil with the addition of manure in uncontaminated soils (Zhen et al., 2020). Li F. et al. (2019) stated that SOM had been increased in addition to reduced bioavailability of Cd with the addition of chicken manure in a Cd-contaminated paddy field. Farmyard manure application significantly decreased Cd bioavailability and increased wheat yield (Bashir et al., 2020). Treatment of contaminated soils with composted manure increased the growth of maize plants in addition to decreased HM uptake (Gul et al., 2016). Huang et al. (2020) observed a promising decrease in Cd and Zn bioavailability and enhanced biomass of B. juncea with the application of manure. Bashir et al. (2021) used animal manure to observe the growth of maize in polluted soil and found a prominent decrease of 58 and 52.4% in shoot and root Cd along with enhanced NPK contents.

Genetic Strategies for Cadmium Remediation

Genetic engineering has played a vital role in improving the phytoremediation abilities of plants in terms of removing or detoxifying hazardous heavy metals in the environment. Several molecular techniques are being widely used to reduce Cd accumulation. Molecular mechanisms underlying Cd interactions and remediation are shown and described in Figure 5.

FIGURE 5

FIGURE 5

Schematic elucidation of molecular mechanisms involved in Cd remediation in plants.

Improvement in Cadmium Tolerance by Harnessing Genetic Variation

Screening of genotypes for low Cd accumulation is the primary step to develop Cd-tolerant genotypes. Utilization of these genotypes will help in the development of transgenic crops with enhanced tolerance. Rice has a main role in the supply of Cd to humans, which causes Cd toxicity in them. The risk of Cd toxicity in human beings can be reduced by identifying rice genotypes with low Cd-accumulating capacity. Considerable genetic variability has been found in polished rice and brown rice ranging from 0.14-1.43 and 0.06–0.99 mg kg–1, respectively (He et al., 2006; Liu et al., 2007). Indica rice displayed higher Cd accumulation in shoots and grains than japonica rice (He et al., 2006; Uraguchi et al., 2009).

In cereals, a substantial amount of genetic variability has been observed in grain legume crops, i.e., soybean (Arao et al., 2003; Sugiyama et al., 2011; Salazar et al., 2012; Vollmann et al., 2015). High or low Cd accumulating genotypes were identified in different crops by analyzing genetic variations present among them. In wheat, genotypes with low Cd accumulation capacity included durum lines 8982-TL-L, CDC-Verona, and Strongfield (Clarke et al., 2002; Pozniak et al., 2009). On the other hand, high Cd accumulating wheat genotypes were Joppa and Carpio (Elias et al., 2015; Elias and Manthey, 2016). Introgression of genes from one plant to another is also a promising genetic engineering technique, as many plants express genes that help in Cd tolerance (Lan et al., 2012; Yuan et al., 2012; Menguer et al., 2013). Aegilops tauschii accessions, i.e., AS623194, AS623402, and AS623402, were recommended to be rich sources of Cd-tolerant genes, as wild species have high genetic variability for Cd accumulation. Identification and inclusion of these genotypes in crop improvement programs will be helpful in developing new Cd-tolerant cultivars. Genes or QTLs controlling the accumulation of Cd can be identified using these lines in mapping populations (Qin et al., 2015).

Genetic Engineering Techniques for Cadmium Tolerance

Genetic engineering along with the development of transgenic plants may help in the cultivation of crops in soils contaminated with Cd. Various approaches in genetic engineering can help in the identification of desirable genes that can be used to develop plants with increased HM tolerance. These genes may assist in translocation and deposition of metals in tissues of transgenic plants along with other characteristics that help in tolerance of metals (Mosa et al., 2016; Sheoran et al., 2016). Recent research has displayed that several genes are involved in regulation of HM tolerance. This may be performed either by overexpression of one gene or by overexpression of multiple genes simultaneously (Bhargava et al., 2012). Therefore, genetic modifications involving transfer or regulation of genes should be studied thoroughly to develop crops tolerant to HM stress (Gerszberg and Hnatuszko-Konka, 2017). Metallothioneins and phytochelatins are key components that can be utilized to protect plants against toxic metals. Several studies have shown the importance of these components in phytoremediation, as HM tolerance was increased in transgenic plants developed using metallothionein genes and synthases (Sunitha et al., 2012).

Gene manipulation is one the most important strategies for producing Cd-tolerant plants. It involves complete understanding of molecular mechanisms involved in Cd stress and can be utilized to develop methods to reduce damages that are caused by toxic metals. This may also help reducing Cd concentration in edible plant parts by breeding crop varieties with low Cd accumulation and more agronomical importance. Most effective molecular techniques used worldwide for Cd tolerance in crop plants have been discussed.

Quantitative Trait Loci Related to Cadmium Uptake and Accumulation

The identification of chromosomal regions governing genes that control Cd tolerance has become an important genetic tool with the discovery of quantitative trait loci (QTLs) using family based method. This method has helped in the illustration of underlying genetic basis of Cd accumulation in various crops (Ishikawa et al., 2005, 2010; Knox et al., 2009; Ueno et al., 2009a,b; Jegadeesan et al., 2010; Jha and Bohra, 2016). In rice, QTLs are supposed to be located on LGs 3, 6, and 8 in chromosome segment substitution lines (CSSLs) developed from the cross between Kasalath (indica) and Koshihikari (japonica) (Ishikawa et al., 2005).

A QTL responsible for Cd accumulation in roots and shoots was found on LGs 6 and 7, while LG 3 consisted of a QTL for root or shoot Cd content. LGs 1, 3, 5, and 8 governed a total of six QTLs responsible for Cd tolerance (Xue et al., 2009). In F2 resulting from a cross between Badari Dhan and Shwe War, it was demonstrated that QTLs controlling 16.1% of total phenotypic variation (PV) related to Cd tolerance was mapped on LG 11 (Ueno et al., 2009a). QTL qLCdG11 for Cd tolerance was also mapped on LG 11 in an RIL population developed from a cross between Fukuhibiki 9 and LAC23. Major QTLs elucidating 85% of PV related to Cd accumulation were reported on LG 7 in rice (Ueno et al., 2009b). Afterward, QTL qGCd7 found on LG 7 explained 35.5% of phenotypic variation by analyzing backcross inbred lines developed by crossing Sasanishiki (japonica) with Habataki (indica). Major QTL qlGCd3 controlling Cd levels in rice grains was discovered by mapping CSSLs developed from a cross between LAC23 and Koshihikari (Abe et al., 2013). A total of 18 Cd-accumulating QTLs in milled rice and 14 in brown rice were reported to be located on LGs 2, 3, 4, 5, and 7 (Da-wei et al., 2018).

Luo et al. (2018) demonstrated CAL1 as a QTL in rice causing 13% change in Cd accumulation in leaves of a double haploid population. CAL1 is responsible for Cd translocation from root to shoot, and rice mutants with CAL1 knockout displayed decreased Cd concentration in leaves (Luo et al., 2018). Cd-accumulating QTLs were mapped in rice by growing an inbred population (743/Katy) derived from Xiang in soil contaminated with Cd revealing two QTLs, i.e., qCd-7 and qCd-2 involved in the process of Cd uptake and accumulation in rice (Li W. et al., 2016; McCouch et al., 2016). Sato et al. (2011) discovered two QTLs in brown rice affecting Cd accumulation, i.e., qLCdG11 and qLCdG3, explaining 9.4–12.9 and 8.3–13.9% of phenotypic variation, respectively. Five most important QTLs were discovered; three of them (gcc3, gcc9, and gcc1) were responsible for grain Cd concentration; scc10 was linked with Cd accumulation in shoots, and the QTL sgr5 was involved in supply of Cd to roots and shoots. Grain Cd accumulation was highly influenced by Srg5 in rice (Abe et al., 2013).

In durum wheat, the gene Cdu1 plays a role in Cd uptake, as reported by Knox et al. (2009), whereas Wiebe et al. (2010) illustrated the role of Cdu1 in accumulation of Cd in wheat grains. Recently, a major QTL on 5BL has been located in durum wheat controlling 54.3% PV for Cd uptake with the help of high-density genotyping (AbuHammad et al., 2016). In an RIL population developed by crossing Divide with D041735, another QTL, “QCdu. ndsu-5B,” has been discovered on 5B for Cd intake and tolerance. In soybean, a QTL for lower accumulation of Cd has been mapped on LGK controlling up to 57.3% of phenotypic variation (Jegadeesan et al., 2010).

Association Studies to Check Plant Response to Cadmium Stress

Advancement in methods used for genome mapping has led to revelation of various significant market trait associations (SMTAs) present in genomes for several traits including Cd intoxication (Huang and Han, 2014). Additionally, elucidation of crop genomes and other techniques, such as genome resequencing and genotyping by sequencing (GNB) to identify SNPs has helped in performing GWAS to study complex plant traits, i.e., HM toxicity and tolerance. Six SMTAs (such as pdil5-1, TaAP2-B, TaAP2-D, DME-5A, and Acc-1) related to genes controlling Cd tolerance were revealed in 235 accessions of Aegilops tauschii by GWAS using 7,185 SNPs.

A total of 17 QTLs for grain Cd accumulation were discovered in rice by GWAS conducted on 276 rice accessions using 416 K SNPs (Liu et al., 2019). A total of 312 out of 1,568 accessions of rice displaying more diversity were selected and evaluated to develop low Cd accumulating germplasm (Li W. et al., 2016; McCouch et al., 2016). Twenty-four rice accessions including 3 Indica accessions linked with reduced accumulation of Cd by up to 0.2 mg kg–1 were selected based on GWAS. A total of 312 accessions including subpopulations of Indica and Japonica rice were analyzed, leading to discovery of 28 QTLs related to Cd uptake and accumulation in plant tissues. Genes, i.e., OsNRAMP5, OsNRAMP1, OsLCD, and OsHMA3, that have been already discovered were also reported in recent GWASs (Li W. et al., 2016; McCouch et al., 2016).

A GWAS was carried out on 100 barley accessions and resulted in identification of several QTLs, i.e., 9 for root Cd accumulation, 21 for shoot Cd, 14 for transport of Cd from roots to shoots, and 15 for grain Cd amassment (Wu et al., 2015). Recently, 63 SMTAs on 5 LGs for leaf Cd were discovered in maize by GWAS using 43,737 SNPs (Zhao et al., 2018). This study also revealed several genes such as GRMZM2G45549 and GRMZM2G124103 coding for vacuolar ATPase, and GRMZM2G175576 for ATPase controlling Zn/Cd transport. Identification of specific DNA markers and accurate phenotyping techniques for study of Cd stress in crop plants will help in better understanding of Cd accumulation mechanism and improvement of genotypes for Cd tolerance.

Cadmium Phytoremediation by Overexpression of Genes

Introduction and overexpression of genes associated with metal uptake and translocation are the most effective and commonly used methods for phytoremediation using transgenics (Shukla et al., 2013; Mani and Kumar, 2014; Das et al., 2016). Various pathways including metal intake by roots, formation of metal-ligands and metal-chelator complexes, deposition of metals in vacuole, and long-distance translocation to shoots through symplast and apoplast can be exploited to enhance metal accumulation in plant tissues, as metal intake is a complex process (Nakamura et al., 2014; Das and Jayalekshmy, 2015). Genes coding for metal ion transporters and chelators are being used to manipulate plant metal uptake and translocation.

Metal transporters are also linked to gene families coding for ZIP proteins that are involved in Fe and Zn transport in cytoplasm. Conolly et al. (2002) reported 150% enhanced accumulation of Cd and Zn when gene coding for AtIRT1 was overexpressed in A. thaliana. However, some ZIP genes are highly specific, and their overexpression does not lead to improved accumulation of HMs like Cd (Tiong et al., 2014). Therefore, another strategy has been exploited in which genes coding for metal transporters and involved in microelements uptake and transport are transformed into plants. When absorption microelements are increased, HM uptake is reduced. These genes manipulate plant’s ability to collect HMs by enhancing or decreasing the effect of ZIP genes. This method may be utilized for phytoremediation of soil contaminated with HMs and for biofortification of crops (Siemianowski et al., 2014; Gong et al., 2015).

Nakamura et al. (2014) developed transgenic plants of Nicotine tabacum by overexpression of cysteine synthase (CS) and serine acetyltransferase (SAT) involved in cysteine biosynthesis. The plants produced by overexpression of these genes displayed enhanced Cd tolerance. He et al. (2016) inserted a homologous corn gene in Arabidopsis by activating methyltransferase gene (CIMT1 protein). Results displayed enhanced Cd tolerance in Arabidopsis by the overexpression of this gene. This gene could be utilized to enhance Cd tolerance in agricultural crops. Lee and Back (2017) overexpressed melatonin-related genes using transgenic OsSNAT1 in rice. The study revealed that transgenic OsSNAT1 provides tolerance to Cd. An expansin gene, TaEXPA2, was isolated from wheat and overexpressed in tobacco plants. This enhanced tolerance to Cd toxicity in tobacco plants and improved seed germination and growth of seedling and roots (Ren et al., 2018).

Expression of OXS3 (OXIDATIVE STRESS 3)-like gene fragments led to reduced accumulation of Cd in rice grains and other plant tissues without affecting yield and amount of minerals, i.e., Cu, Mn, Zn, and Fe (Blanvillain et al., 2009). Hence, this approach seems to be promising for production of Cd-tolerant genotypes without any loss in yield or minerals. OsHMA3 was involved in the transport of Zn to the vacuoles in root cells (Sasaki et al., 2012). The expression of OsHMA3 along with the OsHMA2 promoter had no effect on the growth of plants in vegetative stage. Moreover, when OsHMA3 was expressed under OsHMA2 control, the expression and localization of OsHMA3 in tissues were increased, and significant reduction in Cd concentration was observed because of increased Cd sequestration in roots, nodes, and vacuoles (Shao et al., 2018).

The functional gene OsHMA3 from rice was overexpressed in wheat for Cd sequestration in roots. Cd accumulation in roots was enhanced by up to 110–125%. Reduction in Cd accumulation in wheat grains was observed to be up to 40-folds, while translocation of Cd from roots to shoots was decreased by approximately 10-folds (Zhang L. et al., 2020). This technique offers an effective solution to reduce Cd accumulation in plants, leading to reduced health risks.

Clustered Regularly Interspaced Short Palindromic Repeats/Cas9-Based Genome Editing to Reduce Cadmium Accumulation

Genome editing tools like clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated protein 9 (Cas9) systems (CRISPR/Cas9) can be used for Cd tolerance in plants, i.e., rice (Ishizaki, 2016; Jung et al., 2018). It is possible to develop genotypes with low Cd accumulation without affecting plant growth and yield by developing mutants with transporters having low Cd affinity, such as OsNramp5 and OsLCT1, using the CRISPR/Cas9 technology. Recently, another approach has been discovered that may be helpful in getting desired results, and it involve deletion of large DNA fragments using CRISPR/Cas9.

Conclusion

Higher uptake of Cd leads to toxicity in plants, and reduction of Cd uptake by plants is also imperative for ensuring food safety. As a result, plants that are confined in their habitat are more likely to be exposed to Cd toxicity, which negatively impacts all growth- and yield-related characteristics, resulting in substantial economic losses. In this review, we discussed that plants have an efficient biochemical defense mechanism and utilize numerous physiological and molecular processes to deal with increased Cd exposure to offset its inhibitory effects. Exclusion of excess Cd at the root level, vacuolar sequestration, enzymatic detoxification, and preservation of essential cations are some of the techniques utilized to reduce Cd2+, which are significant disadvantages of Cd toxicity. Cd toxicity can also be reduced using various remediation techniques such as phytoremediation, PGPR inoculation, microbial-assisted remediation, chemical remediation, nutrients utilization, and organic amendments. Moreover, through genetic engineering and molecular breeding, capacity for remediation and tolerance to Cd toxicity can be improved. This review covers all probable processes of Cd toxicity remediation approaches; however there are still some information gaps. As a result, further research is needed to investigate Cd toxicity at the grain level, as well as its impacts on other living biota and the mechanisms of its tolerance at the cell and organelle levels. Significant and consistent QTLs for Cd tolerance were discovered in mapping populations with various genetic origins, as well as chosen donors, which indicated a significant promise for application in improved breeding methods. Although many efforts have been made to reduce Cd toxicity in plants, further research should be carried out by keeping these points in focus. There is a need to identify Cd toxicity pathways at molecular levels for better understanding of Cd toxicity. More detailed studies are required to understand the mechanism of different amendments in reducing Cd toxicity in plants. There is a need for a multidisciplinary approach to identify key target tolerance traits with improved high-throughput screening techniques that can provide valuable insights into the underlying mechanisms of Cd tolerance and homeostasis, especially in agronomic crops, for a better understanding of the genetics of Cd tolerance. To draw a sound conclusion, long-term field trials are required for estimation of a risk and benefit analysis for various management strategies.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Statements

Author contributions

UZ, WJ, and AM: conceptualization. WX and MN: methodology. JK and SH: software. MA: resources. MM and MK: data curation. UZ and FH: writing (original draft preparation). AM, JK, MB, MN, WX, and MI: writing (review and editing). NA and NF: visualization. MI and SH: supervision. MB and MK: project administration. All authors read and agreed to the published version of the manuscript.

