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Plant Signal Behav. Feb 2011; 6(2): 215–222.
Published online Feb 1, 2011. doi:  10.4161/psb.6.2.14880
PMCID: PMC3121981

Cadmium stress tolerance in crop plants

Probing the role of sulfur

Abstract

Plants can't move away and are therefore continuously confronted with unfavorable environmental conditions (such as soil salinity, drought, heat, cold, flooding and heavy metal contamination). Among heavy metals, cadmium (Cd) is a non-essential and toxic metal, rapidly taken up by roots and accumulated in various plant tissues which hamper the crop growth and productivity worldwide. Plants employ various strategies to counteract the inhibitory effect of Cd, among which nutrient management is one of a possible way to overcome Cd toxicity. Sulfur (S) uptake and assimilation are crucial for determining crop yield and resistance to Cd stress. Cd affects S assimilation pathway which leads to the activation of pathway responsible for the synthesis of cysteine (Cys), a precursor of glutathione (GSH) biosynthesis. GSH, a non-protein thiol acts as an important antioxidant in mitigating Cd-induced oxidative stress. It also plays an important role in phytochelatins (PCs) synthesis, which has a proven role in Cd detoxification. Therefore, S assimilation is considered a crucial step for plant survival under Cd stress. The aim of this review is to discuss the regulatory mechanism of S uptake and assimilation, GSH and PC synthesis for Cd stress tolerance in crop plants.

Key words: cadmium, cysteine, glutathione, phytochelatins, stress tolerance, sulfur

Introduction

Abiotic stress is the main factor negatively affecting crop growth and productivity worldwide. Plants are continuously confronted with the harsh environmental conditions (such as soil salinity, drought, heat, cold, flooding and heavy metal contamination). The heavy metal, Cd is commonly released into the arable soil from industrial processes and farming practices1 and has been ranked No. 7 among the top 20 toxins.2 Even at low concentrations, Cd is toxic for most of the plants at concentrations greater than 5–10 µg Cd g−1 leaf dry weight,3 except Cd-hyperaccumulators which can tolerate Cd concentrations of 100 µg Cd g−1 leaf dry weight.46 In spite of its high phytotoxicity, Cd is easily taken up by plant roots and transported to above-ground tissues79 and enters into the food chain where it may pose serious threats to human health.10,11 The International Agency for Research on Cancer in 199312,13 classified Cd as a human carcinogen and, interestingly, it has also been suggested that crops are the main source of Cd intake by humans.14,15 Being highly mobile in phloem,16 Cd can be accumulated in all plant parts which causes stunted growth, chlorosis, leaf epinasty, alters the chloroplast ultrastructure, inhibits photosynthesis, inactivates enzymes in CO2 fixation, induces lipid peroxidation, inhibits pollen germination and tube growth, and also disturbs the nitrogen (N) and sulfur (S) metabolism and antioxidant machinery.1723 Cd can also inhibit the activity of several groups of enzymes such as those of the Calvin cycle,24 carbohydrate metabolism25,26 and phosphorus metabolism.27,28 The effect of Cd on nitrate and S assimilation has been studied in several plants showing an inhibition of the nitrate uptake rate and the activity of the enzymes involved in the N assimilation pathway.11,2935 Alternatively, Cd-caused induction of enzymes of S assimilation pathway has been reported in many plants.19,36,37 Therefore, the regulation of S assimilation may be necessary to ensure an adequate supply of S compounds required for heavy metal tolerance. However, Cd is a non-redox active metal, but it induces the generation of reactive oxygen species (ROS) including superoxide radical (O2•−), hydrogen peroxide (H2O2) and hydroxyl radical (OH) (Fig. 1),38,39 which has to be kept under tight control because the presence of Cd lead to excessive production of ROS causing cell death due to oxidative stress such as membrane lipid peroxidation, protein oxidation, enzyme inhibition and damage to nucleic acid.11,3942 To repair the Cd-induced inhibitory effects of ROS, plants employ ROS-detoxifying antioxidant defense machinery which includes nonenzymatic (glutathione, GSH; ascorbic acid, AsA; α-tocopherol and carotenoids) and enzymatic (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; glutathione reductase, GR; monodehydroascorbate reductase, MDHAR; dehydroascorbate reductase, DHAR; glutathione peroxidase, GPX; guaicol peroxidase, GOPX and glutathione-S-transferase, GST) antioxidants.11,39,43,44 Gao et al.45 reported that Arabidopsis lysophospholipase 2 (lysoPL2) binds acyl-CoA-binding protein 2 (ACBP2) to mediate Cd(II) tolerance in transgenic Arabidopsis thaliana. ACBP2 shows protein-protein interactions with an ethylene-responsive element binding protein (AtEBP) and a farnesylated protein 6 (AtFP6). Overexpression of ACBP2 (acyl-CoA-binding protein 2), lysoPL2 (lysophospholipase 2) and AtFP6 (farnesylated protein 6) in Arabidopsis resulted in tolerance to Cd(II) when compared with wild type. ACBP2 can mediate tolerance to Cd(II)-induced oxidative stress by interacting with two protein partners, AtFP6 and lysoPL2.46

