Antioxidant Systems in Plants and Responses to Salt Stress

Yıl 2019, Cilt: 1 Sayı: 2, 164 - 185, 15.12.2019

Ali Doğru

Öz

Salt stress is one of the abiotic
stresses that limit agricultural productivity. Salinity caused oxidative stress
in plants by accelerating production and accumulation rate of active oxygen
species such as superoxide radical, hydrogen peroxide, hydroxyl radical and
singlet oxygen. However, plants have evolved an efficient antioxidant
protective system by preventing the production or detoxifying active oxygen
species. Enzymatic and non-enzymatic components of this system are responsible
for protecting plants from oxidative damages. Plant species that can increase
their antioxidant activity have generally been accepted to be resistant to salt
stress. In this study, the components of antioxidant system and changes in
these components under salt stress have been discussed.     

Anahtar Kelimeler

Antioxidant System, Oxidative Stress, Salinity

Bitkilerde Antioksidan Sistemler ve Tuz Stresine Verdikleri Yanıtlar

Öz

Tuz stresi tarımsal verimliliği kısıtlayan abiyotik stres faktörlerinden
biridir. Tuz stresi bitkilerde süperoksit radikali, hidrojen peroksit,
hidroksil radikali ve tekil oksijen gibi aktif oksijen türlerinin oluşum ve
birikim hızlarını artırarak oksidatif strese neden olur. Ancak bitkilerde reaktif
oksijen türlerinin oluşumunu engelleyerek ya da oluşan reaktif oksijen
türlerini detoksifiye ederek koruma sağlayan etkili bir antioksidan sistem
gelişmiştir. Bu sistemin enzimatik ve enzimatik olmayan bileşenleri bitkileri
oksidatif hasarlarından korumaktan sorumludur. Tuz stresi altında antioksidan
aktivitesini artırabilen bitki türlerinin tuza dayanıklı olduğu kabul
edilmektedir. Bu derlemede antioksidan sistemin bileşenleri ve tuz stresi
altında bu bileşenlerde meydana gelen değişimler tartışılmıştır.   

Anahtar Kelimeler

Antioksidan Sistem, Oksidatif Stres, Tuzluluk.