Funding

This study was supported by a project of Ministry of Education, Youth and Sports of the Czech Republic (Grant No: FCH-S-21-7398).

Acknowledgments

The authors highly acknowledge the Institute of Soil and Environmental Sciences, and the Department of Agronomy, University of Agriculture Faisalabad, Pakistan.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  • 1

    AbbasA.AzeemM.NaveedM.LatifA.BashirS.AliA.et al (2020). Synergistic use of biochar and acidified manure for improving growth of maize in chromium contaminated soil.Int. J. Phytoremed.225261. 10.1080/15226514.2019.1644286

  • 2

    AbbasT.RizwanM.AliS.AdreesM.Zia-ur-RehmanM.QayyumM. F.et al (2017). Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil.Environ. Sci. Pollut. Res.252566825680. 10.1007/s11356-017-8987-4

  • 3

    AbbasT.RizwanM.AliS.AdreesM.MahmoodA.Zia-ur-RehmanM.et al (2018). Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil.Ecotoxicol. Environ. Saf.148825833. 10.1016/j.ecoenv.2017.11.063

  • 4

    AbbasiS.SadeghiA.SafaieN. (2020). Streptomyces alleviate drought stress in tomato plants and modulate the expression of transcription factors ERF1 and WRKY70 genes.Sci. Hortic.265:109206.

  • 5

    Abd El-MageedT. A.El- SamnoudiI. M.IbrahimA. M.Abd El TawwabA. R. (2018). Compost and mulching modulates morphological, physiological responses and water use efficiency in sorghum (bicolor L. Moench) under low moisture regime.Agric. Water Manage.208431439.

  • 6

    Abdel-LatefA. A. H.HashemA.RasoolS.AbdallahE. F.AlqarawiA.EgamberdievaD.et al (2016). Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review.J. Plant Biol.59407426.

  • 7

    Abd-El-MageedT. A.El-SherifA. M.Abd El-MageedS. A.AbdouN. M. (2019). A novel compost alleviate drought stress for sugar beet production grown in Cd-contaminated saline soil.Agric. Water Manag.226:105831.

  • 8

    AbeT.NonoueY.OnoN.OmotenoM.KuramataM.FukuokaS.et al (2013). Detection of QTLs to reduce cadmium content in rice grains using LAC23/Koshihikari chromosome segment substitution lines.Breed. Sci.63284291. 10.1270/jsbbs.63.284

  • 9

    AbozeidA.YingZ.LinY.LiuJ.ZhangZ.TangZ. (2017). Ethylene improves root system development under cadmium stress by modulating superoxide anion concentration in Arabidopsis thaliana.Front. Plant Sci.8:253.

  • 10

    AbuHammadW. A.MamidiS.KumarA.PirseyediS.MantheyF. A.KianianS. F.et al (2016). Identification and validation of a major cadmium accumulation locus and closely associated SNP markers in North Dakota durum wheat cultivars.Mol. Breed.36:112.

  • 11

    AderholtM.VogelienD. L.KoetherM.GreipssonS. (2017). Phyto- extraction of contaminated urban soils by Panicum virgatum L. enhanced with application of a plant growth regulator (BAP) and citric acid.Chemosphere1758596. 10.1016/j.chemosphere.2017.02.022

  • 12

    AdilM. F.SeharS.ChenG.ChenZ. H.JilaniG.ChaudhryA. N.et al (2020). Cadmium-zinc cross-talk delineates toxicity tolerance in rice via differential genes expression and physiological/ultrastructural adjustments.Ecotoxicol. Environ. Saf.190:110076. 10.1016/j.ecoenv.2019.110076

  • 13

    AfzalM.YuM.TangC.ZhangL.MuhammadN.ZhaoH.et al (2019). The negative impact of cadmium on nitrogen transformation processes in a paddy soil is greater under non-flooding than flooding conditions.Environ. Int.129451460. 10.1016/j.envint.2019.05.058

  • 14

    AhemadM. (2014). Remediation of metalliferous soils through the heavy metal resistant plant growth promoting bacteria: paradigms and prospects.Arab. J. Chem.1213651377. 10.1016/j.arabjc.2014.11.020

  • 15

    AhmadJ.AliA. A.BaigM. A.IqbalM.HaqI.QureshiM. I. (2018). “Role of phytochelatins in cadmium stress tolerance in plants,” in Cadmium Toxicity and Tolerance in Plants, edsHasanuzzamanM.PrasadM. N. V.FujitaM. (Cambridge, MA: Academic Press).

  • 16

    AhmadM. T.AsgharH. N.SaleemM.KhanM. Y.ZahirZ. A. (2015). Synergistic effect of rhizobia and biochar on growth and physiology of maize.Agron. J.10718.

  • 17

    AhmadP.AlyemeniM. N.VijayaL.AlamP.AhangerM. A.AlamriS. A. (2017). Jasmonic acid alleviates negative impacts of cadmium stress by modifying osmolytes and antioxidants in faba bean (Vicia faba L.).Arch. Agron. Soil Sci.6318891899. 10.1080/03650340.2017.1313406

  • 18

    AhmadP.NabiG.AshrafM. (2011). Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) czern. &coss.] plants can be alleviated by salicylic acid.S. Afr. J. Bot.773644. 10.1016/j.sajb.2010.05.003

  • 19

    AhmadS. H.ReshiZ.AhmadJ.IqbalM. (2005). Morpho-anatomical responses of Trigonellafoenum graecum Linn. to induced cadmium and lead stress.J. Plant Biol.486484. 10.1007/bf03030566

  • 20

    AkhterZ.BiZ.AliK.SunC.FiazS.HaiderF. U.et al (2021). In response to abiotic stress, DNA methylation confers epi-genetic changes in plants.Plants10:1096. 10.3390/plants10061096

  • 21

    AliB.GillR. A.YangS.GillM. B.FarooqM. A.LiuD.et al (2015). Regulation of cadmium-induced proteomic and metabolic changes by 5- aminolevulinic acid in leaves of Brassica napus L.PLoS One10:e0123328. 10.1371/journal.pone.0123328

  • 22

    AlleV.KondratovicsU.OsvaldeA.VikmaneM. (2016). Differences in cadmium accumulation and induced changes in root anatomical structures in plants used for food.Agron Res.1412491260.

  • 23

    AlyemeniM. N.AhangerM. A.WijayaL.AlamP.BhardwajR.AhmadP. (2018). Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system.Protoplasma255459469. 10.1007/s00709-017-1162-4

  • 24

    AmirabadS. A.BehtashF.VafaeeY. (2020). Selenium mitigates cadmium toxicity by preventing oxidative stress and enhancing photosynthesis and micronutrient availability on radish (Raphanus sativus L.) cv. Cherry Belle.Environ. Sci. Pollut. Res.271247612490. 10.1007/s11356-020-07751-2

  • 25

    AmirahmadiE.HojjatiS. M.KammannC.GhorbaniM.BiparvaP. (2020). The potential effectiveness of biochar application to reduce soil Cd bioavailability and encourage oak seedling growth.Appl. Sci.10:3410. 10.3390/app10103410

  • 26

    AnjumS. A.TanveerM.HussainS.BaoM.WangL.KhanI.et al (2015). Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation.Environ. Sci. Pollut. Res.221702217030. 10.1007/s11356-015-4882-z

  • 27

    AnjumS. A.TanveerM.HussainS.UllahE.WangL.KhanI.et al (2016). Morpho-physiological growth and yield responses of two contrasting maize cultivars to cadmium exposure.CLEAN Soil Air Water442936. 10.1002/clen.201400905

  • 28

    AnuradhaS.RaoS. S. R. (2009). Effect of 24-epibrassinolide on the photosynthetic activity of radish plants under cadmium stress.Photosynthetica47317320. 10.1007/s11099-009-0050-3

  • 29

    AraoT.AeN.SugiyamaM.TakahashiM. (2003). Genotypic differences in cadmium uptake and distribution in soybeans.Plant Soil251247253. 10.1007/s00726-010-0809-7

  • 30

    AsgherM.KhanM. I. R.AnjumN. A.KhanN. A. (2015). Minimising toxicity of cadmium in plants—role of plant growth regulators.Protoplasma252399413. 10.1007/s00709-014-0710-4

  • 31

    AttintiR.BarrettK. R.DattaR.SarkarD. (2017). Ethylenediaminedisuccinic acid (EDDS) enhances phytoextraction of lead by vetiver grass from contaminated residential soils in a panel study in the field.Environ. Pollut.225524533. 10.1016/j.envpol.2017.01.088

  • 32

    AwasthiM. K.PandeyA. K.BundelaP. S.KhanJ. (2015). Co-composting of organic fraction of municipal solid waste mixed with different bulking waste: characterization of physicochemical parameters and microbial enzymatic dynamic.Bioresour. Technol.182200207. 10.1016/j.biortech.2015.01.104

  • 33

    BabadiM.ZalaghiR.TaghaviM. (2019). A non-toxic polymer enhances sorghum mycorrhiza symbiosis for bioremediation of Cd.Mycorrhiza29375387. 10.1007/s00572-019-00902-5

  • 34

    BagheriV.ShamshiriM. H.ShiraniH.RoostaH. R. (2012). Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress.J. Agric. Sci. Technol.1415911604.

  • 35

    BalestriM.CeccariniA.ForinoL. M. C.ZelkoI.MartinkaM.LuxA.et al (2014). Cadmium uptake, localization and stress-induced morphogenic response in the fern Pteris vittata.Planta23910551064. 10.1007/s00425-014-2036-z

  • 36

    BariM. A.AktherM. S.RezaM. A.KabirA. H. (2019). Cadmium tolerance is associated with the root-driven coordination of cadmium sequestration, iron regulation, and ROS scavenging in rice.Plant Physiol. Biochem.1362233. 10.1016/j.plaphy.2019.01.007

  • 37

    BashirA.RizwanM.Zia-ur-RehmanM.ZubairM.RiazM.QayyumM. F.et al (2020). Application of co-composted farm manure and biochar increased the wheat growth and decreased cadmium accumulation in plants under different water regimes.Chemosphere246110. 10.1016/j.chemosphere.2019.125809

  • 38

    BashirS.GulshanA. B.IqbalJ.HusainA.AlwahibiM. S.AlkahtaniJ.et al (2021). Comparative role of animal manure and vegetable waste induced compost for polluted soil restoration and maize growth.Saudi J. Biol. Sci.2825342539. 10.1016/j.sjbs.2021.01.057

  • 39

    BashirS.RizwanM. S.SalamA.FuQ.ZhuJ.ShaabanM.et al (2018). Cadmium immobilization potential of rice straw-derived biochar, zeolite and rock phosphate: extraction techniques and adsorption mechanism.Bull. Environ. Contam. Toxicol.100727732. 10.1007/s00128-018-2310-z

  • 40

    BhargavaA.CarmonaF. F.BhargavaM.SrivastavaS. (2012). Approaches for enhanced phytoextraction of heavy metals.J. Environ. Manag.105103120. 10.1016/j.jenvman.2012.04.002

  • 41

    BianR. J.LiL. Q.BaoD. D.ZhengJ. W.ZhangX. H.ZhengJ. F.et al (2016). Cd immobilization in a contaminated rice paddy by inorganic stabilizers of calcium hydroxide and silicon slag and by organic stabilizer of biochar.Environ. Sci. Pollut. Res.231002810036. 10.1007/s11356-016-6214-3

  • 42

    BlanvillainR.KimJ. H.WuS.LimaA.OwD. W. (2009). OXIDATIVE STRESS 3 is a chromatin-associated factor involved in tolerance to heavy metals and oxidative stress.Plant J.57654665.

  • 43

    BloemE.HaneklausS.HaenschR.SchnugE. (2016). EDTA application on agricultural soils affects microelement uptake of plants.Sci. Total Environ.577166173. 10.1016/j.scitotenv.2016.10.153

  • 44

    BojorquezC.Frias-EspericuetaM. G.VoltolinaD. (2016). Removal of cadmium and lead by adapted strains of Pseudomonas aeruginosa and Enterobacter cloacae.Rev. Int. Contam. Ambient.32407412.

  • 45

    BoostaniH. R.Najafi-GhiriM.MirsoleimaniA. (2019). The effect of biochars application on reducing the toxic effects of nickel and growth indices of spinach (Spinacia oleracea L.) in a calcareous soil.Environ. Sci. Pollut. Res.2617511760. 10.1007/s11356-018-3760-x

  • 46

    BoraM. S.SarmaK. P. (2021). Anatomical and ultrastructural alterations in Ceratopterispteridoides under cadmium stress: a mechanism of cadmium tolerance.Ecotoxicol. Environ. Saf.218:112285. 10.1016/j.ecoenv.2021.112285

  • 47

    BulakP.WalkiewiczA.BrzezińskaM. (2014). Plant growth regulators- assisted phytoextraction.Biol. Plant5818. 10.1007/s10535-013-0382-5

  • 48

    ÇanakciS.DursunB. (2012). The effect of pre-application of salicylic acid on some physiological and biochemical characteristics of tomato seedling (Lycopersicon esculentum L) growing in cadmium containing media.Afr. J. Biotechnol.1131733178. 10.5897/AJB11.2364

  • 49

    CaoB. I.MaQ.ZhaoQ.WangL.XuK. (2015). Effects of silicon on absorbed light allocation, antioxidant enzymes and ultrastructure of chloroplasts in tomato leaves under simulated drought stress.Sci. Hort.1945362. 10.1016/j.scienta.2015.07.037

  • 50

    ChangQ.WeiD. F.FanW. Q.PanL.HuaD. Z.GuoW. (2018). Effects of arbuscular mycorrhizal symbiosis on growth, nutrient and metal uptake by maize seedlings (Zea mays L.) grown in soils spiked with lanthanum and cadmium.Environ. Pollut.241607615. 10.1016/j.envpol.2018.06.003

  • 51

    ChellaiahE. R. (2018). Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: a mini-review.Appl. Water Sci.8:154. 10.1007/s13201-018-0796-5

  • 52

    ChenB.LuoS.WuY.YeJ.WangQ.XuX.et al (2017). The effects of the endophytic bacterium Pseudomonas fluorescens sasm05 and IAA on the plant growth and cadmium uptake of Sedum alfredii Hance.Front. Microbiol.8:253. 10.3389/fmicb.2017.02538

  • 53

    ChenC.-T.ChenT.-H.LoK.-F.ChiuC.-Y. (2004). Effects of proline on copper transport in rice seedlings under excess copper stress.Plant Sci.166103111. 10.1016/j.plantsci.2003.08.015

  • 54

    ChenH.YangX.GielenG.MandalS.XuS.GuoJ.et al (2019). Effect of biochars on the bioavailability of cadmium and di-(2-ethylhexyl) phthalate to Brassica chinensis L. in contaminated soils.Sci. Total Environ.6784352. 10.1016/j.scitotenv.2019.04.417

  • 55

    ChenL.LongC.WangD.YangJ. (2020). Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators.Chemosphere242:125112. 10.1016/j.chemosphere.2019.125112

  • 56

    ChenQ.LuX.GuoX.PanY.YuB.TangZ.et al (2018a). Differential responses to Cd stress induced by exogenous application of Cu, Zn or Ca in the medicinal plant Catharanthus roseus.Ecotoxicol. Environ. Saf.157266275. 10.1016/j.ecoenv.2018.03.055