Figure 1
Biosynthesis of Cys and S assimilation pathway, incorporation of Cys to GSH biosynthesis, detoxification of Cd2+ derived ROS and compartmentalization of Cd2+ in plant vacuoles. (SO42−, Sulfate; APS, adenosine 5′-phosphosulfate; ATP-S, ...

Literature is full of reports that show the use of different strategies to combat the inhibitory effects of Cd in crop plants, but information on the involvement of mineral nutrition for Cd stress tolerance is limited, but significant.11,20 Other than N, phosphorus (P) and potassium (K), S is a most important macronutrient that plays an important role not only in growth and development of higher plants, but also is associated with stress tolerance in plants.11,47,48 Recently, molecular studies on the mechanism of Cd toxicity revealed the involvement of S metabolism. Higher plants acquire S predominantly in the form of anionic sulfate from the soil that gets converted to nutritionally and functionally important S-containing compounds like cysteine (Cys), methionine (Met), GSH, several co-enzymes, thioredoxins, sulpholipids and vitamins, i.e., biotin, thiamine and ferredoxin, through a cascade of enzymatic steps.48,49 Cys, the initial product of S assimilation, is supposed to be the rate-limiting factor for GSH (γ-glutamyl-cysteinyl-glycine) synthesis,50 which is the most important S-containing antioxidant and redox buffer in plants and plays essential roles within plant metabolism and stress tolerance to ROS51 where it gets oxidized to glutathione disulphide (GSSG). GR mediates the reduction of GSSG to GSH by using NADPH as an electron donor thus regenerates the GSH.52 Studies at cellular level revealed that GSH is a key regulator of redox signaling, which can control gene expression, transcription and translation.50 N and S are important constituents of GSH therefore, upregulation of their biosynthetic pathway can increase the GSH content and thus tolerance to Cd stress. Momose and Iwahashi53 reported the involvement of Cd in the upregulation of various genes involved in S metabolism in Saccharomyces cerevisiae. Barbey et al. reported that exposure to Cd Met4 gets activated which upregulates the biosynthesis of molecules that are involved in S metabolism, such as tripeptide GSH. Furthermore, it has also been noted that Cd inhibits the SCFMet30 pathway therefore prevent the degradation of Met4, a primary transcription factor for genes involved in S metabolism.54 Nazar et al.55 also reported that higher levels of leaf N and S content through the upregulation of its biosynthetic enzymes increased the GSH content more conspicuously in salt tolerant Pusa Vishal than salt sensitive T44.