Kaynakça

• Agarwal, S., Shaheen, R. (2007). Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Brazilian Journal of Plant Physiology, 19, 149-161.
• Agati, G., Azzarello, S., Poolastri, M., and Tattini, M. (2012). Flavonoids as antioxidants in plants: location and functional significance. Plant Science and International Journal of Experimental Plant Biology, 196, 67-76.
• Ahmad, P. Hakeem, K. R., Kumar, A., Ashraf, M., Akram, N. A. (2012). Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). African Journal of Biotechnology, 11(11), 2694-2703.
• Ahmad, P., Jaleel, C. A., Sharma, S. (2010). Antioxidative defence system, lipid peroxidation, proline metabolizing enzymes and biocehmical activityon two genotypes of Morus alba L. subjected to NaCl stress. Russian Journal of Plant Physiology, 57(4), 509-517.
• Alscher, R. G. Donahue, J. L., Cramer, C. L. (1997). Reactive oxygen species and antioxidants: relationship in green cells. Physiologia Plantarum, 100: 224-233.
• Alscher, R. G., Ertürk, N., and Heath, L. S. (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany, 53(372), 1331-1341.
• Aono, M. Kubo, A., Saji, H., Tanaka, K., Kondo, N. (1993). Enhanced tolerance to photooxidative stres of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell and Physiology, 34, 129-135.
• Apel, K. Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stres, and signal transduction. Annual Review of Plant Biology, 55: 373-399.
• Asada, K. (1994). Production and action of active oxygen species in photosynthetic tissue. Boca Raton: CRC Press.
• Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 601-639.
• Asada, K., Urano, M., Takahashi, M. (1973). Subcellular location of superoxide dismutase in spinach leaves and preparation and properties of crystalline spinach superoxide dismutase. European Journal of Biochemistry, 36, 257-266.
• Athar, H. R. Khan, A. Ashraf, M. (2008). Exogenously applied ascorbic acid alleviates salt-induced oxidative stres in wheat. Environmental and Experimental Botany, 63, 224-231.
• Azevedo, R. A. Alas, R. M., Smith, R. J., Lea, P. A. (1998). Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in leaves and roots of wild-type and catalase-deficient mutant of barley. Physiologia Plantarum, 104, 280-292.
• Azpilicueta, C. E. Benavides, M. P., Tomaro, M. L., Gallego, S. M. (2007). Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiology and Biochemistry, 45, 589-595.
• Baldensperger, J. B. (1978). An iron containing superoxide dismutase from the chmeo lithotrophic Thiobacillus denitrificans rt strain. Archives of Microbiology, 119, 237-444.
• Bannister, J. V., Parker, M. W. (1985). The presence of a copper/zinc superoxide dismutase in the bacterium Photobacterium leiognathi: a likely case of gene transfer from eukaryoted to prokaryotes. Proceedings of the National Academy of Sciences, USA, 82, 149-152.
• Bannister, W. H., Bannister, J. V., Barra, D., Bond, J., Bossa, F. (1991). Evolutionary aspects of superoxide dismutase: the copper/zinc enzyme. Free Radical Research Communications, 12-13, 349-361.
• Barro, D., Schinina, M. E., Bossa, F., Puget, K., Durosay, P. (1990). A tetrameric iron superoxide dismutase from the eukaryote Tetrahymena pyridornis. Journal of Biological Chemistry, 265, 17680-17686.
• Bordo, D., Djinovich, K., Bolognesi, M. (1994). Conserved patterns in the Cu, Zn superoxide dismutase family. Journal of Molecular Biology, 238, 366-386.
• Bowler, C., Van Camp, W., Van Montagu, M., Inze, D. (1994). Superoxide dismutases in plants. Critical Reviews in Plant Science, 13, 199-218.
• Briviba, L. O. Klotz, H. (1997). Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological system. Journal of Biological Chemistry, 378, 1259-1265.
• Çakırlar, H. Çiçek, N., Fedina, I., Georgieva K., Doğru A., Velitchkova, M. (2008). NaCl induced cross-acclimation to UV-B radiation in four barley (Hordeum vulgare L.) cultivars. Acta Physiologia Plantarum, 30, 561-567.
• Chalapathi Rao, A. S. V. Reddy, A. R. (2008). Glutathione reductase: a putative redox regulatory system in plant cells. The Netherlands: Springer.
• Chutipaijit, S. Cha-um, S., Sompornpailin, K. (2011). High contents of proline and anthocyanin increase protective response to salinity in Oryza sativa L. spp. indica. Australian Journal of Crop Science, 5, 1191-1198.
• Collins, A. (2001). Carotenoids and genomic stability. Mutation Research, 475, 1-28.
