Environ Sci Pollut Res DOI 10.1007/s11356-015-4532-5

REVIEW ARTICLE

Superoxide dismutase—mentor of abiotic stress tolerance in crop plants Sarvajeet Singh Gill 1 & Naser A. Anjum 2 & Ritu Gill 1 & Sandeep Yadav 3 & Mirza Hasanuzzaman 4 & Masayuki Fujita 5 & Panchanand Mishra 6 & Surendra C. Sabat 6 & Narendra Tuteja 3

Received: 29 December 2014 / Accepted: 12 April 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Abiotic stresses impact growth, development, and productivity, and significantly limit the global agricultural productivity mainly by impairing cellular physiology/biochemistry via elevating reactive oxygen species (ROS) generation. If not metabolized, ROS (such as O2•−, OH•, H2O2, or 1O2) exceeds the status of antioxidants and cause damage to DNA, proteins, lipids, and other macromolecules, and finally cellular metabolism arrest. Plants are endowed with a family of enzymes called superoxide dismutases (SODs) that protects cells against potential consequences caused by cytotoxic O2•− by catalyzing its conversion to O2 and H2O2. Hence, SODs constitute the first line of defense against abiotic stress-accrued enhanced ROS and its reaction products. In the light of recent reports, the present effort: (a) overviews abiotic stresses, ROS, and their metabolism; (b) introduces and discusses SODs and their types, significance, and appraises abiotic stress-

mediated modulation in plants; (c) analyzes major reports available on genetic engineering of SODs in plants; and finally, (d) highlights major aspects so far least studied in the current context. Literature appraised herein reflects clear information paucity in context with the molecular/genetic insights into the major functions (and underlying mechanisms) performed by SODs, and also with the regulation of SODs by post-translational modifications. If the previous aspects are considered in the future works, the outcome can be significant in sustainably improving plant abiotic stress tolerance and efficiently managing agricultural challenges under changing climatic conditions.

Keywords Abiotic stresses . Reactive oxygen species . Oxidative stress . Superoxide dismutase . SOD genetic engineering

Responsible editor: Philippe Garrigues * Sarvajeet Singh Gill [email protected] * Naser A. Anjum [email protected]

3

Plant Molecular Biology Group, International Centre for Genetic Engineering and Biotechnology (ICGEB), Aruna Asaf Ali Marg, New Delhi 110067, India

4

Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka 1207, Bangladesh

5

Department of Applied Biological Science, Faculty of Agriculture, Laboratory of Plant Stress Responses, Kagawa University, Miki-cho, Kita-gun, Kagawa 761-0795, Japan

6

Stress Biology Laboratory, Gene Function and Regulation, Institute of Life Sciences, Bhubaneswar, Odisha 751023, India

* Narendra Tuteja [email protected] 1

Stress Physiology and Molecular Biology Lab, Centre for Biotechnology, MD University, Rohtak, Haryana 124001, India

2

CESAM-Centre for Environmental and Marine Studies and Department of Chemistry, University of Aveiro, 3810193 Aveiro, Portugal

Environ Sci Pollut Res

Introduction Abiotic stress, reactive oxygen species, and their metabolism As a principal cause of global crop failure, abiotic stresses decrease average yields for major crops by more than 50 % (Tuteja et al. 2011). In the present scenario, the changing climatic conditions are making the abiotic stress factors (such as salinity, drought, flood or water logging, high temperature, low temperature, metal toxicity, UV-B radiation, O3, and high light) unpredictable and more severe. Abiotic stresses in isolation and/or combination limit the plant growth, development, and productivity mainly by impairing cellular physiology/biochemistry via promoting oxidative stress. The latter is a physiological condition where a rapid transient production of huge amounts of reactive oxygen species (ROS; such as H2O2, O2•−, OH•, or 1O2) exceeds the status of antioxidants that eventually bring a range of severe consequences including damages to biomolecules such as lipids, proteins, and DNA, and finally, cellular metabolism arrest (Noctor et al. 2002a, b; Gill and Tuteja 2010; Hasanuzzaman et al. 2012; Sharma et al. 2012; Anjum et al. 2015). In fact, ROS are the species derived from the reduction of molecular oxygen (O2) that includes some free radicals such as superoxide (O2•−), hydroxyl radical (OH•), alkoxyl (RO•) and peroxyl (ROO•), and non-radical products like hydrogen peroxide (H2O2) and singlet oxygen (1O2), etc. (Halliwell and Gutteridge 2007; Gill and Tuteja 2010; Sandalio et al. 2013). ROS generation is an inevitable part and by-product in different metabolic processes, where 240 μM s−1 O2•−, and 0.5 μM H2O2 can be observed in plants under optimal growth conditions. Nevertheless, Fig. 1 Simplified scheme highlighting the formation of reactive oxygen species by physical and chemical activation

processes like photosynthesis and respiration happen as a part of common aerobic metabolism, and several cell organelles such as chloroplast, mitochondria, plasma membrane, apoplast, and nucleolus are the main sources of ROS production (Gill and Tuteja 2010; Sandalio et al. 2013). Further, abiotic stresses may significantly enhance the generation of varied ROS (and their reaction products) in plant cells, where stressed cells may exhibit accelerated ROS generation up to 720 μM s −1 O 2 •− and 5–15 μM H 2 O 2 (Mittler 2011; Hasanuzzaman et al. 2012 (Figs. 1, 2, and 3). Distributed in different cell organelles such as chloroplasts, mitochondria, peroxisomes, or apoplast, plant-antioxidant defense machinery, comprising antioxidant enzymes and nonenzymatic antioxidant components metabolize ROS and their reaction products in order to avert oxidative stress condition (Gill and Tuteja 2010; Hasanuzzaman et al. 2012). Major nonenzymatic antioxidants include ascorbic acid (AsA), glutathione (GSH), phenolic compounds, alkaloids, non-protein amino acids, and α-tocopherols. On the other hand, the battery of enzymatic antioxidants includes superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione peroxidase (GPX), guaicol peroxidase (GOPX), peroxidase (POX), glutathione-S-transferase (GST) (Fig. 4; Hasanuzzaman et al. 2012). In brief, AsA is a water-soluble antioxidant, and is considered as the most abundant antioxidant and as a major contributor to the cellular redox state. As an important component of AsA-GSH cycle, AsA reduce H2O2 to H2O by the activity of APX, where AsA is oxidized to dehydroascorbate (DHA). AsA also acts as a signaling molecule in the regulation of senescence and tolerance against different abiotic

Environ Sci Pollut Res Fig. 2 The concept of equilibrium and imbalance between reactive oxygen species and antioxidants. (Energy support also plays an important role in this equilibrium)

stresses (reviewed by Anjum et al. 2014). GSH, a tripeptide, γ-glutamyl-cysteinyl-glycine is a water soluble non-protein thiol compound, is extensively distributed in cytosol and in almost all of the cell organelles (including chloroplasts, endoplasmic reticulum, vacuoles, mitochondria). Apart from its role in a broad range of biochemical processes, GSH is involved in the scavenging of H2O2, OH•, and 1O2 in chloroplast, cytoplasm, apoplast, mitochondria, and peroxisome (Anjum et al. 2012; Gill et al. 2013; Hasanuzzaman et al. 2012). The other major non-enzymatic compounds such as tocopherols (Toc) (in the form of α, β, γ, and δ represent a group of lipophilic antioxidants) (Munné-Bosch 2005), carotenoids (Car) (Mittler 2002), and flavonoids (Olsen et al. 2010; Hernandez et al. 2009; Løvdal et al. 2010) are directly or indirectly contributing to the scavenging of varied ROS and

Fig. 3 Simplified schemes highlighting major sites and possible mechanisms of reactive oxygen species formation in plant cells (Bhattacharjee 2012)

their reaction products. Considering the major enzymatic antioxidants, SOD (electrical conductivity (EC) 1.15.1.1) constitutes the first line of defense against abiotic stress-accrued enhanced ROS and its reaction products where SODs catalyze the dismutation of O2•− to H2O2 and O2 in all subcellular compartments such as chloroplasts, mitochondria, nuclei, peroxisomes, cytoplasm, and apoplasts (Alscher et al. 2002; Gill and Tuteja 2010). CAT, a tetrameric heme containing enzyme, occurs in peroxisomes, glyoxysomes, and related organelles where the dismutates H2O2 into H2O and O2, which is a vital part of antioxidant defense (Garg and Manchanda 2009). CAT is an efficient ROS scavenger mainly due to its highest turnover rate of reaction which can dismutase about 6 million molecules of H2O2 per minute (Gill and Tuteja 2010). APX, a multigene family enzyme can be cellular compartment-

