Skip to main content
SpringerLink
Log in

Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings

  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Manganese (Mn) is an essential element for plant growth but in excess, specially in acidic soils, it can become phytotoxic. In order to investigate whether oxidative stress is associated with the expression of Mn toxicity during early seedling establishment of rice plants, we examined the changes in the level of reactive oxygen species (ROS), oxidative stress induced an alteration in the level of non-enzymic antioxidants and activities of antioxidative enzymes in rice seedlings grown in sand cultures containing 3 and 6 mM MnCl2. Mn treatment inhibited growth of rice seedlings, the metal increasingly accumulated in roots and shoots and caused damage to membranes. Mn treated plants showed increased generation of superoxide anion (O2 .−), elevated levels of H2O2 and thiobarbituric acid reactive substances (TBARS) and decline in protein thiol. The level of nonprotein thiol, however, increased due to Mn treatment. A decline in contents of reduced ascorbate (AsA) and glutathione (GSH) as well as decline in ratios of their reduced to oxidize forms was observed in Mn-treated seedlings. The activities of antioxidative enzymes superoxide dismutase (SOD) and its isoforms Mn SOD, Cu/Zn SOD, Fe SOD as well as guaiacol peroxidase (GPX) increased in the seedlings due to Mn treatment however, catalase (CAT) activity increased in 10 days old seedlings but it declined by 20 days under Mn treatment. The enzymes of Halliwell-Asada cycle, ascorbate peroxidase (APX) monodehydoascorbate reductase (MDHAR), dehyroascorbate reductase (DHAR) and glutathione reductase (GR) increased significantly in Mn treated seedlings over controls. Results suggest that in rice seedlings excess Mn induces oxidative stress, imbalances the levels of antioxidants and the antioxidative enzymes SOD, GPX, APX and GR appear to play an important role in scavenging ROS and withstanding oxidative stress induced by Mn.

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

Access this article

Log in via an institution

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Mooren PD, Chapman SB (eds) Methods in plant ecology. Blackwell Scientific Publication, Oxford, pp 285–344

    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 

  • Bachman GR, Miller WB (1995) Iron chelate inducible iron/manganese toxicity in zonal geranium. J Plant Nutr 18:1917–1929

    Article  CAS  Google Scholar 

  • Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue. Plant Cell Tissue Organ Cult 39:7–12

    Article  Google Scholar 

  • Bandeog˘lu E, Eyidog˘an F, Yu¨cel M, O¨ ktem HA (2004) Antioxidant responses of shoots and roots of lentil to NaCl-salinity stress. Plant Growth Regul 42:69–77

    Article  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 

  • Boojar MMA, Goodarzi F (2008) The copper tolerance strategies and the role of antioxidative enzymes in three plant species grown on copper mine. Chemosphere 67:2138–2147

    Article  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 

  • Carver BF, Ownby JD (1995) Acid soil tolerance in wheat. Adv Agron 54:117–173

    Article  CAS  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 

  • de Kok LJ, Kuiper PJC (1986) Effect of short-term dark incubation with chloride and selenate on the glutathione content of spinach leaf discs. Physiol Plant 68:477–482

    Article  Google Scholar 

  • De Vos CHR, Vonk MJ, Vooijs RV, Schat H (1992) Glutathione depletion due to copper induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858

    Article  PubMed  Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Holzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266

    Article  CAS  Google Scholar 

  • Doulis A, Debian N, Kingston-Smith A, Foyer CH (1997) Characterization of chilling sensitivity in maize: differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037

    PubMed  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 

  • El-jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 24:353–386

    Article  Google Scholar 

  • Fecht-Christoffers MM, Maier P, Horst WJ (2003) Apoplastic peroxidase and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata. Physiol Plant 117:237–244

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188

    Article  CAS  Google Scholar 

  • Galli U, Schuepp H, Brunold C (1996) Thiols in cadmium and copper-treated maize (Zea mays L.). Planta 198:139–143

    Article  CAS  Google Scholar 

  • Gonnelli C, Galardi F, Gabbrielli R (2001) Nickel and copper tolerance and toxicity in three tuscan populations of Silene paradoxa. Physiol Plant 113:507–514

    Article  CAS  Google Scholar 

  • Gonzales A, Lynch J (1999) Subcellular tissue Mn compartmentation in bean leaves under Mn toxicity stress. Aust J Plant Physiol 26:811–822

    Article  Google Scholar 

  • Griffith OW (1980) Determination of glutathione disulphide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  PubMed  CAS  Google Scholar 

  • Hauck M, Paul A, Mulack C, Fritz E, Runge M (2002) Effects of manganese on the viability of vegetative diaspore of the epiphytic lichen Hypogymnia physodes. Environ Exp Bot 47:127–142

    Article  CAS  Google Scholar 

  • Hauck M, Paul A, Gross S, Raubuch M (2003) Manganese toxicity in epiphytic lichens: chlorophyll degradation and interaction with iron and phosphorus. Environ Exp Bot 49:181–191

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hernández JA, Escobar C, Creissen G, Mullineaux PM (2004) Role of hydrogen peroxide and the redox state of ascorbate in the induction of antioxidant enzymes in pea leaves under excess light stress. Funct Plant Biol 31:359–368

