Cadmium Toxicity in Plants

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Cadmium Toxicity in Plants: Unveiling the Physicochemical and Molecular Aspects Rajarshi Ghosh1, Sujit Roy2 1Department

of Chemistry, The University of Burdwan, Burdwan, India; 2Department of Botany, UGC Centre for Advanced Studies, The University of Burdwan, Burdwan, India

1. INTRODUCTION In the modern era, heavy metals are a major environmental pollutant (Berry, 1986; Kevresan et al., 1998). Various heavy metals accumulate in soil through natural processes (lithogenic and pedogenic), while anthropogenic activities such as mining, industrial and urban waste disposal, combustion of fossil fuels, soil runoff, metalworking industries, applications of chemical fertilizers, solid waste disposal from municipalities, and effluents from sewage treatment plants are also significantly contributors to the accumulation of heavy metals in agricultural fields and adjoining regions. Heavy metals may also accumulate in the soil through additional processes, including defective agricultural practices and frequent use of sludge in agricultural land (Foy et al., 1978). Even low levels of heavy metal contamination in the soil for long periods cause changes in different soil properties and thus result in decreased agricultural yields (Salt and Rauser, 1995; Akinola and Ekiyoyo, 2006). The 53 elements placed in the d-block of the periodic table are generally considered “heavy metals” based on their densities (>5 g cm−3). Plant cells make use of only 19 inorganic elements categorized as macroelements (C, O, H, Mg, S, N, Cd, P, and K) and microelements (Cu, Zn, Mn, Fe, Mo, B, Ni, Co, Cl, and Br) based on their requirements in various plant metabolic processes. Plants utilize some heavy metals as microelements for different physiological and biochemical processes; however, increased levels of other heavy metals, such as Cd, Pb, Al, Hg, and Cr, are toxic for plants, causing chlorosis, decreased photosynthetic yield, imbalances in water uptake and nutrient assimilation, and finally reduced biomass production.These factors disrupt the normal patterns of plant growth and development as well as crop productivity (Singh et al., 2016). Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches ISBN 978-0-12-815794-7 https://doi.org/10.1016/B978-0-12-815794-7.00008-4

© 2019 Elsevier Inc. All rights reserved.

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Cadmium (Cd), being a nontransitional element in the periodic table, is toxic in nature because it is soft according to hard and soft acids and bases (HSAB) theory (Nadezda, 2017), which means the dense electron cloud around it (it has [Kr]4d105s2 electronic configuration) can easily be polarized by a positive electric field. In acid–base type reactions, soft–soft and hard–hard type interactions, according to HSAB theory, are always preferred. That is why Cd2+ likes to bind with S2−, which is also soft in nature. For this very reason, Cd(II) contamination in any biological system may be fatal, as it easily binds to the –SH (thiol) group of proteins and hence disrupts their activity. Plants absorb water and other mineral nutrients via the roots that first encounter the heavy metals, and much evidence indicates root-growth inhibition in plants in heavy metal–contaminated soil. These effects may be correlated with reduced mitotic activity in the root meristem (Hossain et al., 2012) following exposure of root meristematic cells to Cr (VI) and Cd2+ ions, which inhibits the cell cycle (Sundaramoorthy et al., 2010) by disrupting the activities of some key cell cycle regulators such as S-phase– specific cyclin-dependent protein kinases. In addition, heavy metals interfere with the auxin transport system in roots, thus inhibiting root growth (Zobel et al., 2007). In developing countries, rapid industrialization, increased anthropogenic activities, and modern agricultural practices have contributed to increased levels of heavy metal contamination in nature and represent a major threat for plant health and crop yield. Soil contamination with heavy metals, such as Cd and lead, creates important stress conditions for plants.Various studies have clearly demonstrated inhibition of seed germination and poor seedling growth in heavy metal–contaminated soil due to the inhibition of DNA metabolism (Zhang et al., 2002; Li et al., 2006). In general, heavy metal ions compete with other essential nutrient metal ions for binding and absorption in the root cell surface. After entering into the plant cell, heavy metal ions interfere with protein structure and function by directly attacking thiol protein groups, causing conformation change in the protein structure and eventually loss of function. Thus, heavy metal ions generate toxic effects inside plant cells. Apart from this, heavy metals activate reactive oxygen species (ROS) generation via oxidative stress and eventually cause oxidative damage to key biomolecules and the photosynthetic apparatus. At physiological, biochemical, and molecular levels, these effects are associated with membrane damage, reduced chlorophyll production, and thus photosynthetic yield, hormonal and nutrient imbalance, inhibition of nucleic acid

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metabolism, and cell division (Singh et al., 2009). When present in excess, heavy metal–mediated toxicity negatively affects plant growth and development and eventually may cause loss of cell viability (Gwozdz et al., 1997; Das et al., 1997; Sandalio et al., 2001; Sharma and Dubey, 2007). To adapt and survive under heavy metal stress, plants have developed sophisticated and coordinated interlinked network systems for detoxification of the harmful effects of heavy metals (Clemens, 2001; Cobbett and Goldsbrough, 2002; Shingu et al., 2005).

