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Combined effects of hypoxia and excess Mn2+ on oxidative stress and antioxidant enzymes in tomato seedlings

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Abstract

Effects of high level of Mn2+ on the changes in ROS generation, root cell viability, antioxidant enzyme activities, and related gene expression in tomato (Solanum lycopersicum L., cv. Zhongza 9) seedlings were studied under normoxic and hypoxia conditions. Mn2+ concentrations, ranged between 10 and 200 μM, led to significantly higher activities of superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APOD), glutathione reductase (GR), and also ascorbic acid (AsA) content in leaves and roots, improved root cell viability, and decreased O ·−2 accumulation compared with the higher Mn2+ level under hypoxia stress, which indicated that low Mn2+ could eliminate the active oxygen and protect the membrane lipid from the hypoxia hurt. When the concentration of Mn2+ reached 400–600 μM under hypoxia stress, the activities of SOD, POD, APOD, and GR and AsA content were decreased remarkably. In contrast, the MDA content was increased at the higher Mn2+ concentration. A number of antioxidant-related genes showed high expression at the lower level of Mn2+. The expression levels of SOD, POD, CAT, APOD, and GR genes were 7.95, 5.27, 3.18, 5.54, and 8.81 times compared to control, respectively. These results illustrated that the appropriate amount of Mn2+ could alleviate the detrimental effects of hypoxia stress, but reversely, the high level of Mn2+ just aggravated the existing damage to the tomato seedlings.

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Abbreviations

APOD:

ascorbate peroxidase

AsA:

ascorbic acid

CAT:

catalase

DO:

dissolved oxygen

FDA:

fluorescein diacetate

GR:

glutathione reductase

NBT:

nitroblue tetrazolium

POD:

peroxidase

RT-PCR:

real-time polymerase chain reaction

SOD:

superoxide dismutase

References

  1. Negra, C., Ross, D.S., and Lanzirotti, A., Oxidizing Behavior of Soil Manganese: Interactions among Abundance, Oxidation State, and pH, Soil Sci. Soc. Am. J., 2005, vol. 69, pp. 87–95.

    Article  CAS  Google Scholar 

  2. Mukhopadhyay, M.J. and Sharma, A., Manganese in Cell Metabolism of Higher Plants, Bot. Rev., 1991, vol. 51, pp. 117–149.

    Article  Google Scholar 

  3. Dimkpa, C.O., Merten, D., Svatoš, A., Büchel, G., and Kothe, E., Metal-Induced Oxidative Stress Impacting Plant Growth in Contaminated Soil Is Alleviated by Microbial Siderophores, Soil Biol. Biochem., 2009, vol. 41, pp. 154–162.

    Article  CAS  Google Scholar 

  4. Drew, M.C., Oxygen Deficiency and Root Metabolism: Injury and Acclimation under Hypoxia and Anoxia, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 223–250.

    Article  PubMed  CAS  Google Scholar 

  5. Blake, L. and Goulding, K.W.T., Effects of Atmospheric Deposition, Soil pH and Acidification on Heavy Metal Contents in Soils and Vegetation of Semi-Natural Ecosystems at Rothamsted Experimental Station, UK, Plant Soil, 2002, vol. 240, pp. 235–251.

    Article  CAS  Google Scholar 

  6. Hauck, M., Paul, A., Gross, S., and Raubuch, M., Manganese Toxicity in Epiphytic Lichens: Chlorophyll Degradation and Interaction with Iron and Phosphorus, Environ. Exp. Bot., 2003, vol. 49, pp. 181–191.

    Article  CAS  Google Scholar 

  7. Shi, Q.H., Zhu, Z.J., Xu, M., Qian, Q.Q., and Yu, J.Q., Effects of Excess Manganese on the Antioxidant System in Cucumis sativus L. under Two Light Intensities, Environ. Exp. Bot., 2006, vol. 58, pp. 197–205.

    Article  CAS  Google Scholar 

  8. El-Jaoual, T. and Cox, D.A., Manganese Toxicity in Plants, J. Plant Nutr., 1998, vol. 24, pp. 353–386.

    Article  Google Scholar 

  9. Kappus, H., Lipid Peroxidation: Mechanisms, Analysis, Enzymology and Biological Relevance, Oxidative Stress, Sies, H., Ed., London: Academic, 1985, pp. 273–310.

    Google Scholar 

  10. Veljovic-Jovanovic, S.D., Noctor, G., and Foyer, C.H., Are Leaf Hydrogen Peroxide Concentrations Commonly Overestimated? The Potential Influence of Artefactual Interference by Tissue Phenolics and Ascorbate, Plant Physiol. Biochem., 2002, vol. 40, pp. 501–507.