    Article  Google Scholar 

  • Horst WJ, Marschner H (1978) Symptome von Mangan-Überschuß bei Bohnen. Z Pflanzenernähr Bodenkd 141:129–142

    Article  CAS  Google Scholar 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Ikegawa H, Yamamoto Y, Matsumoto H (1998) Cell death caused by a combination of aluminum and iron in cultured tobacco cells. Physiol Plant 104:474–478

    Article  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 

  • Kim SY, Lim JH, Park MR, Kim YJ, Park TII, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J Biochem Mol Biol 38(2):218–224

    PubMed  CAS  Google Scholar 

  • Klapheck S, Fliegner W, Zimmer I (1994) Hydroxymethyl-phytochelatins [(gamma- glutamyl-cysteine)n,-Serine] are metal-induced peptides of the Poaceae. Plant Physiol 104:1325–1332

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Kobrehel K, Szalai G, Duviau MP, Bu′za′s Z, Galiba G (2004) Abiotic stress-induced changes in glutathione and thioredoxin levels in maize. Environ Exp Bot 52:101–112

    Article  CAS  Google Scholar 

  • Kuźniak E, Sklodowska M (1999) The effect of Botrytis cinerea infection on ascorbate glutathione cycle in tomato leaves. Plant Sci 148:69–76

    Article  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid and spinach (Spinacea oleracea) chloroplasts: the effect of hydrogen peroxide and paraquat. Biochem J 210:899–903

    PubMed  CAS  Google Scholar 

  • Le Bot J, Kirby EA, van Beusuchem ML (1990) Manganese toxicity in tomato plants: effects on cation uptake and distribution. J Plant Nutr 13:513–525

    Article  Google Scholar 

  • Lei Y, Yin C, Ren J, Li C (2007) Effect of osmotic stress and sodium nitroprusside pretreatment on proline metabolism of wheat seedlings. Biol Plant 51:386–390

    Article  CAS  Google Scholar 

  • Lidon FC, Teixeira MG (2000) Oxygen radical production and control in the chloroplast of Mn-treated rice. Plant Sci 152:7–15

    Article  CAS  Google Scholar 

  • Lucas RE, Davis JF (1961) Relationships between pH values of organic soils and availabilities of 12 plant nutrients. Soil Sci 92:177–182

    Article  CAS  Google Scholar 

  • Maheshwari R, Dubey RS (2009) Nickel induced oxidative stress and the role of antioxidant defense in rice seedlings. Plant Growth Regul 59:37–49

    Article  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 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nelson LE (1983) Tolerance of 20 rice cultivars to excess Al and Mn. Agron J 75:134–138

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Radotic K, Ducic T, Mutavdzic D (2000) Changes in peroxidase activity and isozymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44:105–113

    Article  PubMed  CAS  Google Scholar 

  • Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajnus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rauser WE (1999) Structure and function of metal chelators produced by plants. Cell Biochem Biophys 31:19–48

    Article  PubMed  CAS  Google Scholar 

  • Sandalio LM, Rodriguez-Serrano M, del Rio LA, Romero-Puetas MC (2009) Reactive oxygen species and signalling in cadmium toxicity. In: del Rio LA, Puppo A (eds) Reactive oxygen species and plant signaling. Springer, Berlin, pp 175–189

    Chapter  Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  PubMed  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

    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 

  • Shenker M, Plessner OE, Tel-Or E (2004) Manganese nutrition effects on tomato growth, chlorophyll concentration, and superoxide dismutase activity. J Plant Physiol 161:197–202

    Article  PubMed  CAS  Google Scholar 

  • Shi QH, Zhu Z (2008) Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environ Exp Bot 63:317–326

    Article  CAS  Google Scholar 

  • Shi QH, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Silicon mediated alleviation of Mn toxicity in Cucumis sativus L. in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  PubMed  CAS  Google Scholar 

  • Shi Q, Zhu Z, Xu M, Qian Q, Yu J (2006) Effect of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities. Environ Exp Bot 58:197–205

    Article  CAS  Google Scholar 

  • Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342

    Article  PubMed  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18(2):321–336

    Article  PubMed  CAS  Google Scholar 

  • Subrahmanyam D, Rathore VS (2000) Influence of manganase toxicity on photosynthesis in ricebean (Vigna umbellata) seedlings. Photosynthetica 38:449–453

    Article  CAS  Google Scholar 

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

    Article  CAS  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 

  • Wang YX, Wu YR, Wu P, Yan XL (2002) Molecular marker analysis of manganese toxicity tolerance in rice under greenhouse conditions. Plant Soil 238:227–233

    Article  CAS  Google Scholar 

  • Wang Y, Fang J, Leonard SS, Rao KMK (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443

    Article  PubMed  CAS  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 

  • Wu S (1994) Effect of manganese excess on the soybean plant cultivated under various growth conditions. J Plant Nutr 17:993–1003

    Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. IRRI, Philippines, p 83

    Google Scholar 

  • Zenk MH (1996) Heavy metal detoxification in higher plants: a review. Gene 179:21–30

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Faculty of Science, Banaras Hindu University, Varanasi, 221005, India

    Sarita Srivastava & R. S. Dubey

Authors
  1. Sarita Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. S. Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. S. Dubey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Srivastava, S., Dubey, R.S. 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 (2011). https://doi.org/10.1007/s10725-010-9526-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-010-9526-1

Keywords

Search

Navigation