Effects of Temperature — Heavy Metal Interactions, Antioxidant Enzyme Activity and Gene Expression in Wheat (Triticum aestivum L.) Seedlings


In this study, the effect of heat and chromium (Cr) heavy metal interactions on wheat seedlings (Triticum aestivum L. cv. Ç-1252 and Gun91) was investigated by measuring total chlorophyll and carotenoid levels, catalase (CAT) and ascorbate peroxidase (APX) antioxidant enzyme activities, and MYB73, ERF1 and TaSRG gene expression. Examination of pigment levels demonstrated a decrease in total chlorophyll in both species of wheat under combined heat and heavy metal stress, while the carotenoid levels showed a slight increase. APX activity increased in both species in response to heavy metal stress, but the increase in APX activity in the Gun91 seedlings was higher than that in the Ç-1252 seedlings. CAT activity increased in Gun91 seedlings but decreased in Ç-1252 seedlings. These results showed that Gun91 seedling had higher resistance to Cr and Cr + heat stresses than the Ç-1252 seedling. The quantitative molecular analyses implied that the higher resistance was related to the overexpression of TaMYB73, TaERF1 and TaSRG transcription factors. The increase in the expression levels of these transcription factors was profound under combined Cr and heat stress. This study suggests that TaMYB73, TaERF1 and TaSRG transcription factors regulate Cr and heat stress responsive genes in wheat.


  1. 1.

    Arnon, D. I., Hoagland, D. R. (1940) Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci. 50, 463–485.

    CAS  Google Scholar 

  2. 2.

    Bartels, D. (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance. Trends Plant Sci. 6, 4–286.

    Article  Google Scholar 

  3. 3.

    Çakmak, I. (1994) Activity of ascorbate-dependent H2O2 scavenging enzymes and leaf chlorosis are enhanced in magnesium- and potassium-deficient leaves, but not in phosphorus-deficient leaves. J. Exp. Bot. 45, 1259–1266.

    Article  Google Scholar 

  4. 4.

    Çakmak, I., Marschner, H. (1992) Magnesium defficiency and high-light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 98, 1222–1227.

    Article  Google Scholar 

  5. 5.

    Dash, S., Mohanty, N. (2001) Evaluation of assay for the analysis of thermo tolerance and recovery potentials of seedlings of wheat (Triticum aestivum L.) cultivars. J. Plant Physiol. 158, 1153–1165.

    CAS  Article  Google Scholar 

  6. 6.

    Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., Lepiniec, L. (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573–581.

    CAS  Article  Google Scholar 

  7. 7.

    Food and Agriculture Organization of the United Nations (FAO), (2005) FAO Statistical Databases, http://www.apps.fao.org.

    Google Scholar 

  8. 8.

    Foy, C. D., Chaney, P. L., White, M. C. (1978) The physiology of metal toxicity in plants. Annual Review of Plant Physiol. 29, 551–566.

    Article  Google Scholar 

  9. 9.

    Gibson, L. R., Paulsen, G. M. (1999) Yield components of wheat grown under high temperature stress during reproductive growth. Crop Sci. 39, 1841–1846.

    Article  Google Scholar 

  10. 10.

    He, X., Hou, X., Shen, Y., Huang, Z. (2011) TaSRG, a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis. FEBS Lett. 585, 1231–1237.

    CAS  Article  Google Scholar 

  11. 11.

    He, Y., Li, W., Lv, J., Jia, Y., Wang, M., Xia, G. (2012) Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J. Exp. Bot. 63, 1511–1522.

    CAS  Article  Google Scholar 

  12. 12.

    Kırbağ-Zengin, F., Munzuroğlu, Ö. (2005) The effects of some heavy metals (Ni+2, Co+2, Cr+3, Zn+2) on the amount of chlorophyll and carotenoid in bean (Phaseolus vulgaris L. cv. Strike) seedlings. F.Ü. Fen ve Müh. Bilimleri Dergisi. 17, 164–172. (In Turkish)

    Google Scholar 

  13. 13.

    Klein, M., Geisler, M., Suh, S. J., Kolukisaoglu, H. U., Azevedo, L., Plaza, S., Curtıs, M. D., Richter, A., Weder, B., Schulz, B., Martinoia, E. (2004) Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J. 39, 219–236.

    CAS  Article  Google Scholar 

  14. 14.

