Skip to main content

Advertisement

Log in

Superoxide dismutase—mentor of abiotic stress tolerance in crop plants

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarwal S (2007) Increased antioxidant activity in Cassia seedlings under UV-B radiation. Biol Plant 51:157–160

    CAS  Google Scholar 

  • Agrawal SB, Mishra S (2009) Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L. Ecotoxicol Environ Saf 72:610–618

    CAS  Google Scholar 

  • Ahmed IM, Cao F, Zhang M, Chen X, Zhang G et al (2013) Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE 8(10):e77869

    CAS  Google Scholar 

  • Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radic Biol Med 23:73–479

    Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M, Khan NA (2008a) Ontogenic variation in response of Brassica campestris L. to cadmium toxicity. J Plant Interact 3:189–198

    CAS  Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA (2008b) Growth characteristics and antioxidant metabolism of moongbean genotypes differing in photosynthetic capacity subjected to water deficit stress. J Plant Interact 3:127–136

    CAS  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC et al (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC et al (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple and associated enzymes. Protoplasma 251:1265–1283

    CAS  Google Scholar 

  • Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS et al (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121

    CAS  Google Scholar 

  • Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292

    CAS  Google Scholar 

  • Baccouch S, Chaoui A, El Ferjani E (1998) Nickel toxicity: effects on growth and metabolism of maize. J Plant Nutr 21:577–588

    CAS  Google Scholar 

  • Badawi GH, Yamauchi Y, Shimada E, Sasaki R et al (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928

    Google Scholar 

  • Bagnoli F, Giannino D, Caparrini S, Camussi A, Mariotti D, Racchi ML (2002) Molecular cloning, characterisation and expression of a manganese superoxide dismutase gene from peach (Prunus persica [L.] Batsch). Mol Genet Genomics 267:321–328

    CAS  Google Scholar 

  • Bannister WH, Bannister JV, Barra D, Bond J, Bossa F (1991) Evolutionary aspects of superoxide dismutase: the copper/zinc enzyme. Free Radical Res Commun 12–13:349–361

    Google Scholar 

  • Barra D, Schinina ME, Bossa F, Puget K, Durosay P et al (1990) A tetrameric iron superoxide dismutase from the eucaryote Tetrahymena pyriformis. J Biol Chem 265:17680–17687

    CAS  Google Scholar 

  • Basu U, Good AG, Taylor GJ (2001) Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial maganese superoxide dismutase cDNA are resistant to aluminium. Plant Cell Environ 24:1269–1278

    CAS  Google Scholar 

  • Baum JA, Chandlee JM, Scandalios JG (1983) Purification and partial characterization of a genetically defined superoxide dismutase (SOD-1) associated with maize chloroplasts. Plant Physiol 73:31–35

    CAS  Google Scholar 

  • Bhattacharjee S (2012) The language of reactive oxygen species signaling in plants. J Bot. doi:10.1155/2012/985298

    Google Scholar 

  • Biemelt S, Keetman U, Mock H, Grimm B (2000) Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia. Plant Cell Environ 23:135–144

    CAS  Google Scholar 

  • Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyper-accumulator, Alyssum bertolonii. New Phytol 156:205–215

    CAS  Google Scholar 

  • Bordo D, Djinovic K, Bolognesi M (1994) Conserved patterns in the Cu-Zn superoxide dismutase family. J Mol Biol 238:366–386

    CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2013) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J et al (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732

    CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    CAS  Google Scholar 

  • Bowler C, Van Camp W, Van Montague M, Inze D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218

    CAS  Google Scholar 

  • Burke EJ, Brown SJ, Christidis N (2006) Modelling the recent evolution of global drought and projections for the twenty-first century with the Hadley Centre Climate Model. J Hydrometeor 7:1113–1125

    Google Scholar 

  • Cao X, Ma LQ, Tu C (2004) Antioxidant responses to arsenic in the arsenichyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128:317–325

    CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    CAS  Google Scholar 

  • Chen Z, Pan YH, An LY, Yang WJ, Xu LG, Zhu C (2013) Heterologous expression of a halophilic archaeon manganese superoxide dismutase enhances salt tolerance in transgenic rice. Russ J Plant Physiol 60:359–366

    CAS  Google Scholar 

  • Chew YH, Halliday KJ (2011) A stress-free walk from Arabidopsis to crops. Curr Opin Biotechnol 22:281–286