  • 57

    ChenH.YangX.WangP.WangZ.LiM.ZhaoF. J. (2018b). Dietary cadmium intake from rice and vegetables and potential health risk: a case study in Xiangtan, southern China.Sci. Total Environ.639271277. 10.1016/j.scitotenv.2018.05.050

  • 58

    ChenH.ZhangW.YangX.WangP.McGrathS. P.ZhaoF. J. (2018c). Effective methods to reduce cadmium accumulation in rice grain.Chemosphere207699707. 10.1016/j.chemosphere.2018.05.143

  • 59

    ChenZ.ZhaoY.FanL.XingL.YangY. (2015). Cadmium (Cd) localization in tissues of cotton (Gossypium hirsutum L.), and its phytoremediation potential for Cd-contaminated soils.Bull. Environ. Contam. Toxicol.95784789. 10.1007/s00128-015-1662-x

  • 60

    ChoppalaG.Saifullah, BolanN.BibiS.IqbalM.RengelZ.et al (2014). Cellular mechanisms in higher plants governing tolerance to cadmium toxicity.Crit. Rev. Plant Sci.33374391. 10.1016/j.ecoenv.2015.06.003

  • 61

    ClabeauxB. L.NavarroD. A. G.AgaD. S.BissonM. A. (2011). Cd tolerance and accumulation in the aquatic macrophyte, Chara australis: potential use for charophytes in phytoremediation.Environ. Sci. Technol.4553325338. 10.1021/es200720u

  • 62

    ClarkeJ. M.NorvellW. A.ClarkeF. R.BuckleyW. T. (2002). Concentration of cadmium and other elements in the grain of near-isogenic durum lines.Can. J. Plant Sci.822733. 10.1021/acs.jafc.7b01946

  • 63

    ConollyE. L.FettJ. P.GuerinotM. L. (2002). Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation.Plant Cell1413471357. 10.1105/tpc.001263

  • 64

    CuiG.AiS.ChenK.WangX. (2019). Arbuscular mycorrhiza augments cadmium tolerance in soybean by altering accumulation and partitioning of nutrient elements, and related gene expression.Ecotoxicol. Environ. Saf.171231239. 10.1016/j.ecoenv.2018.12.093

  • 65

    CuypersA.HendrixS.Amaral dos ReisR.De SmetS.DeckersJ.GielenH.et al (2016). Hydrogen peroxide, signaling in disguise during metal phytotoxicity.Front. Plant Sci.7:470. 10.3389/fpls.2016.00470

  • 66

    CuypersA.PlusquinM.RemansT.JozefczakM.KeunenE.GielenH.et al (2010). Cadmium stress: an oxidative challenge.Biometals23927940. 10.1007/s10534-010-9329-x

  • 67

    da Silva CunhaL. F.de OliveiraV. P.do NascimentoA. W. S.da SilvaB. R. S.BatistaB. L.AlsahliA. A.et al (2020). Leaf application of 24-epibrassinolide mitigates cadmium toxicity in young Eucalyptus urophylla plants by modulating leaf anatomy and gas exchange.Physiol. Plant1736787. 10.1111/ppl.13182

  • 68

    DadF. P.KhanW. U. D.TanveerM.RamzaniP. M. A.ShaukatR.MuktadirA. (2020). Influence of iron-enriched biochar on Cd sorption, its ionic concentration and redox regulation of radish under cadmium toxicity.Agriculture11:1. 10.3390/agriculture11010001

  • 69

    DasN.BhattacharyaS.MaitiM. K. (2016). Enhanced cadmium accumulation and tolerance in transgenic tobacco overexpressing rice metal tolerance protein gene OsMTP1 is promising for phytore mediation.Plant Physiol. Biochem.105297309. 10.1016/j.plaphy.2016.04.049

  • 70

    DasR.JayalekshmyV. G. (2015). Mechanism of heavy metal tolerance and improvement of tolerance in crop plants.J. Glob. Biosci.426782698.

  • 71

    Da-weiH.Zhong-huaS.Qian-longL.WeiC.Xiang-jinW.et al (2018). Identification of QTLs associated with cadmium concentration in rice grains. J. Integr. Agric. 17, 6034560347.

  • 72

    DobrikovaA. G.ApostolovaE. L.HanćA.YotsovaE.BorisovaP.SperdouliI.et al (2021). Cadmium toxicity in Salvia sclarea L.: an integrative response of element uptake, oxidative stress markers, leaf structure and photosynthesis.Ecotoxicol. Environ. Saf.209:111851. 10.1016/j.ecoenv.2020.111851

  • 73

    EissaM. A. (2019). Effect of compost and biochar on heavy metals phytostabilization by the halophytic plant old man saltbush [Atriplex nummularia Lindl].Soil Sediment. Contam.28135147. 10.1080/15320383.2018.1551325

  • 74

    ElhitiM.YangC.ChanA.DurninD. C.BelmonteM. F.AyeleB. T.et al (2012). Altered seed oil and glucosinolate levels in transgenic plants overexpressing the Brassica napus SHOOTMERISTEMLESS gene.J. Exp. Bot.6344474461. 10.1093/jxb/ers125

  • 75

    EliasE. M.MantheyF. (2016). Registration of ‘Joppa’ durum wheat.J. Plant Regist.10139144. 10.3198/jpr2015.11.0071crc

  • 76

    EliasE. M.MantheyF.AbuHammadW. (2015). Registration of ‘Carpio’ durum wheat.J. Plant Regist.97882. 10.3198/jpr2014.05.0030crc

  • 77

    ElobeidM.GöbelC.FeussnerI.PolleA. (2012). Cadmium interferes with auxin physiology and lignification in poplar.J. Exp. Bot.6314131421. 10.1093/jxb/err384

  • 78

    ElyamineA. M.MoussaM. G.AfzalJ.RanaM. S.ImranM.ZhaoX.et al (2019). Modified rice straw enhanced cadmium (ii) immobilization in soil and promoted the degradation of phenanthrene in co-contaminated soil.Int. J. Mol. Sci.20:2189. 10.3390/ijms20092189

  • 79

    ErdemH. (2021). The effects of biochars produced in different pyrolysis temperatures from agricultural wastes on cadmium uptake of tobacco plant.Saudi J. Biol. Sci.2839653971. 10.1016/j.sjbs.2021.04.016

  • 80

    EvangelouM. W. H.EbelM.SchaefferA. (2007). Chelate assisted phytoextraction of heavy metals from soil: effect, mechanism, toxicity, and fate of chelating agents.Chemosphere689891003. 10.1016/j.chemosphere.2007.01.062

  • 81

    FarooqH.AsgharH. N.KhanM. Y.SaleemM.ZahirZ. A. (2015). Auxin-mediated growth of rice in cadmium-contaminated soil.Turk. J. Agric. For.39272276. 10.3906/tar-1405-54

  • 82

    FarooqM.UllahA.UsmanM.SiddiqueK. H. M. (2020). Application of zinc and biochar help to mitigate cadmium stress in bread wheat raised from seeds with high intrinsic zinc.Chemosphere260:127652. 10.1016/j.chemosphere.2020.127652

  • 83

    FarooqM. A.NiaziA. K.AkhtarJ.FarooqM.SouriZ.KarimiN.et al (2019). Acquiring control: the evolution of ROS-Induced oxidative stress and redox signaling pathways in plant stress responses.Plant Physiol. Biochem.141353369. 10.1016/j.plaphy.2019.04.039

  • 84

    FrenchK. E. (2017). Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health.Front. Microbiol.8:1403. 10.3389/fmicb.2017.01403

  • 85

    GallegoS. M.PenaL. B.BarciaR. A.AzpilicuetaC. E.IannoneM. F.RosalesE. P.et al (2012). Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms.Environ. Exp. Bot.833346. 10.1016/j.jhazmat.2017.04.058

  • 86

    GarcíaA. C.TavaresO. C. H.de OliveiraD. F. (2020). Biochar as agricultural alternative to protect the rice plant growth in fragile sandy soil contaminated with cadmium.Biocatal. Agric. Biotechnol.29:101829. 10.1016/j.bcab.2020.101829

  • 87

    GargN.ChandelS. (2015). Role of arbuscular mycorrhiza in arresting reactive oxygen species (ROS) and strengthening antioxidant defense in Cajanus cajan (L.) Millsp. nodules under salinity (NaCl) and cadmium (Cd) stress.Plant Growth Regul.75521534. 10.1007/s10725-014-0016-8

  • 88

    GenchiG.SinicropiM. S.LauriaG.CarocciA.CatalanoA. (2020). The effects of cadmium toxicity.Int. J. Environ. Res. Public Health17:3782.

  • 89

    GerszbergA.Hnatuszko-KonkaK. (2017). Tomato tolerance to abiotic stress: a review of most often engineered target sequences.Plant Growth Regul.83175198. 10.1007/s10725-017-0251-x

  • 90

    GhaniA. (2011). Varietal differences in canola (Brassica napus L.) for the growth, yield and yield components exposed to cadmium stress.J. Anim. Plant Sci.215759.

  • 91

    GhassemiH. R.MostajeranA. (2018). TASOS1 and TATM20 genes expression and nutrient uptake in wheat seedlings may be altered via excess cadmium exposure and inoculation with Azospirillumbrasilense sp7 under saline condition.Appl. Ecol. Environ. Res.1617971817. 10.15666/aeer/1602_17971817

  • 92

    GillS. S.KhanN. A.TutejaN. (2011). Differential cadmium stress tolerance in five Indian mustard (Brassica juncea L.) cultivars: an evaluation of the role of antioxidant machinery.Plant Signal. Behav.6293300. 10.4161/psb.6.2.15049

  • 93

    GlickB. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world.Microbiol. Res.1693039. 10.1016/j.micres.2013.09.009

  • 94

    GoelS.GautamA. (2010). Effect of chelating agents on mobilization of metal from waste catalyst.Hydrometallurgy101120125.

  • 95

    GoixS.LévêqueT.XiongT. T.SchreckE.Baeza-SquibanA.GeretF.et al (2014). Environmental and health impacts of fine and ultrafine metallic particles: assessment of threat scores.Environ. Res.133185194. 10.1016/j.envres.2014.05.015

  • 96

    GoncalvesJ. F.NicolosoF. T.BeckerA. G.PereiraL. B.TabaldiL. A.CargneluttiD.et al (2009). Photosynthetic pigments content, δ-aminolevulinic acid dehydratase and acid phosphatase activities and mineral nutrients concentration in cadmium-exposed Cucumis sativus L.J. Biol.64310318. 10.2478/s11756-009-0034-6

  • 97

    GondorO. K.PálM.DarkóÉJandaT.SzalaiG. (2016). Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.).PLoS One11:e0160157. 10.1371/journal.pone.0160157

  • 98

    GongX.YinL.ChenJ.GuC. (2015). Overexpression of the iron transporter NtPIC1 in tobacco mediates tolerance to cadmium.Plant Cell Rep.3419631973. 10.1007/s00299-015-1843-4

  • 99

    GoswamiD.ThakkerJ. N.DhandhukiaP. C. (2016). Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review.Cogent. Food Agric.2:1127500.

  • 100

    GothbergA.GregerE.HolmK.BengtssonB. E. (2004). Influence of nutrient levels on uptake and effects of mercury, cadmium, and lead in water spinach.J. Environ. Qual.3312471255. 10.2134/jeq2004.1247

  • 101

    GouiaH.SuzukiA.BrulfertJ.GhorbalM. H. (2003). Effects of cadmium on the co-ordination of nitrogen and carbon metabolism in bean seedlings.J. Plant Physiol.160367376. 10.1078/0176-1617-00785

  • 102

    GruznovaK. A.BashmakovD. I.MiliauskieneJ.VastakaiteV.DuchovskisP.LukatkinA. S. (2018). The effect of a growth regulator Ribav-Extra on winter wheat seedlings exposed to heavy metals.Zemdirbyste105227234. 10.13080/z-a.2018.105.029

  • 103

    GulS.NazA.KhanA.NisaS.IrshadM. (2016). Phytoavailability and leachability of heavy metals from contaminated soil treated with composted livestock manure.Soil Sediment. Contam.25181194. 10.1080/15320383.2016.1112361

  • 104

    GuoB.LiuC.LiangY.LiN.FuQ. (2019). Salicylic acid signals plant defence against cadmium toxicity.Int. J. Mol. Sci.20:2960. 10.3390/ijms20122960

  • 105

    GuoH.HongC.ChenX.XuY.LiuY.JiangD.et al (2016). Different growth and physiological responses to cadmium of the three Miscanthus species.PLoS One11:e0153475. 10.1371/journal.pone.0153475

  • 106

    GuoZ. H.MiaoX. F. (2010). Growth changes and tissues anatomical characteristics of giant reed (Arundo donax L.) in soil contaminated with arsenic, cadmium and lead.J. Central S. Univ. Technol.17770777. 10.1007/s11771-010-0555-8

  • 107

    GusiatinZ. M.KlimiukE. (2012). Metal (Cu, Cd and Zn) removal and stabilization during multiple soil washing by saponin.Chemosphere86383391. 10.1016/j.chemosphere.2011.10.027

  • 108

    HabibaU.AliS.FaridM.ShakoorM. B.RizwanM.IbrahimM.et al (2015). EDTA enhanced plant growth, antioxidant defense system, and phytoextraction of copper by Brassica napus L.Environ. Sci. Pollut. Res.2215341544. 10.1007/s11356-014-3431-5

  • 109

    HafeezF.RizwanM.SaqibM.YasmeenT.AliS.AbbasT.et al (2019). Residual effect of biochar on growth, antioxidant defense and cadmium (Cd) accumulation in rice in a Cd contaminated saline soil.Pak. J. Agric. Sci.56197204.

  • 110

    HaiderF. U.CoulterJ. A.LiqunC.HussainS.CheemaS. A.WuJ.et al (2022). An overview on biochar production, its implications, and mechanisms of biochar-induced amelioration of soil and plant characteristics.Pedosphere32107130. 10.1016/S1002-0160(20)60094-7

  • 111

    HaiderF. U.LiqunC.CoulterJ. A.CheemaS. A.WuJ.ZhangR.et al (2021a). Cadmium toxicity in plants: impacts and remediation strategies.Ecotoxicol. Environ. Saf.211:111887. 10.1016/j.ecoenv.2020.111887

  • 112

    HaiderF. U.CoulterJ. A.CheemaS. A.FarooqM.WuJ.ZhangR.et al (2021b). Co-application of biochar and microorganisms improves soybean performance and remediate cadmium-contaminated soil.Ecotoxicol. Environ. Saf.214:112112. 10.1016/j.ecoenv.2021.112112

  • 113

    HajebP.SlothJ. J.ShakibazadehS.MahyudinN. A.Afsah-HejriL. (2014). Toxic elements in food: occurrence, binding, and reduction approaches.Compr. Rev. Food Sci. Food Saf.13457472. 10.1111/1541-4337.12068

  • 114

    HakmaouiA.AterM.BokaK.BaronM. (2007). Copper and cadmium tolerance, uptake and effect on chloroplast ultrastructure. Studies on Salix purpurea and Phragmites australis.Z. Naturforschung C62417426. 10.1515/znc-2007-5-616

  • 115

    HalimM. A.MajumderR. K.ZamanM. N. (2015). Paddy soil heavy metal contamination and uptake in rice plants from the adjacent area of Barapukuria coal mine, northwest Bangladesh.Arab. J. Geosci.833913401. 10.1007/s12517-014-1480-1

  • 116

    HamidY.TangL.HussainB.UsmanM.GurajalaH. K.RashidM. S.et al (2019). Efficiency of lime, biochar, Fe containing biochar and composite amendments for Cd and Pb immobilization in a co-contaminated alluvial soil.Environ. Pollut.257:113609. 10.1016/j.envpol.2019.113609

  • 117

    HamidY.TangL.HussainB.UsmanM.LinQ.RashidM. S.et al (2020a). Organic soil additives for the remediation of cadmium contaminated soil sand their impact on the soil-plant system: a review.Sci. Total Environ.707:136121. 10.1016/j.scitotenv.2019.136121

  • 118

    HamidY.TangL.HussainB.UsmanM.GurajalaH. K.RashidM. S.et al (2020b). Efficiency of lime, biochar, Fe containing biochar and composite amendments for Cd and Pb immobilization in a co-contaminated alluvial soil.Environ. Pollut.257:113609.