Environ Sci Pollut Res Fig. 4 Major mechanisms of antioxidant defense by different enzymes in plants. (Dotted lines denote non-enzymatic conversions. R may be an aliphatic, aromatic or heterocyclic group; X may be a sulfate, nitrite or halide group)

specific such as stromal APX (sAPX), and thylakoid-bound APX (tAPX) in chloroplasts, glyoxysomes, and peroxisome membrane-bound APX (mAPX) and cytosolic APX (cAPX). As an important component of AsA-GSH cycle, APX catalyzes conversion of H2O2 to H2O (reviewed by Gill and Tuteja 2010; Anjum et al. 2012, 2014; Hasanuzzaman et al. 2012). In AsA-GSH cycle during ROS-scavenging or its utilization by other enzymes, AsA is oxidized in to MDHA that is then disproportionate into AsA and DHA. In step-bystep reaction, the oxidized AsA is recycled to its reduced form where MDHAR activity is vital that performs NADPH-dependent regeneration of AsA from MDHA (Anjum et al. 2014). GR catalyzes the reduction of oxidized GSH (GSSG) back to its reduced form (GSH) in AsA-GSH cycle with the accompanying oxidation of NADPH. Thus, GR helps to maintain proper GSH/GSSG or cellular redox balance that has significant roles in stress signal transduction (Anjum et al. 2012; Gill and Tuteja 2010). Among other enzymes, GPXs and GSTs, distributed in cellular compartments are a large group of diverse group of enzymes, and are involved in the suppression of oxidative stress via their involvement in the reduction of H2O2 and their reaction products (Noctor et al. 2002b; Dixon et al. 2010; Hasanuzzaman et al. 2012; Gill and Tuteja 2010; Anjum et al. 2012, 2014; Gill et al. 2013). Considering the fact that crop plant exposure to various abiotic stresses is inevitable and that these factors are the major culprit of global crop failure, considerable research works are underway to understand how plants establish their unique mechanisms to respond and tolerate stresses, imposed together or in isolation (Hirayama and Shinozaki 2010; Chew and Halliday 2011; Fu and

Qu 2013). However, the major insights into the key pathways regulating and coordinating the abiotic stress response and tolerance in crop plants are yet to achieve. Thus, in the present effort: (a) SODs, their types and significance are introduced and discussed; (b) modulation of SODs in abiotic-stressed plants is appraised; (c) reports available on genetic engineering of SODs in plants are analyzed; and finally, (d) major aspects so far least studied in the current context are mentioned.

Superoxide dismutases Overview and types Superoxide dismutase (SOD, EC 1.15.1.1) is a metalloenzyme and one of the most effective components of the antioxidant defense system in plant cells against ROS toxicity. SOD was first isolated from bovine blood as a green Cu-protein and was believed to function in Cu-storage (Mann and Keilin 1938). Until reported in plants (McCord and Fridovich 1969), SOD was recognized as a group of metalloproteins having no know function. Later, the role of Cu/Zn-SODs was observed in preparation of veterinary anti-inflammatory drug (Orgotein) (McCord and Fridovich 1988). Available in the concentration of ~10−5 M in most cells, and categorized into three main groups on the basis of the metal cofactor at active site, SODs are believed to occur in all oxygen metabolizing cells and also in all sub-cellular compartments (such as chloroplasts, mitochondria, nuclei, peroxisomes, cytoplasm, and apoplasts) (Alscher et al. 2002; Fink and Scandalios 2002) (Fig. 5). Cu/Zn-

Environ Sci Pollut Res Fig. 5 Localization of superoxide dismutases in plant cell. (Adapted from Alscher et al. 2002, with Permission from Oxford University Press)

SOD has been localized in cytosol, chloroplasts, and peroxisomes. Fe-SOD mainly localized in the chloroplasts and to some extent in peroxisomes and apoplast while Mn-SOD in the mitochondria (Corpas et al. 2006). A fourth group with Ni (II/III) at the active site (Ni-SOD) is also known (Fink and Scandalios 2002). Originally isolated for the first time from Streptomyces seoulensis by Youn et al. (1996), Ni-SODs also catalyze the conversion of O2•− to H2O2 and O2 and were evidenced in cyanobacteria, marine gammaproteobacteria, and a marine eukaryote (Dupont et al. 2008). It is reported that Mn and Fe-SODs are older than Cu/Zn-SODs because they are thought to be generated from the identical ancestral enzyme. On the other hand, Cu/Zn-SODs, evolved separately and do not possess such similarity (Smith and Doolittle 1992). Nevertheless, all the SOD isoforms (Cu/Zn-SOD, Mn-SOD, Fe-SOD) are nuclear coded and, where necessary, are transported to their organellar locations by means of NH2-terminal targeting sequences (Pan et al. 2006). Information specific to major SOD types are briefly discussed in the following subsections. Copper-zinc superoxide dismutase Cu/Zn-SODs, the most abundant class of plant SODs, can be homodimeric (periplasmic and cytosolic; with a molecular weight around 32 kD) and/or homotetrameric (chloroplastic and extracellular) (reviewed by Alscher et al. 2002). However, plants can also exhibit monomeric forms of Cu/Zn-SODs (Kanematsu and Asada 1989; Schinkel et al. 2001). All cellular compartments can exhibit Cu/Zn-SODs; however, they mainly occur in cytosol, chloroplasts, peroxisomes, apoplasts, and nucleus (Karpinska et al. 2004; Karlsson et al. 2005; Kasai et al. 2006; Kim et al. 2008). The sensitivity of cytosolic

Cu/Zn-SOD to H2O2 can be higher than chloroplastic Cu/ZnSOD (Baum et al. 1983; Kwiatowski and Kaniuga 1986). Deduced amino acid sequences of these two isoforms are about 68 % similar. They are ~90 % similar among the chloroplastic Cu/Zn-SODs; whereas, about 80–90 % similarity was found among the cytosolic Cu/Zn-SODs. Chloroplastic Cu/Zn-SOD contains a transit peptide sequence for targeting the protein to the chloroplast; whereas, this type of sequence is not present in the cytosolic Cu/Zn-SOD (Bowler et al. 1994). Cu/Zn-SOD can also be found in peroxisome and represent about 18 % of the total SOD activity therein (Sandalio and del Rio 1987). In Cu/Zn-SODs, bivalent Cu and Zn atoms are connected by a disulfide bond maintaining a non-covalent association (Fridovich 1989). However, out of these two atoms, Cu is more important than Zn and hence, its substitution with another metal, or exclusion from the structure, causes enzyme inactivation (Bordo et al. 1994; Marino et al. 1995). Cu/Zn-SOD has ~150 times the surface area of Cu2+. Therefore, the interaction between O2− and the enzyme has to be with an electrostatic guidance to attract the O2− molecule to the active site of the enzyme (Cudd and Fridovich 1982; Erturk 1999). On the other hand, the role of Zn is structural rather than functional because many reports indicated that substitution of Zn2+ with Co2+, Hg2+, Cd2+, or Cu2+, or even complete elimination of Zn could not significantly affect the activity of SOD (Cudd and Fridovich 1982; Bordo et al. 1994; Marino et al. 1995). However, Zn2+ helps in maintaining the structural stability of the active site of Cu/Zn-SOD (Marino et al. 1995). Recently, a profound effect of the presence of Zn in medium was reported on the synthesis of chloroplastic recombinant Cu/Zn-SOD (Tuteja et al. 2015). It is interesting that upon the replenishment of atmosphere with O 2 , Fe 2+ become unavailable which