Mineral nutrients, especially S, have the potential to provide tolerance to crop plants by means of tripeptide thiol GSH, precursor of PCs which play crucial role in Cd tolerance. Since Cd, a non-essential phytotoxic metal, is considered as one of the potential threats for crop plant productivity; the present review covers the literature on Cd toxicity in crop plants and discusses the potential of S in Cd stress tolerance.

Sulfur Assimilation and Uptake

S has occupied an important place after N, P and K. It is the most important macronutrient for normal growth and development of plants with numerous biological functions56,57 after N, P and K. S is known for its role in the formation of sulfur-containing amino acids (Cys and Met), and synthesis of proteins, vitamins, chlorophyll and GSH involved in stress tolerance.5861 It has been reported that adequate supply of S enhances the photosynthetic potential and growth of crop plants.62 On the other hand, its deficiency regulates the chlorophyll content of leaves, N content and photosynthetic enzymes.63,64

Plants obtain S mainly as sulfate from the soil in addition to sulfur dioxide and hydrogen sulfide from the air, and in a minor extent by leaves and through a cascade of reactions in which S gets converted into sulfide and Cys (Fig. 1).49,65,66 The S assimilation pathway initiates with the uptake of sulfate from soil which is facilitated by sulfate transporters.65 Once sulfate is within cells, it can be stored or can enter the metabolic stream. The induction of the sulfate uptake capacity in Zea mays plants exposed to toxic concentrations of either Cd, Zn or Cu is closely dependent on the upregulation of the high-affinity sulfate transport system (HATS).67 Then it gets activated to adenosine 5′-phosphosulfate (APS). ATP-S is the first enzyme in the sulfate assimilation pathway of plants, and plays a key role in sulfate metabolism by catalyzing the formation of APS and inorganic pyrophosphate (PPi) from sulfate and ATP.68 Genes encoding various organelle ATP-S isoforms have been cloned from Arabidopsis thaliana, Brassica juncea and Solanum tuberosum. The reaction product APS is a branch point intermediate, which can be channelled toward reduction or sulfation.69 APS is reduced to sulfite in the presence of APS reductase (APR),70 and finally sulfite is reduced to sulfide by sulfite reductase (SiR). Sulfide then reacts with O-acetyl serine (OAS) to form Cys by the activity of O-acetylserine(thiol)lyase (OAS-TL) (Fig. 1). Cys is the first organic compound to contain reduced S in plant cells. Cys is further incorporated into proteins, coenzymes and GSH, and serves as the thiol donor for Met and a multitude of other compounds.61 The formation of Cys is a direct coupling step between S and N assimilation in plants.71,72 Cys is the precursor of GSH, a low-molecular weight, water-soluble non-protein thiol compound which protect the plants from various abiotic stresses including heavy metals (Fig. 1).11,20,39,55,73

Cadmium Stress and Sulfur Metabolism

Heavy metal contamination is a serious environmental problem that limits crop productivity worldwide and threatens human health.11,25 The agricultural soil may have toxic levels of heavy metals due to agricultural and industrial practices such as application of pesticides and chemical fertilizers, waste water irrigation, precipitation from heavy coal combustion and smelter wastes and residues from metalliferous mining.11,25 Among heavy metals, Cd is a non-essential, highly phytotoxic metal and significantly damages general plant metabolism even at low concentrations.3,25

Cd is readily taken up by plants, therefore its presence in the food chain is a real threat for animals as well as humans. Cd is classified under the group I of human carcinogens which can lead to renal and lung cancer.74 Cd arrests the plant growth and thus affects the biomass,13,19,75 which can lead to plant death.25 It interferes with photosynthesis, respiration and water relations18,19,24,76 and the process of uptake and translocation of mineral nutrients lead to significant alterations in the normal plant growth.19,77,78 The causes of these dysfunctions include irreversible changes to protein conformation by forming metalthiolate bonds and alteration of the cell wall and membrane permeability by binding to nucleophilic groups79 through the production of ROS.39

