Skip to main content

Advertisement

SpringerLink
Log in

Induction of Oxidative Stress by Sunflower Phytotoxins in Germinating Mustard Seeds

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the phytotoxic effect of sunflower on physiological and biochemical processes during germination of mustard seeds (Sinapis alba L. cv. Nakielska). To exclude the involvement of osmotic stress in seed reaction to phytotoxic compounds, we compared the effect of 10% (w/v) water extract from sunflower (Helianthus annuus L. cv. Ogrodowy) leaves and 28.4% (w/v) polyethylene glycol (PEG) 8000 solution characterized by an equal Ψ = −1 MPa. We evaluated (1) the amount of hydrogen peroxide (H2O2); (2) activities of antioxidant enzymes: superoxide dismutase, catalase, and glutathione reductase; (3) membrane permeability; and (4) level of malondialdehyde (MDA). Both, sunflower compounds and PEG solutions inhibited mustard seed germination, but only phytotoxins caused an increase in the cell membrane permeability, MDA level, H2O2 concentration, and alterations in activities of antioxidant enzymes. Our results demonstrate that despite the activation of the antioxidant system by sunflower phytotoxins, reactive oxygen species accumulation caused cellular damage, which resulted in the decrease of germinability and gradual loss of seed vigor. It seems that the negative effect of sunflower on germination of mustard seeds is mostly because of its toxicity and not to its contribution to osmotic potential.

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

Similar content being viewed by others

References

  • Abrahim, D., Braguini, W. L., Kelmer-Bracht, A. M., and Ishii-Iwamoto, E. L. 2000. Effects of four monoterpenes on germination, primary root growth, and mitochondrial respiration of maize. J. Chem. Ecol. 26:611–624.

    Article  CAS  Google Scholar 

  • Anaya, A. L. and Pelayo-Benavides, H. P. 1997. Allelopathic potential of Mirabilis jalapa L. (Nyctaginaceae): Effects on germination, growth and cell division of some plants. Allelopathy J. 4:57–68.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Azania, A. A. P. M., Azania, C. A. M., Alves, P. L. C. A., Palaniraj, R., Kadian, H. S., Sati, S. C., Rawat, L. S., Dahiya, D. S., and Narwal, S. S. 2003. Allelopathic plants. Sunflower (Helianthus annuus L.). Allelopathy J. 11:1–20.

    Google Scholar 

  • Bailly, C., Benamar, A., Corbineau, F., and Côme, D. 1996. Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol. Plant. 97:104–110.

    Article  CAS  Google Scholar 

  • Bais, H. P., Vepachedu, R., Gilroy, S., Callaway, R. M., and Vivanco, J. M. 2003. Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380.

    Article  PubMed  CAS  Google Scholar 

  • Batish, D. R., Tung, P., Singh, H. P., and Kohli, R. K. 2002. Phytotoxicity of sunflower residues against some summer season crops. J. Agron. Crop Sci. 188:19–24.

    Article  CAS  Google Scholar 

  • Blokhina, O., Virolainen, E., and Fagersted, K. V. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91:179–194.

    Article  PubMed  CAS  Google Scholar 

  • Bogatek, R., Gniazdowska, A., Zakrzewska, W., Oracz, K., and Gawroñski, S. W. 2006. Allelopathic effect of sunflower extracts on mustard seed germination and seedling growth. Biol. Plant. 50:156–158.

    Article  Google Scholar 

  • Bowler, C., Montagu, M. V., and Inze, D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:83–116.

    Article  CAS  Google Scholar 

  • Bradford, M. M. 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.

    Article  PubMed  CAS  Google Scholar 

  • Clairbone, A. 1985. Catalose activity, pp. 283–284, in R. A. Greenwald (ed.). Handbook of Methods of Oxygen Radical Research. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Cruz-Ortega, R., Anaya, A. L., and Ramos, L. 1988. Effects of allelopathic compounds of corn pollen on respiration and cell division of watermelon. J. Chem. Ecol. 14:71–86.