    CAS  Google Scholar 

  • Chirkova TV, Novitskaya LO, Blokhina OB (1998) Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency. Russ J Plant Physiol 45:55–62

  • Cho U, Seo N (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    CAS  Google Scholar 

  • Corpas FJ, Fernández-Ocaña A, Carreras A, Valderrama R, Luque F et al (2006) The expression of different superoxide dismutase forms is cell-type dependent in olive (Olea europaea L.) leaves. Plant Cell Physiol 47:984–994

    CAS  Google Scholar 

  • Cudd A, Fridovich I (1982) Electrostatic interactions in the reaction mechanism of bovine erythrocyte superoxide dismutase. J Biol Chem 257:11443–11447

    CAS  Google Scholar 

  • Dat JF, Pellinen R, Beeckman T, Van De Cotte B, Langebartels C, Kangasjarvi J et al (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621–632

    CAS  Google Scholar 

  • Desingh R, Kanagaraj G (2007) Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. Gen Appl Plant Physiol 33:221–234

    CAS  Google Scholar 

  • Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C et al (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotechnol J 11:976–985

    CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Google Scholar 

  • Diwan H, Khan I, Ahmad A, Iqbal M (2010) Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Regul 61:97–107

    CAS  Google Scholar 

  • Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ 25:687–693

    CAS  Google Scholar 

  • Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350

    CAS  Google Scholar 

  • Duarte B, Silva V, Caçador I (2012) Hexavalent chromium reduction, uptake and oxidative biomarkers in Halimione portulacoides. Ecotoxicol Environ Saf 83:1–7

    CAS  Google Scholar 

  • Dupont CL, Neupane K, Shearer J, Palenik B (2008) Diversity, function and evolution of genes coding for putative Ni‐containing superoxide dismutases. Environ Microbiol 10:1831–1843

    CAS  Google Scholar 

  • Ekmekci Y, Tanyolac D, Ayhana B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

    CAS  Google Scholar 

  • Erturk HN (1999) Responses of superoxide dismutases to oxidative stress in Arabidopsis thaliana. PhD Thesis, Faculty of the Virginia Polytechnic Institute and State University, Blacksburg, Virginia

  • Eyidoğan F, Öktem H, Yücel M (2003) Superoxide dismutase activity in salt stressed wheat seedlings. Acta Physiol Plant 25:263–269

    Google Scholar 

  • Faize M, Faize L, Petri C, Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ et al (2013) Cu/Zn superoxide dismutase and ascorbate peroxidase enhance in vitro shoot multiplication in transgenic plum. J Plant Physiol 170:625–632

    CAS  Google Scholar 

  • FAO (Food, Agriculture Organization of the United Nations) (2004) FAO production year book. FAO, Rome

    Google Scholar 

  • Feng W, Hongbin W, Bing L, Jinfa W (2006) Cloning and characterization of a novel splicing isoform of the iron-superoxide dismutase gene in rice (Oryza sativa L.). Plant Cell Rep 24:734–742

    Google Scholar 

  • Ferreira RR, Fornazier RF, Vitoria AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25:327–342

    CAS  Google Scholar 

  • Fink RC, Scandalios JG (2002) Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399:19–36

    CAS  Google Scholar 

  • Fornazier RF, Ferreira RR, Vitoria AP, Molina SMG et al (2002) Effects of cadmium on antioxidant enzyme activitiesin sugar cane. Biol Plant 45:91–97

    CAS  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    CAS  Google Scholar 

  • Fridovich I (1986) Superoxide dismutases. Adv Enzymol Mol Biol 58:61–97

    CAS  Google Scholar 

  • Fridovich I (1989) Superoxide dismutase: an adaptation to a paramagnetic gas. J Biol Chem 264:7761–7764

    CAS  Google Scholar 

  • Fu LM, Qu LJ (2013) Editorial. What and how, plants do encountering unfavorable stuff? Environ Exp Bot 86:1

    Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev T, Laloi C, Minkov IN et al (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445

    CAS  Google Scholar 

  • Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll content in wheat shoots. Biol Plant 50:653–659

    CAS  Google Scholar 

  • Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  Google Scholar 

  • Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK et al (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212

    CAS  Google Scholar 

  • Gomez JM, Hernandez JA, Jimenez A, del Rio LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plant. Free Radical Res 31(Suppl):11–18

    Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 146:743–749

    Google Scholar 

  • Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol 103:1067–1073

    Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74:1201–1208

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Hartley-Whitaker J, Ainsworth G, Meharg AA (2001) Copper- and arsenate induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ 24:713–722

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–316

    Google Scholar 

  • Hernandez J, Jimenez A, Millineaus P, Sevilla F (2000) Tolerance to pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862

    CAS  Google Scholar 

  • Hernandez I, Chacón O, Rodriguez R, Portieles R, Opez Y, Pujol M, Borrás-Hidalgo O (2009) Black shank resistant tobacco by silencing of glutathione S-transferase. Biochem Biophys Res Commun 387:300–304

    CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052

    CAS  Google Scholar 

  • Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999

    Google Scholar 

  • Iqbal N, Masood A, Nazar R, Syeed S, Khan NA (2010) Photosynthesis, growth and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in cadmium tolerance. Agric Sci China 9:519–527

    CAS  Google Scholar 

  • Israr M, Sahi SV (2006) Antioxidative responses to mercury in the cell cultures of Sesbania drummondii. Plant Physiol Biochem 44:590–595

    CAS  Google Scholar 

  • Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598

    CAS  Google Scholar 

  • Jaleel CA, Manivannan P, Kishorekumar A, Sankar B et al (2007a) Alterations in osmoregulation, antioxidant enzymes and indole alkaloid levels in Catharanthus roseus exposed to water deficit. Colloids Surf B: Biointerfaces 59:150–157

    CAS  Google Scholar 

  • Jaleel CA, Manivannan P, Kishorekumar A, Sankar B, Panneerselvam R (2007b) Calcium chloride effects on salinity induced oxidative stress, proline metabolism and indole alkaloid accumulation in Catharanthus roseus. CR Biol 330:674–683

    CAS  Google Scholar 

  • Jaleel CA, Manivannan P, Lakshmanan GMA, Sridharan R, Panneerselvam R (2007c) NaCl as a physiological modulator of proline metabolism and antioxidant potential in Phyllanthus amarus. CR Biol 330:806–813

    CAS  Google Scholar 

  • Jaleel CA, Gopi R, Manivannan P, Gomathinayagam M, Murali PV, Panneerselvam R (2008a) Soil applied propiconazole alleviates the impact of salinity on Catharanthus roseus by improving antioxidant status. Pestic Biochem Physiol 90:135–139

    CAS  Google Scholar 

  • Jaleel CA, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R (2008b) Triadimefon induced salt stress tolerance in Withania somnifera and its relationship to antioxidant defense system. S Afr J Bot 74:126–132

    Google Scholar 

  • Jia X, Wang WX, Ren L, Chen QJ, Mendu V et al (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59

    CAS  Google Scholar 

  • Kandhari P (2004) Generic differences in antioxidant concentration in the fruit tissues of four major cultivars of apples. Master Thesis, University of Maryland, College Park

  • Kanematsu S, Asada K (1989) Cu/Zn superoxide dismutase in rice: occurrence of an active monomeric enzyme and two types of isozymes in leaf and non-photosynthetic tissues. Plant Cell Physiol 30:381–391

    CAS  Google Scholar 

  • Kanematsu S, Okayasu M, Ueno S (2013) Atypical cytosol-localized Fe-superoxide dismutase in the moss Pogonatum inflexum. Bull Minamikyushu Univ 3A(23):31

    Google Scholar 

  • Karlsson M, Melzer M, Prokhorenko I, Johansson T, Wingsle G (2005) Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans. J Exp Bot 56:2085–2093

    CAS  Google Scholar 

  • Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol 56:255–270

    CAS  Google Scholar 

  • Kasai T, Suzuki T, Ogawa KOK, Inagaki Y, Ichinose Y, Toyoda K, Shiraishi T (2006) Pea extracellular Cu/Zn-superoxide dismutase responsive to signal molecules from a fungal pathogen. J Gen Plant Pathol 72:265–272

    CAS  Google Scholar 

  • Khan NA, Samiullah, Singh S, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:435–444

    CAS  Google Scholar 

  • Kim RH, Smith PD, Aleyasin H, Hayley S, Mount MP et al (2005) Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyrindine (MPTP) and oxidative stress. Proc Natl Acad Sci U S A 102:5215–5220