The effect of Cd on N and S assimilation pathway has been studied in several plants showing an inhibition of the nitrate uptake rate and the activity of the enzymes involved in the nitrate assimilation pathway.3135 It has been reported that metal exposure to plants also leads to a significant alteration in S metabolism.80 It caused induction of enzymes of S assimilation pathway in plants.19,36,37 Cd-led upregulation of S metabolism pathway genes has been reported in Saccharomyces cerevisiae,53 and induction of enzymes involved in the sulfate assimilation pathway in higher plants.19,80,81 Sultr1;1 and Sultr2;1 (which encode two sulfate transporters) have also been found to be upregulated after 2 or 6 h of Cd-treatment and 12–24 h after sulfate-depletion.8183 Nussbaum et al.84 reported that Cd accumulation increased ATP-sulfurylase (ATP-S) and adenosine 5-phosphosulfate reductase (AR) activities in maize seedlings. Guo et al. studied the effect of increasing concentration of Cd on the activities of S assimilation enzymes (ATPS and SAT) in Cd hyperaccumulator and non hyperaccumulator ecotype of Sedum alfredii plants and noted an increase in the activities of ATPS and SAT which contributed towards Cd accumulation in the hyperaccumulator ecotype. Ruegsegger et al. showed that AR activity is induced coordinately with GSH synthetase in Cd-treated pea plants. In fact, the capacity of plants to survive in a polluted environment is partially linked to the efficiency of their reductive sulfate assimilation pathway. Upon metal stress, some genes involved in the S assimilation pathway are known to be transcriptionally activated, resulting in an elevation of enzymatic activity.8790 S has been found to be involved in Cd tolerance mechanism in Arabidopsis thaliana,36,91 Brassica juncea,92,93 Nicotiana tabacum,94 Triticum aestivum19 and Brassica campestris.20

Sulfur-containing Proteins, Peptides, Thiols and Cd Detoxification

Contamination of agricultural soil with heavy metals is a serious problem for plant growth and development. Among heavy metals, Cd is a widespread contaminant with a long biological half-life. Cd has been shown to disturb photosynthetic activity,11,18,19,76 and the process of uptake and translocation of mineral nutrients leads to significant alterations in the normal plant growth and productivity.11,19,77,78 Plants employ various strategies to counteract the Cd-induced oxidative damage. Tukendorf and Rauser80 noted significant alteration in S metabolism under heavy metal stress. Plants obtain S as sulfate from the soil in addition to sulfur dioxide and hydrogen sulfide from the air by leaves, and gets converted into organic S compounds such as Cys, Met and GSH.47,49,55 Cys is the final product of S assimilation pathway, and is supposed to be the rate-limiting factor for GSH biosynthesis.50,52 Overexpression of cytosolic O-acetylserine(thiol)lyase in Arabidopsis thaliana (ecotype columbia) revealed that Cd tolerance was found to be associated with enhanced Cys biosynthesis and Cd accumulation in trichome leaves. It has been suggested that engineering of Cys biosynthesis pathway in plants, together with modification of the number of leaf trichomes, may have the potential for metal tolerance and accumulation.95 Overexpression of Arabidopsis thaliana serine acetyltransferase (SAT; AtSAT1 or AtSerat 2;1) in developing lupin embryos resulted in increases of up to 5-fold O-acetylserine (OAS) and up to 26-fold in free Cys, which suggests that Cys biosynthetic pathway is active in developing seeds and also indicates that SAT activity limits Cys biosynthesis, but that Cys supply does not limit Met biosynthesis.96 Matsuda et al. reported that overexpression of DcCDT1 (Digitaria ciliaris cadmium tolerance 1; encodes a novel 55-amino acid-peptide product containing 15 Cys residues) confers Cd tolerance in transgenic Arabidopsis thaliana plants.

