Skip to main content
Log in

Differential responses of antioxidant enzymes to aluminum toxicity in two rice (Oryza sativa L.) cultivars with marked presence and elevated activity of Fe SOD and enhanced activities of Mn SOD and catalase in aluminum tolerant cultivar

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Seedlings of two Indica rice (Oryza sativa L.) cvs. HUR-105 and Vandana, differing in Al-tolerance were used to identify the key mechanisms involved in their differential behaviour towards Al toxicity. Cv. HUR-105 appeared to be Al sensitive by showing significant reduction (p ≤ 0.01) in root/shoot length, fresh weight, dry weight and water content in presence of 421 μM Al3+ in growth medium whereas cv. Vandana appeared to be fairly Al3+ tolerant. A conspicuous and significant reduction in dry weight of root and shoot was observed in Al sensitive cv. HUR-105 with 178 μM Al3+ treatment for 3 days. Al was readily taken up by the roots and transported to shoots in both the rice cultivars. Localization of absorbed Al was always greater in roots than in shoots. Our results of the production of reactive oxygen species (ROS) H2O2 and O2 .− and activities of major antioxidant enzymes such as total superoxide dismutase (SOD), Cu/Zn SOD, Mn SOD, Fe SOD, catalase (CAT) and guaiacol peroxidase revealed Al induced higher oxidative stress, greater production of ROS and lesser capacity to scavenge ROS in cv. HUR-105 than Vandana. With Al treatment, higher oxidative stress was noted in shoots than in roots. Greatly enhanced activities of SOD (especially Fe and Mn SOD) and CAT in Al treated seedlings of cv. Vandana suggest the role of these enzymes in Al tolerance. Furthermore, a marked presence of Fe SOD in roots and shoots of the seedlings of Al tolerant cv. Vandana and its significant (p ≤ 0.01) increase in activity due to Al-treatment, appears to be the unique feature of this cultivar and indicates a vital role of Fe SOD in Al-tolerance in rice.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Achary VMM, Jena S, Panda KK, Panda BB (2008) Aluminum induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Safety 70:300–310

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Barceló J, Poschenrieder CH (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Basu S, Roychoudhury A, Saha PP, Sengupta DN (2010) Differential antioxidative responses of Indica rice cultivars to drought stress. Plant Growth Regul 60:51–59

    Article  CAS  Google Scholar 

  • Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal Biochem 44:176–287

    Article  Google Scholar 

  • Beers RF, Sizer IW (1952) Colorimetric method for estimation of catalase. J Biol Chem 195:133–139

    PubMed  CAS  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum induced oxidative stress in maize. Phytochem 62:181–189

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminum on lipid peroxidation, superoxide dismutase catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Camejo D, Martí MC, Nicolás E, Alarcón JJ, Jiménez A, Sevilla F (2007) Response of superoxide dismutase isoenzymes in tomato plants (Lycopersicon esculentum) during thermo-acclimation of the photosynthetic apparatus. Physiol Plant 131:367–377

    Article  PubMed  CAS  Google Scholar 

  • Cançado GMA, Nogueira FTS, Camargo SR, Drummond RD, Jorge RA, Menossi M (2008) Gene expression profiling in maize roots under aluminum stress. Biol Plant 53:475–485

    Article  Google Scholar 

  • Cartes P, McManus M, Wulff-Zottele C, Leung S, Gutiérrez-Moraga A, Mora ML (2012) Differential superoxide dismutase expression in ryegrass cultivars in response to short term aluminium stress. Plant Soil 350:353–363

    Article  CAS  Google Scholar 

  • Castilhos G, Farias JG, Schneider AB, Oliveira PH, Nicoloso FT, Schetinger MR, Delatorre CA (2011) Aluminum-stress response in oat genotypes with monogenic tolerance. Environ Exp Bot 74:114–121