  • 119

    HanR. M.LefèvreI.AlbaceteA.Pérez-AlfoceaF.Barba-EspínG.Díaz-VivancosP.et al (2013). Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions.Physiol. Plant.147352368. 10.1111/j.1399-3054.2012.01667.x

  • 120

    HasanM.UddinM.Ara-SharmeenF.IAlharbyH.AlzahraniY.HakeemK. R.et al (2019). Assisting phytoremediation of heavy metals using chemical amendments.Plants8:295. 10.3390/plants8090295

  • 121

    HasanuzzamanM.AlhaithloulH.ParvinK.BhuyanM.TanveerM.MohsinS. M.et al (2019). Polyamine action under metal/metalloid stress: regulation of biosynthesis, metabolism, and molecular interactions.Int. J. Mol. Sci.20:3215. 10.3390/ijms20133215

  • 122

    HasanuzzamanM.BhuyanM.ZulfiqarF.RazaA.MohsinS. M.MahmudJ. A.et al (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator.Antioxidants9:681. 10.3390/antiox9080681

  • 123

    HashemA.AbdallahE. F.AlqarawiA. A.Al-HuqailA. A.EgamberdievaD.WirthS. (2016). Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance.Saudi J. Biol. Sci.23272281. 10.1016/j.sjbs.2015.11.002

  • 124

    HassanW.BanoR.BashirS.AslamZ. (2015). Cadmium toxicity and soil biological index under potato (Solanum tuberosum L.) cultivation.Soil Res.54460468.

  • 125

    HayatS.AliB.HasanS. A.AhmadA. (2007). Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea.Environ. Exp. Bot.603341. 10.1016/j.envexpbot.2006.06.002

  • 126

    HayatS.AlyemeniM. N.HasanS. A. (2012). Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress.Saudi J. Biol. Sci.19325335. 10.1016/j.sjbs.2012.03.005

  • 127

    HayatS.HasanS. A.HayatQ.AhmadA. (2010). Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach.Protoplasma239314. 10.1007/s00709-009-0075-2

  • 128

    HayatS.HayatQ.AlyemeniM. N.AhmadA. (2013). Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress.Acta Bot. Croatica72323335. 10.2478/v10184-012-0019-3

  • 129

    HeD.CuiJ.GaoM.WangW.ZhouJ.YangJ.et al (2019). Effects of soil amendments applied on cadmium availability, soil enzyme activity, and plant uptake in contaminated purple soil.Sci. Total Environ.65413641371. 10.1016/j.scitotenv.2018.11.059

  • 130

    HeJ.ZhuC.RenY.YanY.JiangD. (2006). Genotypic variation in grain cadmium concentration of lowland rice.J. Plant Nutr. Soil Sci.169711716. 10.1002/jpln.200525101

  • 131

    HeL.MaX.LiZ. (2016). Maize oxidative stress 2 homologs enhance cadmium tolerance in Arabidopsis through activation of a putative SAM-dependent methyltransferase gene.Plant Physiol.17116751685. 10.1104/pp.16.00220

  • 132

    HeS.WuQ.HeZ. (2014). Synergetic effects of DA-6/GA3 with EDTA on plant growth, extraction and detoxification of Cd by Lolium perenne.Chemosphere117132138. 10.1016/j.chemosphere.2014.06.015

  • 133

    HongK.TokunagaS.KajiuchiT. (2002). Evaluation of remediation process with plant derived biosurfactant for recovery of heavy metals from contaminated soils.Chemosphere49379387. 10.1016/S0045-6535(02)00321-1

  • 134

    HossainM. A.PiyatidaP.da SilvaJ. A. T.FujitaM. (2012). 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.2012:872875.

  • 135

    HuW.ZhangY.HuangB.TengY. (2017). Soil environmental quality in greenhouse vegetable production systems in eastern China: current status and management strategies.Chemosphere170183195. 10.1016/j.chemosphere.2016.12.047

  • 136

    HuX.LiuX.ZhangX.CaoL.ChenJ.YuH. (2017). Increased accumulation of Pb and Cd from contaminated soil with Scirpustriqueter by the combined application of NTA and APG.Chemosphere188397402. 10.1016/j.chemosphere.2017.08.173

  • 137

    HuangX.HanB. (2014). Natural variations and genome-wide association studies in crop plants.Annu. Rev. Plant Biol.65531551. 10.1146/annurev-arplant-050213-035715

  • 138

    HuangD. F.Ling-LinX.Li-NianY.Zhi-QinW.Jian-ChangY. (2008). Comparison of agronomic and physiological traits of rice genotypes differing in cadmium-tolerance.Acta Agron. Sin.34809817. 10.3724/sp.j.1006.2008.00809

  • 139

    HuangH.LuoL.HuangL.ZhangJ.GikasP.ZhouY. (2020). Effect of manure compost on distribution of Cu and Zn in rhizosphere soil and heavy metal accumulation by Brassica juncea.Water Air Soil Pollut.231110.

  • 140

    HuangJ.LiuZ.LiS.XuB.GongY.YangY.et al (2016). Isolation and engineering of plant growth promoting rhizobacteria Pseudomonas aeruginosa for enhanced cadmium bioremediation.J. Gen. Appl. Microbiol.62258265. 10.2323/jgam.2016.04.007

  • 141

    HuangQ.YuY.WanY.WangQ.LuoZ.QiaoY.et al (2018). Effects of continuous fertilization on bioavailability and fractionation of cadmium in soil and its uptake by rice (Oryza sativa L.).J. Environ. Manag.2151321. 10.1016/j.jenvman.2018.03.036

  • 142

    HuangX.HoS. H.ZhuS.MaF.WuJ.YangJ.et al (2017). Adaptive response of arbuscular mycorrhizal symbiosis to accumulation of elements and translocation in Phragmites australis affected by cadmium stress.J. Environ. Manag.197448455. 10.1016/j.jenvman.2017.04.014

  • 143

    HussainA.AliS.RizwanM.ur RehmanM. Z.JavedM. R.ImranM.et al (2018). Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants.Environ. Pollut.24215181526.

  • 144

    HussainB.AshrafM. N.AbbasA.LiJ.FarooqM. (2021). Cadmium stress in paddy fields: effects of soil conditions and remediation strategies.Sci. Total Environ.754:142188. 10.1016/j.scitotenv.2020.142188

  • 145

    HuybrechtsM.HendrixS.BertelsJ.BeemsterG. T. S.VandammeD.CuypersA. (2020). Spatial analysis of the rice leaf growth zone under controlled and cadmium-exposed conditions.Environ. Exp. Bot.177:104120. 10.1016/j.envexpbot.2020.104120

  • 146

    IbrahimM.LiG.ChanF. K. S.KayP.LiuX. X.FirbankL.et al (2019). Biochar effects potentially toxic elements and antioxidant enzymes in Lactuca sativa L. grown in multi-metals contaminated soil.Environ. Technol. Innov.15:100427.

  • 147

    IjazM.RizwanM. S.SarfrazM.Ul-AllahS.SherA.SattarA.et al (2020). Biochar reduced cadmium uptake and enhanced wheat productivity in alkaline contaminated soil.Int. J. Agric. Biol.2416331640. 10.17957/IJAB/15.1605

  • 148

    IshikawaS.AbeT.KuramataM.YamaguchiM.AndoT.YamamotoT.et al (2010). A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7.J. Exp. Bot.61923934. 10.1093/jxb/erp360

  • 149

    IshikawaS.AeN.YanoM. (2005). Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa).N. Phytol.168345350. 10.1111/j.1469-8137.2005.01516.x

  • 150

    IshizakiT. (2016). CRISPR/Cas9 in rice can induce new mutations in later generations, leading to chimerism and unpredicted segregation of the targeted mutation.Mol. Breed.36:165.

  • 151

    JaishankarM.TsetenT.AnbalaganN.MathewB. B.BeeregowdaK. N. (2014). Toxicity, mechanism and health effects of some heavy metals.Interdiscip. Toxicol.7:60. 10.2478/intox-2014-0009

  • 152

    JanS. U.JamalA.SabarM. A.OrtasI.IsikM.AksahinV.et al (2020). Impact of Zea mays L. waste derived biochar on cadmium immobilization and wheat plant growth.Pak. J. Agri. Sci.5712011210.

  • 153

    JaneczkoA.KoscielniakJ.PilipowiczM.Szarek-LukaszewskaG.SkoczowskiA. (2005). Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress.Photosynthetica43293298. 10.1007/s11099-005-0048-4

  • 154

    JaneeshmaE.PuthurJ. T. (2020). Direct and indirect influence of arbuscular mycorrhizae on enhancing metal tolerance of plants.Arch. Microbiol.202116. 10.1007/s00203-019-01730-z

  • 155

    JanouškováM.PavlíkováD.VosátkaM. (2006). Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil.Chemosphere6519591965. 10.1016/j.chemosphere.2006.07.007

  • 156

    JanuškaitienėI. (2010). Impact of low concentration of cadmium on photosynthesis and growth of pea and barley.Environ. Res. Engg. Manage.532429.

  • 157

    JebaraS. H.ChiboubM.JebaraM. (2018). “Antioxidant responses and gene level expressions of Sulla coronaria inoculated by heavy metals resistant plant growth promoting bacteria under cadmium stress,” in Recent Advances in Environmental Science from the Euro-Mediterranean and Surrounding Regions, Advances in Science, Technology & Innovation, edsKallelA.KsibiM.DhiaH. B.KhélifiN. (Cham: Springer International Publishing).

  • 158

    JegadeesanS.YuK.PovsaV.GawalkoE.MorrisonM. J.ShiC.et al (2010). Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [Glycine max (L.) Merr].Theor. Appl. Genet.121283294. 10.1007/s00122-010-1309-6

  • 159

    JhaU. C.BohraA. (2016). Genomics enabled breeding approaches for improving cadmium stress tolerance in plants.Euphytica208131.

  • 160

    JianfengW.ZhangY.JinJ.LiQ.ChenzhouZ.WenbinN.et al (2017). An intact cytokinin-signaling pathway is required for Bacillus sp. LZR216-promoted plant growth and root system architecture alteration in Arabidopsis thaliana seedlings.Plant Growth Regul.84507518. 10.1007/s10725-017-0357-1

  • 161

    JiangM.LiuS.LiY.LiX.LuoZ.SongH.et al (2019). EDTA-facilitated toxic tolerance, absorption and translocation and phytoremediation of lead by dwarf bamboos.Ecotoxicol. Environ. Saf.170502512.

  • 162

    JiangQ. Y.ZhuoF.LongS. H.Di-ZhaoH.YangD. J.YeZ. H.et al (2016). Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils?Sci. Rep.6:21805. 10.1038/srep21805

  • 163

    JianvL.QixingZ.SongW. (2010). Evaluation of chemical enhancement on phytoremediation effect of Cd-contaminated soils with Calendula officinalis L.Int. J. Phytoremediat.12503515. 10.1080/15226510903353112

  • 164

    JoshiP. M.JuwarkarA. A. (2009). In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals.Environ. Sci. Technol.4358845889. 10.1021/es900063b

  • 165

    JungM. C. (2008). Heavy metal concentration in soils and factors affecting metal uptake by plants in the vicinity of a Korean Cu–W mine.Sensors824132423. 10.3390/s8042413

  • 166

    JungC.Capistrano-GossmannG.BraatzJ.SashidharN.MelzerS. (2018). Recent developments in genome editing and applications in plant breeding.Plant Breed.13719.

  • 167

    Kabata-PendiasA. (1993). Behavioural properties of trace metals in soils.Appl. Geochem.839. 10.1016/S0883-2927(09)80002-4

  • 168

    Kabata-PendiasA.SadurskiW. (2004). “Trace elements and compounds in soil,” in Elements and Their Compounds in the Environment: Occurrence, Analysis and Biological Relevance, edsMerianE.AnkeM.IhnatM.StoepplerM. (Hoboken, NJ: Wiley), 7999.

  • 169

    KamranM.MalikZ.ParveenA.HuangL.RiazM.BashirS.et al (2020). Ameliorative effects of biochar on rapeseed (Brassica napus L.) growth and heavy metal immobilization in soil irrigated with untreated wastewater.J. Plant Growth Regul.39266281.

  • 170

    KamranM.MalikZ.ParveenA.ZongY.AbbasiG. H.RafiqM. T.et al (2019). Biochar alleviates Cd phytotoxicity by minimizing bioavailability and oxidative stress in pak choi (Brassica chinensis L.) cultivated in Cd-polluted soil.J. Environ. Manag.250:109500. 10.1016/j.jenvman.2019.109500

  • 171

    KapoorD.SharmaR.HandaN.KaurH.RattanA.YadavP.et al (2015). Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols.Front. Environ. Sci.3:13. 10.3389/fenvs.2015.00013

  • 172

    KapoorD.SinghS.KumarV.RomeroR.PrasadR.SinghJ. (2019). Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS).Plant Gene19:100182.

  • 173

    KeT.GuoG.LiuJ.ZhangC.TaoY.WangP.et al (2021). Improvement of the Cu and Cd phytostabilization efficiency of perennial ryegrass through the inoculation of three metal-resistant PGPR strains.Environ. Pollut.271:116314. 10.1016/j.envpol.2020.116314

  • 174

    KhanM. A.KhanS.KhanA.AlamM. (2017). Soil contamination with cadmium, consequences and remediation using organic amendments.Sci. Total Environ.60115911605. 10.1016/j.scitotenv.2017.06.030

  • 175

    KhanN.Samiullah, SinghS.NazarR. (2007). Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress.J. Agron. Crop Sci.193435444.

  • 176

    KhannaK.JamwalV. L.KohliS. K.GandhiS. G.OhriP.BhardwajR.et al (2019). Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression.Chemosphere217463474. 10.1016/j.chemosphere.2018.11.005

  • 177

    KirkhamM. B. (2006). Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation, and amendments.Geoderma1371932. 10.1016/j.geoderma.2006.08.024

  • 178

    KloepperJ. W. (1994). “Plant growth-promoting rhizobacteria,” in Plant Growth and Health Promoting Bacteria, ed.MaheshwariD. K. (Cham: Springer Science & Business Media), 137166.

  • 179

    KnoxR. E.PozniakC. J.ClarkeF. R.ClarkeJ. M.HoushmandS.SinghA. K. (2009). Chromosomal location of the cadmium uptake gene (Cdu1) in durum wheat.Genome52741747. 10.1139/g09-042

  • 180

    KoprivovaA.NorthK. A.KoprivaS. (2008). Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots.Plant Physiol.14614081420. 10.1104/pp.107.113175

  • 181

    KrantevA.YordanovaR.JandaT.SzalaiG.PopovaL. (2008). Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants.J. Plant Physiol.165920931. 10.1016/j.jplph.2006.11.014

  • 182

    KrujatzF. (2012). Assessing the toxic effects of nickel, cadmium and EDTA on growth of the plant growth-promoting rhizobacterium Pseudomonas brassicacearum.Water Air Soil Pollut.22312811293.

  • 183

    KubierA.WilkinR. T.PichlerT. (2019). Cadmium in soils and groundwater: a review.Appl. Geochem.108:104388. 10.1016/j.apgeochem.2019.104388

  • 184

    KumarP.EdelsteinM.CardarelliM.FerriE.CollaG. (2015). Grafting affects growth, yield, nutrient uptake, and partitioning under cadmium stress in tomato.HortScience5016541661.

  • 185

    KüpperH.ParameswaranA.LeitenmaierB.TrtilekM.ŠetlíkI. (2007). Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspicaerulescens.New Phytol.175655674. 10.1111/j.1469-8137.2007.02139.x

  • 186

    LambrechtsT.GustotQ.CouderE.HoubenD.IserentantA.LuttsS. (2011). Comparison of EDTA-enhanced phytoextraction and phytostabilisation strategies with Lolium perenne on a heavy metal contaminated soil.Chemosphere8512901298. 10.1016/j.chemosphere.2011.07.034

  • 187

    LanH. X.WangZ. F.WangQ. H.WangM. M.BaoY. M.HuangJ.et al (2012). Characterization of a vacuolar zinc transporter OZT1 in rice (Oryza sativa L.).Mol. Biol. Rep.4012011210.