    CAS  Google Scholar 

  • Kim HJ, Kato N, Kim S, Triplett B (2008) Cu/Zn superoxide dismutases in developing cotton fibers: evidence for an extracellular form. Planta 228:281–292

    CAS  Google Scholar 

  • Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650

    CAS  Google Scholar 

  • Kumar RR, Karajol K, Naik GR (2011) Effect of polyethylene glycol induced water stress on physiological and biochemical responses in pigeonpea (Cajanus cajan L. Millsp.). Recent Res Sci Technol 3:148–152

    Google Scholar 

  • Kuo WY, Huang CH, Liu AC, Cheng CP et al (2013) CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytol 197:99–110

    CAS  Google Scholar 

  • Kwiatowski J, Kaniuga Z (1986) Isolation and characterization of cytosolic and chloroplastic isozymes of Cu-Zn superoxide dismutase from tomato leaves and their relationships to other Cu-Zn superoxide dismutases. Biochim Biophys Acta 874:99–115

    CAS  Google Scholar 

  • Kwon S, Jeong Y, Lee H, Kim J, Cho K, Allen R, Kwak S (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen‐mediated oxidative stress. Plant Cell Environ 25:873–882

    Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS et al (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    CAS  Google Scholar 

  • Leon AM, Palma JM, Corpas FJ, Gomez M, Romero-Puertas MC et al. (2002) Antioxidant enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40:813–820

  • Li Y, Song Y, Shi G, Wang J, Hou X (2009) Response of antioxidant activity to excess copper in two cultivars of Brassica campestris ssp. chinensis Makino. Acta Physiol Plant 31:155–162

    Google Scholar 

  • Liu YT, Chen Z-S, Hong CY (2011) Cadmium-induced physiological response and antioxidant enzyme changes in the novel cadmium accumulator, Tagetes patula. J Hazard Mater 189:724–731

    CAS  Google Scholar 

  • Lokhande VH, Srivastava AK, Srivastava S, Nikam TD, Suprasanna P (2011) Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L. Plant Growth Regul 65:287–298

    CAS  Google Scholar 

  • Lomonte C, Sgherri C, Baker AJM, Kolev SD, Navari-Izzo F (2010) Antioxidative response of Atriplex codonocarpa to mercury. Environ Exp Bot 69:9–16

    CAS  Google Scholar 

  • López-Huertas E, Corpas FJ, Sandalio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536

    Google Scholar 

  • Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71:605–613

    Google Scholar 

  • Madanala R, Gupta V, Deeba F, Upadhyay SK, Pandey V, Singh PK, Tuli R (2011) A highly stable Cu/Zn superoxide dismutase from Withania somnifera plant: gene cloning, expression and characterization of the recombinant protein. Biotechnol Lett 33:2057–2063

    CAS  Google Scholar 

  • Manivannan P, Jaleel CA, Kishorekumar A, Sankar B et al (2007) Changes in antioxidant metabolism of Vigna unguiculata (L.) Walp. by propiconazole under water deficit stress. Colloids Surf B: Biointerfaces 57:69–74

    CAS  Google Scholar 

  • Manivannan P, Jaleel CA, Kishorekumar A, Sankar B, Somasundaram R, Panneerselvam R (2008) Protection of Vigna unguiculata (L.) Walp. plants from salt stress by paclobutrazol. Colloids Surf B: Biointerfaces 61:315–318

    CAS  Google Scholar 

  • Mann T, Keilin D (1938) Haemocuprein and hepatocuprein, copper protein compounds of blood and liver in mammals. Proc R Soc London 126:303–315

    CAS  Google Scholar 

  • Marino M, Galvano M, Cambria A, Polticelli F, Desideri A (1995) Modeling the three-dimensional structure and the electrostatic potential field of two Cu, Zn superoxide dismutase variants from tomato leaves. Protein Eng 8:551–556

    CAS  Google Scholar 

  • Martínez Domínguez D, Córdoba García F, Canalejo Raya A, Torronteras Santiago R (2010) Cadmium-induced oxidative stress and the response of the antioxidative defense system in Spartina densiflora. Physiol Plant 139:289–302

