Advertisement

Cereal Research Communications

, Volume 42, Issue 4, pp 568–577 | Cite as

Oxidative Stress of Maize Roots Caused by a Combination of both Salt Stress and Manganese Deprivation

  • H. Q. Zhao
  • L. Wang
  • J. Hong
  • X. Y. Zhao
  • X. H. Yu
  • L. Sheng
  • C. Z. Hang
  • Y. Zhao
  • A. A. Lin
  • W. H. SiEmail author
  • F. S. HongEmail author
Physiology

Abstract

Salt stress impaired Mn imbalance and resulted in accumulation of ROS, and caused oxidative stress to plants. However, very little is known about the oxidative damage of maize roots caused by exposure to a combination of both salt stress and Mn deprivation. Thus the main aim of this study was to determine the effects of a combination of salt stress and Mn deprivation on antioxidative defense system in maize roots. Maize plants were cultivated in Hoagland’s media. They were subjected to 80 mM NaCl administered in the Mn-present Hoagland’s or Mn-deficient Hoagland’s media for 14 days. The findings indicated that the growth and root activity of maize seedlings cultivated in a combination of both salt stress and Mn deprivation were significantly inhibited; the compatible solute accumulation, malondialdehyde, carbonyl, 8-OHdG, and ROS were higher than those of the individual salt stress or Mn deprivation as expected. Nevertheless, the antioxidative enzymes such as superoxide dismutase, ascorbate peroxidase, glutathione reductase, glutathione-S-transferase and antioxidants such as ascorbic acid, glutathione and thiol were lower than those of the individual salt stress or Mn deprivation. In view of the fact that salt stress impaired Mn nutrition of maize seedlings, the findings suggested that Mn deprivation at the cellular level may be a contributory factor to salt-induced oxidative stress and related oxidative damage of maize roots.

Keywords

salt stress maize manganese deprivation reactive oxygen species antioxidant defense system roots 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

42976_2014_4204568_MOESM1_ESM.pdf (34 kb)
Supplementary material, approximately 35 KB.

