Skip to main content
SpringerLink
Log in

The role of active oxygen in iron tolerance of rice (Oryza sauva L.)

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Iron tolerance of rice (Oryza sativa L.) was investigated using an oxygen depleted hydroculture system. Treatment with high concentrations of Fe2+ induced yellowing and bronzing symptoms as well as iron coatings at the root surface. Root and shoot growth were inhibited by increasing iron concentration in the medium. All symptoms were more pronounced in an iron sensitive cultivar (IR 64) compared to an iron tolerant one (IR 9764-45-2). Superoxide dismutase and peroxidase activity of root extracts of IR 97 were about twice that of IR 64 in untreated control plants. No significant increase of peroxidase activity was detected with increasing iron concentration in the medium. Catalase activity of IR 64 was slightly higher than that of IR 97, independent of iron concentration.

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

Similar content being viewed by others

Abbreviations

SOD:

Superoxide dismutase (EC 1.15.1.1)

POD:

peroxidase (EC 1.11.1.7)

EDTA:

ethylenediamintetraacetic acid

fwt:

fresh weight

Hepes:

(N-[2-hydroxyethyl]piperazine-N′-[2-ethanesulfonic acid])

BSA:

bovine serum albumin

IR 97 IR 9764-45-2:

an iron tolerant rice cultivar

IR 64:

iron sensitive rice cultivar

PM:

plasma membrane

References

  • Ando T (1983) Nature and oxidizing power of rice roots. Plant Soil 72: 57–71

    Google Scholar 

  • Armstrong W (1967) The oxidizing activity of roots in waterlogged soil. Physiol Plant 20: 920–926

    Google Scholar 

  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 90: 109–116

    Google Scholar 

  • Benckiser G, Santiago S, Neue HU, Watanabe J, Ottow JCG (1984) Effect of fertilization on exsudation, dehydrogenase activity, iron reducing populations on Fe2+ formation in the rhizosphere of rice (Oryza sativa) in relation to iron toxicity. Plant Soil 79: 305–316

    Google Scholar 

  • Bergmeyer HU (1970) Methoden zur enzymatischen Analyse. Verlag Chemie, Weinheim

    Google Scholar 

  • Bienfait HF (1985) Regulated redox processes at the plasmalemma of plant root cells and their function in iron uptake. J Bioenerg Biomembr 17: 73–83

    Google Scholar 

  • —, van der Mark F (1983) Phytoferritin and its role in iron metabolism. In: Robb DA, Pierpoint WS (eds) Metals and micronutrients: uptake and utilization by plants. Academic Press, New York, 111–123

    Google Scholar 

  • —, Briel W van den, Mesland-Mul NT (1985) Free space iron pools in roots. Plant Physiol 78: 596–600

    Google Scholar 

  • Braber JM (1980) Catalase and peroxidase in primary bean leaves during development and senescence. Z Pflanzenphysiol 97: 135–144

    Google Scholar 

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

    Google Scholar 

  • van Bremen N, Quijano CC (1977) Factors involved in iron toxicity in the mid-country wetzone of Sri Lanka. IRRI Annu Rep 1977: 70–90

    Google Scholar 

  • Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58: 79–110

    Google Scholar 

  • Cakmak I (1988) Morphologische und physiologische Veränderungen bei Zink-Mangelpflanzen. PhD thesis, University of Hohenheim, Stuttgart, Federal Republic of Germany

    Google Scholar 

  • Cayton MTC, Reyes ED, Neue HU (1985) Effect of zinc fertilization on the mineral nutrition if rices differing in tolerance to zinc deficiency. Plant Soil 87: 319–327

    Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2: 764–775

    Google Scholar 

  • Chen CC, Dixon JB (1980) Iron coatings on rice roots: mineralogy and quantity influencing factors. Soil Sci Soc Am J 44: 635–639

    Google Scholar 

  • Chevrier N, Sarkan F, Chung YS (1988) Oxidative damages and repair inEuglena gracilis exposed to ozone. I. SH groups and lipids. Plant Cell Physiol 29: 321–327

    Google Scholar 

  • Corpas JF, Gomez M, Hemandez JA, del Rio LA (1993) Metabolism of activated oxygen in peroxisomes from twoPisum sativum L. cultivars with different sensitivity to sodium chloride. J Plant Physiol 141: 160–165

    Google Scholar 

  • Dicker E, Cederbaum AI (1991) NADH-dependent generation of reactive oxygen species by microsomes in the presence of iron and redox cycling agents. Biochem Pharmacol 42: 529–535

    Google Scholar 

  • Doke N (1983) Generation of Superoxide anion by potato tuber protoplasts during hypersensitive response to hyphal wall components ofPhytophthora infestons and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol Plant Pathol 23: 359–367

    Google Scholar 

  • Elstner EF (1982) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33: 73–96

    Google Scholar 

  • —, Heupel A (1976) Formation of hydrogen peroxide by isolated cell walls from horseradish. Planta 130: 175–180