    Google Scholar 

  • Martinez CA, Loureiro ME, Oliva MA, Maestri M (2001) Differential responses of superoxide dismutase in freezing resistant Solanum curtilobum and freezing sensitive Solanum tuberosum subjected to oxidative and water stress. Plant Sci 160:505–515

    CAS  Google Scholar 

  • McCord J, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprcin (hemocuprein). J Bioichem 244:6049–6055

    CAS  Google Scholar 

  • McCord JM, Fridovich I (1988) Superoxide dismutase: the first 20 years (1968–1988). Free Radical Biol Med 5:363–369

    CAS  Google Scholar 

  • McKersie BD, Chen Y, de Beus M, Bowley SR, Bowler C et al (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol 103:1155–1163

    CAS  Google Scholar 

  • McKersie BD, Bowley SR, Harjanto E, Le Prince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181

    CAS  Google Scholar 

  • McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848

    CAS  Google Scholar 

  • Miller AF (2004) Superoxide dismutases: active sites that save, but a protein that kills. Curr Opin Chem Biol 8:162–168

    CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindrajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    CAS  Google Scholar 

  • Mishra P, Bhoomika K, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250:3–19

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    CAS  Google Scholar 

  • Mittler R (2011) Oxidative stress in plants. http://biology.unt.edu/ros/pages/rosmetabolismdoc.htm (accessed on 12 March 2015)

  • Mittova V, Guy M, Tal M, Volokita M (2002) Response of the cultivated tomato and its wild salt‐tolerant relative Lycopersicon pennellii to salt‐dependent oxidative stress: increased activities of antioxidant enzymes in root plastids. Free Radical Res 36:195–202

    CAS  Google Scholar 

  • Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up‐regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt‐tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    CAS  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    CAS  Google Scholar 

  • Molina-Rueda JJ, Tsai CJ, Kirby EG (2013) The populus superoxide dismutase gene family and its responses to drought stress in transgenic poplar overexpressing a pine cytosolic glutamine synthetase (GS1a). PLoS ONE 8:e56421

    CAS  Google Scholar 

  • Munné-Bosch S (2005) The role of a-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    CAS  Google Scholar 

  • Mylona PV, Polidoros AN (2010) ROS regulation of antioxidant genes. In: Gupta SD (ed) Reactive oxygen species and antioxidants in higher plants. Science Publishers, pp. 101–127

  • Mylona PV, Polidoros AN, Scandalios JG (1998) Modulation of antioxidant responses by arsenic in maize. Free Radical Biol Med 25:576–585

    CAS  Google Scholar 

  • Mylona PV, Polidoros AN, Scandalios JG (2007) Antioxidant gene responses to ROS-generating xenobiotics in developing and germinated scutella of maize. J Exp Bot 58:1301–1312

    CAS  Google Scholar 

  • Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T et al (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell Online 20:3148–3162

    CAS  Google Scholar 

  • Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou W (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574

    CAS  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002a) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    CAS  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002b) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850

    CAS  Google Scholar 

  • Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2007) Cadmium induced oxidative stress in soybean plants also by the accumulation of δ-aminolaevulinic acid. Biometals 20:841–851

    CAS  Google Scholar 

  • Olsen KM, Hehn A, Jugde H, Slimestad R, Larbat R, Bourgaud F, Lillo C (2010) Identification and characterisation of CYP75A31, a new flavonoid 3050-hydroxylase, isolated from Solanum lycopersicum. BMC Plant Biol 10:21

    Google Scholar 

  • Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 49:157–165

    CAS  Google Scholar 

  • Pavelic D, Arpagaus S, Rawyler A, Braendle R (2000) Impact of postanoxia stress on membrane lipids of anoxia pretreated potato cells. A re-appraisal. Plant Physiol 124:1285–1292

    CAS  Google Scholar 

  • Pitcher LH, Zilinskas BA (1996) Overexpression of copper/zinc superoxide dismutase in the cytosol of transgenic tobacco confers partial resistance to ozone-induced foliar necrosis. Plant Physiol 110:583–588

    CAS  Google Scholar 

  • Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgen Res 17:281–291

    CAS  Google Scholar 

  • Qadir S, Qureshi M, Javed S, Abdin M (2004) Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Sci 167:1171–1181

    CAS  Google Scholar 

  • Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278:38921–38925

    CAS  Google Scholar 

  • Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ et al (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radical Res 31(Suppl):25–32