2. SOURCES OF HEAVY METALS AND ENVIRONMENTAL CHEMICAL TOXICITY Among the known heavy metals, the effects of Cd2+, Cu2+, Hg2+, Ni2+, Pb2+, and Zn2+ have been extensively studied in plants, because these heavy metal elements, when present in elevated concentrations, inhibit plant growth and development via the generation of cytotoxic and genotoxic effects. Cd-mediated chemical toxicity and its detrimental effects on crop growth and yield have become a major concern in agricultural lands adjoining industrial regions. In nonpolluted soil, the Cd concentration generally ranges from 0.04 to 0.32 mM, whereas in heavy metal–contaminated soil, the Cd concentration ranges from 0.32 to more than 1 mM (Sanita di Toppi and Gobbrielli, 1999). Cd is a major heavy metal mainly used in industrial areas and associated with the processing of metals, the smelting of zinc and other metals, and heavy road traffic (Somashekaraiah et al., 1992; Das et al., 1997). Apart from itself, Cd is always present in commercial zinc. Zinc is the lighter congener of Cd in the periodic table. Thus, having close ionic radii and the same oxidation level (i.e. having a close ionic potential that is mathematically expressed as the charge/radius ratio), commercial zinc is generally contaminated with Cd.This makes it difficult to control the introduction of Cd into nature because commercial zinc is extensively used in our daily life as brass, dry cells, pigments, etc. The close ionic potentials of Zn(II) and Cd(II) have one additional serious effect. The latter can easily substitute for Zn(II) in several enzymes and produce system toxicity. In general, heavy metal elements are not metabolized rapidly, and gradually accumulate in the environment and biological systems. In plants, with their intrinsic immobility, the roots are primarily the binding sites for the metal ions, whereas in aquatic plants, almost the whole plant body becomes exposed to heavy metal–polluted water. Furthermore, metal ions are also directly absorbed by leaves due to the deposition of metal ion particles on leaf

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surfaces (Gill, 2014). As mentioned earlier, heavy metal elements accumulate in the environment from various sources, including natural, agricultural, industrial, and domestic effluents, and atmospheric pollutants. In nature, heavy metals originate within the earth’s crust and become available in the soil during the weathering process. Earlier studies have established increased accumulation levels of various heavy metal elements, such as Cd, Co, Cr, Cu, Hg, Mn, Ni, Pb, Sn, and Zn, in geologic plant materials (Kavamura and Esposito, 2010; Wuana and Okieimen, 2011). Igneous rocks, such as olivine, augite, and hornblende, contribute appreciable amounts of Mn, Co, Ni, Cu, and Zn to the soil. Among sedimentary rocks, shale crust contains considerably higher concentrations of various heavy metals, including Cr, Mn, Co, Ni, Cu, Zn, Cd, Sn, Hg, and Pb. Moreover, limestone and sandstone represent an important source of heavy metal elements.Volcanic eruptions and forest fires also significantly contribute high levels of heavy metal elements that eventually accumulate in nature. In agricultural soils, the major sources of heavy metal elements are mainly inorganic and organic fertilizers, contaminated irrigation water, pesticides, and fungicides. In industrial and adjoining regions, heavy metals enter into the environment in the form of particles and vapors from high-temperature metals processing, such as smelting and casting. The vapor forms of heavy metals, which mainly include As, Cd, Cu, Pb, Sn, and Zn, combine with water in the atmosphere to form aerosols that are subsequently dispersed by wind or become precipitated during rainfall, contaminating the soil and water bodies. Mining, erosion from mine wastes, corrosion of metals, and the leaching of heavy metals along with other industrial wastes also contaminate soil and groundwater systems. In addition, processing of plastics, textiles, and microelectronics as well as wood preservation and paper processing, contribute heavy metal elements to the soil. Domestic effluents also regularly contribute increased levels of heavy metal elements and other chemical components into rivers and lakes (Tchounwou et al., 2012).