    Article  CAS  Google Scholar 

  • Cruz-Ortega, R., Anaya, A. L., Gavilanes-Ruiz, M., Sánchez-Nieto, S., and Jimmenez-Estrada, M. 1990. Effect of diacetyl piquerol on the H+-ATPase activity of microsomes from Ipomoea purpurea. J. Chem. Ecol. 16:2253–2261.

    Article  CAS  Google Scholar 

  • Cruz-Ortega, R., Ayala-Cordero, G., and Anaya, L. A. 2002. Allelochemical stress produced by aqueous leachate of Callicarpa acuminata: effects on roots of bean, maize, and tomato. Physiol. Plant. 116:20–27.

    Article  PubMed  CAS  Google Scholar 

  • Czarnota, M. A., Paul, R. N., Dayan, F. E., Nimbal, C. I., and Weston, L. A. 2001. Mode of action, localization of production, chemical nature and activity of sorgoleone: A potent PSII inhibitor in Sorghum spp. root exudates. Weed Technol. 15:813–825.

    Article  CAS  Google Scholar 

  • Dayan, F. E., Romagni, J. G., and Duke, S. O. 2000. Investigating the mode of action of natural phytotoxins. J. Chem. Ecol. 26:2079–2094.

    Article  CAS  Google Scholar 

  • De Gara, L., De Pinto, M. C., and Tommasi, F. 2003. The antioxidant systems vis-a-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem. 41:863–870.

    Article  CAS  Google Scholar 

  • Del Rio, L. A., Corpas, F. J., Sandalio, L. M., Palma, J. M., Gomez, M., and Barroso, J. B. 2002. Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J. Exp. Bot. 53:1255–1272.

    Article  PubMed  Google Scholar 

  • Foyer, C. H. and 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, C. H. and Noctor, G. 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28:1056–1071.

    Article  CAS  Google Scholar 

  • Foyer, C. H., Descourvieres, P., and Kunert, K. J. 1994. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ. 17:507–523.

    Article  CAS  Google Scholar 

  • Foyer, C. H., Souriau, N., Perret, S., Lelandis, M., Kunert, K. J., Pruvost, C., and Jouanin, L. 1995. Overexpression of glutathione reductase but not glutathione synthetase leads to increase in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol. 109:1047–1057.

    Article  PubMed  CAS  Google Scholar 

  • Galindo, J. C. G., Hernandez, A., Dayan, F. E., Tellez, M. R., Macias, F. A., Paul, R. N., and Duke, S. O. 1999. Dehydrozaluzanin C, a natural sesquiterpenolide, causes rapid plasma membrane leakage. Phytochemistry 52:805–813.

    Article  CAS  Google Scholar 

  • Giannopolitis, C. N. and Ries, S. K. 1977. Superoxide dismutases I. Occurrence in higher plants. Plant Physiol. 59:309–314.

    Article  PubMed  CAS  Google Scholar 

  • Gniazdowska, A. and Bogatek, R. 2005. Allelopathic interactions between plants. Multi site action of allelochemicals. Acta Physiol. Plant. 27:395–407.

    Article  CAS  Google Scholar 

  • Goel, A., Goel, A. K., and Sheoran, I. S. 2003. Changes in oxidative stress enzymes during artificial ageing in cotton (Gossypium hirsutum L.) seeds. J. Plant Physiol. 160:1093–1100.

    Article  PubMed  CAS  Google Scholar 

  • Heath, R. L. and Parker, 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 

  • Inze, D. and Montagu, V. 1995. Oxidative stress in plants. Curr. Opin. Biotechnol. 6:153–158.

    Article  CAS  Google Scholar 

  • Irons, S. and Burnside, O. C. 1982. Competitive and allelopathic effect of sunflower (Helianthus annuus). Weed Sci. 30:372–377.

    Google Scholar 

  • Kato-Noguchi, H. and Tanaka, Y. 2003–2004. Effects of capsaicin on plant growth. Biol. Plant. 47:157–159.