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make the insoluble Cu+ into soluble form. Consequently, Cu2+ is being involved in the active sites of SODs as a cofactor (Bannister et al. 1991). Apart from potassium cyanide (KCN), Cu/Zn-SODs can be inhibited by H2O2 (Alscher et al. 2002). Iron and manganese superoxide dismutases Fe-SOD is the first SOD where the Fe was used at its active site as the first metal co-factor. In evolutionary point of view, Fe-SOD is considered as a major constituent of the most ancient SOD group found both in prokaryotes and eukaryotes, and is thought to originate in the plastid before moving to the nuclear genome (Alscher et al. 2002; Fink and Scandalios 2002). Studies on plants have evidenced chloroplast as the location of Fe-SOD. However, in addition to a typical chloroplastic Fe-SOD gene, cytosolic localization of Fe-SOD genes has been recently evidenced in Pogonatum inflexum (Kanematsu et al. 2013). This enzymes is resistant to KCN but is inactivated by H2O2 (Alscher et al. 2002). Existence of two distinct groups of Fe-SOD has been reported so far. Though two identical 20 kD subunit proteins containing 1– 2 g Fe atom at the active center constitute the homo-dimer of the first group, the second group is a tetramer of four equal subunits with 2–4 g Fe atom in the active center, and has molecular weight in the range of 80–90 kD (Barra et al. 1990). The first group of Fe-SOD has been found in Escherichia coli; Photobacterium sepoa; Photobacterium leiognathi; the facultative anaerobe, Thiobacillus denitrificans; the purple sulfur bacterium, Chromatium vinosum; and in different plant species like Ginkgo biloba, Brassica campestris, and Nuphar luteum (reviewed by Alscher et al. 2002). The second Fe-SOD group is found in most of the higher plants. Nevertheless, in addition to one eukaryote, Tetrahymena pyriformis, the proteins of the second Fe-SOD group have been isolated from three prokaryotes namely Mycobacterium tuberculosis, Thermoplasma acisophilum, and Methanobacterium bryantii (reviewed by Alscher et al. 2002). Fe-SOD has been reported to protect chloroplast nucleoids against oxidative stress, and was also considered essential for chloroplast development in Arabidopsis (Myouga et al. 2008). Coming to highlight major features of Mn-SODs, these enzymes carry only one metal atom per subunit, can be both homodimeric and homotetrameric with one Mn (III) atom per subunit, occur in mitochondria and peroxisomes, are resistant to KCN or H2O2, and cannot function without the Mn atom present at their active site (reviewed by Alscher et al. 2002). Notably, the restoration of Mn-SOD is not possible with Fe2+ despite the high similarity of Mn-SOD with Fe-SOD in their primary, secondary, and tertiary structures (Fridovich 1986). Apart from the fact that plant Mn-SODs has high similarities to bacterial Mn-SODs, exhibition of ~65 % sequence

similarity to one another can be possible in plant-Mn-SODs (Bowler et al. 1994; reviewed by Alscher et al. 2002). Significance SODs represent the first line of antioxidant defense against a potent ROS (O2•−) by rapidly converting them into H2O2 and O2. The reactions that take place in this concert are given below: −

ð1Þ

−

ð2Þ

O2 • þ SOD−Mþ2 →O2 þ Mþ O2 • þ 2Hþþ SOD−M þ →H2 O2 þ Mþ2

The sum of these reactions (i and ii) is as the following: −

2O2 • þ 2Hþ →H2 O2 þ O2

ð3Þ

By removing O2•−, SODs decrease the risk of OH• formation via the metal catalyzed Haber-Weiss-type reaction because this reaction has a 10,000-fold faster rate than the spontaneous dismutation (Gill and Tuteja 2010). The outcome of the reaction is the generation of H2O2 which is also a ROS having dual role (toxicity and signaling). H2O2 can be efficiently detoxified, if cellular antioxidant defense machinery becomes sufficient. In one sense, this enzyme is unique that its activity determines the concentrations of O2•− and H2O2, the two Haber-Weiss reaction substrates, and it is therefore likely to be central in the defense mechanism (Bowler et al. 1992; Kandhari 2004). In particular, over expression of Cu/ Zn-SOD genes was correlated with abiotic stress tolerance in many plant species. For instance, Sunkar et al. (2006) reported that the posttranscriptional induction of two Cu/Zn-SOD genes in Arabidopsis was critical for oxidative stress tolerance. Overexpression of a Cu/Zn-SOD (a cytosolic SOD from pea) in transgenic tobacco plants could able to enhance O3 tolerance (Pitcher and Zilinskas 1996). Recently, Madanala et al. (2011) reported that Withania somnifera encoding a highly stable chloroplastic Cu/Zn-SOD conferred enhanced tolerance to exogenous chemicals viz. detergent and ethanol. In addition, apart from the dismutation of O2•−, SOD also helps in overcoming the electrostatic repulsion between two O2•− at neutral pH which happens in two ways: first, Fe-, Mn-, and Cu/Zn-SODs react with only one molecule of O2•− at a time; and second, they exploit electrostatic interactions with the negative charge of O2•− to favor specific binding of substrate but not products (Erturk 1999; Miller 2004). Another important property of Cu/Zn-SOD that has attracted in-depth investigation is its peroxidative reaction. H2O2, the product of oxidative reaction of the enzyme can also be utilized as substrate toward peroxidative mode of reaction, in the presence of bicarbonate ions. The peroxidative reaction is, however, operative under high concentration of H2O2. Therefore, the peroxidative behavior of the enzyme seems to be an additional

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advantage in chloroplastic scavenging of H2O2 wherein bicarbonate is found as a carbon source of carbon fixation. Two important events in the reaction chemistry of Cu/Zn-SOD that remains to be probe further are the presence of the monomeric form of the enzyme in plants, and the in vivo operation of peroxidative activity and their importance under stress conditions. Modulation in abiotic-stressed plants Globally, abiotic stresses such as heat, cold, drought, salinity, and chemical contaminants represent key elements limiting agricultural productivity. Thus, the understanding of the plant responses to these abiotic stresses have become a pre-requisite in order to develop crop plants with the ability to tolerate abiotic stresses (Tuteja and Gill 2013). Nevertheless, as an important component of plant defense machinery within a cell, SODs constitute the first line of defense against abiotic stress-accrued enhanced ROS and its reaction products where SODs catalyze the dismutation of O2•− to H2O2 and O2. The SOD system in higher plants exists in multiple isoforms that are developmentally regulated and highly reactive in response to exogenous stimuli.. The significance of all the SODs has been confirmed in the direct or indirect efficient metabolism of different ROS and its reaction products in a credible number of studies (Table 1). Hereunder, recent reports available on the modulation of SODs in abiotic-stressed plant species are critically appraised. Metal/metalloid stress The studies on SODs in abiotic-stressed plants have been emphasized since particularly, in metal/metalloid-stress, the modulation of SODs stands second to none in terms of its utility among major biochemical biomarkers (Stankovic and Stankovic 2013). The response of SOD to metal/metalloid stress varies considerably depending upon the plant species, developmental stage, metal in the experiment and the exposure time. Cadmium (Cd) mediated enhanced SOD activity has been reported in a number of plants including Bacopa monnieri (Mishra et al. 2006), Brassica juncea (Mobin and Khan 2007), Vigna mungo (Singh et al. 2008), Vigna radiata (Anjum et al. 2008a), Triticum aestivum (Khan et al. 2007), Brassica campestris (Anjum et al. 2008b), Zea mays (Ekmekci et al. 2008), Pisum sativum (Agrawal and Mishra 2009), Oryza sativa (Wu et al. 2006), and Arabidopsis thaliana (Cho and Seo 2005). In contrast, Cd-accrued significantly decreased SOD activity exhibition were reported in Oryza sativa (Guo et al. 2007), Glycine max (Noriega et al. 2007), and Capsicum annuum (Leon et al. 2002). Different genotypes of the same plant differing in metal tolerance may exhibit varied elevations in SOD activity. In this context, Qadir et al. (2004) reported Cd-induced differential elevation