3. CADMIUM: HISTORICAL PERSPECTIVES AND CHEMICAL PROPERTIES The name “cadmium” comes from cadmia, the Latin word for calamine, which are basically zinc-based minerals. In 1817, the Prussian physician Johann Roloff suspected the arsenic contamination in a batch of zinc oxide. Later it was proved that some other, unknown element was present. Meanwhile, Friedrich Stromeyer, a professor at the University of Göttingen, found that zinc carbonate, upon heating, left behind a yellow residue. He also

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suspected the presence of some unknown element. In this way, the new element Cd appeared in the domain of chemistry (Nadezda, 2017). Cd is a member of period 5 and group 12 of the periodic table, has an atomic weight 112.411, and is considered a heavy metal. As mentioned earlier, according to HSAB theory, Cd likes to bind with sulfur, thus creating calcium sulfide (CdS), which is yellow in color. The source of this color is due to transfer of electrical charge (electron density) from the metal (Cd) orbital to the ligand (sulfide) orbital. The intense yellow color of CdS and related compounds (cadmium sulfoselenides) makes these useful pigments, and the typical color is known as “cadmium yellow.” Nowadays, CdS and CdSe nanoparticles are well-known quantum dots. Cd has no known function in higher organisms. Rather, it appears as toxic and because of this, its use in daily life has become limited. In pigments used for various purposes, cadmium sulfides have been replaced by different-colored organic azo compounds.

4. UPTAKE, TRANSPORT, TRANSLOCATION, AND SEQUESTRATION OF CADMIUM IN PLANTS Heavy metals make their entry into plant bodies through suitable transport systems. In higher plants, the uptake of inorganic nutrients and heavy metal ions from the soil is regulated by root exudates and rhizospheric microorganisms. The absence of any direct biological function for heavy metal ions such as Cd and Pb is suggested as the prime reason for the nonexistence of their specific transporters in plants. For instance, arsenic (As), being a chemical analogue of phosphate, enters into plant cells through phosphate transporters (Rogers et al., 2000). Some hyperaccumulators of heavy metals absorb various concentrations of heavy metals. Heavy metal uptake by hyperaccumulating plant species is critically affected by various factors such as soil pH, the availability of water, and the presence of other organic compounds in the rhizosphere. Soil pH acts as an important factor in the dissolution of heavy metals and acidification of the rhizosphere, helping the growth of heavy metal–accumulating plant species. The dissolution of heavy metal ions through complex formation by organic substances released from the rhizosphere of hyperaccumulating plants is known to enhance root absorption (Krishnamurti et al., 1997). Plant cell membrane systems possess various transporters essential for metal uptake and homeostasis. Different heavy metal ions are generally cotransported along with other soil nutrients across the plasma membrane in roots and variations in substrate specificity. The metal transporters, located on the plasma membrane and tonoplast, are important for

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regulation of the physiological concentrations of heavy metals in plant cells. The members of ZIP family transporters, such as ZIP6 and ZIP9 in Arabidopsis halleri and ZTN1 and ZTN2 in Thlaspi caerulescens, are involved in preferential transport of Zn over Cd with decreased Cd uptake under high concentrations of Zn (Weber et al., 2006). In Arabidopsis thaliana, IRT1, another member of the ZIP family of transporters, has been shown to be involved in the transport of Cd2+, Fe2+, Mn2+, Ni2+, and Zn2+ (Rogers et al., 2000). In addition, the NRAMP metal transporters are also known to participate in the transport of various heavy metal ions, particularly Cd2+, Ni2+, Co2+, Cu2+, Mn2+, Zn2+, and Fe2+, across plasma membranes (Nevo and Nelson, 2005). After uptake via transporters in root cells, heavy metal ions are then loaded onto xylem elements and transported to the shoots as complex with various metal ion chelators. The heavy metal–associated (HMA) transporters are P-type ATPases and act as efflux pumps to remove heavy metal ions from cells. In addition, HMAs are involved as internal transporters for loading Cd and Zn metals into xylem elements from adjoining regions. In A. thaliana, AtHMA4 protein acts as a plasma membrane-based P-type ATPase and also is involved in detoxification of Cd to prevent the disruption of cytosolic free Ca2+. AtHMA3 functions as a Zn/Cd transporter and has been shown to be involved in regulating Cd and Zn homeostasis (Mills et al., 2005; Mendoza-Cózatl et al., 2011). Plants activate additional mechanisms for sequestering heavy metal ions into intracellular compartments through the activity of various membrane transporters. In this context, ABC transporters play a crucial role in transporting heavy metals into the vacuole. AtMRP1 and AtMRP2 are two important members of the ABC family of transporters in Arabidopsis and are involved in transporting phytochelatin (PC)–Cd complexes into the vacuole (Song et al., 2014) Again in Arabidopsis, AtPDR8, another ABC family transporter, confers heavy metal tolerance by functioning as an efflux pump for Cd in the plasma membrane of root hairs and epidermal cells (Kim et al., 2007). In Arabidopsis, plasma membrane–based ZIP (ZRT, IRT-like protein) transporters are activated under Zn-limiting conditions and involved in Cd detoxification (Komal et al., 2015).