    Google Scholar 

  • Fagaria NK, Wright RJ, Baligar VC (1988) Rice cultivar evaluation for phosphorus use efficiency. Agron J 80: 741–749

    Google Scholar 

  • Foster JG, Hess JL (1980) Response of SOD and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched with oxygen. Plant Physiol 66: 482–87

    Google Scholar 

  • Foy CD, Changey RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29: 511–566

    Google Scholar 

  • Freisleben HJ, Packer L (1993) Free-radical scavenging activities, interactions and recycling of antioxidants. Biochem Soc Trans 21: 325–330

    Google Scholar 

  • Fridovich I (1986) Biological effects of the Superoxide radical. Arch Biochem Biophys 247: 1–11

    Google Scholar 

  • Hendry GAF, Brocklebank KJ (1985) Iron induced oxygen radical metabolism in waterlogged plants. New Phytol 101: 199–206

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59: 309–314

    Google Scholar 

  • Green MS, Etherington JR (1977) Oxidation of ferrous by rice (Oryza sativa) roots: mechanism for waterlogged tolerance? J Exp Bot 28: 211–245

    Google Scholar 

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

    Google Scholar 

  • Hager A, Meyer-Bertenrath T (1966) Die Isolierung und quantitative Bestimmung der Carotinoide und Chlorophylle von Blättern, Algen und isolierten Chloroplasten mit Hilfe dünnschichtchro-matographischer Methoden. Planta 69: 198–217

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219: 1–14

    Google Scholar 

  • — — (1989) Free radicals in biology and medicine, 2nd edn. Clarendon Press, Oxford

    Google Scholar 

  • Harper DB, Harvey MR (1978) Mechanism of paraquat tolerance in perennial ryegrass. Plant Cell Environ 1: 211–215

    Google Scholar 

  • Ito H, Nobutsuga H, Ohbayashi A, Ohashi Y (1991) Purification and characterization of rice peroxidases. Agric Biol Chem 55: 2445–2454

    Google Scholar 

  • Lantin RS, Neue HU (1988) Iron toxicity: a nutritional disorder in wetland rice. In: 17th Irrigated Rice Meeting Abstracts, Brazil, September 1988, pp 1–16

  • Larson RA (1988) The antioxidants of higher plants. Phytochemistry 27: 969–978

    Google Scholar 

  • Longnecker N (1988) Iron nutrition of plants. Res Rev Plants Animals 1: 143–150

    Google Scholar 

  • McKersie BD, Chen Y, de Beus M, Bowley SR, Bowler C, Inze D, D'Halluin K, Botterman J (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicagosativa L.). Plant Physiol 103: 1155–1163

    Google Scholar 

  • van der Mark F, de Lange T, Bienfait F (1981) The role of ferritin in developing primary bean leaves under various light conditions. Planta 153: 338–342

    Google Scholar 

  • Marschner H (1988) Mechanism of manganese acquisition by roots from soils. In: Graham RD, Uren NC (eds) Manganese in soils and plants. Kluwer, Dordrecht, pp 191–204

    Google Scholar 

  • —, Cakmak I (1989) High light intensity enhance chlorosis and necrosis in leaves of Zn, K and Mg-deficient bean (Phaseolus vulgaris) plants. J Plant Physiol 134: 308–315

    Google Scholar 

  • Matsunaka S (1960) Studies on the respiratory enzyme system of plants I. Enzymatic oxidation of a-naphthylamine in rice plant root. J Biochem 47: 820–829

    Google Scholar 

  • Matters GL, Scandalios JG (1986) Effect of the free radical-generaling herbicide paraquat on the expression of the Superoxide dismutase genes in maize. Biochim Biophys Acta 822: 29–38

    Google Scholar 

  • Monk LS, Faggerstedt KV, Crawford RMM (1989) Oxygen toxicity and Superoxide dismutase as an antioxidant in physiological stress. Physiol Plant 76: 456–459

    Google Scholar 

  • Monteiro HP, Winterbourn CC (1988) The superoxide-dependent transfer of iron from ferritin to transferrin. Biochem J 256: 923–928

    Google Scholar 

  • Nagano T, Hirano T, Hirobe M (1989) SOD mimics based on iron in vivo. J Biol Chem 264: 9243–9249

    Google Scholar 

  • Ottow JCG, Benckiser G, Santiago S, Watanabe I (1988) Iron toxicity of wetland rice (Oryza sativa L.) as a multiple nutritional stress. In: Proceedings 9th Plant Nutrition Colloquium, England. August 22–27, pp 454–457

  • Pantoja O, Willmer CM (1988) Redox activity and peroxidase activity associated with the plasma membrane of guard cell protoplasts. Planta 174: 44–50

    Google Scholar 

  • Peterson DA (1991) Enhanced electron transfer by unsaturated fatty acids and Superoxide dismutase. Free Radie Res Commun 12-13: 161–166