    Article  CAS  Google Scholar 

  • Chaney RL (1988) Plants can utilize iron form Fe-N, N’-di-(2-hydroybenzoyl)- ethylenediamine-N, N’-diacetic acid, a ferric chelate with 106 greater formation constant than Fe-EDDHA. J Plant Nutr 11:1033–1050

    Article  CAS  Google Scholar 

  • Ciamporová M (2002) Morphological and structural responses of plant roots to aluminium at organ, tissue, and cellular levels. Biol Plant 45:161–171

    Article  Google Scholar 

  • Dalton CC, Iqbal K, Turner DA (1983) Iron phosphate precipitation in Murashige and Skoog media. Physiol Plant 57:472–476

    Article  CAS  Google Scholar 

  • Darkó E, Ambrus H, Stefanovits-Bányai E, Fodor J, Bakos F, Barnabás B (2004) Aluminum toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 166:583–591

    Article  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Neill SJ, Hancock JT (2000) Hydrogen peroxide induced gene expression in Arabidopsis thaliana. Free Radical Biol Med 28:773–778

    Article  CAS  Google Scholar 

  • Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Du B, Nian H, Zhang Z, Yang C (2010) Effects of aluminum on superoxide dismutase and peroxidase activities and lipid peroxidation in the roots and calluses of soybeans differing in aluminum tolerance. Acta Physiol Plant 32:883–890

    Article  CAS  Google Scholar 

  • Dufey I, Hakizimana P, Draye X, Lutts S, Bertin P (2009) QTL mapping for biomass and physiological parameters linked to resistance mechanism to ferrous iron toxicity in rice. Euphytica 167:143–160

    Article  CAS  Google Scholar 

  • Egley GH, Paul RN, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. Planta 157:224–232

    Article  CAS  Google Scholar 

  • Exley C (2004) The pro-oxidant activity of aluminum. Free Radical Biol Med 36:380–387

    Article  CAS  Google Scholar 

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665

    Article  PubMed  CAS  Google Scholar 

  • Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Carreras A, Valderrama R, Begara-Morales JC, Hernández LE, Corpas FJ, Barroso JB (2011) Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions. Identification of two new genes of mitochondrial Mn-SOD. J Plant Physiol 168:1303–1308

    Article  PubMed  Google Scholar 

  • Foy CD (1984) Physiological effects of hydrogen, aluminum and manganese toxicities in acid soil. In: Adams F (ed) Soil acidity and liming. American Society of Agronomy, Inc., Madison, WI, pp 57–97

    Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396

    Article  PubMed  CAS  Google Scholar 

  • Giannakoula A, Moustakas M, Syros T, Yupsanis T (2010) Aluminum stress induces up-regulation of an efficient antioxidant system in the Al-tolerant maize line but not in the Al-sensitive line. Environ Exp Bot 67:487–494

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Gunsé B, Poschenrieder C, Barceló J (1997) Water transport properties of roots and root cortical cells in proton- and Al-stressed maize varieties. Plant Physiol 113:595–602

    PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197

    Article  PubMed  CAS  Google Scholar 

  • Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667

    Article  PubMed  CAS  Google Scholar 

  • Jana S, Choudhuri MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354

    Article  Google Scholar 

  • Kaminaka H, Morita S, Tokumoto M, Yokoyama H, Masumura T, Tanaka K (1999) Molecular cloning and characterization of a cDNA for an iron-superoxide dismutase in rice (Oryza sativa L.). Biosci Biotechnol Biochem 63:302–308

    Article  PubMed  CAS  Google Scholar 

  • Kampfenkel K, Van MM, Inzé D (1995) Effects of iron excess on Nicotiana plumbagnifolia plants. Plant Physiol 107:725–735

    PubMed  CAS  Google Scholar 

  • Kang DJ, Seo YJ, Futakuchi K, Vijarnsorn P, Ishii R (2011) Effect of aluminum toxicity on flowering time and grain yield on rice genotypes differing in Al-tolerance. J Crop Sci Biotech 14:305–309