5. PLANT RESPONSES TO CADMIUM STRESS Abiotic stresses are the major causes of more than 50% of the losses in crop yields worldwide for most crops (Bray et al., 2000; Barnabas et al.,

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2008; Rodziewicz et al., 2014; Pandey et al., 2017). Plants, with their intrinsic immobility and obligatory dependence on sunlight, are vastly exposed to various environmental stress factors, including heavy metal elements that activate a wide range of physiological and metabolic responses. After their entry inside the plant cell through specific transporters, heavy metal elements generally bind to the functional sites of structural and functional proteins and membrane lipids, leading to changes in their native conformations, interfering with the production of essential cellular metabolites, creating osmotic imbalances, and finally inhibiting normal cell functioning (Aslam et al., 2014). In addition, heavy metal elements have genotoxic either directly via direct binding and cleavage of DNA or indirectly through oxidative damage of nucleic acids through the production of ROS (Erdei et al., 2002; Nada et al., 2007; Pandey et al., 2009). Some general responses of plants to heavy metal toxicity include reduced seed germination rate and seedling growth, leaf chlorosis, compromised photosynthetic rate, loss of cell turgor, necrosis, and early senescence (Gamalero et al., 2009). Heavy metal ions interfere with the light reaction of photosynthesis and reduce CO2 assimilation via inhibition of activity or disruption of the structural stability of RUBP carboxylase activity through interactions with thiol groups. In addition, heavy metals interfere with the nitrogen metabolism process in plants by inhibiting the activity of key enzymes, such as nitrate reductase (NR), nitrite reductase, glutamine synthetase, glutamine oxoglutarate aminotransferase, and glutamine dehydrogenase, involved in nitrate and ammonia metabolism and assimilation (Chaffei et al., 2003). Plants growing in Cd-contaminated soil frequently suffer from the primary nitrogen assimilation and metabolism process because of inhibition in nitrogen uptake and transport with the inhibition of NR and glutamine synthetase activities. Plant cells respond to heavy metal–mediated toxicity through complex interlinked coordinated mechanisms that include both immediate and long-term responses. The immediate responses are associated with rapid changes in the transcriptional rates of hundreds or even thousands of responsive genes with concomitant changes at physiological and metabolic levels. Long-term responses, on the other hand, are associated with genetic modification and epigenetic changes (Zhang et al., 1998). Regulation of gene expression, which functions as an integral part of plant stress response, generally involves both general and specific changes of transcript levels of stress-responsive genes (Shinozaki and Yamaguchi-Shinozaki, 2000).

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6. PLANT HEALTH UNDER CADMIUM STRESS At relatively low concentrations, Cd interferes with plant metabolism processes (Van Asshe and Clijsters, 1990), whereas at higher concentrations, Cd inhibits plant cell growth and development and growth of the whole plant (Aery and Rana, 2003; Prasad, 1995). The presence of Cd in the soil has been shown to reduce plant growth in various plant species, including soybeans (Dewdy and Ham, 1997) and chickpeas (Hasan et al., 2007b). Earlier reports have shown decreased chlorophyll and carotenoid contents and increased nonphotochemical quenching in Brassica napus due to Cd-mediated toxicity (Larsen et al., 1998). Similar effects have been documented in several other plant species grown under Cd stress (Griffiths et al., 1995; Ferretti et al., 1993; Imai et al., 1996; Pandey et al., 2007). Thus Cd acts as an effective inhibitor of photosynthesis (Chugh and Sawhney, 1999; Vassilev et al., 2005). Cd-mediated oxidative stress and ROS generation cause damage to the photosynthetic apparatus and the light harvesting complex, thus disrupting the structural integrity of photosystems I and II and resulting in decreased photosynthetic yield (Siedlecka and Krupa, 1996). Cd-mediated inhibition of Fe(III) reductase activity in roots leads to Fe(II) deficiency, which again inhibits the overall rate of photosynthesis (Alkantara et al., 1994). In addition, Cd inhibits stomatal opening and thus interferes with transpiration (Poschenrieder et al., 1989). Cd stress-mediated toxicity has been shown to cause decreased protein content in various crops, and the grains with reduced protein content have been reported for crops grown in Cd-contaminated soil (Salgare and Achareke, 1992; Tamas et al., 1997). Cd-mediated cytotoxicity affects the activity of various key enzymes involved in different metabolic pathways and thus plays a pivotal role in regulating plant growth and development. NR acts as the key enzyme in nitrate assimilation pathway and plays important role in the regulation of plant growth and development (Solomonson and Barber, 1990). Elevated level of Cd in the soil has been found to inhibit NR activity and thus nitrate assimilation in various plant species, including maize (Hernandez et al., 1996), pea (Burzynski, 1988), bean and tomato (Quariti et al., 1997) and Cicer arietinum (Hasan et al., 2007a). Cd-mediated inhibition of carbonic anhydrase activity has been reported in several plant species (Siedlecka and Krupa, 1996), while proline accumulation has been shown to be strongly induced in plants under Cd stress (Chandler and Thorpe, 1987; Roy et al., 1992; Singh and Tiwari, 2003), thus leading to change in the intracellular environment.