in SOD activity in Brassica juncea genotypes namely Vardhan, Pusa Bahar, Pusa Bold, BTO, Pusa Jai Kisan, Agrini, Varuna, Kranti, Vaibhav, and Pusa Basant where Pusa Jai Kisan and Pusa Basant, respectively, displayed the highest (13–64 %) and the lowest (15–8 %) Cd-accrued increase in SOD activity over their respective controls. In another study, taking into account the two genotypes (Pusa Jai Kisan and SS2) of Brassica juncea treated with 25 and 50 μmol L−1 Cd, Iqbal et al. (2010) reported increased SOD activity where the extent of increase was higher in Cdsensitive SS2 compared to Cd-tolerant Pusa Jai Kisan. Arsenic (As) exposed Pteris vittata exhibited increased SOD activity in its fronds; whereas, no induction of SOD activity was noticed in the fronds of Pteris ensiformis under the same conditions (Srivastava et al. 2005). This response implies the role of SOD in A s-tolerance and/or hyperaccumulation in Pteris vittata. Similarly, SOD activity was found to increase in Zea mays embryos upon As-exposure (Mylona et al. 1998). In a study performed on As-exposed Brassica juncea (cvs. Varuna and Pusa Bold), SOD activity in the leaves was more at the lower concentrations (50 and 150 μM) in both varieties (Gupta et al. 2009). However, a decreased SOD activity was observed by the authors during a prolonged exposure at 300 μM. Similar to the observations of Cao et al. (2004) and Srivastava et al. (2005), in an Astolerant Holcus lanatus, Hartley-Whitaker et al. (2001) observed a similar case where a decreased SOD activity was noticed at high levels of As exposure. Hence, an increased SOD activity can be related with the increase production of ROS or expression of SOD-encoding genes (Gupta et al. 2009). In arsenate [As(V)] and arsenite [As(III)]-exposed tolerant (TPM-1) and sensitive (TM-4) variety of Brassica juncea, no significant modulation in SOD activity in response to As(III) suggests its efficient chelation at a primary level via thiols in TPM-1. However, a decline in SOD activity in TM-4 indicates toward a mechanism of sensitivity (Srivastava et al. 2010). Exhibition of a differential activity of total SOD in root mitochondria was reported in Pisum sativum plants exposed to environmentally relevant (20 μM) and acute (200 μM) concentrations of Cr (VI) for 7 days. At 20 μM Cr (VI), SOD activity increased by 29 %, whereas 200 μM Cr (VI) produced a significant inhibition (Dixit et al. 2002). Under the exposure of the same Cr levels (0, 50, 100, 200 μM), SOD activity was evidenced higher in Brassica juncea (vs. Vigna radiata), indicating that this plant can efficiently detoxify the toxic O2− radicals produced by the accumulated Cr when compared to Vigna radiata. The upregulation in the SOD activity in Vigna radiata in response to Cr stress was not strong enough to detoxify the O2− radicals completely, thus reflecting lesser tolerance toward Cr stress (Diwan et al. 2010). Increasing Cu concentrations up to 1.5 mM caused increased SOD activity in the leaves of Zea mays cultivars (3223 and 31G98)

+ + −

Salinity (100 and 200 mM NaCl/7 days) Cd (68 μM kg−1 soil) Salinity (100 and 200 mM NaCl/7 days)

Plantago meritima leaves

Pisum sativum leaves Plantago media leaves

Israr et al. (2006) − + × −

Anoxia + re-aeration Cd (25, 50 μM) Cd (10 μM) Cd (25, 50 μM)

Solanum tuberosum cell culture

Tagetes patula leaves

T. patula leaves and roots T. patula roots

Liu et al. (2011)

Pavelic et al. (2000)

Salinity (1000 mM NaCl)

Sesuvium portulacastrum

Lokhande et al. (2011)

+ − +

Hg (0–40 μM) Hg (50 μM) Hg (50 and 100 mg L−1 Hg)

S. drummondii seedlings S. drummondii seedlings S. drummondii seedlings

Israr and Sahi (2006)

Martínez Domínguez et al. (2010)

Agrawal and Mishra (2009) Sekmen et al. (2007)

Sekmen et al. (2007)

Wu et al. (2006)

Guo et al. (2007)

Mishra et al. (2013)

Verma and Dubey (2003) Ushimaru et al. (1999)

Ushimaru et al. (2001)

Duarte et al. (2012)

Mobin and Khan (2007) Kumar et al. (2011)

+

− +

Cd (10, 100, 1000 μM) Cd (0, 250 μM)

Sesbania densiflora leaves

S. drummondii callus

+

Cd (0.01–1.5 mM Cd)

Cd (100 and 500 μM Cd(NO3)2)

O. sativa seedlings

O. sativa shoots and roots

Chirkova et al. (1998)

+ +

Salinity (7 and 14 dS m−1 NaCl for 5–20 days)

O. sativa seedlings −

+ − (plastidic and mitochondria SOD)

Pb (1000 mM Pb; 15 days) Hypoxia (submerged plants)

Oryza sativa seedlings O. sativa seedlings

−

+ +

Hg2+ (10 μM) Hypoxia + re-aeration

M. sativa roots Nelumbo nucifera sedlings

Anoxia

+ (FeSOD and Cu/Zn SOD); −(MnSOD) +

Waterlogging and re-oxygenation Hg2+ (20 or 40 μM)

Lupinus angustifolius Medicago sativa leaves

Cd (50 μM Cd (CdCl2)

− + +

Cr+6 (0, 15, 30 mg L−1) Anoxia + re-aeration Cd (10, 50, 100 μM)

H. portulacoids leaves Iris pseudacorus rhizomes Juncus effusus leaves

O. sativa roots

Shah et al. (2001)

+

Cr+6 (0, 15, 30 mg L−1)

Halimione portulacoids roots

O. sativa roots

Najeeb et al. (2011) Yu and Rengel (1999) Zhou et al. (2008)

+ +

Cd (25, 50, and 100 mg kg−1 soil) Drought (moderate, −0.51 MPa; severe, −1.22 MPa)

B. juncea leaves Cajanus cajan leaves

Cho and Seo (2005) Anjum et al. (2008b)

+ +

Cd (300 and 500 μM of CdCl2) Cd (25, 50, and 100 mg kg−1 soil)

Arabidopsis thaliana seedlings Brassica campestris leaves

References

Response

Growth condition(s)

Summary of representative studies on the responses of superoxide dismutase in major abiotic-stressed plants

Plant species/part(s) studied

Table 1

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Azevedo Neto et al. (2006) (−), (+), and (×) signs indicate increase, decrease or unaltered/unaffected, respectively

Salinity (100 mM NaCl) Zea mays leaves

+

Anjum et al. (2008a)

Singh et al. (2008) +

− + Cd (25, 50, and 100 mg Cd kg−1 soil) Drought (100, 75, and 50 % field capacities)

−1

soil) Cd (25, 50, and 100 mg Cd kg

− Anoxia

Vigna mungo leaves

+

V. mungo roots V. radiata (cv. Pusa 9531, PS 16) leaves

Biemelt et al. (2000) ×

Anoxia

Chirkova et al. (1998)

Sairam et al. 2005 + (Kharchia 65 > HD 2687)

Triticum aestivum cv. Kharchia 65, HD 2687 leaves T. aestivum roots

Salinity (100 and 200 mM NaCl; 30 and 40 days after sowing) Hypoxia

Growth condition(s) Plant species/part(s) studied

Table 1 (continued)

