Skip to main content
Springer Nature Link
Log in

Overaccumulation of glycine betaine alleviates the negative effects of salt stress in wheat

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

To investigate the physiological mechanisms of glycinebetaine (GB) involved in the improvement of salt tolerance of wheat, three transgenic wheat (Triticum aestivum L.) lines-T1, T4, and T6-and the wild-type (WT) line Shi4185 were used. The transgenic lines were generated by introducing the BADH gene encoding betaine aldehyde dehydrogenase, which was cloned from Atriplex hortensis L. The BADH gene induced overexpression of GB in transgenic lines. Salt stress was induced by adding 200 mM NaCl, and the osmotic adjustment (OA), ion homeostasis, and antioxidant characteristics of wheat plants were observed. Under salt stress, the OA in the transgenic wheat lines was significantly higher than that in WT; this may be attributed to GB itself and/or the GB-induced overaccumulation of other osmolytes, such as free proline, soluble protein, and soluble sugar. Moreover, the transgenic lines could maintain the lower Na+ and Cl− concentrations in their leaves by accumulating these ions in the sheaths in order to protect the leaves from ion toxicity; however, these lines maintained a higher K+ concentration in the leaves since K+ functions as an osmolyte and maintains ion homeostasis in the leaf cells. Furthermore, the in vivo overaccumulated GB could enhance or stabilize the activity of antioxidant enzymes that can scavenge reactive oxygen species (ROS) and mitigate oxidative damage of biomembranes. The experimental results suggest that GB overexpression can enhance the salt tolerance of transgenic plants by regulating ion homeostasis, enhancing OA, and scavenging ROS.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

GB:

glycinebetaine

OA:

osmotic adjustment

POD:

peroxidase

PS:

photosystem

SOD:

superoxide dismutase

WT:

wild type

References

  1. Zhu, J.K., Plant Salt Tolerance, Trends Plant Sci., 2001, vol. 6, pp. 66–71.

    Article  PubMed  CAS  Google Scholar 

  2. Chen, T.H. and Murata, N., Enhancement of Tolerance to Abiotic Stress by Metabolic Engineering of Betaines and Other Compatible Solutes, Curr. Opin. Plant Biol., 2002, vol. 5, pp. 250–257.

    Article  PubMed  CAS  Google Scholar 

  3. Sakamoto, A. and Murata, N., The Role of Glycinebetaine in the Protection of Plants from Stress: Clues from Transgenic Plants, Plant Cell. Environ., 2002, vol. 25, pp. 163–171.

    Article  PubMed  CAS  Google Scholar 

  4. Robinson, S.P. and Jones, G.P., Accumulation of Glycinebetaine in Chloroplast Provides Osmotic Adjustments during Salt Stress, Aust. J. Plant Physiol., 1986, vol. 13, pp. 659–668.

    Article  CAS  Google Scholar 

  5. Rajasekaran, L.R., Kriedemann, P.E., Aspinall, D., and Paleg, L.G., Physiological Significance of Proline and Glycinebetaine: Maintaining Photosynthesis during NaCl Stress in Wheat, Photosynthetica, 1997, vol. 34, pp. 357–366.

    Article  CAS  Google Scholar 

  6. Rhodes, D. and Hanson, A.D., Quaternary Ammonium and Tertiary Sulfonium Compounds in Higher Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1993, vol. 44, pp. 357–384.

    Article  CAS  Google Scholar 

  7. Ma, X.L., Wang, Y.J., Xie, S.L., Wang, C., and Wang, W., Glycinebetaine Application Ameliorates Negative Effects of Drought Stress in Tobacco, Russ. J. Plant Physiol., 2007, vol. 54, pp. 472–479.

    Article  CAS  Google Scholar 

  8. Bates, L.S., Waldren, R.P., and Tear, I.D., Rapid Determination of Free Proline for Water Stress Studies, Plant Soil, 1973, vol. 39, pp. 205–207.