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Increased Cd content in the soil has been shown to cause decreased biomass formation in mung beans and inhibits the interaction of Rhizobium in chickpea root nodules, thus reducing dry mass formation (Shen et al., 2010; Rana and Ahmad, 2002). In general, Cd-contaminated soil shows a considerable decrease in the population of nitrogen-fixing bacteria and inhibition in root nodule formation. The presence of Cd in the soil has been shown to inhibit the nodulation process and nitrogenase activity in several plant species, including Glycine max, Pisum sativum (Dhingra and Priefer, 2006), Phaseolus vulgaris (Dewdy and Ham, 1997), and Trifolium repens. Cd contamination in soil causes simultaneous decrease in leghemoglobin content and nitrogenase activity (Comba et al., 1998), while Cd2+mediated oxidative stress has been shown to cause senescence of root nodules in soybeans (Balestrasse et al., 2001).

7. CADMIUM STRESS STIMULATES AND INTEGRATES VARIOUS SIGNALING PATHWAYS IN PLANTS Plant response to heavy metal stress involves a coordinated signaling network that is activated rapidly after sensing the presence of a heavy metal signal. The existence of a heavy metal element in the extracellular environment activates different signaling networks, such as the Ca–calmodulin pathway, phytohormonal response, and ROS-mediated signaling, and also involves the mitogen-activated protein kinase (MAPK)-mediated phosphorylation cascade. Ca2+ signaling has been found to be an intrinsic component of various abiotic stress signaling networks (Carroll et al., 1998; PerfusBarbeoch et al., 2002; Wilkins et al., 2016). Elevated levels of heavy metals generally affect the stability of Ca2+-channels, leading to increased calcium flux into the cell. The intracellular free calcium then acts as a common second messenger for heavy metal–mediated abiotic stress responses and regulates the expressions of important target genes involved in heavy metal transportation, metabolism, and tolerance. Studies in yeast cells (Saccharomyces cerevisiae) have shown involvement of Ca2+ following exposure to increased levels of various heavy metal elements, particularly Cd2+. The rise in cytosolic Ca2+ in the presence of Cd2+ has been found to be outcome of transportation of external Ca2+ through the Cch1p/Mid1p channel (Ruta et al., 2014). Based on the dose and potential for the generation of hydroxyl radicals, heavy metals like Cd regulate the level of cytosolic Cd2+ ions in roots.

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Previously, the impact of heavy metals, particularly Cd on ROS generation and the activation of nitric oxide (NO) and MAPK networks has been extensively reviewed in diverse plant species (Chmielowska-Bak et al., 2014). Cd has received special attention because of its relation with Ca in terms of size and is suggested as disruptive to the Ca2+-mediated signaling network after entering into plant cells. Cd affects plant cells via depolarization of the root epidermal plasma membrane, thus impairing Ca2+ influx and leading to root growth inhibition (Li et al., 2012). In A. thaliana, earlier studies have indicated that exposure of plants to increased levels of Cd inhibits root hair growth, disordering the Ca2+ influx and finally affecting the terminal cytosolic Ca2+ gradient that is essential for root growth (Fan et al., 2011). The intracellular levels of various phytohormones and the hormonal balance have been found to be important for regulating the signaling networks that are activated in response to heavy metal stress. This mechanism involves the cross-talks of the phytohormone signaling network with other signaling pathways, such as the ROS, NO, and MAPK signaling pathways (Liptáková et al., 2012; Wang et al., 2013), Exogenous applications of phytohormones have been shown to be beneficial for plants in neutralizing the harmful effects of heavy metal–mediated toxicity (Agami and Mohamed, 2013; Masood et al., 2016). In Arabidopsis, mustard, pea, and soybean, increased ethylene biosynthesis after Cd treatment has been reported (Arteca and Arteca, 2007; Rodríguez-Serrano et al., 2009). In onion (Allium cepa) and tomato (Lycopersicum esculentum), the role of ethylene has been implicated in the accumulation of H2O2 after Cd treatment (Liu et al., 2008). Cd treatment induces abscisic acid biosynthesis in the roots of various plant species (Stroinski et al., 2010). In general, it has been suggested that heavy metal stress activates ethylene production in plant cells that further generates signals for the synthesis of other phytohormones, such as auxins and cytokinins, while H2O2 accumulation following Cd stress activates antioxidant production. Together these effects may lead to improved tolerance against Cd-mediated cytotoxicity. In Glycine max (soybean), Cd stress in seedlings induces ethylene biosynthesis and also expression of genes related to polyamine metabolism, NO generation, and MAPK cascades (Chmielowska-Bąak et al., 2013), suggesting the integration of different signaling networks in response to heavy metal stress. MAPK signaling networks have also been shown to regulate plant responses to heavy metal stress. In Medicago sativa (alfalfa), exposure of seedlings to increased levels of Cd ions activates four MAPKs—SIMK, MMK2,

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MMK3, and SAMK (Jonak et al., 2014). A novel MAPK, OsMSRMK2 has been shown to be activated in response to excess levels of Cd in japonica rice cultivar (Agrawal et al., 2002). In Arabidopsis, the accumulation of physiological concentrations of Cd and ROS activate MPK3 and MPK6 transcript expression in a time-dependent manner (Liu et al., 2010), again demonstrating cross-talk between redox signaling and the MAPK network under Cd stress. Overall, these observations clearly indicate the involvement of various signaling pathways, including the phytohormone, calcium, and MAP kinase cascades in plant cells in response to Cd stress.

