Skip to main content
SpringerLink
Log in

Effects of exogenous polyamines on nitrate tolerance in cucumber

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

Abstract

Putrescine (Put), spermidine (Spd), and spermine (Spm) are the major polyamines (PAs) in plant, which are not only involved in the regulation of plant developmental and physiological processes, but also play key roles in modulating the defense response of plants to diverse environmental stresses. In this study, Cucumis sativus L. seedlings were cultivated in nutrient solution and sprayed with three kinds of PAs (Put, Spd, and Spm). The effects of PAs were investigated on excess nitrate stress tolerance of C. sativus by measuring growth and nitrogen (N) metabolism parameters. The contents of NO −3- N, NH +4- N, proline and soluble protein in leaves were increased; while plant height, leaf area, shoot fresh and dry weight, root fresh weight were decreased under 140 mM NO −3 treatment for 7 d. In addition, the activities of nitrate reductase (NR), glutamate synthase (GOGAT), and glutamate dehydrogenase (GDH) were significantly inhibited under 140 mM NO −3 treatment for 7 d. With foliar treatment by 1 mM Spd or Spm under stress treatment, the contents of Spm, Put, and Spd in leaves increased significantly, except that Spm content decreased under Spd treatment. The activities of NR, glutamine synthetase (GS), GOGAT and GDH and plant height, leaf area, shoot fresh and dry weights were significantly increased. The contents of proline and soluble protein in leaves were significantly enhanced. In contrast, the accumulation of NO −3- N and NH +4- N were significantly decreased. However, there were minor differences in activities of N metabolism enzymes and the content of osmotic adjustment substances under 1 mM Put treatment. These findings suggest that 1 mM exogenous Spm or Spd could enhance the capacity of N metabolism, promote growth and increase resistance to high concentrations of NO −3 . The ameliorating effect of Spd was the best, and that of Put the worst.

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

Access this article

Log in via an institution

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

Abbreviations

GDH:

glutamate dehydrogenase

GOGAT:

glutamate synthase

GS:

glutamine synthetase

NiR:

nitrite reductase

NR:

nitrate reductase

NRA:

nitrate reductase activity

PAs:

polyamines

Put:

putrescine

Spd:

spermidine

Spm:

spermine

References

  1. Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism, in Advances in Photosynthesis and Respiration, Foyer, C.H. and Noctor, C., Eds., Dordrecht: Springer-Verlag, 2002, vol. 12.

  2. Ju, X.T., Kou, C.L., Christie, P., Dou, Z.X., and Zhang, F.S., Changes in the soil environment from excessive application of fertilizers and manures to two contrasting intensive cropping systems on the North China Plain, Environ. Pollut., 2007, vol. 145, pp. 497–506.

    Article  CAS  PubMed  Google Scholar 

  3. Zhu, J.H., Li, X.L., Christie, P., and Li, J.L., Environmental implications of low nitrogen use efficiency in excessively fertilized hot pepper (Capsicum frutescens L.) cropping systems, Agric. Ecosyst. Environ., 2005, vol. 111, pp. 70–80.

    Article  Google Scholar 

  4. Xue, J.C., Bi, D.Y., Li, J.J., Yin, Y.X., and Wu, Z.H., The factors and methods of physiological barrier in protected cultivation, Soils Fert., 1994, vol. 1, pp. 4–9.

    Google Scholar 

  5. Yang, F.J., Wang, X.F., Wei, M., Ren, Z.Y., and Yan, T., Changes of endogenous polyamines and hormone responsing to stress in cucumber seedling, Plant Nutr. Fert. Sci., 2008, vol. 14, pp. 1129–1136.

    CAS  Google Scholar 

  6. Zhang, G.W., Liu, Z.L., Zhou, J.G., and Zhu, Y.L., Effects of Ca(NO3)2 stress on oxidative damage, antioxidant enzymes activities and polyamine contents in roots of grafted and non-grafted tomato plants, Plant Growth Regul., 2008, vol. 56, pp. 7–19.

    CAS  Google Scholar 

  7. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., Carrasco, P., and Tiburcio, A.F., Polyamines: molecules with regulatory functions in plant abiotic stress tolerance, Planta, 2010, vol. 231, pp. 1237–1249.