    Google Scholar 

  • Rossa MM, de Oliveira MC, Okamoto OK et al (2002) Effect of visible light on superoxide dismutase (SOD) activity in the red alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta). J Appl Phycol 14:151–157

    CAS  Google Scholar 

  • Ruzsa SM, Mylona P, Scandalios JG (1999) Differential responses of antioxidant genes in maize leaves exposed to ozone. Redox Rep 4:95–103

    CAS  Google Scholar 

  • Sairam R, Srivastava G (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162:897–904

    CAS  Google Scholar 

  • Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91

    CAS  Google Scholar 

  • Sakamoto A, Okumura T, Kaminaka H, Sumi K, Tanaka K (1995) Structure and differential response to abscisic acid of two promoters for the cytosolic copper/zinc-superoxide dismutase genes, SodCcl and SodCc2, in rice protoplasts. FEBS Lett 358:62–66

    CAS  Google Scholar 

  • Sandalio LM, del Rio LA (1987) Localization of superoxide dismutase in glyoxysomes from Citrullus vulgaris: functional implications in cellular metabolism. J Plant Physiol 127:395–409

    CAS  Google Scholar 

  • Sandalio LM, del Rio LA (1988) Intra-organellar distribution of superoxide dismutase in plant peroxisomes (glyoxysomes and leaf peroxisomes). Plant Physiol 88:1215–1218

    CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plant. J Exp Bot 52:2115–2126

    CAS  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Ríıo LA (2013) Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. Subcel Biochem 69:231–255

    CAS  Google Scholar 

  • Scandalios JG (1997) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, Plainview

    Google Scholar 

  • Schinkel H, Hertzberg M, Wingsle G (2001) A small family of novel Cu/Zn-superoxide dismutases with high isoelectric points in hybrid aspen. Planta 213:272–279

    CAS  Google Scholar 

  • Sehmer L, Alaoui-Sasse B, Dizangremel P (1995) Effect of salt stress on growth and on the detoxifying pathway of pedunculate oak seedlings (Quercus robur L.). J Plant Physiol 147:144–151

    CAS  Google Scholar 

  • Sekmen AH, Turkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131:399–411

    CAS  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

  • Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494

    CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221

    CAS  Google Scholar 

  • Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038

    CAS  Google Scholar 

  • Sharma I, Pati P, Bhardwaj R (2011) Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 33:1723–1735

    CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 37:1–26

    Google Scholar 

  • Simonovicova M, Tamás L, Huttová J, Mistrík I (2004) Effect of aluminium on oxidative stress related enzymes activities in barley roots. Biol Plant 48:261–266

    CAS  Google Scholar 

  • Singh S, Khan NA, Nazar R, Anjum NA (2008) Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. Am J Plant Physiol 3:25–32

    CAS  Google Scholar 

  • Smith MW, Doolittle RF (1992) A comparison of evolutionary rates of the two major kinds of superoxide dismutases. J Mol Evol 34:175–184

    CAS  Google Scholar 

  • Sreenivasasulu N, Grinm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt tolerant and salt sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109:435–442

    Google Scholar 

  • Srivastava AK, Bhargava P, Rai LC (2005) Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum. World J Microbiol Biotechnol 22:1291–1298

    Google Scholar 

  • Srivastava S, Srivastava AK, Suprasanna P, D’Souza SF (2010) Comparative antioxidant profiling of tolerant and sensitive varieties of Brassica juncea L. to arsenate and arsenite exposure. Bull Environ Contam Toxicol 84:342–346

    CAS  Google Scholar 

  • Stankovic S, Stankovic RA et al (2013) Bioindicators of toxic metals. In: Lichtfouse E (ed) Environmental chemistry for a sustainable world, vol 2. Springer, Berlin, p 80

    Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dsmutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    CAS  Google Scholar 

  • Talukdar D (2013) Growth responses and leaf antioxidant metabolism of grass pea (Lathyrus sativus L.) genotypes under salinity stress. ISRN Agron. doi:10.1155/2013/284830

    Google Scholar 

  • Tanyolac D, Ekmekc Y, Unalan S (2007) Changes in photochemi-cal and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere 67:89–98

  • Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxity. Plant Mol Biol 14:501–511