    Article  CAS  Google Scholar 

  9. Tissue, D.T. and Wright, S.J., Effect of Seasonal Water Availability on Phenology and the Annual Shoot Carbohydrate Cycle of Tropical Forest Shrubs, Funct. Ecol., 1995, vol. 9, pp. 518–527.

    Article  Google Scholar 

  10. Bensadoun, A. and Weinstein, D., Assays of Proteins in the Presence of Interfering Materials, Anal. Biochem., 1976, vol. 70, pp. 241–250.

    Article  PubMed  CAS  Google Scholar 

  11. Beauchamp, C. and Fridovich, I., Superoxide Dismutase: Improved Assays and an Assay Applicable to Acrylamide Gels, Anal. Biochem., 1971, vol. 44, pp. 276–287.

    Article  PubMed  CAS  Google Scholar 

  12. Cakmak, I. and Marschner, H., Magnesium Deficiency and High Light Intensity Enhance Activities of Superoxide Dismutase, Ascrobate Peroxidase and Glutathione Reductase in Bean Leaves, Plant Physiol., 1992, vol. 98, pp. 1222–1227.

    Article  PubMed  CAS  Google Scholar 

  13. Prochazkova, D., Sairam, R.K., Srivastava, G.C., and Singh, D.V., Oxidative Stress and Antioxidant Activity as the Basis of Senescence in Maize Leaves, Plant Sci., 2001, vol. 161, pp. 765–771.

    Article  CAS  Google Scholar 

  14. Lima, A.L.S., DaMatta, F.M., Pinheiro, H.A., Totola, M.R., and Loureiro, M.E., Photochemical Responses and Oxidative Stress in Two Clones of Coffea canephora under Water Deficit Conditions, Environ. Exp. Bot., 2002, vol. 47, pp. 239–247.

    Article  CAS  Google Scholar 

  15. Guo, B.H., Zhang, Y.M., Li, H.J., Du, L.Q., Li, Y.X., Zhang, J.S., Chen, S.Y., and Zhu, Z.Q., Transformation of Wheat with a Gene Encoding for the Betaine Aldehyde Dehydrogenase (BADH), Acta Bot. Sinica, 2000, vol. 42, pp. 279–283.

    Google Scholar 

  16. Gorhan, J., Betains in Higher Plants: Biosynthesis and Role in Stress Metabolism, Amino Acids and Their Derivatives in Higher Plants, Wallsgrove, R.M., Ed., Cambridge, UK: Cambridge Univ. Press, 1995, pp. 171–203.

    Google Scholar 

  17. Saneoka, H., Nagasaka, C., Hahn, D.T., Yang, W.J., Premachandra, G.S., Joly, R.J., and Rhodes, D., Salt Tolerance of Glycinebetaine-Deficient and -Containing Maize Lines, Plant Physiol., 1995, vol. 107, pp. 631–638.

    PubMed  CAS  Google Scholar 

  18. Ding, Z.S., Zhang, Y.M., Zhang, G.R., Wen, Z.Y., and Guo, B.H., The Effect of Foreign Betaine Aldehyde Dehydrogenase Gene on the Synthesis of Betaine in Wheat, Acta Agric. Boreali-Sinica, 2003, vol. 18, pp. 40–42.

    Google Scholar 

  19. Kishitani, S., Takanami, T., Suzuki, M., Yokoi, S., Ishitani, M., Alavarez-Nakase, A.M., and Takabe, T., Compatibility of Glycinebetaine in Rice Plants: Evaluation Using Transgenic Rice Plants with a Gene for Peroxisomal Betaine Aldehyde Dehydrogenase from Barley, Plant, Cell Environ., 2000, vol. 23, pp. 107–114.

    Article  CAS  Google Scholar 

  20. Ma, Q.Q., Zou, Q., Li, Y.H., Li, D.Q., and Wang, W., Amelioration of the Water Status and Improvement of the Anti-Oxidant Enzyme Activities by Exogenous Glycinebetaine in Water-Stressed Wheat Seedlings, Acta Agron. Sinica, 2004, vol. 4, pp. 321–328.