    Article  PubMed  Google Scholar 

  8. Paschalidis, K.A. and Roubelakis-Angelakis, K.A., Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/ expansion, and differentiation, Plant Physiol., 2005, vol. 138, pp. 142–152.

    CAS  Google Scholar 

  9. Kasukabe, Y., He, L.X., Nada, K., Misawa, S., Ihara, I., and Tachibana, S., Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress regulated genes in transgenic Arabidopsis thaliana, Plant Cell Physiol., 2004, vol. 45, pp. 712–722.

    Article  CAS  PubMed  Google Scholar 

  10. Duan, J.J., Li, J., Guo, S.R., and Kang, Y.Y., Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity, J. Plant Physiol., 2008, vol. 165, pp. 1620–1635.

    Article  CAS  PubMed  Google Scholar 

  11. Houdusse, F., Zamarreño, A.M., Garnica, M., and García-Mina, J., The importance of nitrate in ameliorating the effects of ammonium and urea nutrition on plant development: the relationships with free polyamines and praline plant concentrations, Funct. Plant Biol., 2005, vol. 32, pp. 1057–1067.

    Article  CAS  Google Scholar 

  12. Touchette, B.W. and Burkholder, J.M., Carbon and nitrogen metabolism in the seagrass, Zostera marina L.: environmental control of enzymes involved in carbon allocation and nitrogen assimilation, J. Exp. Mar. Biol. Ecol., 2007, vol. 350, pp. 216–233.

    CAS  Google Scholar 

  13. Scheible, W.R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., Schindelasch, D., Thimm, O., Udvardi, M.K., and Stitt, M., Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen, Plant Physiol., 2004, vol. 136, pp. 2483–2499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wang, X.H., Wang, X.F., Yang, F.J., Wei, M., Shi, Q.H., Jiao, J., and Liu, Q.X., Effects of exogenous spermine on activities of antioxidant enzymes and photosynthesis in cucumber seedlings under NO3–stress, Plant Nutr. Fert. Sci., 2010, vol. 16, pp. 1020–1026 [in Chinese].

    CAS  Google Scholar 

  15. Papiya, R., Kamala, N., Sen Gupta, D.N., and Bharati, G., Spermidine treatment to rice seedlings NO3− recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars, Plant Sci., 2005, vol. 168, pp. 583–591.

    Article  Google Scholar 

  16. Ndayiragije, A. and Lutts, S., Do exogenous polyamines have an impact on the response of a salt-sensitive rice cultivar to NaCl? J. Plant Physiol., 2006, vol. 163, pp. 506–516.

    Article  CAS  PubMed  Google Scholar 

  17. Suzanne, N.R. and David, M.P., Leaf area predication model for cucumber from linear measurements, Hortic. Sci., 1987, vol. 22, pp. 1264–1266.

    Google Scholar 

  18. Giné, M.F., Bergamin, F.H., Zagatto, E.A.G., and Reis, B.F., Simultaneous determination of nitrate and nitrite by flow injection analysis, Anal. Chim. Acta, 1980, vol. 114, pp. 191–197.

    Article  Google Scholar 

  19. Krom, M.D., Spectrophotometric determination of ammonia: study of a modified Berthelot reaction using salicylate and dichloroisocyanurate, Analyst, 1980, vol. 105, pp. 305–316.

    Article  CAS  Google Scholar 

  20. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  CAS  PubMed  Google Scholar 

  21. Hageman, R.H. and Hucklesby, D.P., Nitrate reduction from higher plants, Methods Enzymol., 1971, vol. 23, pp. 491–503.

    Article  Google Scholar 

  22. Kanamori, T. and Matsumoto, H., Glutamine synthetase from rice plant roots, Arch. Biochem. Biophys., 1972, vol. 152, pp. 404–412.