    Article  Google Scholar 

  • Kinraide TB (1991) Identity of the rhizotoxic aluminum species. In: Wright RJ, Baligar VC, Murrmann RP (eds) Plant-soil interactions at low pH. Kluwer, Dordrecht, pp 717–728

    Chapter  Google Scholar 

  • Kochian LV, Hoekenga OA, Magalhaes JV, Pineros MA (2009) Maize Aluminum Tolerance. In: Wessler S, Bennetzen J (eds) Handbook of maize: its biology. Springer-Verlag, Berlin Heidelberg, pp 367–380

  • Kumar S, Mohan M, Datta R (2002) Passive diffusion sampling of sulfur dioxide in India: impact assessment on arid areas. Sci China Ser D 45:137–141

    Article  CAS  Google Scholar 

  • Lin CC, Kao CH (2001) Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant Soil 230:135–143

    Article  CAS  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • Ma B, Wan J, Shen Z (2007) H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. Plant Growth Regul 52:91–100

    Article  CAS  Google Scholar 

  • Makau M, Masito SS, Gweyi-Onyango JP (2011) A rapid hydroponic screening of field and horticultural crops for aluminium tolerance. Afr J Hort Sci 4:48–59

    Google Scholar 

  • Matsumoto H, Motoda H (2012) Aluminum toxicity recovery processes in root apices. Possible association with oxidative stress. Plant Sci 185(186):1–8

    Article  PubMed  Google Scholar 

  • Meriga B, Attitala IH, Ramgopal M, Ediga A, Kavikishor PB (2010) Differential tolerance to aluminum toxicity in rice cultivars: involvement of antioxidative enzymes and possible role of aluminum resistant locus. Acad J Plant Sci 3:53–63

    Google Scholar 

  • Milla MAR, Butler E, Huete AR, Wilson C, Anderson O, Gustafson JP (2002) Expressed sequence tag-based gene expression analysis under aluminum stress in rye. Plant Physiol 130:1706–1716

    Article  PubMed  CAS  Google Scholar 

  • Mishra S, Dubey RS (2006) Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol 163:927–936

    Article  PubMed  CAS  Google Scholar 

  • Mishra HP, Fridovich I (1972) The role of superoxide anion in auto-oxidation of the epinephrine and sample assay for SOD. J Biol Chem 247:3170–3175

    Google Scholar 

  • Mishra P, Bhoomika K, Dubey RS (2011) Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma. doi:10.1007/s00709-011-0365-3

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

    Article  PubMed  CAS  Google Scholar 

  • Nguyen VT, Burow MD, Nguyen HT, Le BT, Le TD, Paterson AH (2001) Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor Appl Genet 102:1002–1010

    Article  CAS  Google Scholar 

  • Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, ORYZA RUFIPOGON Griff., into Indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593

    PubMed  CAS  Google Scholar 

  • Panda SK, Matsumoto H (2010) Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. Biometals 23:753–762

    Article  PubMed  CAS  Google Scholar 

  • Pereira LM, Tabaldi LA, Gonçalves JF, Jucoski GO, Pauletto MM, Weis SN, Nicoloso FT, Borher D, Rocha JBT, Schetinger MRC (2006) Effect of aluminum on δ-aminolevulinic acid dehydratase (ALA-D) and the development of cucumber (Cucumis sativus). Environ Exp Bot 57:106–115

    Article  CAS  Google Scholar 

  • Pereira JF, Zhou G, Delhaize E, Richardson T, Zhou M, Ryan PR (2010) Engineering greater aluminum resistance in wheat by over-expressing TaALMT1. Ann Bot 106:205–214

    Article  PubMed  CAS  Google Scholar 

  • Römheld V, Marschner H (1981) Iron deficiency stress induced morphological and physiological changes in root tips of sunflower. Physiol Plant 53:354–360

    Article  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  PubMed  CAS  Google Scholar 