    Google Scholar 

  21. Moghaieb, R.E.A., Saneoka, H., and Fujita, K., Effect of Salinity on Osmotic Adjustment, Glycinebetaine Accumulation and the Betaine Aldehyde Dehydrogenase Gene Expression in Two Halophytic Plants, Salicornia europaea and Suaeda maritime, Plant Sci., 2004, vol. 166, pp. 1345–1349.

    Article  CAS  Google Scholar 

  22. Huo, Y.Q., Zhang, Y.M., and Guo, B.H., Effect of the Insertion of Exogenous Gene of Betaine Aldehyde Dehydrogenase (BADH) on Salt and Drought Resistance of Wheat, J. Hebei Agric. Sci., 2003, vol. 7, pp. 1–4.

    Google Scholar 

  23. Munns, R., Genes and Salt Tolerance: Bringing Them Together, New Phytol., 2005, vol. 167, pp. 645–663.

    Article  PubMed  CAS  Google Scholar 

  24. Ottow, E.A., Brinker, M., Teichmann, T., Fritz, E., Kaiser, W., Brosche, M., Kangasjarvi, J., Jiang, X., and Polle, A., Populus euphratica Displays Apoplastic Sodium Accumulation, Osmotic Adjustment by Decreases in Calcium and Soluble Carbohydrates, and Develops Leaf Succulence under Salt Stress, Plant Physiol., 2005, vol. 139, pp. 1762–1772.

    Article  PubMed  CAS  Google Scholar 

  25. Longnecker, D.E., The Influence of High Sodium upon Fruiting and Shedding Boll Characteristics, Fiber Properties and Yields of Two Cotton Species, Soil Sci., 1974, vol. 118, pp. 387–396.

    Article  Google Scholar 

  26. Munns, R., Comparative Physiology of Salt and Water Stress. Plant, Cell Environ., 2002, vol. 25, pp. 239–250.

    Article  CAS  Google Scholar 

  27. Bartoli, C.G., Simontacchi, M., Tambussi, E., Beltrano, J., Montaldi, E., and Puntarulo, S., Drought and Watering-Dependent Oxidative Stress: Effect on Anti-Oxidant Content in Triticum aestivum L. Leaves, Exp. Bot., 1999, vol. 50, pp. 375–383.

    Article  CAS  Google Scholar 

  28. Smirnoff, N. and Cumbes, Q.J., Hydroxyl Radical Scavenging Activity of Compatible Solutes, Photochemistry, 1989, vol. 28, pp. 1057–1060.

    Article  CAS  Google Scholar 

  29. Luo, Y., Li, W.M., and Wang, W., Trehalose: Protector of Antioxidant Enzymes or Reactive Oxygen Species Scavenger under Heat Stress? Environ. Exp. Bot., 2008, vol. 63, pp. 378–384.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, College of Life Science, Shandong Agricultural University, Tai’an, Shandong, 271018, China

    C. Liang, X. Y. Zhang, Y. Luo, G. P. Wang, Q. Zou & W. Wang

  2. Agricultural Institute of Xintai City, Xintai, Shandong, 271200, China

    C. Liang

Authors
  1. C. Liang
    View author publications

    Search author on:PubMed Google Scholar

  2. X. Y. Zhang
    View author publications

    Search author on:PubMed Google Scholar

  3. Y. Luo
    View author publications

    Search author on:PubMed Google Scholar

  4. G. P. Wang
    View author publications

    Search author on:PubMed Google Scholar

  5. Q. Zou
    View author publications

    Search author on:PubMed Google Scholar

  6. W. Wang
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to C. Liang.

Additional information

Published in Russian in Fiziologiya Rastenii, 2009, vol. 56, No. 3, pp. 410–417.

This text was submitted by the authors in English.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liang, C., Zhang, X.Y., Luo, Y. et al. Overaccumulation of glycine betaine alleviates the negative effects of salt stress in wheat. Russ J Plant Physiol 56, 370–376 (2009). https://doi.org/10.1134/S1021443709030108

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443709030108

Key words