Skip to main content
SpringerLink
Log in

Contribution of a plasma membrane redox system to the superoxide production by wheat root cells

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Wound stress activated wheat root cells to produce oxygen radicals. The production was accompanied by an increased permeability for potassium ions and a depolarization of the plasma membrane. Various electron donors, such as the nonpenetrating donor potassium ferrocyanide as well as NADH and NADPH, caused the amplification of superoxide production by root cells. The\(O_2 ^{. - } \)-generating system in wheat root cells was found to be considerably sensitive to diphenylene iodonium, which is generally considered as a suicide inhibitor of neutrophil NADPH oxidase, and to other inhibitors of flavoprotein activity, chlorpromazine and quinine. The xenobiotic compound amidopyrine caused activation of the\(O_2 ^{. - } \)-generating system, which was depressed by DPI. The\(O_2 ^{. - } \)-generating system in root cells was shown to be significantly dependent on calcium content. Calcium loading of the root cells induced a powerful increase of the superoxide release. Data obtained indicate that superoxide generation is one of the early events of the wound stress response. Redox systems of the plasma membrane may be involved in the superoxide production in response to wound stress and detoxification of xenobiotic compounds in root cells.

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

DPI:

diphenylene iodonium

MP:

membrane potential

\(O_2 ^{. - } \) :

superoxide anion radical

ROS:

reactive-oxygen species

SOD:

superoxide dismutase

References

  • Auh CK, Murphy TM (1995) Plasma-membrane redox enzyme is involved in the synthesis of\(O_2 ^{. - } \) and H2O2 by phytophthora elicitor-stimulated rose cells. Plant Physiol 107: 1241–1247

    Google Scholar 

  • Abramson JJ, Salama G (1989) Critical sulfhydryls regulate calcium release from sarcoplasmic reticulum. J Bioenerg Biomembr 21: 283–294

    Google Scholar 

  • Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9: 1559–1572

    Google Scholar 

  • Alvarez ME, Pennel RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 1–20

    Google Scholar 

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

    Google Scholar 

  • Barber MJ, Kay CJ (1996) Superoxide production during reduction of molecular oxygen by assimilatory nitrate reductase. Arch Biochem Biophys 326: 227–232

    Google Scholar 

  • Bolwell GP, Butt VS, Davies DR, Zimmerlin A (1995) The origin of the oxidative burst in plants. Free Radical Res 23: 517–532

    Google Scholar 

  • —, Davies DR, Gerrish C, Auh C-K, Murphy TM (1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol 116: 1379–1385

    Google Scholar 

  • Cazale AC, Rouet-Mayer MA, Barbier-Brygoo H, Mathieu Y, Lauriere C (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiol 16: 659–669

    Google Scholar 

  • Cross AR, Jones OTG (1986) The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils: specific labelling of a component polypeptide of the oxidase. Biochem J 237: 111–116

    Google Scholar 

  • Doke N, Miura Y, Sanchez LM, Park HJ, Noritake T, Yoshioka H, Kawakita K (1996) The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defense. Gene 179: 45–51

    Google Scholar 

  • Döring O, Lüthje S, Böttger M (1998) To be or not to be — a question of plasma membrane redox? Prog Bot 56: 328–354

    Google Scholar 

  • Dwyer SC, Legendre L, Low PS, Leto TL (1996) Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochim Biophys Acta 1289: 231–237

    Google Scholar 

  • Fridovich I (1984) Overview: biological sources of 02 −. Methods Enzymol 105: 59–61

    Google Scholar 

  • Geletyuk VI, Kazachenko VN (1987) Synchronization of potassium channel activity of mollusc neurones induced by ferricyanide and barium. Biofizika 32: 73–78

    Google Scholar 

  • Gordon LK, Minibayeva FV, Rakhmatullina DF, Alyabyev AJ, Loseva NL, Nikolaev BA (1995) Thermogenesis of wheat root cells under the modification of functional activity of plasmalemma and xenobiotic detoxification. Dokl Akad Nauk Russ 341: 714–716

    Google Scholar 

  • Haley A, Russell AJ, Wood N, Allan AC, Knight M, Campbell AK, Trewavas AJ (1995) Effects of mechanical signalling on plantcell cytosolic calcium. Proc Natl Acad Sci USA 92: 4124–4128

    Google Scholar 

  • Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 1–13

    Google Scholar 

  • Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352: 524–526

    Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275

    Google Scholar 

  • Lygin AV, Gordon LK, Alexeyeva VJ, Balashova TK (1990) The change of the sterol content and fatty acid composition of phospholipids during the process of adaptive ageing of excised wheat roots. Fiziol Biokhim Kult Rast 22: 581–586

    Google Scholar 

  • Merzlyak MN, Ivanova DG, Reshetnikova IV, Guzhova NV, Goldshtein NI (1991) Hydrogen peroxide-induced luminol-dependent chemiluminescence of potato leaf wound diffusates. Biokhimiya 56: 1798–1805

    Google Scholar 

  • Minibayeva FV, Rakhmatullina DF, Gordon LK, Vylegzhanina NN (1997) Role of superoxide in the formation of unspecific adaptive syndrome of root cells. Dokl Akad Nauk Russ 355: 554–556

    Google Scholar 

  • Misra HR, Fridovich I (1972) The univalent reduction of oxygen by reduced flavins and quinones. J Biol Chem 247: 188–192

    Google Scholar 

  • Moran JF, Becana M, Iturbeormaetxe I, Frechilla S, Klucas RV, Apariciotejo P (1994) Drought induces oxidative stress in pea plants. Planta 194: 346–352

    Google Scholar 

  • Murphy TM, Auh C-K (1996) The superoxide synthases of plasma membrane preparations from cultured rose cells. Plant Physiol 110: 621–629

    Google Scholar 

  • Prasad TK (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J 10: 1017–1026

    Google Scholar 

  • Pugin A, Franchisse J-M, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogen in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9: 2077–2091

    Google Scholar 

  • Racker E (1967) Bioenergetic mechanisms. Mir, Moscow

    Google Scholar 

  • Safina GF, Gordon LK, Alexeeva VY, Bichurina AA (1978) On hydroxylation activity of plant tissues. Fiziol Rast 25: 70–73

    Google Scholar 

  • Segal AW, Abo A (1993) The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci 18: 43–47

    Google Scholar 

  • Velikanov GA, Tsentsevitskii AN, Nuriev IK, Evarestov AS, Gordon LK (1992) Intercellular transfer of water and ions in roots of sunflower seedlings. Fiziol Rast 39: 649–655

    Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681–692

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biochemistry and Biophysics, Russian Academy of Sciences, P.O. Box 30, 420503, Kazan, Russian Federation

    F. V. Minibayeva, O. P. Kolesnikov & L. K. Gordon

Authors
  1. F. V. Minibayeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. P. Kolesnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. K. Gordon
    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

Minibayeva, F.V., Kolesnikov, O.P. & Gordon, L.K. Contribution of a plasma membrane redox system to the superoxide production by wheat root cells. Protoplasma 205, 101–106 (1998). https://doi.org/10.1007/BF01279299

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01279299

Keywords

Search

Navigation