8. PROTECTION AGAINST CADMIUM STRESS— THE CHELATION MECHANISM Plant cells have developed a vast array of mechanisms to alleviate the harmful effects of heavy metal–mediated toxicity. Several morphological features such as leaf trichomes, thick epidermal cuticle, lignified of cell walls, and root mycorrhizae provide the primary level of defense against heavy metal stress (Hall, 2002). Trichomes are important structures as they have the capacity for immediate storage of heavy metals for subsequent detoxification (Harada et al., 2010). In addition, trichomes release some secondary metabolites to neutralize the harmful effects of heavy metals (Hauser, 2014). Apart from this, plant cells synthesize various other components, including low-molecular-weight proteins, metallochaperones or chelators (PCs, polyamines, nicotianamine, glutathione, etc.), metallothioneins, phenylpropanoid compounds (flavonoids, anthocyanins), and amino acids (proline and histidine) to mitigate the harmful effects of heavy metal stress (Sharma and Dietz, 2006; Dalvi and Bhalerao, 2013). PCs are a thiol group containing low-molecular-weight peptides, produced by PC synthase from glutathione (GSH) and represent one of the major classes of heavy metal chelators in plants (Vatamaniuk et al., 2001). PCs also are a family of metal-binding peptides with high binding affinity to heavy metal for metal homeostasis and detoxification.The synthesis and accumulation of PCs have been shown to be strongly activated in plants under Cd stress. However, in Brassica juncea, exposure to Cd for long periods causes threefold higher accumulation of PCs in leaves than in roots (Heiss et al., 2003). Overexpression of yeast cadmium factor 1 in Arabidopsis has been shown to confer improved tolerance to Cd stress. In addition to PCs, other intracellular ligands, such as glutathione and various polycarboxylic acids, play important roles in the binding and

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detoxification of Cd (Shanthala et al., 2006). Vacuolar sequestration of Cd prevents free circulation of Cd ions in the cytosol (Sanita di Toppi and Gabrielli, 1999). Different organic acids, such as malate, citrate, and oxalate, may confer metal tolerance via the transportation of metals through the xylem and sequestrating of ions in the vacuole. Several reports have also indicated the role of proline in increasing resistance to heavy metal stress in plants. Proline is involved in scavenging of heavy metal–induced ROS generation via detoxification of hydroxyl radicals and quenching of singlet oxygen species (Emamverdian et al., 2015). Metallothioneins (MTs) are another important class of small, low-molecular-weight cysteine-rich polypeptides that play an important role in the detoxification of various metal ions such as Cd, Cu, Zn, and As in plants (Du et al., 2012; Cai and Ma, 2003). MTs mainly operate through cellular sequestration and transport, thereby maintaining homeostasis of intracellular metal ions. In soybean (G. max), various MTs, such as MT1, MT2, and MT3, participate in the Cd detoxification (Pagani et al., 2012).

9. MOLECULAR ASPECTS OF CADMIUM-MEDIATED TOXICITY—ACTIVATION OF OXIDATIVE AND GENOTOXIC STRESS RESPONSE IN THE PLANT GENOME Nonjudicious use of chemical fertilizers, including pesticides, insecticides, fungicides, and other chemical fertilizers, is a major source of chemical toxicity in agricultural fields, resulting in heavy metal contamination of soil, groundwater, and associated water sources. The agricultural fields adjoining industrial regions often contain elevated levels of various heavy metals such as Cd, copper (Cu), lead (Pb), chromium (Cr), and mercury (Hg). Increased intracellular concentrations of heavy metals generally cause oxidative damage to cellular components via ROS generation, disrupt the cellular redox system, and create oxidative stress, while ROSmediated damage in the nuclear genome induces genotoxic stress if it remains unrepaired (Dutta et al., 2018). Plant cells have developed two major antioxidant defense mechanisms against oxidative damage. One such mechanism is associated with the activation of various antioxidant enzymes, such as superoxide dismutase, catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR). These enzymes are involved in direct inactivation of reactive free radicals. The other mechanism involves synthesis and accumulation of nonenzymatic antioxidant compounds, such as phenylpropanoids (flavonoids, tannins, and lignin), GSH,