Response

References

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(Tanyolac et al. 2007). Treatment of Triticum aestivum plants with high Ni concentration resulted in a decrease in activity of SOD (Gajewska et al. 2006) and in hairy root of Alyssum bertolonii and Nicotiana tobaccum (Boominathan and Doran 2002) but an opposite effect has been observed in Zea mays shoots under Ni exposure (Baccouch et al. 1998). Five SOD isoforms were detected in the leaves of Hgexposed Medicago sativa (Zhou et al. 2008). The authors observed the significantly increased total SOD activity with 20 or 40 μM Hg2+. A concentration dependent increase in SOD activity was observed up to 50 mg L−1 of Hg (Israr et al. 2006). The activity slightly decreased at the concentration of 100 mg L−1 Hg; however, the activity was appreciably higher with respect to the control, where the authors noted 3.86- and 3.55-fold higher SOD activity in the presence of 50 and 100 mg L−1 Hg, respectively, (vs. control). In another study on the same plant, SOD activity first increased up to a concentration of 40 μM Hg and then declined in the presence of 50 μM Hg (Israr and Sahi 2006). In Atriplex codonocarpa, Lomonte et al. (2010) observed a significant Hg-induced increase in SOD activity in the roots which peaked to a maximum at 0.1 mg L−1 Hg; whereas, in shoots, SOD activity increased gradually and leveled off at 0.1 mg L−1 Hg. Moreover, in shoots and roots, two isoforms of SOD were detected that were identified as Cu/Zn-SODs. In aluminum (80 and 160 μM Al) exposed Oryza sativa root and shoot, increase in the concentrations of Al3+ in the growth medium concomitantly increased the SOD activity (Sharma and Dubey 2007). The authors also observed about 28–39 % increase in the activity of Cu/Zn-SOD, 32–52 % increase in the activity of Fe-SOD, and 49–53 % increase in Mn-SOD activity were observed in the shoots of 160 μM Al3+ stressed Oryza sativa seedlings (Sharma and Dubey 2007). Simonovicova et al. (2004) reported increased SOD activity in Hordeum vulgare cv. Alfor root tips under Al stress at 72 h. A significantly increased SOD activity has been reported in two cultivars of Brassica campestris under Cu stress (Li et al. 2009). In a recent study, elevated SOD activity has also been reported in the leaves of nickel (0.5, 1.0, and 1.5 mM Ni)-exposed Rhaphanus sativus (Sharma et al. 2011). Concerning metal/metalloid impact on SOD isoforms, the activity staining for SOD in Glycine max revealed seven isozymes in the leaves and eight in the roots, corresponding to Mn-SOD and Cu/Zn SOD isozymes. Although a clear effect of Cd on plant growth was observed, the activities of the SOD isozymes were unaltered (Ferreira et al. 2002). In Saccharum officinarum seedlings, several isozymes have been observed, but growth in the presence of Cd did not result in any significant alteration in SOD activity (Fornazier et al. 2002). In Pisum sativum plants, a strong reduction in chloroplastic and cytosolic Cu/Zn-SODs by Cd was reported and to a lesser extent for Fe-SOD, while Mn-SOD was only affected by the highest Cd concentration tested. This showed that Mn-SOD

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was the isozyme more resistant to Cd (Sandalio et al. 2001). In the leaf peroxisomes of Cd-exposed Pisum sativum, the MnSOD activity did not change in response to Cd treatment (Romero-Puertas et al. 1999). In Cd (10, 25, and 50 μM CdCl2)-exposed Tagetes patula, Liu et al. (2011) reported significantly increased and decreased activity of both Cu/ZnSOD and Mn-SOD isoforms, respectively, in the leaves and roots with CdCl2 treatment (vs. control); whereas, the activity of Fe-SOD did not change in the leaves or roots after 14 days of Cd treatment. Furthermore, on pre-incubation with specific inhibitors, Fe-SOD was not observed in the leaves of Tagetes patula, but the isoforms of Mn-SOD and Cu/Zn-SOD were induced by CdCl2 treatment. The authors conclude that mainly Cu/Zn-SOD and Mn-SOD but not Fe-SOD contributed to enhanced SOD activity in leaves. Drought and salinity stress A major part (>22 %) of the agricultural soils on the globe is affected by salinity (FAO 2004). Nevertheless, the areas under drought are also expanding that is expected to increase further (Burke et al. 2006). Drought and salinity have been the most important abiotic stresses limiting global agricultural production. The frequent co-occurrence of both the stresses in natural and agricultural ecosystems has been credibly evidenced where salinity has been considered as an outcome of drought stress condition (Munns 2002; Chaves et al. 2009; Ahmed et al. 2013). Therefore, plant-SOD responses will be discussed hereunder considering drought and salinity together. Enhanced SOD activity has been found in a number of drought-exposed plants including Catharanthus roseus (Jaleel et al. 2007a), Vigna unguiculata (Manivannan et al. 2007), and Oryza sativa (Sharma and Dubey 2005). Whereas, the examples of an increased SOD activity in salinity-exposed plants include Catharanthus roseus (Jaleel et al. 2007b, 2008a), Phyllanthus amarus (Jaleel et al. 2007c), Withania somnifera (Jaleel et al. 2008b), and Vigna unguiculata (Manivannan et al. 2008). However, in Triticum aestivum, SOD activity increased or remained unchanged in the early phase of drought but decreased with prolonged water stress (Zhang and Kirkham 1995). SOD can protect photosystem II against O2•− generated by oxidative and water stress (Martinez et al. 2001). In a recent study, the Tibetan wild Hordeum vulgare genotypes XZ16 and XZ5 were reported to exhibit significantly increased SOD activity under drought and salinity alone and combined treatments during anthesis period (Ahmed et al. 2013). The requirement of the intrinsically higher SOD levels has been advocated in halophytes in order to rapidly induce the H2O2 Bsignature,^ and to trigger a cascade of adaptive responses (both genetic and physiological); whereas, the other enzymatic antioxidants may play significant role in decreasing the basal levels of H2O2, once the signaling has been processed (Bose et al. 2013). On the

perspective of SOD modulation in salinity-stressed plants, considerable variations in SOD activity in response to salt stress are evident at inter-specific or intra-specific level. The activity of SOD and its isoform Cu/Zn-SOD increased in both the salt tolerant and sensitive cultivars of Oryza sativa against salinity (Mishra et al. 2013). Earlier also, it has been shown that salinity increases SOD activity in salt-tolerant cultivars and decreases it in salt-sensitive cultivars, in both leaves (Dionisio-Sese and Tobita 1998; Hernandez et al. 2000) and roots (Shalata et al. 2001). While examining the long-term effects of salt stress in two salt-tolerant lines (Kharchia65, KRL19) and two salt-sensitive lines (HD2009, HD2687) of Triticum aestivum, Sairam et al. (2005) observed the exhibition of a higher increase in SOD activity by the salt tolerant line Kharchia65 when compared to the salt sensitive line HD2687. Drought and salinity can also differentially modulate isoforms of Mn-SOD, Cu/Zn-SOD, and Fe-SOD. In liquorice (Glycyrrhiza uralensis) possessing three SOD isoforms, the Mn-SOD, Cu/Zn-SOD, and Fe-SOD, Pan et al. (2006) reported Cu/Zn-SOD as the most abundant. In high NaCl (2 %) exposed Glycyrrhiza uralensis, the activity of Mn-SOD enhanced, while Cu/Zn-SOD activity decreased and Fe-SOD activity remained affected. The authors concluded that in Glycyrrhiza uralensis, Mn-SOD responded positively to salt stress, as has also been found earlier with Pisum sativum (Gomez et al. 1999). The activity of other SOD isoform, i.e., Cu/Zn-SOD remained at a relative high level under both drought and salinity levels (Pan et al. 2006). An induction of a novel Mn-SOD band was also observed in Glycyrrhiza uralensis subjected to 2 % NaCl, that was not observed when 15 % PEG-induced drought stress and 1.5 % NaCl stresses were imposed. The authors concluded the occurrence of a MnSOD gene family in Glycyrrhiza uralensis which was differently expressed under different stress conditions (Pan et al. 2006). In a recent study, in 150-mM NaCl-exposed Lathyrus sativus genotypes B1, BioL-212, PUSA-90-2, WBK-CB-14, LR3, and LR4, Talukdar (2013) concluded that (i) the increased SOD activity in B1, BioL-212, LR3, and LR4 lines (vs. control) was purely due to over-activity of both Cu/Zn I and II isoforms; and (ii) the significant enhancement in SOD activity at 30 days of growth after commencement of treatment (DAC) was mainly due to the origin of a new Mn-SOD I isoform in LR3, one Fe SOD isoform in LR4 line, and two new Mn-SOD isoforms (I and II), in addition to existing Cu/ Zn isoforms. Since the authors were unable to observe no new SOD isoforms at 60 DAC, the further increase in activity of SOD was attributed to enhanced expression of existing isoforms, visualized as stronger intensity. Earlier also, the supply of NaCl has been reported to enhance the activity of Cu-ZnSOD II in Triticum aestivum seedlings (Eyidoğan et al. 2003). Since Cu-Zn-SOD isoform is predominantly present in chloroplast and cytosol; Mn-SOD is located in peroxisomes and