  • 188

    LataS.KaurH. P.MishraT. (2019). Cadmium bioremediation: a review.Int. J. Pharm. Sci. Res.1041204128. 10.13040/IJPSR.0975-8232

  • 189

    LeeK.BackK. (2017). Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield.J. Pineal Res.62114. 10.1111/jpi.12392

  • 190

    LeegoodR. (1993). “Carbon metabolism,” in Photosynthesis and Production in a Changing Environment, edsHallD. O.ScurlockJ. M. O.Bolhar-NordenkampfH. R.LeegoodR. C.LongS. P. (Cham: Springer), 247267.

  • 191

    LehmannA.LeifheitE.RilligM. (2017). “Mycorrhizas and soil aggregation,” in Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage, edsJohnsonN. C.GehringC.JansaJ. (Amsterdan: Elsevier). 10.1111/j.1469-8137.2004.01181.x

  • 192

    LehmannA.RilligM. C. (2015). Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - A meta-analysis.Soil Biol. Biochem.81147158. 10.1016/j.soilbio.2014.11.013

  • 193

    LentiniM.De LilloA.ParadisoneV.LibertiD.LandiS.EspositoS. (2018). Early responses to cadmium exposure in barley plants: effects on biometric and physiological parameters.Acta Physiol. Plant.40111. 10.1007/s11738-018-2752-2

  • 194

    LiD. D.ZhouD. M. (2012). Acclimation of wheat to low-level cadmium or zinc generates its resistance to cadmium toxicity.Ecotoxicol. Environ. Saf.79264271.

  • 195

    LiF.LiZ.MaoP.LiY.LiY.McBrideM. B.et al (2019). Heavy metal availability, bioaccessibility, and leachability in contaminated soil: effects of pig manure and earthworms.Environ. Sci. Pollut. Res.262003020039. 10.1007/s11356-018-2080-5

  • 196

    LiJ.YuJ.DuD.LiuJ.LuH.YanC. (2019). Analysis of anatomical changes and cadmium distribution in Aegicerascorniculatum (L.) Blanco roots under cadmium stress.Mar. Pollut. Bull.149:110536. 10.1016/j.marpolbul.2019.110536

  • 197

    LiL.ChenJ.HeQ.DaudM. K.ZhuS. (2012). Characterization of physiological traits, yield and fiber quality in three upland cotton cultivars grown under cadmium stress.Aust. J. Crop Sci.615271533.

  • 198

    LiQ.LuY.ShiY.WangT.NiK.XuL.et al (2013). Combined effects of cadmium and fluoranthene on germination, growth and photosynthesis of soybean seedlings.J. Environ. Sci.2519361946.

  • 199

    LiS.ChenJ.IslamE.WangY.WuJ.YeZ.et al (2016). Cadmium-induced oxidative stress, response of antioxidants and detection of intracellular cadmium in organs of moso bamboo (Phyllostachys pubescens) seedlings.Chemosphere153107114. 10.1016/j.chemosphere.2016.02.062

  • 200

    LiS.SunX.LiS.LiuY.MaQ.ZhouW. (2021). Effects of amendments on the bioavailability, transformation and accumulation of heavy metals by pakchoi cabbage in a multi-element contaminated soil.RSC Adv.1143954405. 10.1039/D0RA09358K

  • 201

    LiW.WuS.LiuY.JinG.ZhaoH.FanL.et al (2016). Genome-wide profiling of genetic variation in Agrobacterium-transformed rice plants.J. Zhejiang Univ. Sci. B17992996. 10.1631/jzus.B1600301

  • 202

    LiX.GitauM. M.HanS.FuJ.XieY. (2017a). Effects of cadmium-resistant fungi Aspergillus aculeatus on metabolic profiles of bermudagrass [Cynodondactylon (L.) Pers.] under Cd stress.Plant Physiol. Biochem.1143850. 10.1016/j.plaphy.2017.02.014

  • 203

    LiX.HanS.WangG.LiuX.AmomboE.XieY.et al (2017b). The fungus Aspergillus aculeatus enhances salt-stress tolerance, metabolite accumulation, and improves forage quality in perennial ryegrass.Front. Microbiol.8:1664. 10.3389/fmicb.2017.01664

  • 204

    LiY.LuoJ.YuJ.XiaL.ZhouC.CaiL.et al (2018). Improvement of the phytoremediation efficiency of Neyraudiareynaudiana for lead-zinc mine-contaminated soil under the interactive effect of earthworms and EDTA.Sci. Rep.8:6417. 10.1038/s41598-018-24715-2

  • 205

    LiY.WangL.YangL.LiH. (2014). Dynamics of rhizosphere properties and antioxidative responses in wheat (Triticum aestivum L.) under cadmium stress.Ecotoxicol. Environ. Saf.1025561. 10.1016/j.ecoenv.2014.01.004

  • 206

    LiZ.ZhangR.ZhangH. (2018). Effects of plant growth regulators (DA-6 and 6-BA) and EDDS chelator on phytoextraction and detoxification of cadmium by Amaranthus hybridus Linn.Int. J. Phytoremed.2011211128. 10.1080/15226514.2017.1365348

  • 207

    LiaoM.XieX. M. (2004). Cadmium release in contaminated soils due to organic acids.Pedosphere14223228.

  • 208

    LinH.FangC.LiY.LinW.HeJ.LinR.et al (2016). Effect of silicon on grain yield of rice under cadmium-stress.Acta Physiol. Plant.38113. 10.1007/s11738-016-2177-8

  • 209

    LinR.WangX.LuoY.DuW.GuoH.YinD. (2007). Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.).Chemosphere698998. 10.1016/j.chemosphere.2007.04.041

  • 210

    LiuF.LiuX.DingC.WuL. (2015). The dynamic simulation of rice growth parameters under cadmium stress with the assimilation of multi-period spectral indices and crop model.Field Crops Res.183225234. 10.1016/j.fcr.2015.08.004

  • 211

    LiuJ.QianM.CaiG.YangJ.ZhuQ. (2007). Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain.J. Hazard. Mater.143443447. 10.1016/j.jhazmat.2006.09.057

  • 212

    LiuJ. N.ZhouQ.SunT.MaL. Q.WangS. (2008). Identification of and chemical enhancement of two ornamental plants for phytoremediation.Bull. Environ. Contam. Toxicol.80260265. 10.1007/s00128-008-9357-1

  • 213

    LiuJ. N.ZhouQ. X.WangS.SunT. (2009). Cadmium tolerance and accumulation of Althaea rosea Cav. and its potential as a hyperaccumulation under chemical enhancement.Environ. Monit. Assess.149419427. 10.1007/s10661-008-0218-5

  • 214

    LiuL.LiJ. W.YueF. X.YanX. W.WangF. Y.BlosziesS.et al (2018). Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil.Chemosphere194495503. 10.1016/j.chemosphere.2017.12.025

  • 215

    LiuM.SunJ.LiY.XiaoY. (2017). Nitrogen fertilizer enhances growth and nutrient uptake of Medicago sativa inoculated with Glomus tortuosum grown in Cd-contaminated acidic soil.Chemosphere167204211.

  • 216

    LiuX.ChenS.ChenM.ZhengG.PengY.ShiX.et al (2019). Association study reveals genetic loci responsible for arsenic, cadmium and lead accumulation in rice grain in contaminated farmlands.Front. Plant Sci.10:61. 10.3389/fpls.2019.00061

  • 217

    LiuY.XiaoT.NingZ.LiH.TangJ.ZhouG. (2013). High cadmium concentration in soil in the Three Gorges region: geogenic source and potential bioavailability.Appl. Geochem.37149156. 10.1016/j.apgeochem.2013.07.022

  • 218

    LizaS. J.ShethiK. J.RashidP. (2020). Effects of cadmium on the anatomical structures of vegetative organs of chickpea (Cicer arientinum L.).Dhaka Univ. J. Biol. Sci.294552. 10.3329/dujbs.v29i1.46530

  • 219

    LongC.WangD.ChenL.JiangW. J.XiangM. W. (2017). Effect of four kinds of phytohormones on U and Cd accumulation in Helianthus annuus.Chin. J. Environ. Eng.1132513256.

  • 220

    Lozano-RodriguezE.HernandezL. E.BonayP.Carpena-RuizR. O. (1997). Distribution of cadmium in shoot and root tissues1.J. Exp. Bot.48123128. 10.1093/jxb/48.1.123

  • 221

    LuoJ.LiX.JinY.TraoreI.DongL.YangG.et al (2020). Effects of arbuscular mycorrhizal fungi glomus mosseae on the growth and medicinal components of Dysosma versipellis under copper stress.Bull. Environ. Contam. Toxicol.107924930. 10.1007/s00128-019-02780-1

  • 222

    LuoJ. S.HuangJ.ZengD. L.PengJ. S.ZhangG. B.MaH. L.et al (2018). A defensin-like protein drives cadmium efflux and allocation in rice.Nat. Commun.919. 10.1038/s41467-018-03088-0

  • 223

    MaJ.NiX.HuangQ.LiuD.YeZ. (2021). Effect of bamboo biochar on reducing grain cadmium content in two contrasting wheat genotypes.Environ. Sci. Pollut. Res.281740517416. 10.1007/s11356-020-12007-0

  • 224

    MahajanP.KaushalJ. (2018). Role of phytoremediation in reducing cadmium toxicity in soil and water.J. Toxicol.2018116. 10.1155/2018/4864365

  • 225

    MaksimovićI.KastoriR.KrstićL.LukovićJ. (2007). Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings.Biol. Plant.51589592. 10.1007/s10535-007-0129-2

  • 226

    MaksymiecW.KrupaZ. (2002). Jasmonic acid and heavy metals in Arabidopsis plants-a similar physiological response to both stressors?J. Plant Physiol.159509515. 10.1078/0176-1617-00610

  • 227

    MaksymiecW.KrupaZ. (2006). The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana.Environ. Exp. Bot.57187194. 10.1016/j.envexpbot.2005.05.006

  • 228

    ManiD.KumarC. (2014). Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation.Int. J. Environ. Technol.11843872. 10.1007/s13762-013-0299-8

  • 229

    ManzoorM.GulI.KallerhoffJ.ArshadM. (2019). Fungi-assisted phytoextraction of lead: tolerance, plant growth—promoting activities and phytoavailability.Environ. Sci. Pollut. Res.262378823797. 10.1007/s11356-019-05656-3

  • 230

    Martínez DomínguezD.Córdoba GarcíaF.Canalejo RayaA.Torronteras SantiagoR. (2010). Cadmium-induced oxidative stress and the response of the antioxidative defense system in Spartina densiflora.Physiol. Plant.139289302. 10.1111/j.1399-3054.2010.01368.x

  • 231

    MauryaA. K. (2020). “Oxidative stress in crop plants,” in Agronomic Crops, ed.HasanuzzamanM. (Singapore: Springer).

  • 232

    McCouchS. R.WrightM. H.TungC. W.MaronL. G.McNallyK. L.FitzgeraldM.et al (2016). Open access resources for genome-wide association mapping in rice.Nat. Commun.7114. 10.1038/ncomms10532

  • 233

    Medynska-JuraszekA.Cwielag-PiaseckaI. (2020). Effect of biochar application on heavy metal mobility in soils impacted by copper smelting processes.Pol. J. Environ. Stud.2917491757. 10.15244/pjoes/108928

  • 234

    Medyńska-JuraszekA.BednikM.ChohuraP. (2020). Assessing the influence of compost and biochar amendments on the mobility and uptake of heavy metals by green leafy vegetables.Int. J. Environ. Res. Public Health17:7861.

  • 235

    MehdizadehL.FarsaraeiS.MoghaddamM. (2021). Biochar application modified growth and physiological parameters of Ocimumciliatum L. and reduced human risk assessment under cadmium stress.J. Hazard. Mater.409:124954. 10.1016/j.jhazmat.2020.124954

  • 236

    MengD.LiJ.LiuT.LiuY.YanM.HuJ.et al (2019). Effects of redox potential on soil cadmium solubility: insight into microbial community.J. Environ. Sci.75224232. 10.1016/j.jes.2018.03.032

  • 237

    MengJ.ZhongL.WangL.LiuX.TangC.ChenH.et al (2018). Contrasting effects of alkaline amendments on the bioavailability and uptake of Cd in rice plants in a Cd-contaminated acid paddy soil.Environ. Sci. Pollut. Res.2588278835. 10.1007/s11356-017-1148-y

  • 238

    MenguerP. K.FarthingE.PeastonK. A.RicachenevskyF. K.FettJ. P.WilliamsL. E. (2013). Functional analysis of the rice vacuolar zinc transporter OsMTP1.J. Exp. Bot.6428712883. 10.1093/jxb/ert136

  • 239

    MishraS.TripathiR. D.SrivastavaS.DwivediS.TrivediP. K.DhankherO. P.et al (2009). Thiol metabolism play significant role during cadmium detoxification by Ceratophyllumdemersum L.Bioresour. Technol.10021552161. 10.1016/j.biortech.2008.10.041

  • 240

    MizushimaM.FerreiraB.FrançaM.AlmeidaA. A.CortezP.SilvaJ.et al (2019). Ultrastructural and metabolic disorders induced by short-term cadmium exposure in Avicenniaschaueriana plants and its excretion through leaf salt glands.Plant Biol.21844853. 10.1111/plb.12992

  • 241

    Mokarram-KashtibanS.HosseiniS. M.KouchaksaraeiM. T.YounesiH. (2019). Biochar improves the morphological, physiological and biochemical properties of white willow seedlings in heavy metal-contaminated soil.Arch. Biol. Sci.71281291. 10.2298/ABS180918010M

  • 242

    MolinaA. S.LugoM. A.PerezChacaM. V.Vargas-GilS.ZirulnikF.LeporatiJ.et al (2020). Effect of arbuscular mycorrhizal colonization on cadmium-mediated oxidative stress in Glycine max (L.) Merr.Plants9:108. 10.3390/plants9010108

  • 243

    MondalS. C.SarmaB.FarooqM.NathD. J.GogoiN. (2020). Cadmium bioavailability in acidic soils under bean cultivation: role of soil additives.Int. J. Environ. Sci. Technol.17153160. 10.1007/s13762-019-02263-0

  • 244

    MongkhonsinB.NakbanpoteW.MeesungnoenO.PrasadM. N. V. (2019). “Adaptive and tolerance mechanisms in herbaceous plants exposed to cadmium,” in Cadmium Toxicity and Tolerance in Plants, edsHasanuzzamanM.PrasadM. N. V.FujitaM. (Cambridge, MA: Academic Press), 73109.

  • 245

    MoradiR.PourghasemianN.NaghizadehM. (2019). Effect of beeswax waste biochar on growth, physiology and cadmium uptake in saffron.J. Clean. Prod.22912511261. 10.1016/j.jclepro.2019.05.047

  • 246

    MoreiraF. M. D. S.FerreiraP. A. A.VilelaL. A. F.CarneiroM. A. C. (2015). “Symbioses of plants with rhizobia and mycorrhizal fungi in heavy metal-contaminated tropical soils,” in Heavy Metal Contamination of Soils, 1st Edn, edsSherametiI.VarmaA. (Switzerland: Springer).

  • 247

    MosaK. A.SaadounI.KumarK. (2016). Potential biotechnological strategies for the cleanup of heavy metals and metalloids.Front. Plant Sci.7:303. 10.3389/fpls.2016.00303

  • 248

    MoslehiA.FeizianM.HiguerasP.EisvandH. R. (2019). Assessment of EDDS and vermicompost for the phytoextraction of Cd and Pb by sunflower (Helianthus annuus L.).Int. J. Phytoremed.21191199. 10.1080/15226514.2018.1501336

  • 249

    MuhammadD.ChenF.ZhaoJ.ZhangG.WuF. (2009). Comparison of EDTA- and citric acid-enhanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angustifolia.Int. J. Phytoremediat.11558574. 10.1080/15226510902717580

  • 250

    MurgeseP.SantamariaP.LeoniB.CrecchioC. (2020). Ameliorative effects of PGPB on yield, physiological parameters, and nutrient transporter genes expression in barattiere (Cucumis melo L.).J. Soil Sci. Plant Nutr.20784793. 10.1007/s42729-019-00165-1

  • 251

    Myśliwa-KurdzielB.StrzałkaK. (2002). “Influence of metals on biosynthesis of photosynthetic pigments,” in Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants, edsPrasadM. N.StrzalkaK.StrzałkaK. (Cham: Springer Science & Business Media), 201227.

