Skip to main content
SpringerLink
Log in

Protective role of exogenous spermidine against paraquat toxicity in radish chloroplasts

  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

When radish chloroplasts were pretreated with 1 mM spermidine (Spd) and then exposed to 30 M paraquat (PQ), they improved their tolerance to subsequent PQ-induced oxidative damages. That included the decreases in the contents of chlorophyll, protein, and ascorbate, as well as the increases in malondialdehyde (MDA) and H2O2 levels. Analysis of antioxidant enzymes showed that Spd pretreatment effectively prevented the PQ-induced decreases in the total activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX). In contrast, the normally enhanced activities of dehydroascorbate reductase (DHAR) and glutathione reductase (GR) in PQ-treated chloroplasts were reversed by Spd pretreatment In a native gel assay, the Cu/ZnSOD isozyme, which disappeared under the PQ alone treatment, was significantly recovered when tissues were pretreated with Spd. The dominant APX4 isozyme activity, which was preferentially decreased in response to PQ alone treatment, was also strongly reactivated by earlier Spd exposure. Therefore, we suggest that Spd could play a substantial role in protecting the radish chloroplasts from PQ stress. Furthermore, the enhancement of the Cu/ZnSOD and APX4 isozymes by Spd pretreatment seems to be responsible for prevention of the PQ-induced decreases in the total activities of SOD and APX, thereby providing a tolerance to PQ toxicity.

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

Literature Cited

  • Arnon Dl (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase inBeta vulgaris. Plant Physiol 24: 1–15

    Article  PubMed  CAS  Google Scholar 

  • Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321

    Article  PubMed  CAS  Google Scholar 

  • Bernt E, Bergmeyer HU (1974) Inorganic peroxides,In HU Bergmeyer, ed, Methods of Enzymatic Analysis, Vol 4. Academic Press, pp 2246–2248

  • Bors W, Langebartels C, Michel C, Sandermann H Jr (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochem 28:1589–1595

    Article  CAS  Google Scholar 

  • Borsani O, Diaz P, Agius MF, Valpuesta V, Monza J (2001) Water stress generates an oxidative stress through the induction of a specific Cu/Zn superoxide dismutase inLotus corniculatus leaves. Plant Sci 161:757–763

    Article  CAS  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Marti N-Tanguy J (1999) Polyamines and environmental chalenges: Recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bowler C, Camp YW, Montagu MV, Inze D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid 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 

  • Carley E, Wolosiuk RA, Hertig CM (1983) Regulation of the activation of chloroplast fructose-1, 6-bisphosphatase. Inhibition by spermidine and spermine. Biochem Biophys Res Commun 115:707–710

    Article  Google Scholar 

  • Dhindsa RS, Plumb-Dhinda R, Thorpe TA (1981) Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 52:93–101

    Article  Google Scholar 

  • Drolet G, Dumbroff EB, Legge RL, Thompson JE (1986) Radical scavenging properties of polyamines. Phy- tochem 25:367–371

    CAS  Google Scholar 

  • Edwards EA, Enard C, Creissen GP, Mullineaux PM (1994) Synthesis and properties of glutathione reductase in stressed peas. Planta 192:137–143

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: 1. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Giardi MT, Masojidek J, Godde D (1997) Effects of abiotic stresses on the turnover of the D1 reaction centre II protein. Physiol Plant 101:635–642

    Article  CAS  Google Scholar 

  • Gillham DJ, Dodge AD (1987) Chloroplast superoxide and hydrogen peroxide scavenging systems from pea leaves: Seasonal variations. Plant Sci 50:105–109

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hossain MA, Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts in dark by addition of hydrogen peroxide: Its production by ascorbate. Plant Cell Physiol 25:1285–1295

    CAS  Google Scholar 

  • Keiser WM (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377–382

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage TI4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lidon FC, Henriques FS (1993) Oxygen metabolism in higher plant chloroplasts. Photosynthetica 29:249–279

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martinez CA, Loureiro ME, Oliva MA, Maestri M (2001) Differential responses of superoxide dismutase in freezing resistantSolanum curtilobum and freezing sensitiveSolanum curtilobum subjected to oxidative and water stress. Plant Sci 160:505–515

    Article  PubMed  CAS  Google Scholar 

  • Mehta RA, Fawcett TW, Porath D, Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Bio Chem 267:2810–2816

    CAS  Google Scholar 

  • Mills WR, Joy KW (1980) A rapid method for isolation of purified, physiologically active chloroplasts, used to study the intracellular distribution of amino acids in pea leves. Planta 148:75–83

    Article  CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazo- lium. Anal Biochem 212:540–546

    Article  PubMed  CAS  Google Scholar 

  • Munne-Bosch S, Alegre L (2002) Plant aging increases oxidative stress in chloroplasts. Planta 214:608–615

    Article  PubMed  CAS  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 

  • Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative stress defense in transgenic potato expressing tomato Cu/Zn, superoxide dismutase. Theor Appl Genet 85:568–576

    Article  CAS  Google Scholar 

  • Rao MV, Hale BA, Ormrod DP (1995) Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol 109:421–432

    PubMed  CAS  Google Scholar 

  • Robinson JM, Smith MG, Gibbs M (1980) Influence of hydrogen peroxide upon carbon dioxide photoassimilation in the spinach chloroplasts. Plant Physiol 65:755–759

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sen Gupta A, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993a) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 90:1629–1633

    Article  CAS  Google Scholar 

  • Sen Gupta A, Webb RR, Holaday AS, Allen RD (1993b) Overexpression of superoxide dismutase protects plants from oxidative stress: Induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants. Plant Physiol 103:1067–1073

    CAS  Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    Article  PubMed  CAS  Google Scholar 

  • Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa K, Yokota A, Shigeoka S (1998) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428:47–51

    Article  PubMed  CAS  Google Scholar 

  • Tadolini B (1988) Polyamine inhibition of lipo-peroxidation: The influence of polyamines on iron oxidation in the presence of compounds mimicking phospholipid polar heads. Biochem J 249:33–36

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tiburcio AF, Altabella T, Borrell A, Masgrau C (1997) Polyamine metabolism and its regulation. Physiol Plant 100:664–674

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Ye B, Gressel J (1994) Constitutive variation of ascorbate peroxidase activity during development parallels that of superoxide dismutase and glutathione reductase in paraquat resistant Conyza. Plant Sci 102:147–151

    Article  CAS  Google Scholar 

  • Ye B, Muller HH, Zhang J, Gressel J (1997) Constitutively elevated levels of putrescine and putrescine-generating enzymes correlated with oxidant stress resistance inConyza bonariensis and wheat. Plant Physiol 115:1443–1451

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K, Yabuta Y, lshikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stress. Plant Physiol 123:223–233

    Article  PubMed  CAS  Google Scholar 

  • Yu Q, Rengel Z (1999) Drought and salinity differentially influence activities of superoxide dismutases in narrowleafed lupinus. Plant Sci 142:1–11

    Article  CAS  Google Scholar 

  • Zheleva D, Tsonev T, Sergiev I, Karanov E (1994) Protective effect of exogenous polyamines against atrazine in pea plants. J Plant Growth Regul 13:203–211

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Life Sciences, Kangwon National University, 200-701, Chunchon, Korea

    Sun-mi Ahn & Chang-Duck Jin

Authors
  1. Sun-mi Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chang-Duck Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chang-Duck Jin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahn, Sm., Jin, CD. Protective role of exogenous spermidine against paraquat toxicity in radish chloroplasts. J. Plant Biol. 47, 338–347 (2004). https://doi.org/10.1007/BF03030549

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03030549

Keywords

Search

Navigation