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mitochondria and FeSODs are mainly chloroplastidic (Alscher et al. 2002), Talukdar (2013) suggested the participation of SOD isoforms in different cellular compartments to combat NaCl-induced generation of free radicals in the present material. In a number of instances, the loss of the ability to scavenge free radicals during stress has attributed to a decrease in the activity of antioxidant enzymes including SOD (Mittova et al. 2002; Desingh and Kanagaraj 2007). In Oryza sativa, the salt-tolerant varieties exhibited higher SOD activity and lower lipid peroxidation than the salt-sensitive varieties (Dionisio-Sese and Tobita 1998). In Lycopersicon esculentum and citrus, salt tolerance was attributed to the increased activity of SOD (Mittova et al. 2004). Enhanced oxidative stress tolerance was also observed in the plants overexpressing FeSOD (Van Camp et al. 1996). The significant increase in the activity of SOD in the NaCl (200 mM NaCl for 1, 2, and 5 days)-stressed Hordeum vulgare root was highly correlated with the increased expression of the constitutive isoforms as well as the induced ones (Kim et al. 2005). In another study, NaCl salinity (50, 100, and 150 mM) exposed Gossypium hirsutum varieties (Arya-Anubam and LRA-5166) exhibited a progressively increased SOD activity. However, the activity of SOD was markedly higher in var. Arya-Anubam than in var. LRA-5166 at all salinity levels (Desingh and Kanagaraj 2007). Salinity induced increase in SOD activity has also been reported in Quercus robur (Sehmer et al. 1995), Setaria italica (Sreenivasasulu et al. (2000), and Pisum sativum (Hernandez et al. 2000). In NaCl (25–50 mM)-exposed Lycopersicon esculentum, different SOD types were detected in the root peroxisomes of the two species Lem and Lpa. In Lem, SOD activity was comprised of matrix Cu-Zn-SOD (mainly the matrix isozyme); while, that of Lpa was comprised of both MnSOD (mainly the matrix isozyme) and Cu-Zn-SOD (exclusively the membrane-bound isozyme) (Mittova et al. 2004). It was suggested that the matrix-SOD functions as the main detoxifier of O2− produced by xanthine oxidase activity (Sandalio and del Rio 1988), while the membrane-bound SOD scavenges O 2 − generated by the membranal NAD(P)H-dependent O 2− production site described by López-Huertas et al. (1999). The authors considered the increased matrix-Mn-SOD activity in root peroxisomes of salttreated Lpa plants as a signal of the matrix O2− production dominance over that of the membrane under salinity. In contrast, when compared to Cu-Zn-SOD, the Mn-SOD was evidenced insensitive to inhibition by H2O2 (Scandalios 1997). Thus, Mittova et al. (2004) argued the possibility of the inherent Mn-SOD activity (as observed only in Lpa peroxisomes) for protecting these organelles to cope better with a high H2O2 content. Sairam and Srivastava (2002) studied the effects of long-term, medium level (electrical conductivity of extract (ECe)=6.85 dS m−1) NaCl salinity in tolerant (Kharchia 65) and susceptible (HD 2687) T. aestivum genotypes. Total SOD activity was highest in chloroplastic fraction followed by

mitochondrial, and lowest in cytosolic fraction. Kharchia 65 showed more SOD activity than HD 2687. The authors detected high Mn-SOD activity also in cytosolic fraction. However, Mn-SOD activity in both the fractions was higher in Kharchia 65, and further increased under salt stress. Cytosolic Mn-SOD activity was very rudimentary, suggesting that cytosolic Mn-SOD has very little role in the scavenging of salinity induced production of O2− radical. Additionally, the authors observed Cu-Zn-SOD in all the three fractions, the highest being in chloroplast followed by mitochondria and cytosol. In Kharchia 65, though salinity increased the CuZn-SOD activity in both cytosolic and chloroplastic fractions, in mitochondria, there was very little or no increase in Cu-ZnSOD activity due to salinity but this genotype maintained higher activity than HD 2687. Concerning Fe-SOD, it was predominantly present in chloroplastic fraction, while some activity was also detected in cytosolic and mitochondrial fractions. Here also, a higher activity was observed in Kharchia 65, both in control and salt-stressed plants than HD 2687. Under salt stress, Fe-SOD activity increased only slightly in cytosolic and mitochondrial fractions and significantly in chloroplastic fraction. Salinity-induced increase in chloroplastic Fe-SOD has been reported in Pisum sativum (Gomez et al. 1999). Other stresses An increase in transcript levels for mitochondrial Mn-SOD, chloroplastic Fe-SOD, and cytosolic Cu/Zn-SOD has been reported in paraquat-Nicotiana plumbaginifolia in the presence of light (Tsang et al. 1991); whereas, the authors noted an induction in the expression of only cytosolic Cu/Zn-SOD under dark condition. Compelling evidence for induction of both genes and enzyme activities to paraquat- and benzyl viologen-produced O2•−O2− were shown by Mylona et al. (2007) in Zea mays embryos. O2•− was evidenced to upregulate the SOD activity and also to induce the expression of mitochondrial Mn-SOD, cytosolic Cu/Zn-SOD genes (Mylona et al. 2007). O3 is an atmospheric pollutant that breaks down in the apoplast forming mainly O2•− and H2O2. In Zea mays seedling, acute (single) or chronic (3, 6, and 10 consecutive days) exposure led to exhibition of increases in transcript levels of mitochondrial Mn-SOD and cytosolic Cu/ Zn-SODs in leaves (Ruzsa et al. 1999). However, transcript level of chloroplastic Cu/Zn-SOD was evidenced down-regulated. In Gracilariopsis tenuifrons, the blue light wavelength has been evidenced to exert a greater induction of SOD activity than other specific wavelengths (Rossa et al. 2002). UV B (7.5 and 15.0 kJ m−2) irradiation was reported to cause elevated SOD activity in Cassia auriculata seedlings by Agarwal (2007). An increase in Mn-SOD protein expression was also observed in CAT1AS Nicotiana tabacum leaves exposed to high light (Dat et al. 2003); whereas, increased total SOD

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activity was observed by Azevedo et al. (1998) in Hordeum vulgare catalase-deficient mutants RPr 79/4 after the plants were taken out from 0.7 % CO2. The condition of hypoxia (restricted oxygen supply in waterlogged and compacted soil) has also been extensively reported to modulate SOD activity in different plant species (Yu and Rengel 1999; Ushimaru et al. 1999, 2001; Biemelt et al. 2000; Pavelic et al. 2000) (Table 1).

Genetic engineering of plant superoxide dismutases Owing to their significant physiological role in plant responses to environmental stresses, SOD genes such as Cu/ Zn-SODs have been extensively characterized in a number of plant species including Arabidopsis thaliana (Kliebenstein et al. 1998), Triticum aestivum (Wu et al. 1999), and Oryza sativa (Sakamoto et al. 1995). However, the examples of plants, where Mn-SODs have been characterized, includes peach (Bagnoli et al. 2002), Zea mays (White and Scandalios 1988), and Oryza sativa (Feng et al. 2006). Particularly, in oxidative-stressed Arabidopsis thaliana, out of the seven SODs—three Fe-SODs denoted FSD1, FSD2, and FSD3; three Cu/Zn-SODs denoted CSD1, CSD2, and CSD3; and one Mn-SOD denoted MSD1—that were evidenced to be present in Arabidopsis thaliana, both at the messenger RNA (mRNA) and the protein level (Kliebenstein et al. 1998). Moreover, FSD2 exhibited increases in response to UV irradiation as well as to high light at the mRNA level. However, ozone exposure did not let any response in FSD2 mRNA. Hence, the significance of a circadian clock in the control of FSD1 at the mRNA level was confirmed (Kliebenstein et al. 1998). Tables 2 and 3 list characterized SOD, respectively, in Arabidopsis thaliana and Oryza sativa.

