Skip to main content
Log in

Phthalic Acid Induces Oxidative Stress and Alters the Activity of Some Antioxidant Enzymes in Roots of Malus prunifolia

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

Abstract

Apple replant is a widespread agricultural problem documented in all of the major fruit-growing regions of the world. In order to better understand the phytotoxic mechanisms induced by allelochemicals involved with this problem, Malus prunifolia plants were grown hydroponically to the six-leaf-stage in the presence of phthalic acid (0 or 1 mM) for 5, 10, or 15 days. Apple plants were evaluated for: shoot and root length, fresh and dry weight, malondialdehyde (MDA) content, hydrogen peroxide (H2O2) content, superoxide radical (O2 ·−) generation rate, and antioxidant enzyme activities. Shoot and root lengths and fresh and dry weights of M. prunifolia decreased in plants exposed to phthalic acid. MDA and H2O2 content increased in phthalic acid-treated plants as did the generation rate of O2 ·− in M. prunifolia roots. The activities of superoxide dismutase (EC 1.15.1.1), peroxidase (EC 1.11.1.7), catalase (EC 1.11.1.6), ascorbate peroxidase (EC 1.11.1.11), glutathione reductase (EC 1.6.4.2), dehydroascorbate reductase (EC 1.8.5.1), and monodehydroascorbate reductase (EC 1.6.5.4) increased in phthalic acid-stressed roots compared with control roots. These results suggest that activation of the antioxidant system by phthalic acid led to the formation of reactive oxygen species that resulted in cellular damage and the decrease of M. prunifolia growth.

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

Access this article

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

Similar content being viewed by others

References

  • Aebi, H. 1984. Catalase in vitro. Meth. Enzymol. 105:121–126.

    Article  PubMed  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  Google Scholar 

  • Asao, T., Kitazawa, H., Tomita, K., Suyama, K., Yamamoto, H., Hosoki, T., and Pramanik, M. H. R. 2004. Mitigation of cucumber autotoxicity in hydroponic culture using microbial strain. Sci. Hortic 99:207–214.

    Article  Google Scholar 

  • Bai, R., Zhao, X., Ma, F. W., and Li, C. Y. 2009. Identification and bioassay of allelopathic substances from the root exudates of Malus prunifolia. Allelopathy J. in press.

  • Batish, D. R., Singh, H. P., Setia, N., Kaur, S., and Kohli, R. K. 2006. 2-Benzoxazolinone (BOA) induced oxidative stress, lipid peroxidation and changes in some antioxidant enzyme activities in mung bean (Phaseolus aureus). Plant Physiol. Biochem. 44:819–827.

    Article  PubMed  Google Scholar 

  • Batish, D. R., Singh, H. P., Kaur, S., Kohli, R. K., and Yadav, S. S. 2008. Caffeic acid affects early growth, and morphogenetic response of hypocotyl cuttings of mung bean (Phaseolus aureus). J. Plant Physiol 165:297–305.

    Article  PubMed  Google Scholar 

  • Baziramakenga, R., Leroux, G. D., and Simard, R. R. 1995. Effects of benzoic and cinnamic acids on membrane permeability of soybean roots. J. Chem. Ecol. 21:1271–1285.

    Article  Google Scholar 

  • Beauchamp, C., and Fridovich, I. 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal. Biochem 44:276–287.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Borner, H. 1959. The apple replant problem. I. The excretion of phlorizin from apple root residues. Contrib. Boyre Thompson Inst 20:39–54.

    Google Scholar 

  • Chai, Q., and Feng, F. X. 2007. Identification of root exudation of Zea mays L. and allelopathy of 1,2-benzenedicarboxylic acid. J. Gansu Agric. Univ 5:43–48(in Chinese).

    Google Scholar 

  • Cho, U. H., and Seo, N. H. 2005. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Dalton, D. A., Russell, S. A., Hanus, F. J., Pascoe, G. A., and Evans, H. J. 1986. Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. PNAS 83:3811–3815.

    Article  PubMed  Google Scholar 

  • Dhindsa, R. S., Plumb-Dhindsa, P., and Thorpe, T. A. 1981. Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J. Exp. Bot 32:93–101.

    Article  Google Scholar 

  • Ding, J., Sun, Y., Xiao, C. L., Yan, K. S., Zhou, H., and Yu, J. Q. 2007. Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J. Exp. Bot 58:3765–3773.

    Article  PubMed  Google Scholar 

  • Elstner, E. F., and Heupel, A. 1976. Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal. Biochem 70:616–620.