    Article  CAS  PubMed  Google Scholar 

  23. Groat, R.G. and Vance, C.P., Root nodule enzymes of ammonia assimilation in alfalfa (Medicago sativa L.), Plant Physiol., 1981, vol. 67, pp. 1198–1203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Loulakakis, K.A. and Roubelakis-Angelakis, K.A., Intracellular localization and protein of NADH-glutamate dehydrogenase from Vitis vinifera L.: purification and characterization of the major leaf isoenzyme, J. Exp. Bot., 1990, vol. 41, pp. 1223–1230.

    Article  CAS  Google Scholar 

  25. Hu, X.H., Zhang, Y., Shi, Y., Zhang, Z., Zou, Z.R., Zhang, H., and Zhao, J.Z., Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress, Plant Physiol. Biochem., 2012, vol. 57, pp. 200–209.

    Article  CAS  PubMed  Google Scholar 

  26. Yang, X.Y., Wang, X.F., Wei, M., Hikosaka, S., and Goto, E., Response of ammonia assimilation in cucumber seedlings to nitrate stress, J. Plant Biol., 2010, vol. 53, pp. 173–179.

    Article  CAS  Google Scholar 

  27. Yang, X.Y., Wang, X.F., Wei, M., Hikosaka, S., and Goto, E., Changes in growth and photosynthetic capacity of cucumber seedlings in response to nitrate stress, Braz. J. Plant Physiol., 2009, vol. 21, pp. 309–317.

    Article  Google Scholar 

  28. Lamaze, T., Sentenac, H., and Grignon, C., Orthophosphate relations of root: effects on orthophosphate influx, accumulation and secretion into the xylem, J. Exp. Bot., 1987, vol. 38, pp. 923–934.

    CAS  Google Scholar 

  29. Dominique, L., Pascal, L., and Alain, G., Gene expression of the NO3− transporter NRT1.1 and the nitrate reductase NIA1 is repressed in Arabidopsis roots by NO2–, the product of reduction, Plant Physiol., 2003, vol. 132, pp. 958–967.

    Google Scholar 

  30. Feng, J., Volk, R.J., and Jackson, W.A., Source and magnitude of ammonium generation in maize roots, Plant Physiol., 1998, vol. 118, pp. 835–841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Walch-Liu, P., Neumann, G., Bangerth, F., and Engels, C., Rapid effects of nitrogen form on leaf morphogenesis in tobacco, J. Exp. Bot., 2000, vol. 51, pp. 227–237.

    Article  CAS  PubMed  Google Scholar 

  32. Balal, R.M., Khan, M.M., Shahid, M.A., Mattson, N.S., Abbas, T., Ashfaq, M., Garcia-Sanchez, F., Ghazanfer, U., Gimeno, V., and Iqbal, Z., Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt tolerant and salt sensitive Citrus rootstocks under NaCl stress, J. Am. Soc. Hortic. Sci, 2012, vol. 137, pp. 86–95.

    CAS  Google Scholar 

  33. Minocha, R., Aber, J.D., Long, S., Magill, A.H., and McDowell, W., Foliar polyamine and inorganic ion content in relation to soil and soil solution chemistry in two fertilized forest stands at the Harvard forest, Massachusetts, Plant Soil, 2000, vol. 222, pp. 119–137.

    Article  CAS  Google Scholar 

  34. Shen, W.Y., Nada, K., and Tachibana, S., Involvement of polyamines in the chilling tolerance of cucumber cultivars, Plant Physiol., 2000, vol. 124, pp. 431–439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Horticulture Science and Engineering, Shandong Agricultural University, State Key Laboratory of Crop Biology, Tai’an, China

    X. H. Wang, S. J. Wang, Z. Chen, B. Gong, X. F. Wang, M. Win, Q. H. Shi, Y. Li & F. J. Yang

  2. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Huanghuai Region), Ministry of Agriculture, Tai’an, China

    X. F. Wang, Q. H. Shi & F. J. Yang

Authors
  1. X. H. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. J. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. X. F. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Win
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Q. H. Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Y. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. F. J. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. J. Yang.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X.H., Wang, S.J., Chen, Z. et al. Effects of exogenous polyamines on nitrate tolerance in cucumber. Russ J Plant Physiol 63, 549–557 (2016). https://doi.org/10.1134/S1021443716040166

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443716040166

Keywords

Search

Navigation