• Comba, M. E. Benavides, M. P., Tomaro, M. L. (1998). Effect of salt stress on antioxidant defence system in soybean root nodules. Australian Journal of Plant Physiology, 25, 665–671.
• Creissen, G. Firmin, J., Fryer, M., Kular, B., Leyland, N., Reynolds, H., Pastori, G., Wellburn, F., Baker, N., Wellburn, A., Mullineaux, P. (1999). Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. The Plant Cell, 11, 1277-1291.
• Creissen, G. P. Broadbent, P., Kular, B., Reynolds, H., Wellburn, A. R., Mullineaux, P. M. (1994). Manipulation of glutathione reductase in transgenic plants: implications for plant responses to environmental stress. Proceeding Royal Society Edinburg, 102B, 167-175.
• Crowell, D. N., Amasino, R. M. (1991). Induction of the spesific mRNAs in cultured soybean cells during cytokinin or auxin starvation. Plant Physiology, 95, 711-715.
• Czarnocka, W., Karpinski, S. (2018). Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stress. Free Radical Biology and Medicine, 122, 4-20.
• Del Rio, L. A. Corpas, F. J., Sandalio, L. M., Palma, J. M., Gomez, M. Barroso, J. B. (2002). Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany, 53, 1255-1272.
• delRio, L. A., Sandalio, L. M., Palma, J. M., Bueno, P., Corpas, F. J. (1992). Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radical in Biology and Medicine, 13, 557-580.
• Doğru, A. (2006). Kolza (Brassica napus L. ssp. oleifera)’nın bazı kışlık çeşitlerinde düşük sıcaklık toleransı ile ilgili fizyolojik ve biyokimyasal parametrelerin araştırılması. Doktora Tezi, Hacettepe Üniversitesi, Fen Bilimleri Enstitüsü, Ankara.
• Doğru, A., (2014, Haziran). Farklı mısır genotiplerinde tuz stresinin antioksidan sistem üzerindeki etkileri. 22. Ulusal Biyoloji Kongresi (s. 430). Eskişehir: Osman Gazi Ünversitesi.
• Doğru, A., Yılmaz Kaçar, M. (2019). A Preliminary study on salt tolerance of some barley genotypes. SAU Journal of Science, 23(5), 755-762.
• Droillard, M. J., Paulin, A. (1990). Isozymes of superoxide dismutase in mitochondria and peroxisomes isolatd from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiology, 94, 1187-1192.
• Edrewa, A. (2005). Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agriculture, Ecosystem and Environment, 106, 119-133.
• Elstner, E. F. (1991). Mechanisms of oxygen activation in different comportments of plant cells. Rockville MD, American Society of Plant Physiologists.
• Eltayeb, A. E. Kawano, N., Badawi, G. H., Kaminaka, H., Sanekata, T., Shibahara, T., Inanaga, S., Tanaka, K. (2007). Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta, 225, 1255-1264.
• Eyidoğan, F., Öz, M. T. (2005). Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiologiae Plantarum, 29, 485-493.
• Farouk, S. (2011). Ascorbic acid and -tocopherol minimize salt-induced wheat leaf senescence. Journal of Stress Physiology and Biochemistry, 7, 58–79.
• Foster, J. G., Edwards, G. E. (1980). Localization of superoxide dismutase in leaves from C3 and C4 plants. Plant Cell and Physiology, 21, 895-906.
• Foyer, C. H. Noctor, G. (2005). Redox homeostis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17, 1866-1875.
• Foyer, C. H. Souriau, N., Perret, S., Lelandais, M., Kunert, K. J., Pruvost, C., Jouanin, L. (1995). Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiology, 109, 1047-1057.
• Fridovich, I. (1986). Superoxide dismutases. Advances in Enzymology and Related Areas of Molecular Biology, 58, 61-97.
• Frugoli, J. A. Zhong, H. H., Nuccio, M. L., McCourt, P., McPeek, M. A., Thomas, T. L., McClung, C. R. (1996). Catalase is encoded by a multigene family in Arabidopsis thaliana (L.). Plant Physiology, 112, 327-336.
• Gapinska, M., Skladowska, M., Gabara, B. (2008). Effect of shlor- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiologiae Plantarum, 30, 11-18.
• Garg, G., Manchanda, R. (2009). ROS generation in plants: boon or bane. Plant Biosystem, 143, 8-96.
• Gill, S. S., Anjum, N. A., Gill, R., Yadav, S., Hasanuzzaman, M., Fujita, M., Mishra, P., Sabat, S. C., and Tuteja, N. (2015). Superoxide dismutase-mentor of abiotic stress tolerance in crop plants. Environmental Science and Pollution Research International, 22, 10375-10394.
• Gossett, D. R. Banks, S. W., Millhollon, E. P., Lucas, M. C. (1996). Antioxidant response to NaCl stress in a control and a NaCl-tolerant cotton cell line grown in the presence of paraquat, buthionine sulfoximine and exogenous glutathione. Plant Physiology, 112, 803-809.