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carotenoids, ascorbate, and proline, which play key roles in the detoxification of heavy metal–induced ROS and the subsequent removal of free radicals via scavenging to mitigate heavy metal–mediated toxicity (Michalak, 2006; Sharma et al., 2012; Štolfa et al., 2015). Among the various heavy metals, Cd frequently induces oxidative stress in plants via ROS generation and may inactivate the nonenzymatic antioxidant defense (Cho and Seo, 2005). Cd-induced oxidative stress often inhibits biomembrane functioning in plants through membrane lipid peroxidation (Gratao et al., 2005). Cd stress-mediated lipid peroxidation along with increased lipoxygenase activity with reduced superoxidase activity has been reported in Helianthus annuus. Cd stress-mediated activation of peroxidase activity has been reported in various plant species. In other cases, Cd stress has been shown to inhibit the activity of various antioxidant enzymes such as CAT and APX (John et al., 2007). Various studies have demonstrated a clear link between heavy metal– induced oxidative stress and genotoxicity via ROS-mediated DNA damage and genome instability. ROS, generated in plant cells after exposure to abiotic stress such as heavy metals, acts as a key agent of DNA damage, mutagenesis, and genome instability, causing deterioration in plant growth and development and loss of crop productivity. ROS induces various forms of DNA damage, among which 7, 8-dihydro-8-oxoguanine is predominant. Oxidative damage to DNA often causes single- and doublestrand breaks and results in structural abnormalities in chromosomes. These factors severely affect plant growth and development during the early stages of germination due to inhibition of DNA replication and transcription, thus causing loss of cell viability and germination efficiency. Seed germination in heavy metal–contaminated soil is often associated with oxidative stress and ROS generation, resulting in the accumulation of various forms of DNA damage, reducing the germination potential of seeds (Zucca et al., 2013; Mourato et al., 2012). Chickpea (C. arietinum) plants cultivated in soil polluted with various heavy metals such as Cd, Pb, Cr, and Zn have shown decreased seed germination rates with reduced root length. In addition to morphoanatomical defects, the seedlings displayed increased frequency of chromosomal abnormalities, including bridges, laggards, stickiness, and chromosome fragmentation (Siddiqui, 2015). In Vicia faba, an elevated level of Cd accumulation in soil causes ROS-mediated oxidative damage of membrane lipids and also induces a considerable percentage of DNA double-strand breaks and genome instability (Lin et al., 2007).

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10. STRESS ADAPTATION STRATEGY—TRANSCRIPTIONAL AND EPIGENETIC REGULATION IN PLANTS UNDER CADMIUM STRESS Plants respond to stress conditions via rapid change in the expression levels of stress-responsive genes. Therefore, transcriptional regulation of gene expression under heavy metal stress acts as an important and integral part of the stress response network in plants (Roy, 2016). Various transcription factors have been shown to play key roles in regulating plant responses to heavy metal–induced stress through the induction and repression of stress-responsive genes. Transcriptional response under Cd stress has been extensively studied in several plant species. The MYB and WRKY family of transcription factors have been found to be activated in plants after heavy metal stress (Opdenakker et al., 2012). In Arabidopsis, the MYB4 transcription factor, an R2R3-type MYB domain protein, shows strong inducible expression after exposure to Cd and Zn. Interestingly, other members such as MYB43, MYB48, and MYB124 have shown specific induction in roots only in response to Cd stress (van de Mortel et al., 2008). Furthermore, MYB72 and bHLH100, members of the helix–loop–helix transcription factor family, have been found to be involved in heavy metal homeostasis under Cd stress (Sivitz et al., 2012). In Alpine pennycress (T. caerulescens), MYB28 and WRKY53 (a WRKY-binding protein) showed upregulated expression after Cd stress. It has been suggested that the members of WRKY, basic leucine zipper (bZIP), bHLH, MYB, and ethylene-responsive factor (ERF) transcription factor families play crucial roles in regulating specific responses in plants after Cd stress by governing the expression of target genes (Wei et al., 2008). However, Cd-stress related transcriptional response generally operates via the similar signaling networks involved with other abiotic stresses such as soil salinity, temperature extremes, drought, and desiccation, indicating functional overlap of Cd-responsive transcription factors in additional abiotic stress-related signaling pathways as part of general stress response in plants (Fusco et al., 2005). Cd stress has been shown to regulate the expression of ERF1 and ERF2 (ethylene response factor one and 2), which belong to the ethylene-responsive elementbinding protein family/APETALA2. ERF1 and ERF2 bind to dehydration responsive elements (DREs) and to several other pathogenesis-related promoters (Singh et al., 2002). DREB2A (dehydration-responsive element-binding protein 2A) has been shown to be induced by Cd stress