GSH-abundant and ubiquitous thiol is a major reservoir of non-protein reduced S, which plays an important role in protein synthesis and nucleic acids, and works as a modulator of enzyme activity. GSH acts as a signal and controls the regulation of S nutrition.52 It is an important component of cellular defense in plants, where it gets oxidized to GSSG that should be converted back to GSH in plant cells to perform normal physiological functions. GR plays a crucial role in the reduction of GSSG to GSH which maintains a highly reduced state of GSH/GSSG and AsA/DHA ratios, and protects the plants from Cd-induced oxidative stress. Singla-Pareek et al. reported the role of GSH in the detoxification of reactive ketoaldehydes such as methyl glyoxal which is considered a potential target for engineering salinity stress tolerance in plants. GSH also plays an important role in heavy metal tolerance by PC biosynthesis99 and as transport a form of Cys.100 Liedschulte et al. reported that transgenic tobacco plants expressing γ-glutamylcysteine ligase-glutathione synthetase from Streptococcus thermophilus (StGCL-GS) showed significantly higher GSH accumulation in the leaves of transgenic plants than wild-type plants and it was further increased by the additional sulphate fertilizer. Cai et al.102 studied the effect of exogenously applied GSH on the performance of Cd-sensitive (cv. Xiushui63) and tolerant (cv. Bing97252) rice cultivars under Cd stress and noted that exogenous GSH significantly alleviated Cd-induced growth inhibition and markedly reduced Cd uptake in both genotypes. However, its effect was found to be Cd-dose- and genotype-dependent Cd-induced changes in mineral concentration/accumulation and chlorophyll content in rice seedlings. It was reported that higher increase in GSH production has no impact on normal plant growth, whereas, it increased plant tolerance to abiotic stress. Following Cd stress, significant increase in GR activity has been reported in many plants.11,18,19,39,76,103 Rodríguez-Serrano et al. reported that exposure to Cd leads to the induction of transcripts for the enzymes of GSH biosynthesis following oxidative stress. Therefore, GR and GSH are the important components of the antioxidant machinery in plants to protect them from ROS induced oxidative damage.39,105,106 Among S-containing proteins and peptides, the PCs, metallothionins (MTs) and GSH are of significant importance for Cd stress tolerance.99 S metabolism tightly regulates the biosynthesis of PCs in plants. Cys and GSH are actively involved in PC synthesis and also in metal sequestration in plants.107 The additional S ions have been shown to enhance the stability of the PC-Cd2+ complex.108 A major part of S incorporated into various organic molecules is located in-SH groups in proteins (Cys-residues) or non-protein thiols.109 Thiol groups have redox properties and hence play important roles in the stress response of plants. The -SH/S-S status controls the three-dimensional molecular structure of proteins.49 On the other hand, S-containing proteins and peptides play a crucial role in the survival of plants under Cd.

Glutathione Biosynthesis and Cd Stress Tolerance

Plants employ various strategies to cope with the toxic effects of Cd. The induction of defense pathways is a key feature, among which complexation with PCs, MTs, GSH and sequestration within vacuoles is of significant importance.11,107 GSH is a tripeptide (γ-glutamyl-cysteinyl-glycine) which acts as a storage and transport form of reduced S and control of S assimilation and plays important roles including cell differentiation, cell death, control of redox status, protection against biotic and abiotic stresses, protein folding, precursor of PCs and detoxification of xenobiotics.110,111 Furthermore, GSH acts as an antioxidant, quenching the ROS generated in response to various stresses.39 Ogawa et al.112 noted that endogenous GSH content play important role in the timing of flowering in Arabidopsis thaliana and it is regulated by photosynthetically synthesized ATP therefore have direct correlation with photosynthetic efficiency of plants.