  • 252

    NaeemM. A.ShabbirA.AmjadM.AbbasG.ImranM.MurtazaB.et al (2020). Acid treated biochar enhances cadmium tolerance by restricting its uptake and improving physio-chemical attributes in quinoa (Chenopodium quinoa Willd.).Ecotoxicol. Environ. Saf.191:110218. 10.1016/j.ecoenv.2020.110218

  • 253

    NajeebU.JilaniG.AliS.SarwarM.XuL.ZhouW. (2011). Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid.J. Hazard. Mater.186565574. 10.1016/j.jhazmat.2010.11.037

  • 254

    NakamuraM.OchiaiT.NojiM.OguraY.SuzukiK.YoshimotoN.et al (2014). An improved tolerance to cadmium by overexpression of two genes for cysteine synthesis in tobacco.Plant Biotechnol.31141147. 10.5511/plantbiotechnology.14.0130a

  • 255

    NejadZ. D.JungM. C.KimK. H. (2017). Remediation of soils contaminated with heavy metals with an emphasis on immobilization technology.Environ. Geochem. Health40927953. 10.1007/s10653-017-9964-z

  • 256

    NguyenT. Q.SesinV.KisialaA.EmeryR. J. N. (2020). Phytohormonal roles in plant responses to heavy metal stress-implications for using macrophytes in phytoremediation of aquatic ecosystems.Environ. Toxicol. Chem.40722. 10.1002/etc.4909

  • 257

    NianL.ZhangX.YiX.LiuX.AinU. L.YangY.et al (2021). Genome-wide identification of ABA receptor PYL/RCAR gene family and their response to cold stress in Medicago sativa L.Physiol. Mol. Biol. Plants2719791995. 10.1007/s12298-021-01066-3

  • 258

    NigamN.KhareP.YadavV.MishraD.JainS.KarakT.et al (2019). Biochar-mediated sequestration of Pb and Cd leads to enhanced productivity in Mentha arvensis.Ecotoxicol. Environ. Saf.172411422. 10.1016/j.ecoenv.2019.02.006

  • 259

    NikolićN.ZorićL.CvetkovićI.PajevićS.BoriševM.OrlovićS.et al (2017). Assessment of cadmium tolerance and phytoextraction ability in young Populus deltoides L. and Populus× euramericana plants through morpho-anatomical and physiological responses to growth in cadmium enriched soil.iForest Biogeosci. For.10:635. 10.3832/ifor2165-010

  • 260

    NoriegaG. O.BalestrasseK. B.BatlleA.TomaroM. L. (2007). Cadmium induced oxidative stress in soybean plants also by the accumulation of δ-aminolevulinic acid.Biometals20841851. 10.1007/s10534-006-9077-0

  • 261

    NowackB. (2002). Environmental chemistry of aminopolycarboxylate chelating agents.Environ. Sci. Technol.3640094016. 10.1021/es025683s

  • 262

    OkemA.KulkarniM. G.StadenJ. V. (2015). Enhancing phytoremediation potential of Pennisetum clandestinumHochst in cadmium- contaminated coil using smoke-water and smoke-isolated karrikinolide.Int. J. Phytoremed.1710461052. 10.1080/15226514.2014.981245

  • 263

    OstrowskiM.CiarkowskaA.JakubowskaA. (2016). The auxin conjugate indole-3- acetyl-aspartate affects responses to cadmium and salt stress in Pisum sativum L.J. Plant Physiol.1916372. 10.1016/j.jplph.2015.11.012

  • 264

    PalansooriyaK. N.ShaheenS. M.ChenS. S.TsangD. C. W.HashimotoY.HouD.et al (2020). Soil amendments for immobilization of potentially toxic elements in contaminated soils: a critical review.Environ. Int.134:105046. 10.1016/j.envint.2019.105046

  • 265

    PanF.LuoS.ShenJ.WangQ.YeJ.MengQ.et al (2017). The effects of endophytic bacterium SaMR12 on Sedum alfredii Hance metal ion uptake and the expression of three transporter family genes after cadmium exposure.Environ. Sci. Pollut. Res.2493509360. 10.1007/s11356-017-8565-9

  • 266

    ParmarP.KumariN.SharmaV. (2013). Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress.Bot. Stud.5416. 10.1186/1999-3110-54-45

  • 267

    PereiraB. F. F.de AbreuC. A.HerpinU.de AbreuM. F.BertonR. S. (2010). Phytoremediation of lead by jack beans on a Rhodic Hapludox amended with EDTA.Sci. Agric.67308318. 10.1590/S0103-90162010000300009

  • 268

    PierattiniE. C.FranciniA.RaffaelliA.SebastianiL. (2017). Surfactant and heavy metal interaction in poplar: a focus on SDS and Zn uptake.Tree Physiol.38109118. 10.1093/treephys/tpx155

  • 269

    Piotrowska-NiczyporukA.BajguzA.ZambrzyckaE.Godlewska- ZylkiewiczB. (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae).Plant Physiol. Biochem.525265. 10.1016/j.plaphy.2011.11.009

  • 270

    PompeuG. B.VilhenaM. B.GratãoP. L. (2017). Abscisic acid-deficient sit tomato mutant responses to cadmium-induced stress.Protoplasma254771783. 10.1007/s00709-016-0989-4

  • 271

    PozniakC.FoxS.KnottD. (2009). CDC Verona durum wheat.Can. J. Plant Sci.89321324. 10.4141/CJPS08117

  • 272

    QayyumM. F.LiaquatF.RehmanR. A.GulM.Zia ul HyeM.RizwanM.et al (2017). Effects of co-composting of farm manure and biochar on plant growth and carbon mineralization in an alkaline soil.Environ. Sci. Pollut. Res.242606026068. 10.1007/s11356-017-0227-4

  • 273

    QayyumM. F.RehmanR. A.LiaqatS.IkramM.AliS.RizwanM.et al (2019). Cadmium immobilization in the soil and accumulation by spinach (Spinacia oleracea) depend on biochar types under controlled and field conditions.Arab. J. Geosci.12111. 10.1007/s12517-019-4681-9

  • 274

    QiF.LambD.NaiduR.BolanN. S.YanY.OkY. S.et al (2018). Cadmium solubility and bioavailability in soils amended with acidic and neutral biochar.Sci. Total Environ.61014571466. 10.1016/j.scitotenv.2017.08.228

  • 275

    QianqianM.HaiderF. U.FarooqM.AdeelM.ShakoorN.JunW.et al (2022). Selenium treated Foliage and biochar treated soil for improved lettuce (Lactuca sativa L.) growth in Cd-polluted soil.J. Cleaner Prod.335:130267. 10.1016/j.jclepro.2021.130267

  • 276

    QinP.WangL.LiuK.MaoS.LiZ.GaoS.et al (2015). Genome wide association study of Aegilops tauschiitraits under seedling-stage cadmium stress.Crop J.3405415. 10.1016/j.cj.2015.04.005

  • 277

    QiuZ.TanH.ZhouS.CaoL. (2014). Enhanced phytoremediation of toxic metals by inoculating endophytic Enterobacter sp. CBSB1 expressing bifunctional glutathione synthase.J. Hazard Mater.2671720. 10.1016/j.jhazmat.2013.12.043

  • 278

    QuartacciM. F.PinzinoC.SgherriC. L.Dalla VecchiaF.Navari-IzzoF. (2000). Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat.Physiol. Plant.1088793. 10.1034/j.1399-3054.2000.108001087.x

  • 279

    RadyM. M. (2011). Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress.Sci. Hort.129232237. 10.1016/j.scienta.2011.03.035

  • 280

    RadyM. M.HemidaK. A. (2015). Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of poly- amines.Ecotoxicol. Environ. Saf.119178185. 10.1016/j.ecoenv.2015.05.008

  • 281

    RafiqueM.HaqueK.HussainT.AmnaC.JavedH. (2017). Biochemical Talk in the Rhizoshperic Microbial Community for Phytoremediation.Hauppauge, NY: Nova Science Publishers.

  • 282

    RafiqueM.OrtasI.RizwanM.SultanT.ChaudharyH. J.IşikM.et al (2019). Effects of Rhizophagusclarus and biochar on growth, photosynthesis, nutrients, and cadmium (Cd) concentration of maize (Zea mays) grown in Cd-spiked soil.Environ. Sci. Pollut. Res.262068920700. 10.1007/s11356-019-05323-7

  • 283

    RajkumarM.SandhyaS.PrasadM. N. V.FreitasH. (2012). Perspectives of plant-associated microbes in heavy metal phytoremediation.Biotechnol. Adv.3015621574. 10.1016/j.biotechadv.2012.04.011

  • 284

    RaklamiA.OufdouK.TahiriA. I.Mateos-NaranjoE.Navarro-TorreS.Rodríguez-LlorenteI. D.et al (2019). Safe cultivation of Medicago sativa in metal-polluted soils from semi-arid regions assisted by heat-and metallo-resistant PGPR.Microorganisms7:212. 10.3390/microorganisms7070212

  • 285

    RasheedR.AshrafM. A.HussainI.HaiderM. Z.KanwalU.IqbalM. (2014). Exogenous proline and glycinebetaine mitigate cadmium stress in two genetically different spring wheat (Triticum aestivum L.) cultivars.Braz. J. Bot.37399406. 10.1007/s40415-014-0089-7

  • 286

    RehmanA.ShahzadB.HaiderF. U.AhmedH. A. I.LeeD.-J.ImS. Y.et al (2022a). “An introduction to brassinosteroids: history, biosynthesis, and chemical diversity,” in Brassinosteroids in Plant Developmental Biology and Stress Tolerance, edsYuJ. Q.AhammedG. J.KrishnaP. (Cambridge, MA: Academic Press).

  • 287

    RehmanA.ShahzadB.HaiderF. U.Moeen-ud-dinM.UllahA.KhanI. (2022b). “Brassinosteroids in plant response to high temperature stress,” in Brassinosteroids in Plant Developmental Biology and Stress Tolerance, edsYuJ. Q.AhammedG. J.KrishnaP. (Cambridge, MA: Academic Press).

  • 288

    RemansT.OpdenakkerK.SmeetsK.MathijsenD.VangronsveldJ.CuypersA. (2010). Metal-specific and NADPH oxidase dependent changes in lipoxygenase and NADPH oxidase gene expression in Arabidopsis thaliana exposed to cadmium or excess copper.Funct. Plant Biol.37532544. 10.1071/FP09194

  • 289

    RenT.ChenN.MahariW. A. W.XuC.FengH.JiX.et al (2021). Biochar for cadmium pollution mitigation and stress resistance in tobacco growth.Environ. Res.192:110273. 10.1016/j.envres.2020.110273

  • 290

    RenY.ChenY.AnJ.ZhaoZ.ZhangG.WangY.et al (2018). Wheat expansin gene TaEXPA2 is involved in conferring plant tolerance to Cd toxicity.Plant Sci.270245256. 10.1016/j.plantsci.2018.02.022

  • 291

    RiazM.YanL.WuX.HussainS.AzizO.WangY.et al (2018). Boron alleviates the aluminum toxicity in trifoliate orange by regulating antioxidant defense system and reducing root cell injury.J. Environ. Manage.208149158. 10.1016/j.jenvman.2017.12.008

  • 292

    RizwanM.AliS.AbbasT.Zia-Ur-RehmanM.HannanF.KellerC.et al (2016). Cadmium minimization in wheat: a critical review.Ecotoxicol. Environ. Saf.1304353. 10.1016/j.ecoenv.2016.04.001

  • 293

    RizwanM.AliS.QayyumM. F.OkY. S.Zia-ur-RehmanM.AbbasZ.et al (2017). Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: a critical review.Environ. Geochem. Health39259277. 10.1007/s10653-016-9826-0

  • 294

    RizwanM.AliS.Ur RehmanM. Z.MaqboolA. (2019a). A critical review on the effects of zinc at toxic levels of cadmium in plants.Environ. Sci. Pollut. Res.2662796289. 10.1007/s11356-019-04174-6

  • 295

    RizwanM.AliS.Ur RehmanM. Z.RinklebeJ.TsangD. C.BashirA.et al (2018). Cadmium phytoremediation potential of Brassica crop species: a review.Sci. Total Environ.63111751191. 10.1016/j.scitotenv.2018.03.104

  • 296

    RizwanM.NoureenS.AliS.AnwarS.Zia-ur-RehmanM.QayyumM. F.et al (2019b). Influence of biochar amendment and foliar application of iron oxide nanoparticles on growth, photosynthesis, and cadmium accumulation in rice biomass.J. Soils Sediments1937493759. 10.1007/s11368-019-02327-1

  • 297

    RoddaM. S.LiG.ReidR. J. (2011). The timing of grain Cd accumulation in rice plants: the relative importance of remobilisation within the plant and root Cd uptake post-flowering.Plant Soil347105114. 10.1007/s11104-011-0829-4

  • 298

    Rodríguez-SerranoM.Romero-PuertasM. C.ZabalzaA.CorpasF. J.GómezM.Del RíoL. A.et al (2006). Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo.Plant Cell Environ.2915321544. 10.1111/j.1365-3040.2006.01531.x

  • 299

    Romero-PuertasM.Rodríguez-SerranoM.CorpasF.GomezM. D.Del RioL.SandalioL. (2004). Cadmium-induced subcellular accumulation of O2•− and H2O2 in pea leaves.Plant Cell Environ.2711221134. 10.1111/j.1365-3040.2004.01217.x

  • 300

    RostamiS.AzhdarpoorA. (2019). The application of plant growth regulators to improve phytoremediation of contaminated soils: a review.Chemosphere220818827. 10.1016/j.chemosphere.2018.12.203

  • 301

    RoychoudhuryA.GhoshS.PaulS.MazumdarS.DasG.DasS. (2016). Pre-treatment of seeds with salicylic acid attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean (Vigna radiata L. wilczek).Acta Physiol. Plant.38118. 10.1007/s11738-015-2027-0

  • 302

    SaeedQ.XiukangW.HaiderF. U.KucerikJ.MumtazM. Z.HolatkoJ.et al (2021). Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms.Int. J. Mol. Sci.21:10529. 10.3390/ijms221910529

  • 303

    SaeidA.ProchownikE.Dobrowolska-IwanekJ. (2018). Phosphorus solubilization by Bacillus species.Molecules23:2897. 10.3390/molecules23112897

  • 304

    SaekiK.KunitoT. (2012). Influence of chloride ions on cadmium adsorptions by oxides, hydroxides, oxyhydroxides, and phyllosilicates.Appl. Clay Sci.62–635862. 10.1016/j.clay.2012.04.018

  • 305

    SaifullahM. E.QadirM.de CaritatP.TackF. M. G.Du LaingG.ZiaM. (2009). H. EDTA-assisted Pb phytoextraction.Chemosphere7412791291. 10.1016/j.chemosphere.2008.11.007

  • 306

    SakouhiL.RahouiS.MassoudM. B.MunemasaS.FerjaniE. E.MurataY.et al (2016). Calcium and EGTA alleviate cadmium toxicity in germinating chickpea seeds.J. Plant Growth Regul.3510641073. 10.1007/s00344-016-9605-2

  • 307

    SalazarM. J.RodriguezJ. H.NietoG. L.PignataM. L. (2012). Effects of heavy metal concentrations (Cd, Zn and Pb) in agricultural soils near different emission sources on quality, accumulation and food safety in soybean [Glycine max (L.) Merrill].J. Hazard. Mater.233244253. 10.1016/j.jhazmat.2012.07.026

  • 308

    SangthongC.SetkitK.PrapagdeeB. (2016). Improvement of cadmium phytoremediation after soil inoculation with a cadmium-resistant Micrococcus sp.Environ. Sci. Pollut. Res.23756764. 10.1007/s11356-015-5318-5

  • 309

    SárváriÉ (2008). Effect of Cd on the iron re-supply-induced formation of chlorophyll-protein complexes in cucumber.Acta Biol. Szegediensis52183186.

  • 310

    SarwarN.MalhiS. S.ZiaM. H.NaeemA.BibiS.FaridG. (2010). Role of mineral nutrition in minimizing cadmium accumulation by plants.J. Sci. Food Agric.90925937. 10.1002/jsfa.3916

  • 311

    SasakiA.YamajiN.YokoshoK.MaJ. F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice.Plant Cell2421552167.