• Gossett, D. R. Millhollon, E. P., Lucas, M. C. (1994). Antioxidant response to NaCl stress in salt tolerant and salt sensitive cultivars of cotton. Crop Science, 34, 706-714.
• Gueta-Dahan, Y. Yaniv, Z., Zilinskas, B. A., Ben-Hayyim, G. (1997). Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta, 203, 460-469.
• Harinasut, P., Poonsopa, D., Roengmongkol, K., Charoensataporn, R. (2003). Salinity effects on antioxidant enzymes in mulberry cultivars. Science Asia, 29, 109-113.
• Hasanuzzaman, M. Fujita, M. (2011). Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biological Trace Element Research, 143, 1758-1776.
• He, L. Ban, Y., Inoue, H., Matsuda, N., Liu, J., Moriguch, T. (2008). Enhancement of spermidine content and antioxidant capacity in transgenic pear shoots overexpressing apple spermidine synthase in response to salinity and hyperosmosis. Phytochemistry, 69, 2133-2141.
• Hefni, M. Abdel Kader, D. Z. (2006). Antioxidant-enzymatic system as selection criteria for salt tolerance in forage sorghum genotypes (Sorghum bicolor L. Moench). Netherlands: Springer.
• Hernandez, J. A. Campillo, A., Jimenez, A., Alacon, J. J., Sevilla, F. (1999). Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytologist, 141, 241-251.
• Hernandez, J. Jimenez, A., Mullineaux, P., Sevilla, F. (2000). Tolerance of pea plants (Pisum sativum) to long term salt stress is associated with induction of antioxidant defences. Plant Cell and Environment, 23, 853-862.
• Hollander-Czytko, H. Grabowski, J., Sandorf, I., Weckermann, K., Weiler, E. W. (2005). Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. Journal of Plant Physiology, 162, 767-770.
• Hussain, T. M. Chandrasekhar, T., Hazara, M., Sultan, Z., Saleh, B.Z., Gopal, G.R. (2008). Recent advances in salt stress biology – a review. Biotechnology and Molecular Biology Review, 3, 8-30.
• Jackson, C., Dench, J., Moore, A. L., Halliwell, B., Foyer, C. H., Hall, D. O. (1978). Subcellular localization and identification of superoxide dismutase in the leaves of higher plants. European journal of Biochemistry, 91, 339-344.
• Jimenez, J. A. Hernandez, G., Pastori, L. A., del Rio, F. (1998). Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiology, 118, 1327-1335.
• Kamal-Eldin, A. Appelqvist, L. A. (1996). The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids, 31, 671-701.
• Kanematsu, S., asada, K. (1978). Superoxide dismutase from an anaerobic photosynthetic bacterium, Chromatium vinosum. Archives of Biochemistry and Biophysics, 185, 473-482.
• Kanematsu, S., Asada, K. (1990). Characteristic amino acid sequences of chloroplast and cytosol izozymes of CuZn-superoxide dismutase in spinach, rice and horsetail. Plant and Cell Physiology, 31, 99-112.
• Kennedy, B. F. De Fillippis, L. F. (1999). Physiological and oxidative response to NaCl of the salt tolerant Grevillea ilicifolia and the salt sensitive Grevillea arenaria. Journal of Plant Physiology, 155, 746-754.
• Khan, N. A., Singh, S. (2008). Abiotic Stress and Plant Responses. New Delhi: IK International.
• Khavarinejad, R. A. Mostofi, Y. (1998). Effects of NaCl on photosynthetic pigments, saccharides, and chloroplast ultrastructure in leaves of tomato cultivars. Photosynthetica, 35, 151-154.
• Khavarinejad, R. A., Chaparzadeh, N. (1998). The effects of NaCl and CaCl2 on photosynthesis and growth of alfalfa plants. Photosynthetica, 35(3), 461-466.
• Kirby, T. W., Lancester Jr. J. R., Fridovich, I. (1981). Isolation and characterization of the iron-containing superoxide dismutase of Methanobacterium bryantii. Archieves of Biochemistry and Biophysics, 210, 140-148.
• Kliebenstein, D. J., Monde, R., Last, R. L. (1998). Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology, 118, 637-650.
• Koji, Y. Shiro, M., Michio, K., Mitsutaka, T. Hiroshi, M. (2009). Antioxidant capacity and damages caused by salinity stress in apical and basal regions of rice leaf. Plant Production Science, 12, 319-326.
• Kukreja, S., Nandval, A. S., Kumar, N., Sharma, S. K., Unvi, V., Sharma, P. K. (2005). Plant water status, H2O2 scavenging enzymes, ethylene evolution, and membrane integrity of Cicer arietinum roots as affected by salinity. Biologia Plantarum, 49, 305-308.
• Kusunose, E., Ichihara, K., Noda, Y., Kusunose, M. (1976). Superoxide dismutase from Mycobacterium tuberculosus. Journal of Biochemistry (Tokyo), 80, 1343-1352.