The tripeptide, GSH, is synthesized enzymatically by two enzyme-catalyzed steps in spite of coded by genes. Various genes encoding the enzymes required for GSH synthesis have been isolated and found to be encoded in the nuclear genome.113 It exists in two interchangeable forms GSH and GSSG.110 GSH is synthesized in two ATP-dependent steps. γ-glutamylcysteine (γ-EC) is synthesized from L-glutamate and Cys by the enzyme γ-glutamylcysteine synthetase (γ-ECS; encoded by GSH1 in Arabidopsis thaliana) in the first step, where, γ-ECS catalyze the formation of peptide bond between L-glutamate and Cys. In the second step, the enzyme glutathione synthetase (GS; encoded by GSH2 in Arabidopsis thaliana) catalyzes the formation of a peptide bond between the α-amino group of glycine and the cysteinyl carboxyl group of γ-EC. γ-ECS, the enzyme used in the first step of GSH biosynthesis is found to be regulatory enzyme and its activity is regulated by GSH in feedback mechanism.114,115 Cys, a final product of S assimilation pathway, is supposed to be the rate-limiting factor for GSH biosynthesis (Fig. 1).50,52,58 Therefore, GSH biosynthesis can be tightly linked to S assimilation pathway.48,58 GSH have the ability to directly scavenge the metal induced ROS such as O2•−, H2O2 and OH (Fig. 1).39 It also protects the membranes by maintaining α-tocopherol and zeaxanthin in the reduced state.39 Additionally, GSH is a substrate for GPX and GST.39 The physiological functions of GSH have been mainly attributed to its reduced form (GSH) in plants; however, it gets oxidized to GSSG. Therefore, it is important to keep high proportion of GSH in the reduced state by the activity of GR with the oxidation of NADPH.39

Plenty of reports witnessed the enhanced biosynthesis of GSH following various environmental stresses in various plant species.11,39 The concentration of cellular GSH has a major effect on its antioxidant function, and it varies considerably under Cd stress. Furthermore, it has been reported that increased GSH content is correlated with the ability of plants to tolerate metal-induced oxidative stress.116 Contrarily, low level of GSH content is correlated with Cd sensitivity, may be due to limited PCs synthesis.117 Therefore, manipulation of GSH biosynthesis in plants under stress leads to enhanced tolerance to ROS.118 Feedback inhibition of γ-ECS by GSH has been considered as a fundamental central point for GSH synthesis. In vitro studies with the enzymes from tobacco and parsley cells showed that the plant γ-ECS was inhibited by GSH.44 Oxidation of GSH to GSSG decreases GSH levels and allows increased γ-ECS activity under stressed conditions.44 Antioxidant activity in the leaves and chloroplast of Phragmites australis Trin. (cav.) ex Steudel was associated with a large pool of GSH, protecting the activity of many photosynthetic enzymes against the thiophilic bursting of Cd exerting a direct important protective role in the presence of Cd.119 Cai et al.120 reported that exogenously applied GSH significantly increased chlorophyll content, net photosynthetic rate, maximal photochemical efficiency of PSII (Fv/Fm) and effective PSII quantum yield Y(II) in Cd exposed plants. Further, GSH addition significantly increased root GSH content in plants under Cd exposure and induced upregulation in PCs Bing 97252 (Cd tolerant) throughout than Xiushui63 (Cd sensitive). Increased concentration of GSH has been observed with the increasing Cd concentration in various plants.119124