Overexpression of SOD genes in different plants has been credibly reported to improve plant tolerance to various stresses. Wang et al. (2005) evidenced the improved ability of Oryza sativa against methyl viologen (MV) and drought stress where the Pisum sativum Mn-SOD gene was expressed in Oryza sativa chloroplast. In another instance, the overexpression of Cu/Zn-SOD gene in Nicotania tabacum plants was confirmed to improve its resistance to oxidative stress (Gupta et al. 1993), and tolerance to MV and pure cercosporin was achieved in sugar beet by transferring a Lycopersicon esculentum SOD gene (Tertivanidis et al. 2004). Introduction of SOD genes into plants has been evidenced to help plants to more efficiently eliminate ROS under MV or environmental stresses such as chilling, ozone, water deficit, and salt stresses (Foyer et al. 1994; Bowler et al. 1991; McKersie et al. 1993, 1999; Gupta et al. 1993; Van Camp et al. 1996; Wang et al. 2005). However, no improvements in stress tolerance were observed in several transgenic plants with extra-genetic SODs (Tepperman and Dunsmuir 1990; Sunkar et al. 2006; Jia et al. 2009). The role of the complexity of the ROS detoxification system as well as the differences of SOD isoenzymes have been advocated as the major factors in this context (Kwon et al. 2002; Mylona and Polidoros 2010). Expression of yeast SOD2 in transgenic rice results in increased salt tolerance (Zhao et al. 2006). Overexpression of Oryza sativa cytosolic Cu/Zn-SOD in Nicotania tabacum chloroplasts has been reported to enhance tolerance to salt stress and water deficit (Badawi et al. 2004). The transformed plants exhibited their improved photosynthetic performance during photo-oxidative stresses such as high salt, drought, and PEG treatment (vs. untransformed plants). A Mn-SOD gene (TaMn-SOD) from Tamarix androssowii, under the control of the CaMV35S promoter, was introduced by Wang et al. (2010) into poplar (Populus davidiana × Populus bolleana).

Table 2

List of superoxide dismutases characterized in Arabidopsis thaliana

Sl. No.

Locus ID

Name

Amino acid

Mol. Wt. (kDa)

Isoelectric point

EST/cDNA

Intron

Alt. Spl.

Subcellular localization (putative)

ATCSD1 ATCCS1 ATCSD2

152 320 216

15.0976 33.8510 22.2438

5.3805 5.4585 7.0152

486/7 153/13 394/8

7 5 7

2 3

Cytosol Chloroplast Chloroplast

AT5G18100

ATCSD3

164

16.9409

7.7274

70/4

6

2

Nuclear

AT3G10920 AT3G56350

ATMSD1 ATMSD2

231 241

25.4438 26.8915

8.8353 6.7566

228/6 13/2

5 5

2

Mitochondria Extracellular

AT4G25100 AT5G23310 AT5G51100

ATFSD1 ATFSD3 ATFSD2

212 263 305

23.7907 30.3602 34.6637

6.5148 8.6958 4.6028

279/12 42/6 41/5

6 7 8

5

Chloroplast, cytosol Chloroplast Chloroplast

Cu/Zn SOD 1 AT1G08830 2 AT1G12520 3 AT2G28190 4 Mn SOD 5 6 Fe SOD 7 8 9

Environ Sci Pollut Res Table 3

List of superoxide dismutases characterized in rice (Oryza sativa)

Sl. No. Locus ID (TIGR)

Gene name Amino acids Mol. Wt. Isoelectric cDNA (KOME) Ortholog (kDa) point

Cu/Zn SOD 1 LOC_Os03g11960 OsCSD1 2 LOC_Os03g22810 3 LOC_Os04g48410 4 LOC_Os07g46990 5 LOC_Os08g44770 Mn SOD 6 LOC_Os05g25850 Fe SOD 7 LOC_Os06g02500 8 LOC_Os06g05110

Intron Alternative Subcellular splicing localization (putative)

165

16.52

7.41

AK073785

AT5G18100 6

4

OsCSD2 OsCCS1 OsCSD3 OsCSD4

271 313 153 212

27.87 32.23 15.08 21.30

6.74 5.89 6.41 6.22

AK061662 AK120348 AK243377 AK059841

AT1G08830 AT1G12520 AT1G08830 AT2G28190

9 5 7 7

0 2 2 2

Cytosolic, peroxisome Cytosolic Chloroplastic Cytosolic Chloroplastic

OsMSD

232

25.00

7.04

AK104160

AT3G10920 5

2

Mitochondrion

OsFSD1 OsFSD2

392 256

43.42 29.48

5.44 9.09

AK111656 AK062073

AT5G51100 7 AT5G23310 8

0 2

Chloroplastic Chloroplastic

In transgenic plants, the authors noted an enhanced SOD activity that was accompanied by significantly decreased lipid peroxidation (measured as malondialdehyde, MDA) and electrolyte leakage (measured as electrical conductivity, EC) when compared to wild-type (WT) plants under NaCl stress. The transformation of Sod1 complementary DNA (cDNA) (a cDNA encoding a cytosolic Cu/Zn-SOD in Oryza sativa from the mangrove plant Avicennia marina has been evidenced to increase tolerance to MV-mediated oxidative stress in comparison to wild type (WT). The transgenic Oryza sativa also exhibited tolerance to salinity stress at 150 mM NaCl for 8 days while, WT plants wilted at the end of the hydroponic stress treatment (Prashanth et al. 2008). Wang et al. (2005) developed transgenic Oryza sativa plants expressing MnSOD in chloroplasts under the control of a stress-inducible promoter. In transgenic plants, the authors achieved a higher SOD activity, which led to enhanced drought tolerance. However, the extent of SOD over-expression required to protect plants from oxidative stress is not yet clear. In this context, a 30- to 50-fold increase in chloroplastic SOD activity of transgenic tobacco plants transformed with petunia Cu/ZnSOD failed to provide any detectable changes in oxidative stress resistance (Tepperman and Dunsmuir 1990). On the other, Pisum sativum Cu/Zn-SOD transformed transgenic Nicotiana tabacum plants exhibited a threefold increase in the total SOD activity (Gupta et al. 1993). Triticum aestivum Mn-SOD-transformed Brassica napus plants exhibited a 1.5to 2.5-fold increase in total SOD activity where an increased oxidative resistance was evidenced compared with the WT controls (Basu et al. 2001). Earlier, a positive response to drought was reported to occur as a consequence of overexpressing a single transgenic Mn-SOD targeted to chloroplasts in Medicago sativa (McKersie et al. 1996). Since chloroplasts are the major sites for ROS production, therefore especially

sensitive to ROS damage (Foyer et al. 1994), Wang et al. (2005) fused the pMn-SOD gene with a chloroplast transit peptide sequence in order to target the pMn-SOD to the chloroplast. Surprisingly, the authors observed a significant protective effect against drought stress as a result of a relatively small increase in total SOD activity in T1 plants. Earlier, Bowler et al. (1991) reported a decreased cellular damage by O2•− in transgenic Nicotiana tabacum with Mn-SOD in its chloroplasts and mitochondria; whereas, the over-expression of Arabidopsis Fe-SOD in transgenic Zea mays chloroplast has also been evidenced to enhance MV tolerance (Van Breusegem et al. 1999). Simultaneous overexpression of both Cu/Zn-SOD and APX in transgenic tall Festuca arundinacea plants has been evidenced to confer increased tolerance to a wide range of abiotic stresses including MV, H2O2, and the heavy metals such as As, Cd, and Cu (Lee et al. 2007). In a recent work by Molina-Rueda et al. (2013), the drought response of populus SOD gene family was investigated. Through in silico analysis of populus genome, the authors identified 12 SOD genes and 2 genes encoding Cuchaperones for SOD (CCSs). The poplar SODs were confirmed to form three phylogenetic clusters in accordance with their distinct metal co-factor requirements and gene structure. In addition, nearly all poplar SODs and CCSs were evidenced to occur in duplicate derived from whole genome duplication, in sharp contrast to their predominantly single-copy Arabidopsis orthologs. Moreover, the drought stress was found to trigger plant-wide downregulation of the plastidic copper SODs (CSDs), with a concomitant upregulation of plastidic iron SODs (FSDs) in glutamine synthetase (GS) poplar relative to the wild type; this was confirmed at the activity level. The authors also found evidence for coordinated downregulation of other copper proteins, including plastidic CCSs and polyphenol oxidases, in GS poplar under drought