    Article  CAS  Google Scholar 

  • Kupidłowska, E., Gniazdowska, A., Stępień, J., Corbineau, F., Vinel, D., Skoczowsk, A., Janeczko, A., and Bogatek, R. 2006. Impact of sunflower (Helianthus annuus L.) extracts upon reserve mobilization and energy metabolism in germinating mustard (Sinapis alba L.) seeds. J. Chem. Ecol. DOI 10.1007/s10886-006-9183-z.

  • Leather, G. R. 1983. Sunflowers (Helianthus annuus) are allelopathic to weeds. Science 31:37–42.

    Google Scholar 

  • Lehman, M. E. and Blum, U. 1999. Evaluation of ferulic acid uptake as a measurement of allelochemical dose: effective concentration. J. Chem. Ecol. 25:2585–2600.

    Article  CAS  Google Scholar 

  • Macias, F. A., Varela, R. M., Torres, A., and Molinillo, J. M. G. 1993. Potential allelopathic guaianolides from cultivar sunflower leaves, var. SH-222. Phytochemistry 34:669–674.

    Article  CAS  Google Scholar 

  • Macias, F. A., Varela, R. M., Torres, A., and Molinillo, J. M. G. 1996. Potential allelopathic sesquiterpene lactones from sunflower leaves. Phytochemistry 43:1205–1215.

    Article  CAS  Google Scholar 

  • Macias, F. A., Varela, R. M., Torres, A., Oliva, R. M., and Molinillo, J. M. G. 1997. Bioactive norsesquiterpenes from Helianthus annuus with potential allelopathic activity. Phytochemistry 48:631–636.

    Article  Google Scholar 

  • Macias, F. A., Oliva, R. M., Varela, R. M., Torres, A., and Molinillo, J. M. G. 1999. Allelochemicals from sunflower leaves cv. Peredovick. Phytochemistry 52:613–621.

    Article  CAS  Google Scholar 

  • Macias, F. A., Varela, R. M., Torres, A., and Molinillo, J. M. G. 2000. Potential allelopathic activity of natural plant heliannanes: a proposal of absolute configuration and nomenclature. J. Chem. Ecol. 26:2173–2186.

    Article  CAS  Google Scholar 

  • Macias, F. A., Varela, R. M., Torres, A., Galindo, J. L. G., and Molinillo, J. M. G. 2002. Allelochemicals from sunflowers: chemistry, bioactivity and applications, pp. 73–87, in Inderjit and A. U. Mallik (eds.). Chemical Ecology of Plants: Allelopathy in Aquatic and Terrestrial Ecosystems. Birkhauser Verlag, Basel.

    Google Scholar 

  • Maffei, M., Bertea, C. M., Garneri, F., and Scanneri, S. 1999. Effect of benzoic acid hydroxy- and methoxy-ring substituents during cucumber (Cucumis sativus L.) germination. I. Isocitrate lyase and catalase activity. Plant Sci. 141:139–147.

    Article  CAS  Google Scholar 

  • Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405–409.

    Article  PubMed  CAS  Google Scholar 

  • Moore, R. P. 1973. Tetrazolium staining for assessing seed quality, pp. 347–366, in W. Heydecker (ed.). Seed Ecology. Butterworths, London.

    Google Scholar 

  • Musculo, A., Panuccio, M. R., and Sidari, M. 2001. The effect of phenols on respiratory enzymes in seed germination. Respiratory enzyme activities during germination of Pinus laricio seeds treated with phenols extracted from different forest soils. Plant Growth Regul. 35:31–35.

    Article  Google Scholar 

  • O’Kane, D., Gill, V., Boyd, P., and Burdon, R. 1996. Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198:371–377.

    Article  PubMed  CAS  Google Scholar 

  • Peng, S. L., Wen, J., and Guo, Q. F. 2004. Mechanism and active variety of allelochemicals. Acta Bot. Sin. 46:757–766.

    Google Scholar 

  • Peñuelas, J., Ribas-Carbo, M., and Giles, L. 1996. Effect of allelochemicals on plant respiration and oxygen isotope fractionation by alternative oxidase. J. Chem. Ecol. 22:801–805.