  • 312

    SatoH.ShirasawaS.MaedaH.NakagomiK.KajiR.OhtaH.et al (2011). Analysis of QTL for lowering cadmium concentration in rice grains from ‘LAC23’.Breed. Sci.61196200. 10.1270/jsbbs.61.196

  • 313

    SellJ.KayserA.SchulinR.BrunnerI. (2005). Contribution of ectomycorrhizal fungi to cadmium uptake of poplars and willows from a heavily polluted soil.Plant Soil277245253. 10.1007/s11104-005-7084-5

  • 314

    SemidaW. M.RadyM. M.Abd El-MageedT. A.HowladarS. M.AbdelhamidM. A. (2015). Alleviation of cadmium toxicity in common bean (Phaseolus vulgaris L.) plants by the exogenous application of salicylic acid.J. Hortic. Sci. Biotechnol.908391. 10.1080/14620316.2015.11513156

  • 315

    ShahK.NahakpamS.ChaturvediV.SinghP. (2019). “Cadmium-induced anatomical abnormalities in plants,” in Cadmium Toxicity and Tolerance in Plants, edsHasanuzzamanM.PrasadM. N. V.FujitaM. (Amsterdam: Elsevier), 111139. 10.1016/b978-0-12-814864-8.00005-x

  • 316

    ShahK.SinghP.NahakpamS. (2013). Effect of cadmium uptake and heat stress on root ultrastructure, membrane damage and antioxidative response in rice seedlings.J. Plant Biochem. Biotechnol.22103112. 10.1007/s13562-012-0116-3

  • 317

    ShahidM.AustruyA.EchevarriaG.ArshadM.SanaullahM.AslamM.et al (2014). EDTA-enhanced phytoremediation of heavy metals: a review.Soil Sediment. Contam.23389416. 10.1080/15320383.2014.831029

  • 318

    ShahidM.DumatC.KhalidS.NiaziN. K.AntunesP. M. (2016). Cadmium bioavailability, uptake, toxicity and detoxification in soil plant system.Rev. Environ. Contam. Toxicol.24173137. 10.1007/398_2016_8

  • 319

    ShahkolaieS. S.BaranimotlaghM.DordipourE.KhormaliF. (2020). Effects of inorganic and organic amendments on physiological parameters and antioxidant enzymes activities in Zea mays L. from a cadmium-contaminated calcareous soil.S. Afr. J. Bot.128132140. 10.1016/j.sajb.2019.10.007

  • 320

    ShahzadB.TanveerM.CheZ.RehmanA.CheemaS. A.SharmaA.et al (2018). Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review.Ecotoxicol. Environ. Saf.147935944. 10.1016/j.ecoenv.2017.09.066

  • 321

    ShakirovaF. M.AllagulovaC. R.MaslennikovaD. R.KlyuchnikovaE. O.AvalbaevA. M.BezrukovaM. V. (2016). Salicylic acid-induced protection against cadmium toxicity in wheat plants.Environ. Exp. Bot.1221928. 10.1016/j.envexpbot.2015.08.002

  • 322

    SharafA. E. M. M.FarghalI. I.SofyM. R. (2009). Role of gibberellic acid in abolishing the detrimental effects of Cd and Pb on broad bean and lupin plants.Res. J. Agric. Biol. Sci.5668673.

  • 323

    SharmaR. K.ArchanaG. (2016). Cadmium minimization in food crops by cadmium resistant plant growth promoting rhizobacteria.Appl. Soil Ecol.1076678. 10.1016/j.apsoil.2016.05.009

  • 324

    SharmaS.AnandG.SinghN.KapoorR. (2017). Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism.Front. Plant Sci.8:906. 10.3389/fpls.2017.00906

  • 325

    SharmaS. S.KumarV. (2002). Responses of wild type and abscisic acid mutants of Arabidopsis thaliana to cadmium.J. Plant Physiol.15913231327. 10.1078/0176-1617-00601

  • 326

    ShaoJ. F.XiaJ.YamajiN.ShenR. F.MaJ. F. (2018). Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter.J. Exp. Bot.6927432752.

  • 327

    SheoranV.SheoranA. S.PooniaP. (2016). Factors affecting phytoextraction: (a review).Pedosphere26148166. 10.1016/S1002-0160(15)60032-7

  • 328

    ShiP.ZhuK.ZhangY.ChaiT. (2016). Growth and cadmium accumulation of Solanum nigrum L. seedling were enhanced by heavy metal-tolerant strains of Pseudomonas aeruginosa.Water Air Soil Pollut.227:459.

  • 329

    ShiyuQ. I. N.HongenL. I. U.ZhaojunN. I. E.RengelZ.WeiG. A. O.ChangL. I.et al (2020). Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: a review.Pedosphere30168180. 10.1016/S1002-0160(20)60002-9

  • 330

    ShuklaD.KesariR.TiwariM.DwivediS.TripathiR. D.NathP.et al (2013). Expression of Ceratophyllumdemersumphytochelatin synthase, CdPCS1, in Escherichia coli and Arabidopsis enhances heavy metal(loid)s accumulation.Protoplasma25012631272. 10.1007/s00709-013-0508-9

  • 331

    SiemianowskiO.BarabaszA.KendziorekM.RuszczyńskaA.BulskaE.WilliamsL. E.et al (2014). AtHMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier.J. Exp. Bot.6511251139. 10.1093/jxb/ert471

  • 332

    SigfridssonK. G.BernátG.MamedovF.StyringS. (2004). Molecular interference of Cd2+ with Photosystem II.Biochim. Biophys. Acta Bioenerget.16591931. 10.1016/j.bbabio.2004.07.003

  • 333

    SilberA.Bar-YosefB.SuryanoS.LevkovitchI. (2012). Zinc adsorption by perlite: effects of pH, ionic strength, temperature, and pre-use as growth substrate.Geoderma170159167.

  • 334

    SilvaS. A.TechioV. H.de CastroE. M.de FariaM. R.PalmieriM. J. (2013). Reproductive, cellular, and anatomical alterations in Pistia stratiotes L. plants exposed to cadmium.Water Air Soil Pollut.22418.

  • 335

    SinghG.PankajU.ChandS.VermaR. (2019). Arbuscular mycorrhizal fungi assisted phytoextraction of toxic metals by Zea mays L. from tannery sludge.Soil Sediment. Contam.28729746. 10.1080/15320383.2019.1657381

  • 336

    SinghP.SinghI.ShahK. (2020). Alterations in antioxidative machinery and growth parameters upon application of nitric oxide donor that reduces detrimental effects of cadmium in rice seedlings with increasing days of growth.S. Afr. J. Bot.131283294. 10.1016/j.sajb.2020.02.022

  • 337

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

  • 338

    SinghS.PrasadS. M. (2016). Kinetin ameliorates cadmium induced toxicity on growth, pigments and photosynthesis by regulating antioxidant potential in tomato seedlings.Int. J. Sci. Eng. Appl. Sci.2110.

  • 339

    SinghS.PrasadS. M. (2017). Effects of 28-homobrassinoloid on key physiological attributes of Solanum lycopersicum seedlings under cadmium stress: photosynthesis and nitrogen metabolism.Plant Growth Reg.82161173. 10.1007/s10725-017-0248-5

  • 340

    SinghS.SinghA.SrivastavaP. K.PrasadS. M. (2018). Cadmium toxicity and its amelioration by kinetin in tomato seedlings vis-à-vis ascorbate-glutathione cycle.J. Photochem. Photobiol. B Biol.1787684. 10.1016/j.jphotobiol.2017.10.025

  • 341

    SkrebskyE. C.TabaldiL. A.PereiraL. B.RauberR.MaldanerJ.CargneluttiD.et al (2008). Effect of cadmium on growth, micronutrient concentration, and δ-aminolevulinic acid dehydratase and acid phosphatase activities in plants of Pfaffia glomerata.Braz. J. Plant Physiol.20285294. 10.1590/S1677-04202008000400004

  • 342

    SohailM. I.RehmanM. Z.RizwanM.YousafB.AliS.HaqM. A.et al (2020). Efficiency of various silicon rich amendments on growth and cadmium accumulation in field grown cereals and health risk assessment.Chemosphere244112. 10.1016/j.chemosphere.2019.125481

  • 343

    SohailM. I.Zia-ur-RehmanM.MurtazaG.WahidM. A. (2019). Chemical investigations of Si-rich organic and inorganic amendments and correlation analysis between different chemical composition and Si contents in amendments.Arab. J. Geosci.12:47. 10.1007/s12517-018-4215-x

  • 344

    SongW.ChenS.LiuJ.ChenL.SongN.LiN.et al (2015). Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution.J. Integr. Agric.1418451854. 10.1016/S2095-3119(14)60926-6

  • 345

    SongY.JinL.WangX. (2017). Cadmium absorption and transportation pathways in plants.Int. J Phytoremed.19133141. 10.1080/15226514.2016.1207598

  • 346

    StroińskiA.GiżewskaK.ZielezińskaM. (2013). Abscisic acid is required in transduction of cadmium signal to potato roots.Biol. Plant.57121127. 10.1007/s10535-012-0135-x

  • 347

    SugiyamaM.AeN.HajikaM. (2011). Developing of a simple method for screening soybean seedling cadmium accumulation to select soybean genotypes with low seed cadmium.Plant Soil341413422.

  • 348

    SuksabyeP.PimthongA.DhurakitP.MekvichitsaengP.ThiravetyanP. (2016). Effect of biochars and microorganisms on cadmium accumulation in rice grains grown in Cd-contaminated soil.Environ. Sci. Pollut. Res. Int.23962973. 10.1007/s11356-015-4590-8

  • 349

    SullivanT. S.McBrideM. B.ThiesJ. E. (2013). Soil bacterial and archaeal community composition reflects high spatial heterogeneity of pH, bioavailable Zn, and Cu in a metalliferous peat soil.Soil Biol. Biochem.66102109. 10.1016/j.soilbio.2013.06.021

  • 350

    SunS.WangH.YuH.ZhongC.ZhangX.PengJ.et al (2013). GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation.J. Exp. Bot.6416371647. 10.1093/jxb/ert021

  • 351

    SunS.ZhouX.CuiX.LiuC.FanY.McBrideM. B.et al (2020). Exogenous plant growth regulators improved phytoextraction efficiency by Amaranths hypochondriacus L. in cadmium contaminated soil.Plant Growth Reg.902940. 10.1007/s10725-019-00548-5

  • 352

    SunithaM. S.PrashantS.KumarS. A.RaoS. R. I. N. A. T. H.NarasuM. L.KishorP. K. (2012). Cellular and molecular mechanisms of heavy metal tolerance in plants: a brief overview of transgenic plants over-expressing phytochelatin synthase and metallothionein genes.Plant Cell Biotechnol. Mol. Biol.1399104.

  • 353

    TamásL.DudíkováJ.ĎurčekováK.HaluškováL’HuttováJ.MistríkI. (2009). Effect of cadmium and temperature on the lipoxygenase activity in barley root tip.Protoplasma235:17. 10.1007/s00709-008-0027-2

  • 354

    TangX.ZengG.FanC.ZhouM.TangL.ZhuJ.et al (2018). Chromosomal expression of CadR on Pseudomonas aeruginosa for the removal of Cd (II) from aqueous solutions.Sci. Total Environ.63613551361. 10.1016/j.scitotenv.2018.04.229

  • 355

    TanveerM.ShabalaS. (2022). “Entangling the interaction between essential and nonessential nutrients: implications for global food security,” in Plant Nutrition and Food Security in the Era of Climate Change, ed.KumarV. (Cambridge, MA: Academic Press), 125.

  • 356

    TanwarA.AggarwalA.CharayaM. U.KumarP. (2015). Cadmium remediation by arbuscular mycorrhizal fungus–colonized celery plants supplemented with ethylenediaminetetraacetic acid.Bioremediat. J.19188200. 10.1080/10889868.2014.995371

  • 357

    TaoS.SunL.MaC.LiL.LiG.HaoL. (2013). Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium.Plant Soil372309318. 10.1007/s11104-013-1749-2

  • 358

    TeiriH.PourzamaniH.HajizadehY. (2018). Phytoremediation of VOCs from indoor air by ornamental potted plants: a pilot study using a palm species under the controlled environment.Chemosphere197375381.

  • 359

    TimperioA. M.D’AmiciG. M.BartaC.LoretoF.ZollaL. (2007). Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves.J. Exp. Bot.5836953710. 10.1093/jxb/erm219

  • 360

    TiongJ.McDonaldG. K.GencY.PedasP.HayesJ. E.ToubiaJ.et al (2014). HvZIP7 mediates zinc accumulation in barley (Hordeum vulgare) at moderately high zinc supply.New Phytol.201131143. 10.1111/nph.12468

  • 361

    TranT. A.PaunovaS.NedevaD.PopovaL. (2011). Nitric oxide alleviates cadmium toxicity on photosynthesis in pea plants.ComptesRendus de l’AcademieBulgare des Sci.6411371142.

  • 362

    TranT. A.PopovaL. P. (2013). Functions and toxicity of cadmium in plants: recent advances and future prospects.Turk. J. Bot.37113. 10.3906/bot-1112-16

  • 363

    UenoD.KonoI.YokoshoK.AndoT.YanoM.MaJ. F. (2009a). A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa).N. Phytol.182644653. 10.1111/j.1469-8137.2009.02784.x

  • 364

    UenoD.KoyamaE.KonoI.AndoT.YanoM.MaJ. F. (2009b). Identification of a novel major quantitative trait locus controlling distribution of Cd between roots and shoots in rice.Plant Cell Physiol.5022232233. 10.1093/pcp/pcp160

  • 365

    UllahA.HengS.MunisM. F. H.FahadS.YangX. (2015). Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review.Environ. Exp. Bot.1172840. 10.1016/j.envexpbot.2015.05.001

  • 366

    UnsalV.DalkıranT.ÇiçekM.KölükçüE. (2020). The role of natural antioxidants against reactive oxygen species produced by cadmium toxicity: a review.Adv. Pharm. Bull.10:184. 10.34172/apb.2020.023

  • 367

    UpadhyayS. K.SinghJ. S.SinghD. P. (2011). Exopolysaccharide producing plant growth promoting rhizobacteria under salinity condition.Pedosphere21214222. 10.1016/s1002-0160(11)60120-3

  • 368

    UraguchiS.MoriS.KuramataM.KawasakiA.AraoT.IshikawaS. (2009). Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice.J. Exp. Bot.60:2677. 10.1093/jxb/erp119

  • 369

    VaralakshmiL. R.GaneshamurthyA. (2013). Phytotoxicity of cadmium in radish and its effects on growth, yield, and cadmium uptake.Commun. Soil Sci. Plant Anal.4414441456. 10.1080/00103624.2013.767344

  • 370

    VermaS.VermaP. K.MeherA. K.BansiwalA. K.TripathiR. D.ChakrabartyD. (2017). A novel fungal arsenic methyltransferase, WaarsM reduces grain arsenic accumulation in the transgenic rice plant.J. Hazard. Mater.344626634. 10.1016/j.jhazmat.2017.10.037

  • 371

    VestenaS.CambraiaJ.RibeiroC.OliveiraJ. A.OlivaM. A. (2011). Cadmium-induced oxidative stress and antioxidative enzyme response in water hyacinth and salvinia.Braz. J. Plant Physiol.23131139. 10.1590/S1677-04202011000200005

  • 372

    ViolanteA.CozzolinoV.PerelomovL.CaporaleA.PignaM. (2010). Mobility and bioavailability of heavy metals and metalloids in soil environments.J. Soil Sci. Plant Nutr.10268292. 10.4067/S0718-95162010000100005

  • 373

    VollmannJ.LosakT.PachnerM.WatanabeD.MusilovaL.HlusekJ. (2015). Soybean cadmium concentration: validation of a QTL affecting seed cadmium accumulation for improved food safety.Euphytica203177184. 10.1007/s10681-014-1297-8

  • 374

    WahidA.GhaniA. (2008). Varietal differences in mungbean (Vigna radiata) for growth, yield, toxicity symptoms and cadmium accumulation.Ann. Appl. Biol.1525969. 10.1111/j.1744-7348.2007.00192.x

  • 375

    WangF.ChenF.CaiY.ZhangG.WuF. (2011). Modulation of exogenous glutathione in ultrastructure and photosynthetic performance against Cd stress in the two barley genotypes differing in Cd tolerance.Biol. Trace Elem. Res.14412751288.