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conditions. Wang et al. (2004) constructed the transgenic Arabidopsis overexpressing Mn-SOD where, the activity of Mn-SOD as well as that of Cu/Zn-SOD and Fe-SODs was higher than that of wild type. Additionally, when treated with 150 mM NaCl, the transgenic plants grew well and exhibited lower lipid peroxidation product (MDA), while the wild type plants withered gradually, this indicated the enhanced salttolerance of transgenic Arabidopsis. The studies on transgenic plants with suppressed SOD have provided substantial evidences of O2•− regulation of antioxidant gene expression. In this context, Rizhsky et al. (2003) performed the transcriptome analysis of knockdown Arabidopsis plants with suppressed expression of chloroplastic Cu/Zn-SOD (CSD2) and reported the exhibition of induced chloroplast and nuclear encoded genes as a result of O2•− accumulation under optimal conditions (Rizhsky et al. 2003). In addition, induced nuclear genes included also FeSOD. A comparative transcriptome analyses performed by Gadjev et al. 2006) among wild-type Arabidopsis plants exposed to paraquat or ozone and transgenic plants with suppressed Cu/Zn-SOD under optimal conditions revealed the exhibition of induction of a number of chloroplast and nuclear encoded genes. Wu et al. (2012) cloned and functionally characterized three SOD genes from halophyte Salicornia europaea (a typical halophyte that is capable of surviving in 3.5 % salinity) and Thellungiella halophile (a close relative of Arabidopsis can withstand 500 mM NaCl; Zhu 2001). The authors characterized the Mn-SOD and Cu/Zn-SOD gene from Salicornia europaea, and transferred these two genes and ThMSD into BL21 Escherichia coli by constructed prokaryotic expression vectors. Through optimization of the inducing concentration of isopropyl β-D-thiogalactopyranoside (IPTG), the authors tested the salt tolerance of these three SODs under 6.5 and 7.5 % NaCl stress. The results demonstrate that the recombinants BL21 (pET30-SeMSD) 20 and BL21 (pET30-ThMSD) show better tolerance to salinity stress in comparison with the control stain BL21 (pET30), but the recombinant BL21 (pET30-SeCSD) has not displayed increased salt tolerance. Recently, in order to investigate new gene resource for enhancing Oryza sativa-tolerance to salt stress, Mn-SOD gene from halophilic archaeon (Natrinema altunense sp.) (NaMn-SOD) was isolated and introduced into Oryza sativa cv. Nipponbare by Agrobacterium-mediated transformation (Chen et al. 2013). The transformants (L1 and L2) showed some NaMn-SOD expression and increased total SOD activity, which contributed to higher efficiency of ROS elimination under salt stress. The levels of O2•− and H2O2 were significantly decreased. In addition, they exhibited higher levels of photosynthesis, whereas lower relative ion leakage and MDA content compared to wild-type plants. The authors were able to obtain transgenic seedlings that were phenotypically healthier, where the heterologous expression of NaMn-SOD improved salt tolerance in Oryza sativa was

evidenced by the exhibition of significantly decreased levels of O2•− and H2O2. In another recent study, under the control of the CaMV35S promoter, Diaz-Vivancos et al. (2013) obtained salt stress tolerant transgenic plums by ectopically expressing cytosolic SOD. Transgenic plantlets exhibited higher contents of non-enzymatic antioxidants glutathione and ascorbate than non-transformed control, which correlated with lower H2O2 accumulation. The overexpression of Cu/Zn-SOD was reported to enhance in vitro shoot multiplication in transgenic plum (Faize et al. 2013). The authors generated transgenic plum plantlets overexpressing the cytSOD gene in cytosol under the control of the constitutive promoter CaMV35S. Three transgenic lines with upregulated SOD at transcriptional levels that showed silenced cytAPX expression displayed an elevated in vitro multiplication rate. In contrast to the discussed above reports, where the overexpression of SOD in plants was reported to render them stress-tolerant, in some transgenics, the overexpression of cytosolic or chloroplastic SOD provided only moderate or minimal tolerance, attributed to the type of overexpressed SOD and its subcellular localization (Allen et al. 1997). To this end, Sunkar et al. (2006) worked out the microRNA (miRNA) molecule significance in the regulation of antioxidant gene expression. In Arabidopsis, Sunkar et al. (2006) identified miR398, a repressor of cytosolic (CSD1) and chloroplastic (CSD2) Cu/Zn-SOD expression. The authors observed an increased tolerance to paraquat- and salt-induced oxidative stress in transgenic Arabidopsis plants exhibiting downregulation of miR398 and overexpression of the CSD2. Thus, the existence of a direct connection between miRNA pathway and CSD1 and CSD2 post-transcriptional regulation was revealed. Later, miR398 and its target sites on cytosolic and chloroplastic Cu/Zn-SOD mRNA were reported to be conserved in dicotyledonous and monocotyledonous plants (Sunkar et al. 2006). The studies by Jia et al. (2009) in ABA or salt stressexposed Populus tremula and Arabidopsis thaliana revealed the existence of a twofold posttranscriptional regulation of SOD genes by miR398: a dynamic regulation within a plant species and a differential regulation between different plant species. Hence, it would be interesting to work out the role of ROS-mediated regulation, ROS-mediated signaling, and to elucidate the signal transduction pathways involved therein (Mylona and Polidoros 2010).

Conclusions and future perspectives Non-metabolized ROS and their reaction products exceed the status of antioxidants under adverse conditions, cause cellular metabolism arrest, and eventually impair plant growth and development. However, a first line of defense against abiotic stress-accrued enhanced ROS and its reaction products, SODs protect cells against cytotoxic O2•−-led potential consequences

Environ Sci Pollut Res

in cells by catalyzing its conversion to O2 and H2O2. Plants may possess several distinct types of SOD, each differing with respect to the metal at the active site. Cu/Zn-SOD has been localized in cytosol, chloroplasts, peroxisomes; whereas, FeSODs are mainly localized in chloroplasts and in some extent to peroxisomes and apoplast, and the Mn-SODs mainly occur in the mitochondrion. All SOD-isoforms (Cu/Zn-SOD; MnSOD; Fe-SOD) are nuclear coded and have been extensively evidenced to be modulated by various abiotic stress factors. Literature is full on the physiological and biochemical aspects of SODs in plants under various stresses; however, there seems a lack of reports on exhaustive molecular genetics in the current context. Role and underlying mechanisms of FeSODs-mediated protection of cells against oxidative stress and the development of organelles (such as chloroplast) are known (Myouga et al. 2008; Kuo et al. 2013); however, efforts should be made to unveil the molecular/genetic insights into previous aspects in context also with Cu/Zn and MnSODs. Little is known about the regulation of SOD types by post-translational modifications (Holzmeister et al. 2015). If performed, these studies can help us in producing transgenic plants exhibiting suppressed SODs, and high capacity for the regulation of elevated cellular O2•−. Metallic nanoparticles are being rapidly contaminating varied environmental compartments, and these nanoparticles can be accumulated in plants. Metallic nanoparticles such as nanoscale Cu, Fe and Zn may interact with SODs and modulate their biochemistry and functions since Cu, Fe and Zn are structural constituents of SODs. Hence, studies on the potential interaction of SOD isoforms (Cu/Zn-SOD, Mn-SOD, Fe-SOD) with Cu, Fe, and Zn nanoparticles can be promising under the umbrella of Bnanometallomics,^ Additionally, more exhaustive research on the BSOD isoform-bioinformatics^ can confirm potential antiquity among SOD isoforms (Cu/Zn-SOD, Mn-SOD, Fe-SOD). Acknowledgments SSG, RG, and NT would like to acknowledge the receipt of funds from DST, CSIR, and UGC, Govt. of India, New Delhi. NAA (SFRH/BPD/84671/2012) is grateful to the Portuguese Foundation for Science and Technology (FCT) and the Aveiro University Research Institute/Centre for Environmental and Marine Studies (CESAM) (UID/ AMB/50017/2013) for partial financial supports. The authors apologize if some references related to the main theme of the current review could not be cited due to space constraint.

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