    Google Scholar 

  • Polle A, Krings B, Rennenberg H (1989) Superoxide dismutase activity in needles of Norwegian spruce trees (Picea abies L.). Plant Physiol 90: 1310–1315

    Google Scholar 

  • Ponnamperuma FN, Bradfield R, Peech M (1955) Physiological disease of rice attributable to iron toxicity. Nature 175: 265

    Google Scholar 

  • Price AH, Hendry GAF (1991) Iron-catalyzed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ 14: 477–484

    Google Scholar 

  • Rabinowitch HD, Fridovich I (1983) Superoxide radicals, superoxide dismutases and oxygen toxicity in plants. Photochem Photobiol 37: 679–690

    Google Scholar 

  • del Rio LA, Sandalio LM, Yanez J, Gomez M (1985) Induction of a manganese-containing Superoxide dismutase in leaves ofPisum sativum L. by high nutrient levels of zinc and manganese. J Inorg Biochem 24: 25–34

    Google Scholar 

  • — —, Palma JM (1990) A new cellular function for peroxisomes related to oxygen free radicals? Experientia 46: 989–992

    Google Scholar 

  • —, Sevilla F, Sandalio LM, Palma JM (1991) Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Radie Res Comm 12–13: 819–828

    Google Scholar 

  • Römheld V, Marschner H (1986 a) Mobilization of iron in the rhi zosphere of different plant species. In: Trinker B, Läuchli A (eds) Advances in plant nutrition, vol 2. Praeger, New York, pp 155–204

    Google Scholar 

  • — — (1986 b) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80: 175–180

    Google Scholar 

  • —, (1987) Existence of two different strategies for the acquisition of iron in higher plants. In: Winkelmann G, van der Helm D, Neila JB (eds) Iron transport in microbes, plants and animals. VCH, Weinheim, pp 353–374

    Google Scholar 

  • Rush JD, Maskos Z, Koppenol WH (1990) Reactions of iron (II) nucleotide complexes with hydrogen peroxide. FEBS Lett 261: 121–123

    Google Scholar 

  • Saalthiel Y, Glazer A, Bocion PF, Gressel J (1988) Cross tolerance to herbicidal and environmental oxidants of plant biotypes tolerant to paraquat, sulfur dioxide, and ozone. Pesticide Biochem Physiol 31: 13–23

    Google Scholar 

  • Salin ML (1988) Plant Superoxide dismutase: a means of coping with oxygen radicals. Curr Top Plant Biochem Physiol 7: 188–200

    Google Scholar 

  • Sies H (1985) Oxidative stress. Academic Press, London

    Google Scholar 

  • Spitz DR, Oberley LW (1989) An assay for Superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 179: 8–18

    Google Scholar 

  • Tadano T (1976) Studies on the methods to prevent iron toxicity in the lowland rice. Univ Hokkaido Memoirs Fac Agric 10: 22–68

    Google Scholar 

  • Takagi S (1976) Naturally occurring-chelating compounds in oat- and rice-root washings. I. Activity measured and preliminary characterization. Soil Sci Plant Nutr 22: 423–433

    Google Scholar 

  • Tanaka A, Loe R (1966) Some mechanisms involved in the development of iron toxicity symptoms in rice plants. Soil Sci Plant Nutr 12: 32–38

    Google Scholar 

  • Thompson JE, Legge RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105: 317–344

    Google Scholar 

  • Ushimaru T, Shibasaka M, Tsuji H (1992) Development of the O2 −-detoxification system during adaptation to air of submerged rice seedlings. Plant Cell Physiol 33: 1065–1071

    Google Scholar 

  • Vianello A, Macri F (1991) Generation of Superoxide anion and hydrogen peroxide at the surface of plant cells. J Bioenerg Biomembr 23: 409–423

    Google Scholar 

  • Vladimirov YA (1980) Lipid peroxidation in mitochondrial membrane. Adv Lipid Res 17: 173–249

    Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling enhanced photooxidation: evidence for the role of singlet oxygen and Superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83: 278–282

    Google Scholar 

  • Yamanouchi M, Yoshida S (1981) Physiological mechanisms of rice's tolerance for iron toxicity. In: IRRI Saturday Seminar, June 6th, 1981, pp 1–8

Download references

Author information

Authors and Affiliations

  1. Institut für Allgemeine Botanik, Universität Hamburg, Ohnhorststrasse 18, D-22609, Hamburg, Federal Republic of Germany

    O. Döring & S. Lüthje

  2. Abteilung Biogeochemie, Otto-Hahn-Institut, Max-Planck-Institut für Chemie, Mainz

    K. Bode & M. Böttger

  3. The International Rice Research Institute, Manila

    H. -U. Neue

Authors
  1. K. Bode
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. Döring
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Lüthje
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. -U. Neue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Böttger
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bode, K., Döring, O., Lüthje, S. et al. The role of active oxygen in iron tolerance of rice (Oryza sauva L.). Protoplasma 184, 249–255 (1995). https://doi.org/10.1007/BF01276928

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01276928

Keywords

Search

Navigation