    Article  Google Scholar 

  • Politycka, B. 1996. Peroxidase activity and lipid peroxidation in roots of cucumber seedlings influenced by derivatives of cinnamic and benzoic acids. Acta Physiol. Plant. 18:365–370.

    CAS  Google Scholar 

  • Politycka, B. 1998. Phenolics and the activities of phenylalanine ammonia-lyase, phenol-β-glucosyltransferase and β-glucosidase in cucumber roots as affected by phenolics allelochemicals. Acta Physiol. Plant. 20:405–410.

    Article  CAS  Google Scholar 

  • Romero-Romero, T., Sanchez-Nieto, S., San Juan-Badillo, A., Anaya, A. L., and Cruz-Ortega, R. 2005. Comparative effects of allelochemical and water stress in roots of Lycopersicon esculentum Mill. (Solanaceae). Plant Sci. 168:1059–1066.

    Article  CAS  Google Scholar 

  • Scandalios, J. G. 1993. Oxygen stress and superoxide dismutase. Plant Physiol. 101:7–12.

    PubMed  CAS  Google Scholar 

  • Scandalios, J. G., Guan, L., and Polidoros, A. N. 1997. Catalases in plants: gene structure, properties, regulation and expression, pp. 343–406, in J. G. Scandalios (ed.). Oxidative Stress and the Molecular Biology of Antioxidant Defences. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Scebba, F., Sebastiani, L., and Vitagliano, C. 1998. Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedling under cold acclimation. Physiol. Plant. 104:747–752.

    Article  CAS  Google Scholar 

  • Shon, M. K. and Einhellig, F. A. 1982. Allelopathic effects of cultivated sunflower on grain sorghum. Bot. Gaz. 143:505–510.

    Article  Google Scholar 

  • Vranova, E., Inze, D., and van Breusegem, F. 2002. Signal transduction during oxidative stress. J. Exp. Bot. 53:1227–1236.

    Article  PubMed  CAS  Google Scholar 

  • Weir, T. L., Park, S.-W., and Vivanco, J. M. 2004. Biochemical and physiological mechanisms mediated by allelochemicals. Curr. Opin. Plant Biol. 7:472–479.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, R. E. and Rice, E. L. 1968. Allelopathy as expressed by Helianthus annuus and its role in old-field succession. Bull. Torrey Bot. Club 95:432–448.

    Article  CAS  Google Scholar 

  • Yu, J. Q., Ye, S. F., Zhang, M. F., and Hu, W. H. 2003. Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem. Syst. Ecol. 31:129–139.

    Article  CAS  Google Scholar 

  • Zeng, R. S., Luo, S. M., Shi, Y. H., Shi, M. B., and Tu, C. Y. 2001. Physiological and biochemical mechanism of allelopathy of secalonic acid F on higher plants. Agron. J. 93:72–79.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Stewart A. Brown, Professor Emeritus of Trent University, Peterborough, Ontario, Canada for assistance in preparing the English version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Plant Physiology, Warsaw Agricultural University, Nowoursynowska 159, 02-776, Warsaw, Poland

    Krystyna Oracz, Agnieszka Gniazdowska & Renata Bogatek

  2. Physiologie Végétale Appliquée, Université Pierre et Marie Curie-Paris 6, Boite Courrier 152, 4 place Jussieu, 75252, Paris Cédex 05, France

    Christophe Bailly, Daniel Côme & Francoise Corbineau

Authors
  1. Krystyna Oracz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christophe Bailly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agnieszka Gniazdowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Côme
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francoise Corbineau
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renata Bogatek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renata Bogatek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oracz, K., Bailly, C., Gniazdowska, A. et al. Induction of Oxidative Stress by Sunflower Phytotoxins in Germinating Mustard Seeds. J Chem Ecol 33, 251–264 (2007). https://doi.org/10.1007/s10886-006-9222-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9222-9

Keywords

Search

Navigation