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and binds to the DRE motif of Rd29A (desiccation-responsive) gene, leading to Cd stress-induced expression of the Rd29A protein (Suzuki et al., 2001). In B. juncea, BjCdR15, an orthologue of TGA3 protein, shows rapid induction after brief exposure to Cd and plays a key role in the regulation of expression of various metal transporter genes involved in long-distance root-to-shoot transport of Cd2+ ions. Overexpression of the BjCdR15 gene in transgenic A. thaliana and tobacco plants confers increased tolerance to Cd stress (Farinati et al., 2010). OBF5, a member of the bZIP family of transcription factors, has been shown to be involved in the regulation of expression of glutathione S-transferase under Cd stress. Epigenetic modifications also play a key role in modulating gene expression in plants under various stress conditions, including heavy metal–mediated toxicity. Three major epigenetic mechanisms, DNA methylation, histone modifications, and microRNA-regulated target gene expression, control genome functioning following exposure to stress conditions (Chuang and Jones, 2007). The small RNA molecule regulates the differential pattern of DNA methylation (hypo- and hypermethylation) in various regions of the genome in response to stress. In hemp and clover, exposure to heavy metal induces hypomethylation at several genomic loci (Aina et al., 2004). More recently, it has shown that transgenerational changes in homologous recombination frequency in the progeny population confer better tolerance to heavy metal stress compared with that in the original parental population (Rahavi et al., 2011). Modifications of chromatin structure also act as an essential epigenetic regulatory factor in the regulation of stress-responsive genes and thus stress adaptation in plants (Roy, 2016). Two major pathways regulate the structural stability of chromatin. One is dependent on the histone gene repressor, while the other involves the activity of chromatin assembly factor-1, which is intimately associated with DNA replication. Four major types of histone modifications have been identified—acetylation, methylation, phosphorylation, and ubiquitination (Zhang and Reinberg, 2001). Histone modifications affect gene expression via the modulating of chromatin structure and accessibility of transcription factors at the site of transcription under various abiotic stress conditions, including heavy metal stress (Kim et al., 2008). Analysis of growth and developmental patterns in maize seedlings under heavy metal stress have shown

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that the combination of hyperacetylation and hypoacetylation patterns of specific lysine residues on H3 and H4 histone tails in the promoter regions of cell cycle regulatory genes are important for regulating the expression of cell cycle-related genes following heavy metal stress (Zhao et al., 2014). Various studies have already demonstrated the importance of transcriptional and epigenetic control in the regulation of gene expression in plant genomes under stress. However, detailed information in the context of heavy metal stress is still limited. Additional research is essential to shed more light on the molecular aspects of heavy metal– mediated stress responses and adaptations in plants growing in common heavy metal–contaminated soil.

11. PERSPECTIVE AND CONCLUSIONS Heavy metal stress-mediated effects on plant growth, development, and crop productivity have become a major concern in the past couple decades. Along with the pressure of population growth, the harmful effects of environmental stress on plant health is a major constraint on global food crop production and crop security. These facts are also connected with increasing demand for improvement of abiotic stress tolerance traits in crop plants. Plants respond to abiotic factors such as heavy metal stress at morphoanatomical, physiological, biochemical, and molecular levels to cope with and adjust to stress conditions. In addition, dynamic epigenetic regulation plays a key role in the regulation of plant stress response and has become an important field of research for crop improvements. Genetic engineering technologies for the development of heavy metal stress tolerance in crop plants mainly depend on the manipulation of expression of stress-responsive genes that encode proteins for stress signaling and synthesis of metabolites for heavy metal stress tolerance. Specific targeting and genetic modification of heavy metal stress-responsive genes and the associated transcription factors, metabolites, and additional proteins have been found to be beneficial for improvements in the stress-tolerance capacity of plants. However, the transfer of technology from laboratory conditions to the field requires further extensive research. In general, abiotic stresses are complex in nature and quite difficult to manage under field conditions. Therefore, the development of in-depth knowledge and technology for using biotechnological approaches will provide important future avenues for improved crop performance under heavy metal stress.

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ACKNOWLEDGMENTS The authors sincerely thank CSIR, Govt. of India (Ref. No. 38(1417)/16/EMR-II, dated: 17/05/2016 to SR) and the Department of Higher Education, Science and Technology and Biotechnology (Ref. No. 781(Sanc.)/ST/P/S&T/4G-4/2013 dated 04-12-2014 to RG) for providing necessary financial support. We apologize to all authors whose work was not cited due to space limitations.

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FURTHER READING Eng, B.H., Guerinot, M.L., Eide, D., Saier, M.H., 1998. Membr. J. Biol. 166, 1–7. Grennan, A.K., 2011. Metallothioneins,. A diverse protein family. Plant Physiol. 155 (4), 1750–1751. Meharg, A.A., Hartley-Whitaker, J., 2002. Arsenic up take and metabolism in arsenic resistant and non-resistant plant species. N. Phytol. 154, 29–43. https://doi.org/10.1046/ j.1469-8137.2002.00363.x.