    CAS  Google Scholar 

  • Tertivanidis K, Goudoula C, Vasilikiotis C, Hassiotou E, Perl-Treves R, Tsaftaris A (2004) Superoxide dismutase transgenes in sugarbeets confer resistance to oxidative agents and the Fungus C. beticola. Transgenic Res 13:225–233

    CAS  Google Scholar 

  • Tsang EWT, Bowler C, Herouart D, Van Camp W, Villarroel R et al (1991) Differential regulation of superoxide dsimutases in plants exposed to environmental stresses. Plant Cell 3:783–792

    CAS  Google Scholar 

  • Tuteja N, Gill SS (2013) Crop improvement under adverse conditions, 1st edn. Springer, New York

    Google Scholar 

  • Tuteja N, Tiburcio AF, Fortes AM, Bartels D (2011) Plant abiotic stress. Introduction to PSB special issue. Plant Signal Behav 6:173–174

    Google Scholar 

  • Tuteja N, Mishra P, Yadav S, Tajrishi M, Baral S, Sabat SC (2015) Heterologous expression and biochemical characterization of a highly active and stable chloroplastic CuZn-superoxide dismutase from Pisum sativum. BMC Biotechnol 15:3

    Google Scholar 

  • Ushimaru T, Kanematsu S, Shibasaka M, Tsuji H (1999) Effect of hypoxia on the antioxidative enzymes in aerobically grown rice (Oryza sativa) seedlings. Physiol Plant 107:181–187

    CAS  Google Scholar 

  • Ushimaru T, Kanematsu S, Katayama M, Tsuji H (2001) Antioxidative enzymes in seedlings of Nelumbo nucifera germinated under water. Physiol Plant 112:39–46

    CAS  Google Scholar 

  • Van Breusegem F, Slooten L, Stassart J, Moens T, Botterman J et al (1999) Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol 40:515–523

    Google Scholar 

  • Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overexpressing Fe-superoxide dismutase in chloroplasts. Plant Physiol 112:1703–1714

    Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655

    CAS  Google Scholar 

  • Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677

    CAS  Google Scholar 

  • Wang FZ, Wang QB, Know SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472

    CAS  Google Scholar 

  • Wang Y, Qu G, Li H, Wu Y, Wang C, Liu G, Yang C (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124

    CAS  Google Scholar 

  • White JA, Scandalios JG (1988) Isolation and characterization of a cDNA for mitochondrial manganese superoxide dismutase (SOD-3) of maize and its relation to other manganese superoxide dismutases. Biochi Biophys Acta Gene Struct Express 951:61–70

    CAS  Google Scholar 

  • Wu G, Wilen RW, Robertson AJ, Gusta LV (1999) Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120:513–520

    CAS  Google Scholar 

  • Wu FB, Dong J, Jia GX, Zheng SJ, Zhang GP (2006) Genotypic differences in the responses of seedling growth and Cd toxicity in rice (Oryza sativa L.). Agric Sci China 5:68–76

    CAS  Google Scholar 

  • Wu F, Yu M, Lu ML, LI J, Wang RF, Wang XL (2012) Cloning and functional characterization of three superoxide dismutases genes from halophyte Salicornia europaea and Thellungiella halophila. Acta Bot Boreali-Occidentalia Sinica 10:005

    Google Scholar 

  • Youn HD, Kiln EJ, Roe JH, Hah YC, Kang SO (1996) A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J 318:889–896

    CAS  Google Scholar 

  • Yu Q, Rengel Z (1999) Drought and salinity differentially influence activities of superoxide dismutase in narrow-leafed lupins. Plant Sci 142:1–11

    CAS  Google Scholar 

  • Zhang J, Kirkham M (1995) Water relations of water-stressed, split-root C4 (Sorghum bicolor; Poaceae) and C3 (Helianthus annuus; Asteraceae) plants. Am J Bot 82:1220–1229

    Google Scholar 

  • Zhao F, Guo S, Zhang H, Zhao Y (2006) Expression of yeast SOD2 in transgenic rice results in increased salt tolerance. Plant Sci 170:216–224

    CAS  Google Scholar 

  • Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509

    CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trend Plant Sci 6:66–71

    CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sarvajeet Singh Gill, Naser A. Anjum or Narendra Tuteja.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gill, S.S., Anjum, N.A., Gill, R. et al. Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res 22, 10375–10394 (2015). https://doi.org/10.1007/s11356-015-4532-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4532-5

Keywords

Navigation