• Larson, R. A. (1988). The antioxidants of higher plants. Phytochemistry, 27, 969-978.
• Lechno, S. Zamzki, E., Tel-Or, E. (1997). Salt stress induced responses in cucumber plants. Journal of Plant Physiology, 150, 206-211.
• Maeda, H. Sakuragi, Y., Bryant, D. A., DellaPenna, D. (2005). Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiology, 138, 1422-1435.
• Martin, Jr. J. P., Fridovich, I. (1981). Evidence for a natural gene transfer from the ponyfish to its bioluminescent bacterial symbiont Photobacter leiognathi. The close relationship between bacteriocuprein and the copper-zinc superoxide dismutase of teleos fishes. Journal of Biological Chemistry, 256, 6080-6089.
• Meyer, A. J. (2008). The integration of glutathione homeostasis and redox signaling. Plant Physiology, 165 1390-1403.
• Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405-410.
• Mittler, R. Zilinskas, B. A. (1992). Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. Journal of Biological Chemistry, 267, 21802-21807.
• 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. Journal of Experimental Botany, 55, 1105-1113.
• 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 Research, 36, 195–202.
• Mullineaux, P. M. Rausch, T. (2005). Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthetic Research, 86, 459-474.
• Munne-Bosch, S. (2005). The role of -tocopherol in plant stress tolerance. Journal of Plant Physiology, 162, 743-748.
• Niyogi, K. K. Shih, C., Chow, W. S., Pogson, B. J., DellaPenna, D., Bjorkman, O. (2001). Photoprotection in a zeaxanthin-and lutein-deficient double mutant of Arabidopsis. Photosynthetic Research, 67, 139-145.
• Noctor, G. Gomez, L., Vanacker, H., Foyer, C. H. (2002). Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. Journal of Experimental Botany, 53, 1283-1304.
• Noctor, G., Foyer, C. H. (1998). A re-evaluation of the ATP:NADPH budget during C3 photosynthesis. A contribution from nitrate assimilation and its associated respiratory activity. Journal of Experimental Botany, 49, 1895-1908.
• Ogawa, K., Kanematsu, S., Asada, K. (1997). Generation of superoxide anion and localization of CuZn superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell and Physiology, 38, 1118-1126.
• Okada, S., Kanematsu, S., Asada, K. (1979). Intracellular distribution of manganese and ferric superoxide dismutase in blue-green algae. FEBS Letters, 103, 106-110.
• Pan, Y., Wu, L. J., Yu, Z. L. (2006). Effect of salt and drought stress on antioxidant enzyme activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fish). Plant Growth Regulation, 49, 157-165.
• Panda, S. K. (2001). Response of green gram seeds under salinity stress. Indian Journal of Plant Physiology., 6, 438-440.
• Panda, S. K. Upadhyay, R. K. (2004). Salt stress injury induces oxidative alterations and antioxidative defence in the roots of Lemna minor. Biologia Plantarum, 48, 249-253.
• Parida, A. Das, A. B., Das, P. (2002). NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. Journal of Plant Biology, 45, 28-36.
• Parida, A. K. Das, A. B. (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety, 60, 324-349.
• Parida, A.K. Das, A.B., Mohant, P. (2004). Investigations on the antioxidative defense responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regulation, 42, 213-226.
• Polidoros, N. A. Scandalios, J. G. (1999). Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione-S-transferase gene expression in maize (Zea mays L.). Plant Physiology, 106, 112-120.
• Puget, K., Michelson, A. M. (1974). Iron containing superoxide dismutases from luminous bacteria. Biochimie, 56, 1255-1267.
• Rausch, T. Wachter, A. (2005). Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science, 10, 503-509.
• Reddy, A. R. Raghavendra, A. S. (2006). Photooxidative stress. The Netherlands: Springer.
• Reddy, C. D., Venkaiah, B. (1982). Studies on izoenzymes of superoxide dismutase from mung bean (Vigna radiata) seedlings. Journal of Plant Physiology, 116, 279-284.
• Romero-Puertas, M. C. Corpas, F.J., Sandalio, L. M., Leterrier, M., Rodriguez Serrano, M., del Rio, L. A.J., Palma, M. (2006). Glutathione reductase from pea leaves:response to abiotic stress and characterization of the peroxisomal isozyme. New Phytologist, 170, 43-52.