  • 376

    WangH.GaoB.WangS.FangJ.XueY.YangK. (2015). Removal of Pb(II), Cu(II), and Cd(II) from aqueous solutions by biochar derived from KMnO4 treated hickory wood.Bioresour. Technol.197356362.

  • 377

    WangK.LiuY.SongZ.WangD.QiuW. (2019). Chelator complexes enhanced Amaranthus hypochondriacus L. phytoremediation efficiency in Cd-contaminated soils.Chemosphere237:124480. 10.1016/j.chemosphere.2019.124480

  • 378

    WangS.LiuJ. (2014). The effectiveness and risk comparison of EDTA with EGTA in enhancing Cd phytoextraction by Mirabilis jalapa L.Environ. Monit. Assess.186751759. 10.1007/s10661-013-3414-x

  • 379

    WenE.YangX.ChenH.ShaheenS. M.SarkarB.XuS.et al (2020). Iron-modified biochar and water management regime-induced changes in plant growth, enzyme activities, and phytoavailability of arsenic, cadmium and lead in a paddy soil.J. Hazard. Mater.407:124344. 10.1016/j.jhazmat.2020.124344

  • 380

    World Health Organization [WHO] (2007). Health Risks of Heavy Metals from Long-Range Transboundary Air Pollution.Copenhagen: World Health Organization.

  • 381

    WuF.ZhangG.DominyP.WuH.BachirD. M. (2007). Differences in yield components and kernel Cd accumulation in response to Cd toxicity in four barley genotypes.Chemosphere708392.

  • 382

    WiebeK.HarrisN.FarisJ.ClarkeJ.KnoxR. E.TaylorG. J.et al (2010). Targeted mapping of Cdu1-B, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum).Theor. Appl. Genet.12110471058. 10.1007/s00122-010-1370-1

  • 383

    WodalaB.EitelG.GyulaT.ÖrdögA.HorváthF. (2012). Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P 700 absorbance in pea leaves.Photosynthetica50380386. 10.1007/s11099-012-0045-3

  • 384

    WuB.HeT.WangZ.QiaoS.WangY.XuF.et al (2020). Insight into the mechanisms of plant growth promoting strain SNB6 on enhancing the phytoextraction in cadmium contaminated soil.J. Hazard Mater.385:121587. 10.1016/j.jhazmat.2019.121587

  • 385

    WuD.SatoK.MaJ. F. (2015). Genome-wide association mapping of cadmium accumulation in different organs of barley.New Phytol.208817829. 10.1111/nph.13512

  • 386

    WuZ.WuW.ZhouS.WuS. (2016). Mycorrhizal inoculation affects Pb and Cd accumulation and translocation in pakchoi (Brassica chinensis L.).Pedosphere261326. 10.1016/S1002-0160(15)60018-2

  • 387

    XiaoR.WangP.MiS.AliA.LiuX.LiY.et al (2019). Effects of crop straw and its derived biochar on the mobility and bioavailability in Cd and Zn in two smelter-contaminated alkaline soils.Ecotoxicol. Environ. Saf.181155163. 10.1016/j.ecoenv.2019.06.005

  • 388

    XieY.SuL.HeZ.ZhangJ.TangY. (2021). Selenium inhibits cadmium absorption and improves yield and quality of cherry tomato (Lycopersicon esculentum) under cadmium stress.J. Soil Sci. Plant Nutr.271247612490. 10.1007/s42729-021-00427-x

  • 389

    XuD.ChenZ.SunK.YanD.KangM.ZhaoY. (2013). Effect of cadmium on the physiological parameters and the subcellular cadmium localization in the potato (Solanum tuberosum L.).Ecotoxicol. Environ. Saf.97147153. 10.1016/j.ecoenv.2013.07.021

  • 390

    XuS. S.LinS. Z.LaiZ. X. (2015). Cadmium impairs iron homeostasis in Arabidopsis thaliana by increasing the polysaccharide contents and the iron-binding capacity of root cell walls.Plant Soil3927185. 10.1007/s11104-015-2443-3

  • 391

    XuW.LiY.HeJ.MaQ.ZhangX.ChenG.et al (2010). Cd uptake in rice cultivars treated with organic acids and EDTA.J. Environ. Sci.22441447.

  • 392

    XueD.ChenM.ZhangG. (2009). Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.).Euphytica165587596. 10.1007/s10681-008-9785-3

  • 393

    XueZ. C.GaoH. Y.ZhangL. T. (2013). Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings.Biol. Plant.57587590. 10.1007/s10535-013-0318-0

  • 394

    YangP.ZhouX. F.WangL. L.LiQ. S.ZhouT.ChenY. K.et al (2018). Effect of phosphate-solubilizing bacteria on the mobility of insoluble cadmium and metabolic analysis.Int. J. Environ. Res. Public Health15:1330. 10.3390/ijerph15071330

  • 395

    YangY.GeY.ZengH.ZhouX.PengL.ZengQ. (2017). Phytoextraction of cadmium contaminated soil and potential of regenerated tobacco biomass for recovery of cadmium.Sci. Rep.7:7210. 10.1038/s41598-017-05834-8

  • 396

    YangY.XiongJ.TaoL.CaoZ.TangW.ZhangJ.et al (2020). Regulatory mechanisms of nitrogen (N) on cadmium (Cd) uptake and accumulation in plants: a review.Sci. Total Environ.708:135186. 10.1016/j.scitotenv.2019.135186

  • 397

    YanL.RiazM.WuX.DuC.LiuY.LvB.et al (2018). Boron inhibits aluminuminduced toxicity to citrus by stimulating antioxidant enzyme activity.J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev.36145163. 10.1080/10590501.2018.1490513

  • 398

    YaoP.ZhouH.LiX.WeiL.WangJ.ZhangS.et al (2021). Effect of biochar on the accumulation and distribution of cadmium in tobacco (Yunyan 87) at different developmental stages.Ecotoxicol. Environ. Saf.207:111295. 10.1016/j.ecoenv.2020.111295

  • 399

    YingR. R.QiuR. L.TangY. T.HuP. J.QiuH.ChenH. R.et al (2010). Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata.J. Plant Physiol.1678187. 10.1016/j.jplph.2009.07.005

  • 400

    YounisU.MalikS. A.RizwanM.QayyumM. F.OkY. S.ShahM. H. R.et al (2016). Biochar enhances the cadmium tolerance in spinach (Spinacia oleracea) through modification of Cd uptake and physiological and biochemical attributes.Environ. Sci. Pollut. Res.232138521394. 10.1007/s11356-016-7344-3

  • 401

    YousafB.LiuG.WangR.Zia-ur-RehmanM.RizwanM. S.ImtiazM.et al (2016). Investigating the potential influence of biochar and traditional organic amendments on the bioavailability and transfer of Cd in the soil–plant system.Environ Earth Sci.75:374. 10.1007/s12665-016-5285-2

  • 402

    YousafM. T. B.NawazM. F.KhawajaH. F.GulS.AliS.AhmadI.et al (2019). Ecophysiological response of early stage Albizia lebbeck to cadmium toxicity and biochar addition.Arab. J. Geosci.1218. 10.1007/s12517-019-4296-1

  • 403

    YuH. Y.LiuC.ZhuJ.LiF.DengD. M.WangQ.et al (2016). Cadmium availability in rice paddy fields from a mining area: the effects of soil properties highlighting iron fractions and pH value.Environ Pollut.2093845. 10.1016/j.envpol.2015.11.021

  • 404

    YuL.GaoR.QinghuaS.WangX.WeiM.YangF. (2013). Exogenous application of sodium nitroprusside alleviated cadmium induced chlorosis, photosynthesis inhibition and oxidative stress in cucumber.Pak. J. Bot.45813819.

  • 405

    YuR.LiD.DuX.XiaS.LiuC.ShiG. (2017). Comparative transcriptome analysis reveals key cadmium transport-related genes in roots of two pakchoi (Brassica rapa L. ssp. chinensis) cultivars.BMC Genom.18:587. 10.1186/s12864-017-3973-2

  • 406

    YuanL.YangS.LiuB.ZhangM.WuK. (2012). Molecular characterization of a rice metal tolerance protein, OsMTP1.Plant Cell Rep.316779. 10.1007/s00299-011-1140-9

  • 407

    YuanP.WangJ.PanY.ShenB.WuC. (2019). Review of biochar for the management of contaminated soil: preparation, application and prospect.Sci. Total Environ.659473490. 10.1016/j.scitotenv.2018.12.400

  • 408

    ZaheerI. E.AliS.MuhammadR.FaridM.ShakoorM. B.GillR. A.et al (2015). Citric acid assisted phytoremediation of copper by Brassica napus L.Ecotoxicol. Environ. Saf.120310317. 10.1016/j.ecoenv.2014.03.007

  • 409

    ZainabN.DinB. U.JavedM. T.AfridiM. S.MukhtarT.KamranM. A.et al (2020). Deciphering metal toxicity responses of flax (Linumusitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils.Plant Physiol. Biochem.1529099. 10.1016/j.plaphy.2020.04.039

  • 410

    ZawoznikM. S.GroppaM. D.TomaroM. L.BenavidesM. P. (2007). Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana.Plant Sci.173190197. 10.1016/j.plantsci.2007.05.004

  • 411

    ZeeshanN.NasirA. A.HaiderF. U.NaveedK.NaseerS.MurtazaG. (2021). Risk assessment of trace metals deposition and growth of Abelmochus esculentus L. on industrially polluted soils ofFaisalabad, Pakistan.Pak. J. Agri. Sci.58881889. 10.21162/PAKJAS/21.409

  • 412

    ZhanF.LiB.JiangM.YueX.HeY.XiaY.et al (2018). Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize.Environ. Sci. Pollut. Res.252433824347. 10.1007/s11356-018-2487-z

  • 413

    ZhangC.YuZ. G.ZengG. M.JiangM.YangZ. Z.CuiF.et al (2014). Effects of sediment geochemical properties on heavy metal bioavailability.Environ. Int.73270281. 10.1016/j.envint.2014.08.010

  • 414

    ZhangC. J.ChenL.ShiD. W.ChenG. X.LuC. G.WangP.et al (2007). Characteristics of ribulose-1, 5-bisphosphate carboxylase and C4 pathway key enzymes in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage.S. Afric. J. Bot.732228. 10.1016/j.sajb.2006.05.002

  • 415

    ZhangF.LiuM.LiY.CheY.XiaoY. (2019). Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa.Sci. Total Environ.65511501158. 10.1016/j.scitotenv.2018.11.317

  • 416

    ZhangG.FukamiM.SekimotoH. (2002). Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage.Field Crops Res.779398. 10.1016/S0378-4290(02)00061-8

  • 417

    ZhangL.GaoC.ChenC.ZhangW.HuangX. Y.ZhaoF. J. (2020). Overexpression of rice OsHMA3 in wheat greatly decreases cadmium accumulation in wheat grains.Environ. Sci. Technol.541010010108. 10.1021/acs.est.0c02877

  • 418

    ZhangM.LiuX.YuanL.WuK.DuanJ.WangX.et al (2012). Transcriptional profiling in cadmium-treated rice seedling roots using suppressive subtractive hybridization.Plant Physiol. Biochem.507986. 10.1016/j.plaphy.2011.07.015

  • 419

    ZhangS.QuanL.ZhuY.YanJ.HeX.ZhangJ.et al (2020). Differential effects of three amendments on the immobilisation of cadmium and lead for Triticum aestivum grown on polluted soil.Environ. Sci. Pollut. Res.274043440442. 10.1007/s11356-020-10079-6

  • 420

    ZhaoF. J.MaY.ZhuY. G.TangZ.McGrathS. P. (2015). Soil contamination in China: current status and mitigation strategies.Environ. Sci. Technol.49750759. 10.1021/es5047099

  • 421

    ZhaoJ.YangW.ZhangS.YangT.LiuQ.DongJ.et al (2018). Genome-wide association study and candidate gene analysis of rice cadmium accumulation in grain in a diverse rice collection.Rice11:61. 10.1186/s12284-018-0254-x

  • 422

    ZhaoK.LiuX.XuJ.SelimH. M. (2010). Heavy metal contaminations in a soil–rice system: identification of spatial dependence in relation to soil properties of paddy fields.J. Hazard. Mater.181778787. 10.1016/j.jhazmat.2010.05.081

  • 423

    ZhenH.JiaL.HuangC.QiaoY.LiJ.LiH.et al (2020). Long-term effects of intensive application of manure on heavy metal pollution risk in protected-field vegetable production.Environ. Pollut.263:114552. 10.1016/j.envpol.2020.114552

  • 424

    ZhouC.ZhuL.MaZ.WangJ. (2017). Bacillus amyloliquefaciens SAY09 increases cadmium resistance in plants by activation of auxin-mediated signaling pathways.Genes8:173. 10.3390/genes8070173

  • 425

    ZhuW.DuW.ShenX.ZhangH.DingY. (2017). Comparative adsorption of Pb and Cd by cow manure and its vermicompost.Environ. Pollut.2278997. 10.1016/j.envpol.2017.04.048

  • 426

    ZhuY.WangH.LvX.ZhangY.WangW. (2020). Effects of biochar and biofertilizer on cadmium-contaminated cotton growth and the ant oxidative defense system.Sci. Rep.10112. 10.1038/s41598-020-77142-7

  • 427

    ZhuoF.ZhangX. F.LeiL. L.YanT. X.LuR. R.HuZ. H.et al (2020). The effect of arbuscular mycorrhizal fungi and biochar on the growth and Cd/Pb accumulation in Zea mays.Int. J. Phytoremediation2210091018. 10.1080/15226514.2020.1725867

  • 428

    Zia-ur-RehmanM.ZafarM.WarisA. A.RizwanM.AliS.SabirM.et al (2020). Residual effects of frequently available organic amendments on cadmium bioavailability and accumulation in wheat.Chemosphere244:125548. 10.1016/j.chemosphere.2019.125548

  • 429

    ZivkovicL. I.RikalovicM.CvijovicG. G.KazazicS.VrvicM.BrceskiI.et al (2018). Cadmium specific proteomic responses of a highly resistant Pseudomonas aeruginosasan ai.RSC Adv.810541 10549.

  • 430

    ZouariM.ElloumiN.AhmedC. B.DelmailD.RouinaB. B.AbdallahF. B.et al (2016). Exogenous proline enhances growth, mineral uptake, antioxidant defense, and reduces cadmium-induced oxidative damage in young date palm (Phoenix dactylifera L.).Ecol. Engg.86202209. 10.1016/j.ecoleng.2015.11.016

  • 431

    ZulfiqarU.AyubA.HussainS.WaraichE. A.El-EsawiM. A.IshfaqM.et al (2021). Cadmium toxicity in plants: recent progress on morpho-physiological effects and remediation strategies.J. Soil Sci. Plant Nutr.[Epub ahead of print]. 10.1007/s42729-021-00645-3

  • 432

    ZulfiqarU.FarooqM.HussainS.MaqsoodM.HussainM.IshfaqM.et al (2019). Lead toxicity in plants: impacts and remediation.J. Environ. Manage250:109557. 10.1016/j.jenvman.2019.109557

Summary

Keywords

cadmium, contamination, abiotic stress, plant physiology and growth, remediation

Citation

Zulfiqar U, Jiang W, Xiukang W, Hussain S, Ahmad M, Maqsood MF, Ali N, Ishfaq M, Kaleem M, Haider FU, Farooq N, Naveed M, Kucerik J, Brtnicky M and Mustafa A (2022) Cadmium Phytotoxicity, Tolerance, and Advanced Remediation Approaches in Agricultural Soils; A Comprehensive Review. Front. Plant Sci. 13:773815. doi: 10.3389/fpls.2022.773815

Received

10 September 2021

Accepted

02 February 2022

Published

09 March 2022

Volume

13 - 2022

Edited by

Ann Cuypers, Hasselt University, Belgium

Reviewed by

Bhumi Nath Tripathi, Indira Gandhi National Tribal University, India; Mohsin Tanveer, University of Tasmania, Australia

Updates

Copyright

*Correspondence: Wang Xiukang, Adnan Mustafa,

†These authors have contributed equally to this work

This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Outline

Figures

Cite article

Copy to clipboard


Export citation file


Share article

Article metrics