References

  1. Able A.J., Guest D.I., Sutherland M.W. 1998. Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoopspores of Phytophthora parasitica var. nicotianae. Plant Physiol 117:491–499.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agrawal S.B., Rathore D. 2007. Changes in oxidative stress defense system in wheat (Triticum aestivum L.) and mung bean (Vigna radiata L.) cultivars grown with and without mineral nutrients and irradiated by supplemental ultraviolet-B. Environ. Exp. Bot. 59:21–33.CrossRefGoogle Scholar
  3. Arabawa T., Timasheff S.N. 1985. The stabilization of proteins by osmolytes. Biophys. J. 47:411–414.CrossRefGoogle Scholar
  4. Arnon D.I., Hoagland D.R. 1940. Crop production in artificial solutions and in soil with special reference to factors affecting yields and absorption of inorganic nutrients. Soil Sci. 50:463–484.Google Scholar
  5. Asada K. 1999. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601–639.PubMedCrossRefGoogle Scholar
  6. Ashraf M. 2009. Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol. Adv. 27:84–93.PubMedCrossRefGoogle Scholar
  7. Ashraf M., Foolad M.R. 2007. Roles of glycinebetaine and praline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59:206–216.CrossRefGoogle Scholar
  8. Azevedo Neto A.D., Prisco J.T., Enéas-Filho J., Braga de Abreu C.E., Gomes-Filho E. 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot. 56:87–94.CrossRefGoogle Scholar
  9. Bartoli C.G., Simontacchi M., Tambussi E., Beltrano J., Montaldi E., Puntarulo S. 1999. Drought and watering-dependent oxidative stress: Effect on antioxidant content in Triticum aestivum L. leaves. J. Exp. Bot. 50:373–381.CrossRefGoogle Scholar
  10. Bates L.S. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207.CrossRefGoogle Scholar
  11. Beauchamp C., Fridovich I. 1971. Superoxide dismutase: Improved assays and assay applicable to acrylamide gels. Anal. Biochem. 44:276–286.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bidar G., Pruvot C., Garçon G., Verdin A., Shirali P., Douay F. 2008. Seasonal and annual variations of the metal uptake, bioaccumulation and toxicity in Trifolium repens and Lolium perenne growing in a heavy metal contaminated field. Environ. Sci. Pollut. Res. 16:42–53.CrossRefGoogle Scholar
  13. Buege J.A., Aust S.D. 1978. Microsomal lipid peroxidation. Meth. Enzymol. 52:302–310.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Costa C., Dwyer L.M., Hamilton R.I., Hamel C., Nantais L., Smith D.L. 2000. A sampling method for measurement of large root systems with scanner-based image analysis. Agron. J. 92:621–627.CrossRefGoogle Scholar
  15. Cramer G.R., Epstein E., Läuchli A. 1991. Effects of sodium, potassium and calcium on salt-stressed barely. II. Elemental analysis. Physiol. Plant 81:197–202.CrossRefGoogle Scholar
  16. Cramer G.R., Nowak R.S. 1992. Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stresses barely. Physiol. Plant 84:600–605.CrossRefGoogle Scholar
  17. Crawford N.M., Kahn M.L., Leustek T., Long S.R. 2000. Nitrogen and sulfur. In: Buchanan B.B., Gruissem W., Jones R.L. (eds), Biochemistry and Molecular Biology of Plants. ASPP. Rockville, USA, pp. 786–849.Google Scholar
  18. Fagan J.M., Bogdan G.S., Sohar I. 1999. Quantitation of oxidative damage to tissue proteins. Int. J. Biochem. Cell Biol. 31:751–757.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Foyer C.H., Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 133:21–25.PubMedCrossRefPubMedCentralGoogle Scholar
  20. Gong X.L., Liu C., Wang Y., Zhao X.Y., Zhou M., Hong M.M., Wang S.S., Wang L., Hong F.S. 2010. Inhibition of the photosynthesis in maize caused by manganese deficiency. Cereal Res. Commun. 38:353–365.CrossRefGoogle Scholar
  21. Gong X.L., Liu C., Zhou M., Hong M.M., Luo L.Y., Wang L., Wang Y., Cai J.W., Gong S.J., Hong F.S. 2011. Oxidative damages of maize seedlings caused by exposure to a combination of potassium deficiency and salt stress. Plant Soil 340:443–452.CrossRefGoogle Scholar
  22. Habig W.H., Jakoby W.B. 1981. Assay for differentiation of glutathione-S-transferases. Methods Enzymol. 77:398–405.PubMedCrossRefGoogle Scholar
  23. Hasegawa P.M., Bressan R.A., Zhu J.K., Bohnert H.J. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 51:463–499.PubMedCrossRefGoogle Scholar
  24. Hernández J.A., Almansa M.S. 2002. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol. Plant 115:251–257.PubMedCrossRefGoogle Scholar
  25. Hissin P.J., Hilf R. 1976. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74:214–226.PubMedCrossRefGoogle Scholar
  26. Hoque M.A., Okuma E., Banu M.N.A., Nakamura Y., Shimoishi Y., Murata Y. 2007a. Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J. Plant Physiol. 164:553–561.PubMedCrossRefGoogle Scholar
  27. Hoque M.A., Banu M.N.A., Okuma E., Amako K., Nakamura Y., Shimoishi Y., Murata Y. 2007b. Exogenous proline and glycinebe-taine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J. Plant Physiol. 164:1457–1468.PubMedCrossRefGoogle Scholar