    Lee, T. G., Jang, C. S., Kim, J. Y., Kim, D. S., Park, J. H., Kim, D. Y., Seo, Y. W. (2007) A MYB transcription factor (TaMYB1) from wheat roots is expressed during hypoxia iroles in response to the oxygen concentration in root environment and abiotic stresses. Physiol. Plant. 129, 375–385.

    CAS  Article  Google Scholar 

  15. 15.

    Li, D., Zhou, D., Wang, P., Li, L. (2011) Temperature affects cadmium-induced phytotoxicity involved in subcellular cadmium distribution and oxidative stress in wheat roots. Ecotoxicol. Environ. Saf. 74, 2029–2035.

    CAS  Article  Google Scholar 

  16. 16.

    Lichtenthaler, H., Wellburn, A. R. (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 603, 591–593.

    Article  Google Scholar 

  17. 17.

    MacFarlane, G. R., Burchett, M. D. (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the Grey mangrove, Avicennia marina (Forsk.). Vierh. Mar. Pollut. Bull. 42, 233–240.

    CAS  Article  Google Scholar 

  18. 18.

    Öncel, I., Keleş, Y., Üstün, A. S. (2000) Interactive effects of temperature and heavy metal stress on the growth and some biochemical compounds in wheat seedlings. Environ. Poll. 107, 315–320.

    Article  Google Scholar 

  19. 19.

    Panda, S. K., Choudhury, S. (2005) Chromium stress in plants. Braz. J. Plant Physiol. 17, 95–102.

    CAS  Article  Google Scholar 

  20. 20.

    Porra, R. J. (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Res. 73, 149–156.

    CAS  Article  Google Scholar 

  21. 21.

    Ristic, Z., Bukovnik, U., Prasad, P. V. (2007) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Sci. 47, 2067–2073.

    CAS  Article  Google Scholar 

  22. 22.

    Shanker, A. K., Cervantes, C., Loza-Tavera, C., Avudainayagam, S. (2005) Chromium toxicity in plants. Environ. International 31, 739–753.

    CAS  Article  Google Scholar 

  23. 23.

    Shinozaki, K., Yamaguchi-Shinozaki, K. (1996) Molecular responses to drought and cold stress. Curr. Opin. Biotech. 7, 161–167.

    CAS  Article  Google Scholar 

  24. 24.

    Singh, K. B., Foley, R. C., Oñate-Sánchez, L. (2002) Transcription factors in plant defense and stress responses. Current Opin. Plant Biol. 5, 430–436.

    CAS  Article  Google Scholar 

  25. 25.

    Tamura, T., Hara, K., Yamaguchi, Y., Koizumi, N., Sano, H. (2003) Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor-like protein from tobacco pla_ts. Plant Physiology 131, 454–462.

    CAS  Article  Google Scholar 

  26. 26.

    Van Der Mescht, A., De Ronde, J. A., Van Der Merwe, T., Rossouw, F. T. (1998) Changes in free proline concentrations and polyamine levels in potato leaves during drought stress. S. African J. Sci. 94, 347–350.

    Google Scholar 

  27. 27.

    Vassilev, A., Lidon, F. C., Matos, M. C., Ramalho, J. C., Yordanov, I. (2002) Photosynthetic performance and content of some nutrients in cadmium- and copper-treated barley plants. J. Plant Nutr. 25, 2343–2360.

    CAS  Article  Google Scholar 

  28. 28.

    Ward, J. M., Schroder, J. I. (1994) Calcium-activated K+ channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6, 669–683.

    CAS  Article  Google Scholar 

  29. 29.

    Xu, Z. S., Xia, L. Q., Chen, M., Cheng, X. G., Zhang, R. Y., Li, L. C., Ma, Y. Z. (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol. Biol. 65, 719–732.

    CAS  Article  Google Scholar 

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Ergün, N., Özçubukçu, S., Kolukirik, M. et al. Effects of Temperature — Heavy Metal Interactions, Antioxidant Enzyme Activity and Gene Expression in Wheat (Triticum aestivum L.) Seedlings. BIOLOGIA FUTURA 65, 439–450 (2014). https://doi.org/10.1556/ABiol.65.2014.4.8

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  • Heat
  • chromium
  • wheat
  • MYB73
  • ERF1
  • TaSRG
  • antioxidant enzyme