Phytochelatins and Cd Detoxification

Plants respond to heavy metal toxicity by synthesis of PCs. S, being a component of PC, plays an important role in their synthesis and ultimately in detoxification of Cd through the formation of Cd-binding peptides (CdBP).99 PCs [(γ-GluCys)n-Gly], the Cys-rich peptides are synthesized enzymatically using GSH as a substrate by phytochelatin synthase (PCS) which is found to be activated upon exposure to heavy metals such as Cd.99,107 PCs bind to toxic Cd ions and subsequently transported to the vacuole for Cd tolerance (Fig. 1).125,126 Cys, γ-EC, GSH and PCs are found to play important role in Cd stress tolerance in plants.127 Heavy metals and precursors of PC synthesis (Cys & GSH) are found to activate the PC synthesis in plants for possible metal stress tolerance by making ‘Low Molecular Weight’ (LMW) complex with Cd which acquire acid labile S at the tonoplast and form a ‘High Molecular Weight’ (HMW) complex.25,67,99,128 Plenty of literature available on Cd toxicity and tolerance in various crop plants suggests the role of PCs in Cd detoxification and tolerance.129137 Zhang et al.136 reported Cd induced synthesis of PCs in various tissues of Sedum alfredii. Higher PC2 levels (109–270%) in Cd-exposed red spruce cells suggested the importance of elevated PC synthesis for Cd tolerance.107 Cd sensitivity was found to be correlated with PC accumulation in Cd-sensitive Arabidopsis mutants.138 Furthermore, Inouhe et al.130 confirmed the sensitivity of cultured cells of azuki beans to Cd due to the lack of PCs activity. Sachiko et al. carried out point mutations into the PC synthase by replacing Cys358, Cys359, Cys363 and Cys366 residues with Ala and noted lower PC synthesis ability of mutant than the wild-type enzyme. Furthermore, mutant PC synthase experienced more damage than wild type under oxidative conditions which suggest the importance of Cys-rich region of PC synthase for antioxidant activity. Zhang et al.139 studied the relationship between PC synthesis and Cd accumulation in Cd hyperaccumulator Sedum alfredii and suggested that suggest that PCs do not detoxify Cd in roots but might act as the major intracellular Cd detoxification mechanism in shoots like in non-resistant plants.

Employing transgenic approaches it has been confirmed that PCs play important role in Cd tolerance in many plants. Zhu et al.92,93 overexpressed the γ-glutamylcysteine synthetase gene from E. coli in Brassica juncea, resulting in increased biosynthesis of GSH and PCs and an increased tolerance to Cd. A similar approach was taken with Arabidopsis; γ-glutamylcysteine synthetase was expressed in both sense and antisense orientations, resulting in plants with a wide range of GSH levels.117 Wojas et al. studied the changes in the subcellular PC, GSH, γ-glutamylcysteine and Cd vacuolar and cytosolic distribution in AtPCS1 and CePCS expressing tobacco plants. It has been reported that decrease in PCs cytosolic and vacuolar pool resulted in Cd hypersensitivity in AtPCS1 because of decreased Cd detoxification capacity. On the other hand, enhanced Cd tolerance of CePCS plants was accompanied by an increased cytosolic and vacuolar SH of PC/Cd ratio which resulted in efficient Cd detoxification. The expression of Arabidopsis PCS in the yeast mutant deficient in PCS resulted in Cd tolerance but sensitive to Cu which suggests that PCS cannot be used in bioremediation of Cd in Cu contaminated sites.141

Conclusion

Sulfur has been ignored, which leads to S deficiency in agricultural soils and thus productivity. S metabolism plays a crucial role in plant's life and it also acts as a signaling molecule for cellular communication with the environment. S is known for its role in the formation of sulfur-containing amino acids (Cys and Met), synthesis of proteins, vitamins, chlorophyll, GSH and PCs which have crucial role in metal tolerance. S metabolism initiates with the uptake of sulfate which is facilitated by sulfate transporters. Therefore, sulfate transporter genes might be a potential target to facilitate sulfate entry in plants. Cys is the first organic compound to contain reduced S in plant cells which is further incorporated into proteins, coenzymes and GSH and serves as the thiol donor for Met. Cys is also a direct coupling step between S and N assimilation as well as the precursor of GSH, a low molecular weight, water-soluble non-protein thiol compound which protect the plants from various abiotic stresses including heavy metals. The coordination of S assimilation pathway has been reported with N and carbon assimilation. Better understanding of the molecular mechanism of coordination of S assimilation with N and C metabolism can also be a potential target for abiotic stress tolerance. Therefore, engineering of S assimilation pathway or external supply of S to plants under stress can be exploited for abiotic stress tolerance.

Acknowledgements

Work on plant abiotic stress tolerance in N.T.'s laboratory is partially supported by Department of Biotechnology (DBT), Government of India.

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