    Article  PubMed  Google Scholar 

  • Fernandez, C., Voiriot, S., Mevy, J. P., Vila, B., Ormeno, E., Dupouyet, S., and Melou, A. B. 2008. Regeneration failure of Pinus halepensis Mill.: The role of autotoxicity and some abiotic environmental parameters. For. Ecol. Manage 255:2928–2936.

    Article  Google Scholar 

  • Forman, H. J., Torres, M., and Fukuto, J. 2002. Redox signaling. Mol. Cell. Biochem 234:49–62.

    Article  PubMed  Google Scholar 

  • Grace, S. C., and Logan, B. A. 1996. Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640.

    PubMed  Google Scholar 

  • Hao, Z. P., Wang, Q., Christie, P., and Li, X. L. 2007. Allelopathic potential of watermelon tissues and root exudates. Sci. Hortic. 112:315–320.

    Article  Google Scholar 

  • Hoagland, D. R. 1920. Optimum nutrient solutions for plants. Science 52:562–564.

    Article  PubMed  Google Scholar 

  • Lara-Nunez, A., Romero-Romero, T., Ventura, J. L., Blancas, V., Anaya, A. L., and Cruz-Ortega, R. 2006. Allelochemical stress causes inhibition of growth and oxidative damage in Lycopersicon esculentum Mill. Plant Cell Environ 29:2009–2016.

    Article  PubMed  Google Scholar 

  • Lee, J. G., Lee, B. Y., and Lee, H. J. 2006. Accumulation of phytotoxic organic acids in reused nutrient solution during hydroponic cultivation of lettuce (Lactuca sativa L.). Sci. Hortic 110:119–128.

    Article  Google Scholar 

  • Lin, C. C., and Kao, C. H. 2000. Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155.

    Article  Google Scholar 

  • Lin, R. Z., Wang, X. R., Luo, Y., Du, W. C., Guo, H. Y., and Yin, D. Q. 2007. Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98.

    Article  PubMed  Google Scholar 

  • Masia, A. 2003. Physiological effects of oxidative stress in relation to ethylene in post-harvest produce, pp. 165–197, in D. M. Hodges (ed.). Postharvest Oxidative Stress in Horticultural CropsFood Products Press, New York.

    Google Scholar 

  • Miyake, C., and Asada, K. 1992. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553.

    Google Scholar 

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

    Google Scholar 

  • Oracz, K., Bailly, C., Gniazdowska, A., Come, D., Corbineau, F., and Bogatek, R. 2007. Induction of oxidative stress by sunflower phytotoxins in germinating mustard seeds. J Chem Ecol 33:251–264.

    Article  PubMed  Google Scholar 

  • Patterson, B. D., Macrae, E. A., and Ferguson, I. B. 1984. Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal. Biochem 139:487–492.

    Article  PubMed  Google Scholar 

  • Romero-Romero, T., Sanchez-Nieto, S., Sanjuan-Badillo, A., Amaua, 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  Google Scholar 

  • Sanchez-Moreiras, A. M., and Reigosa, M. J. 2005. Whole plant response of lettuce after root exposure to BOA (2(3H)-Benzoxazolinone). J. Chem. Ecol 31:2689–2703.

    Article  PubMed  Google Scholar 

  • Sofo, A., Dichio, B., Xiloynnis, C., and Masia, A. 2004. Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree. Plant Sci 166:293–302.

    Article  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  Google Scholar 

  • Wu, F. Z., Huang, C. H., and Zhao, F. Y. 2002. Effects of phenolic acids on growth and activities of membrane protective enzymes of cucumber seedlings. Agric. Sci. China 35:821–825.

    Google Scholar 

  • Ye, S. F., Zhou, Y. H., Sun, Y., Zou, L. Y., and Yu, J. Q. 2006. Cinnamic acid causes oxidative stress in cucumber roots, and promotes incidence of Fusarium wilt. Environ. Exp. Bot 56:255–262.

    Article  Google Scholar 

  • Yu, J. Q., and Matsui, Y. 1997. Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J. Chem. Ecol 23:817–827.

    Article  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  Google Scholar 

  • Zhang, J. H., Mao, Z. Q., Wang, L. Q., and Shu, H. R. 2007. Bioassay and identification of root exudates of three fruit tree species. J. Integr. Plant. Biol 49:257–261.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Fund of Shaanxi province and Talent Support Program of Northwest A&F University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fengwang Ma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bai, R., Ma, F., Liang, D. et al. Phthalic Acid Induces Oxidative Stress and Alters the Activity of Some Antioxidant Enzymes in Roots of Malus prunifolia . J Chem Ecol 35, 488–494 (2009). https://doi.org/10.1007/s10886-009-9615-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-009-9615-7

Keywords

Navigation