• Saha, P. Chatterjee, P., Biswas, A. K. (2010). NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L. Wilczek). Indian Journal of Experimental Biology, 48, 593-600.
• Salin, M. L. (1988). Toxic oxygen species and protective system of the chloroplast. Physiologia Plantarum, 72, 681-689.
• Salin, M. L., Bridges, S. M. (1980). Localization of superoxide in chloroplasts from Brassica campestris. Zeitschrift für Pflanzenphysiologie, 99, 37-47.
• Salin, M. L., Bridges, S. M. (1981). Absence of the iron-containing superoxide dismutase in mitochondria from mustard (Brassica campestris). Biochemical Journal, 195, 229-223.
• Sandalio, L. M., delRio, L. A. (1987). Localization of superoxide dismutase in glyoxysomes from Citrullus vulgaris: functional implications in cellular metabolism. Journal of Plant Physiology, 127, 395-409.
• Scandalios, J. G. (1990). Response of plant antioxidant defense genes to environmental stress. Advances in Genetic, 28, 1-41.
• Searcy, K. B., Searcy, D. G. (1981). Superoxide dismutase from the Archeobacterium Thermoplasma acidophylum. Biochimica et Biophysica Acta, 670, 39-46.
• Sheokand, S. Bhankar, V., Sawhney, V. (2010). Ameliorative effect of exogenous nitric oxide on oxidative metabolism in NaCl treated chickpea plants. Brazilian Journal of Plant Physiology, 22, 81-90.
• Sieferman-Harms, D. (1987). The light harvesting function of carotenoids in photosynthetic membrane. Plant Physiology, 69, 561-568.
• Singh, S., Anjum, N. A., Khan, N. A., Nazar, R. (2008). Abiotic Stress and Plant Responses. New Delhi: IK International.
• Smirnoff, N. (2000). Ascorbic acid: metabolism and functions of a multifacetted molecule. Current Opinion in Plant Biology, 3, 229-235.
• Smith, M. W., Doolittle, R. F. (1992). A comparison of evolutionary rates of the two major kinds of superoxide dismutases. Journal of Molecular Evolution, 34, 175-184.
• Srivastava, A. K., Bhargava, P., Rai, L. C. (2005). Salinity and copper-induced oxidative damage and changes in antioxidative defence system of Anabaena doliolum. World Journal of Microbial Biology, 22, 1291-1298.
• Sudhakar, C. Lakshmi, A., Giridarakumar, S. (2001). Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba) under NaCl salinity Plant Science, 161, 613-619.
• Szarka, A. Horemans, N., Kovacs, Z., Grof, P., Mayer, M., Banhegyi, G. (2007). Dehydroascorbate reduction in plant mitochondria is coupled to the respiratory electron transfer chain. Plant Physiology, 129, 225-232.
• Takahashi, M. A., Asada, K. (1983). Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Archieves of Biochemistry and Biophysics, 226, 558-566.
• Tausz, M. Ircelj, H., Grill, D. (2004). The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid. Journal of Experimental Botany, 55, 1955-1962.
• Trebst, A. Depka, B., Holländer-Czytko, H. (2002). A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Letter, 516, 156-160.
• Ushimaru, T. Nakagawa, T., Fujioka, Y., Daicho, K., Naito, M., Yamauchi, Y., Nonaka, H., Amako, K., Yamawaki, K., Murata, N. (2006). Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. Journal of Plant Physiology, 163, 1179-1184.
• Van Camp, W., Bowler, C., Villarroel, R., Tsanh E. W., van Montagu, M, Inze, D. (1990). Characterization of iron superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli. Proceedings of the National Academy of Sciences, USA, 87, 9903-9907.
• Wang, Y., Wisniewski, M., Meilan, R., Uratsu, S. L., Cui, M. G., Dandekar, A., Fuchigami, L. (2007). Ectopic expression of Mn-SODin Lycopersicon esculentum leads to enhanced tolerance to salt and oxidative stress. Journal of Applied Horticulture, 9, 3-8.
• Wang, Y., Ying, Y., Chen, J., Wang, X. C. (2004). Transgenik Arabidopsis overexpressing Mn-SOD enhanced salt tolerance. Plant Science, 167, 671-677.
• Wu, G. Wei, Z. K., Shao, H. B. (2007). The mutual responses of higher plants to environment: physiological and microbiological aspects. Biointerfaces, 59, 113-119.
• Xiang, C. Werner, V., Christensen, E. M., Oliver, D. J. (2001). The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiology, 126, 564-574.
• Yost, Jr. F. J., Fridovich, I. (1973). An iron-containing superoxide dismutase from Escherichia coli . Journal of Biological Chemistry, 248, 4905-4908.
• Zhu, D., Scandalios, J. G. (1993). Maize mitochondrial manganese superoxide dismutases are encoded by a differentially expressed multigene family. Proceedings of the National Academy of Sciences, USA, 90, 9310-9314.