    Article  CAS  Google Scholar 

  11. Jabs, T., Dietrich, R.A., and Dangl, J.L., Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide, Science, 1996, vol. 273, pp. 1853–1855.

    Article  PubMed  CAS  Google Scholar 

  12. Giannopolitis, C.N. and Ries, S.K., Superoxide Dismutases. I. Occurrence in Higher Plants, Plant Physiol., 1977, vol. 59, pp. 309–314.

    Article  PubMed  CAS  Google Scholar 

  13. Cakmak, I., Erenoglu, B., Gulut, K.Y., Derici, R., and Romheld, V., Light Mediated Release of Phytosiderophores in Wheat and Barley under Iron or Zinc Deficiency, Plant Soil, 1998, vol. 202, pp. 309–315.

    Article  CAS  Google Scholar 

  14. Nakano, Y. and Asada, K., Purification of Ascorbate Peroxidase in Spinach Chloroplasts; Its Inactivation in Ascorbate-Depleted Medium and Reactivation by Monodehydroascorbate Radical, Plant Cell Physiol., 1987, vol. 28, pp. 131–140.

    CAS  Google Scholar 

  15. Foyer, C.H. and Halliwell, B., The Presence of Glutathione and Glutathione Reductase in Chloroplasts: A Proposed Role in Ascorbic Acid Metabolism, Planta, 1976, vol. 133, pp. 21–25.

    Article  Google Scholar 

  16. Polle, A., Otter, T., and Seifert, F., Apoplastic Peroxidases and Lignification in Needles of Norway Spruce (Picea abies L.), Plant Physiol., 1994, vol. 106, pp. 53–60.

    PubMed  CAS  Google Scholar 

  17. Livak, K.J. and Schmittgen, T.D., Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method, Methods, 2001, vol. 25, pp. 402–408.

    Article  PubMed  CAS  Google Scholar 

  18. Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z.X., and Yu, J.Q., Reactive Oxygen Species Are Involved in Brassinosteroid-Induced Stress Tolerance in Cucumber, Plant Physiol., 2009, vol. 150, pp. 801–814.

    Article  PubMed  CAS  Google Scholar 

  19. Fukao, T. and Bailey-Serres, J., Plant Responses to Hypoxia — Is Survival a Balancing Act? Trends Plant Sci., 2004, vol. 9, pp. 449–456.

    Article  PubMed  CAS  Google Scholar 

  20. Bai, T.H., Li, C.Y., Ma, F.W., Feng, F.J., and Shu, H.R., Responses of Growth and Antioxidant System to Root-Zone Hypoxia Stress in Two Malus Species, Plant Soil, 2010, vol. 327, pp. 95–105.

    Article  CAS  Google Scholar 

  21. Garnczarska, M. and Bednarski, W., Effect of a Short-Term Hypoxic Treatment Followed by Re-Aeration on Free Radicals Level and Antioxidative Enzymes in Lupine Roots, Plant Physiol. Biochem., 2004, vol. 42, pp. 233–240.

    Article  PubMed  CAS  Google Scholar 

  22. Narayanan, S., Ruma, D., Gitika, B., Sharma, S.K., Pauline, T., Sai, Ram, M., Ilavazhagan, G., Sawhney, R.C., Kumarand, D., and Banerjee, P.K., Antioxidant Activities of Seabuckthorn (Hippophae rhamnoides) during Hypoxia Induced Oxidative Stress in Glial Cells, Mol. Cell Biochem., 2005, vol. 278, pp. 9–14.

    Article  PubMed  CAS  Google Scholar 

  23. Ozden, M., Demirel, U., and Kahraman, A., Effects of Proline on Antioxidant System in Leaves of Grapevine (Vitis vinifera L.) Exposed to Oxidative Stress by H2O2, Sci. Horticult., 2009, vol. 119, pp. 163–168.

    Article  CAS  Google Scholar 

  24. Badiani, M., Dannibale, A., Poalocci, A., Miglietta, F., and Raschi, A., The Antioxidant Status of Soybean (Glycine max Merrill.) Leaves Grown under Natural CO2 Enrichment in the Field, Aust. J. Plant Physiol., 1993, vol. 20, pp. 275–284.

    Article  CAS  Google Scholar 

  25. Laloi, C., Apel, K., and Danon, A., Reactive Oxygen Signaling: The Latest News, Curr. Opin. Plant Biol., 2004, vol. 7, pp. 323–328.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to J. M. Li.

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Li, J.M., Chen, S.C., Liu, A.R. et al. Combined effects of hypoxia and excess Mn2+ on oxidative stress and antioxidant enzymes in tomato seedlings. Russ J Plant Physiol 59, 670–678 (2012). https://doi.org/10.1134/S102144371205010X

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