  • Samac DA, Tesfaye M (2003) Plant improvement for tolerance to aluminum in acid soils—a review. Plant Cell Tiss Org Cult 75:189–207

    Article  CAS  Google Scholar 

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Sharma P, Dubey RS (2008) Mechanism of aluminium toxicity and tolerance in higher plants. In: Hemantaranjan A (ed) Advances in plant physiology 10. Scientific Publishers (India), Jodhpur, pp 145–179

    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. doi:10.1155/2012/217037

  • Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet 109:1361–1368

    Article  PubMed  CAS  Google Scholar 

  • Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16

    Article  CAS  Google Scholar 

  • Tabaldi LA, Cargnelutti D, Gonçalves JF, Pereira LB, Castro G, Maldaner J, Rauber R, Rossato LV, Bisognin DA, Schetinger MRC, Nicoloso FT (2009) Oxidative stress is an early symptom triggered by aluminum in Al-sensitive potato plantlets. Chemosphere 76:1402–1409

    Article  PubMed  CAS  Google Scholar 

  • Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum L.) roots during aluminum induced growth inhibition. Physiol Plant 112:353–358

    Article  PubMed  CAS  Google Scholar 

  • Tahara K, Yamanoshita T, Norisada M, Hasegawa I, Kashima H, Sasaki S, Kojima K (2008) Aluminum distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminum resistance. Plant Soil 307:167–178

    Article  CAS  Google Scholar 

  • Tamás L, Huttová J, Mistrík I, Simonovicová M, Siroká B (2006) Aluminum induced drought and oxidative stress in barley roots. J Plant Physiol 163:781–784

    Article  PubMed  Google Scholar 

  • Tseng MJ, Liu C-W, Yiu J-C (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833

    Article  PubMed  CAS  Google Scholar 

  • Valle SR, Carrasco J, Pinochet D, Calderini DF (2009) Grain yield, above-ground and root biomass of Al-tolerant and Al-sensitive wheat cultivars under different soil aluminum concentrations at field conditions. Plant Soil 318:299–310

    Article  CAS  Google Scholar 

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

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Von Uexkull HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Wang FZ, Wang QB, Kwon 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

    Article  PubMed  CAS  Google Scholar 

  • Wang JP, Raman H, Zhang GP, Mendham N, Zhou MX (2006) Review: aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods. J Zhejiang Univ Sci B 10:769–787

    Article  Google Scholar 

  • Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147:1181–1191

    Article  PubMed  CAS  Google Scholar 

  • Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Ni J, He C (2000) QTLs and epistatis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100:1295–1303

    Article  CAS  Google Scholar 

  • Yamamoto Y, Rikiishi S, Chang YC, Ono K, Kasai M, Matsumoto H (1994) Quantitative estimation of aluminum toxicity in cultured tobacco cells: correlation between aluminium uptake and growth inhibition. Plant Cell Physiol 35:575–583

    CAS  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for plant physiological studies of rice, 3rd edn. International Rice Research Institute, Manila, pp 61–66

    Google Scholar 

  • Zhou G, Delhaize E, Zhou M, Ryan PR (2011) Biotechnological solutions for enhancing the aluminium resistance of crop plants. In: Shanker A, Venkateswarlu B, (eds) Abiotic stress in plants—mechanisms and adaptations. Intech-Open Access Publisher, pp 119–142

Download references

Acknowledgments

Financial support to carry out this work was provided by Department of Science and Technology, Government of India, New Delhi in the form of a Major Research Project (No. SP/SO/PS-29/05) to RSD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. S. Dubey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhoomika, K., Pyngrope, S. & Dubey, R.S. Differential responses of antioxidant enzymes to aluminum toxicity in two rice (Oryza sativa L.) cultivars with marked presence and elevated activity of Fe SOD and enhanced activities of Mn SOD and catalase in aluminum tolerant cultivar. Plant Growth Regul 71, 235–252 (2013). https://doi.org/10.1007/s10725-013-9824-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-013-9824-5

Keywords

Navigation