  28. Izzo R., Navari-Izzo F., Quartacci M.F. 1991. Growth and mineral absorption in maize seedlings as affected by increasing NaCl concentrations. J. Plant Nutr. 14:687–699.CrossRefGoogle Scholar
  29. John G., Scandalios J.G. 1993. Oxygen stress and superoxide dismutase. Plant Physiol. 101:7–12.CrossRefGoogle Scholar
  30. Kampfenkel K., Van Montagu M., Inzé D. 1995. Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal. Biochem. 225:165–167.PubMedCrossRefGoogle Scholar
  31. Khedr A.H.A., Abbas M.A., Wahid A.A.A., Quick W.P., Abogadallah G.M. 2003. Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J. Exp. Bot. 54:2553–2562.PubMedCrossRefGoogle Scholar
  32. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:265–275.Google Scholar
  33. Marschner H. 1995. Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, New York, USA.Google Scholar
  34. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405–410.CrossRefGoogle Scholar
  35. Munns R., Cramer G.R., Ball M.C. 1999. Interactions between rising CO2, soil salinity and plant growth. In: Luo Y., Mooney H.A. (eds), Carbon Dioxide and Environmental Stress. Academic, London, UK, pp. 139–167.CrossRefGoogle Scholar
  36. Noctor G., Foyer C.H. 1998. Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 49:249–279.PubMedCrossRefGoogle Scholar
  37. Noctor G., Gomez L., Vanacker H., Foyer C.H. 2002. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 53:1283–1304.PubMedCrossRefGoogle Scholar
  38. Noreen Z., Ashraf M., Akram N.A. 2010. Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). J. Agron. Crop. Sci. 196:273–285.Google Scholar
  39. Nourooz-Zadeh J., Tajaddini-Sarmadi J., Wolff S.P. 1994. Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine. Anal. Biochem. 220:403–409.PubMedCrossRefGoogle Scholar
  40. Qu C.X., Gong X.L., Liu C., Hong M.M., Wang L., Hong F.S. 2011. Inhibition of nitrogen and photosynthetic carbon assimilation of maize seedlings by exposure to a combination of salt stress and potassium-deficient stress. Biol. Trace Elem. Res. 144:1159–1174.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Qu C.X., Liu C., Gong X.L., Li C.X., Hong M.M., Wang L., Hong F.S. 2012. Impairment of maize seedling photosynthesis caused by a combination of potassium deficiency and salt stress. Environ. Exp. Bot. 75:134–141.CrossRefGoogle Scholar
  42. Reuveni R., Karchi M.Z., Kuc J. 1992. Peroxidase activity as a biochemical marker for resistance of muskmelon (Cucumis melo) to seudoperno spora cubensis. Phytopathol. 82:749–753.CrossRefGoogle Scholar
  43. Rodríguez-Serrano M., Romero-Puertas M.C., Zabalza A., Corpas F.J., Gómez M., Del Río L.A., Sandalio L. 2006. Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ. 29:1532–1544.PubMedCrossRefGoogle Scholar
  44. Ruiz-Lozano J.M., Azcón R., Gómez M. 1996. Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol. Plant 98:767–772.CrossRefGoogle Scholar
  45. Shalata A., Mittova V., Volokita M., Guy M., Tal M. 2001. Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: The root antioxidative system. Physiol. Plant 112:487–494.PubMedCrossRefGoogle Scholar
  46. Shiau S.Y., Yeh A.I. 2004. On-line measurement of rheological properties of wheat flour extrudates with added oxido-reductants, acid, and alkali. J. Food Eng. 62:193–202.CrossRefGoogle Scholar
  47. Smirnoff N. 2005. Antioxidants and Reactive Oxygen Species in Plants. Blackwell Publishing, Oxford, UK.CrossRefGoogle Scholar
  48. Stadtman E.R., Levine R.L. 2003. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25:207–218.PubMedCrossRefGoogle Scholar
  49. Steponkus P.L., Lanphear F.O. 1967. Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol. 42:1423–1426.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Sudhir P., Murthy S.D.S. 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486.CrossRefGoogle Scholar
  51. Szalai G., Janda T. 2009. Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J. Agronomy Crop. Sci. 195:165–171.CrossRefGoogle Scholar
  52. van Hoorn J.W., Katerji N., Hamdy A., Mastrorilli M. 2001. Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution from the soil. Agric. Water Manage. 51:87–98.CrossRefGoogle Scholar
  53. Yemm E.W., Willis A.J. 1954. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57:508–514.PubMedPubMedCentralGoogle Scholar
  54. Zhao K.F., Li F.Z. 1999. Halophytes in China. Science Press, Beijing, China.Google Scholar
  55. Zou Q. 1995. Guide to Physiological and Biochemical Experiments. Agriculture Press, Beijing, China, pp. 30–31.Google Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2014

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • H. Q. Zhao
    • 1
    • 2
  • L. Wang
    • 3
  • J. Hong
    • 1
  • X. Y. Zhao
    • 1
  • X. H. Yu
    • 1
  • L. Sheng
    • 1
  • C. Z. Hang
    • 1
  • Y. Zhao
    • 1
  • A. A. Lin
    • 1
  • W. H. Si
    • 4
    Email author
  • F. S. Hong
    • 1
    Email author
  1. 1.Medical College of Soochow UniversitySuzhouChina
  2. 2.College of Life SciencesAnhui Agriculture UniversityHefeiChina
  3. 3.Library of Soochow UniversitySuzhouChina
  4. 4.Suzhou Polytechnical College of AgricultureSuzhouChina

Personalised recommendations