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.
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
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
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
Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radic Biol Med 23:73–479
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
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
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
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
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
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
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
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
Baccouch S, Chaoui A, El Ferjani E (1998) Nickel toxicity: effects on growth and metabolism of maize. J Plant Nutr 21:577–588
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
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
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
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
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
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
Bhattacharjee S (2012) The language of reactive oxygen species signaling in plants. J Bot. doi:10.1155/2012/985298
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
Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyper-accumulator, Alyssum bertolonii. New Phytol 156:205–215
Bordo D, Djinovic K, Bolognesi M (1994) Conserved patterns in the Cu-Zn superoxide dismutase family. J Mol Biol 238:366–386
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
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
Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116
Bowler C, Van Camp W, Van Montague M, Inze D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218
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
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
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
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
Chew YH, Halliday KJ (2011) A stress-free walk from Arabidopsis to crops. Curr Opin Biotechnol 22:281–286
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
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
Cudd A, Fridovich I (1982) Electrostatic interactions in the reaction mechanism of bovine erythrocyte superoxide dismutase. J Biol Chem 257:11443–11447
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
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
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
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9
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
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
Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350
Duarte B, Silva V, Caçador I (2012) Hexavalent chromium reduction, uptake and oxidative biomarkers in Halimione portulacoides. Ecotoxicol Environ Saf 83:1–7
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
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
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
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
FAO (Food, Agriculture Organization of the United Nations) (2004) FAO production year book. FAO, Rome
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
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
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
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
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
Fridovich I (1986) Superoxide dismutases. Adv Enzymol Mol Biol 58:61–97
Fridovich I (1989) Superoxide dismutase: an adaptation to a paramagnetic gas. J Biol Chem 264:7761–7764
Fu LM, Qu LJ (2013) Editorial. What and how, plants do encountering unfavorable stuff? Environ Exp Bot 86:1
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
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
Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
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
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
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
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol 103:1067–1073
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
Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, Oxford
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
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
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
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
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
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
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
Israr M, Sahi SV (2006) Antioxidative responses to mercury in the cell cultures of Sesbania drummondii. Plant Physiol Biochem 44:590–595
Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598
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
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
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
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
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
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
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
Kanematsu S, Okayasu M, Ueno S (2013) Atypical cytosol-localized Fe-superoxide dismutase in the moss Pogonatum inflexum. Bull Minamikyushu Univ 3A(23):31
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Mann T, Keilin D (1938) Haemocuprein and hepatocuprein, copper protein compounds of blood and liver in mammals. Proc R Soc London 126:303–315
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
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
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
McCord J, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprcin (hemocuprein). J Bioichem 244:6049–6055
McCord JM, Fridovich I (1988) Superoxide dismutase: the first 20 years (1968–1988). Free Radical Biol Med 5:363–369
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
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
McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848
Miller AF (2004) Superoxide dismutases: active sites that save, but a protein that kills. Curr Opin Chem Biol 8:162–168
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
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
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
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
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
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
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
Munné-Bosch S (2005) The role of a-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Ruzsa SM, Mylona P, Scandalios JG (1999) Differential responses of antioxidant genes in maize leaves exposed to ozone. Redox Rep 4:95–103
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
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
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
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
Sandalio LM, del Rio LA (1988) Intra-organellar distribution of superoxide dismutase in plant peroxisomes (glyoxysomes and leaf peroxisomes). Plant Physiol 88:1215–1218
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
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
Scandalios JG (1997) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, Plainview
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
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
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
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
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
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
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
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
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
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
Smith MW, Doolittle RF (1992) A comparison of evolutionary rates of the two major kinds of superoxide dismutases. J Mol Evol 34:175–184
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
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
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
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
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
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
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
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
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
Tuteja N, Gill SS (2013) Crop improvement under adverse conditions, 1st edn. Springer, New York
Tuteja N, Tiburcio AF, Fortes AM, Bartels D (2011) Plant abiotic stress. Introduction to PSB special issue. Plant Signal Behav 6:173–174
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
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
Ushimaru T, Kanematsu S, Katayama M, Tsuji H (2001) Antioxidative enzymes in seedlings of Nelumbo nucifera germinated under water. Physiol Plant 112:39–46
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
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
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
Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677
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
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
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
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
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
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
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
Yu Q, Rengel Z (1999) Drought and salinity differentially influence activities of superoxide dismutase in narrow-leafed lupins. Plant Sci 142:1–11
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
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
Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509
Zhu JK (2001) Plant salt tolerance. Trend Plant Sci 6:66–71
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
Corresponding authors
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4532-5