Plant Growth Regulation

, Volume 72, Issue 3, pp 257–268 | Cite as

Exogenous application of free polyamines enhance salt tolerance of pistachio (Pistacia vera L.) seedlings

  • Fereshteh Kamiab
  • Alireza Talaie
  • Masood Khezri
  • Amanallah Javanshah
Original paper


The protective effects of free polyamines (PAs) against salinity stress were investigated for pistachio seedlings (Pistacia vera cv. Badami-Zarand) in a controlled greenhouse. Seedlings were treated with 25, 50, 100 and 150 mM of salts including NaCl, CaCl2 and MgCl2. Foliar treatments of putrescine, spermidine (Spd) and spermine (Spm) (0.1 and 1 mM) were applied during the salinity period. Results showed that growth characteristics of pistachio seedlings decreased under salinity stress and the application of PAs efficiently reduced the adverse effects of salt stress. PAs reduced the severe effects of salt stress in pistachio seedlings neither by increasing the activities of peroxidase and ascorbate peroxidase nor by increasing the proline content but by increasing the activities of superoxide dismutase and catalase and decreasing the hydrogen peroxide (H2O2) activity. PAs treated seedlings showed a lower Na+:K+ ratio and Cl in leaves suggesting the role of PAs in balancing the ion exchange and better Na+:K+ discrimination under salt stress condition. These results showed the promising potential use of PAs especially Spm and Spd for reducing the negative effects of salinity stress and improving the growth of pistachio seedlings.


Putrescine Spermidine Spermine Antioxidant enzymes Na+:K+ ratio 



Ascorbate peroxidase




Hydrogen peroxide








Reactive oxygen species


Sodium adsorption ratio


Superoxide dismutase







The authors would like to thank Dr. Zahra Pakkish and Dr. Mehdi Sarcheshmehpour for their guidance on enzyme assays and salt treatments.


  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  2. Alkhani H, Ghorbani M (1992) A contribution to the halophytic vegetation and flora of Iran. In: Lieth H, Al Masoom A (eds) Towards the rational use of high salinity tolerant plants. Kluwer, Dordrecht, pp 35–44Google Scholar
  3. Amri E, Mirzaei M, Moradi M, Zare K (2011) The effect of spermidin and putrescine polyamine on growth of pomegranate (Punica granatum) in salinity circumstance. Int J Plant Physiol Biochem 3:43–49Google Scholar
  4. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  5. Bastam N, Baninasab B, Ghobadi C (2013) Improving salt tolerance by exogenous application of salicylic acid in seedlings of pistachio. Plant Growth Regul 69:275–284CrossRefGoogle Scholar
  6. Bates L, Waldren PP, Teare JD (1973) Rapid determination of the free proline of water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Becana M, Dalton DA, Moran JF, Iturbe OI, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidant in legume nodules. Physiol Plant 109:372–381CrossRefGoogle Scholar
  8. Bors W, Langebartels C, Michel C, Sandermann H (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28:1589–1595CrossRefGoogle Scholar
  9. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  10. Bradford MN (1979) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  11. Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose AS, Engupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. J Plant Physiol 116:192–199CrossRefGoogle Scholar
  13. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annal Bot 103:551–560CrossRefGoogle Scholar
  14. Das S, Bose A, Gosh B (1995) Effect of salt stress on polyamine metabolism in Brassica compestris. Photochemistry 39:283–285CrossRefGoogle Scholar
  15. De Pascale S, Maggio A, Barbieri G, Ruggiero C (2003) Physiological response of pepper (Capsicum annuum L.) to salinity and drought. J Am Soc Hortic Sci 128:48–54Google Scholar
  16. Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus-the protective role of polyamines. BBA-Bioenergetics 1767:272–280PubMedCrossRefGoogle Scholar
  17. Dionisio-Sesc LM, Tobita S (1998) Antioxidant response of rice seedling to salinity stress. Plant Sci 35:1–9CrossRefGoogle Scholar
  18. Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635PubMedCrossRefGoogle Scholar
  19. Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to a biotic stress. Bot Acta 110:197–207CrossRefGoogle Scholar
  20. Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I Occurrence in higher plants. Plant Physiol 59:309–314PubMedCentralPubMedCrossRefGoogle Scholar
  21. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  22. Hedge JE, Hofreiter BT (1962) Estimation of starch by anthrone reagent. In: Whistler RL, Be-Miller JN (eds) Methods in carbohydrate chemistry. Academic Press, New YorkGoogle Scholar
  23. Janicka-Russak ML, Kabala KK, Mlodzinska E, Klobus G (2010) The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. J Plant Physiol 167:261–269PubMedCrossRefGoogle Scholar
  24. Kara M, Mishra D (1976) Catalase, peroxidase, polyphenoloxidase activities during since leaf senescence. Plant Physiol 54:315–319CrossRefGoogle Scholar
  25. Karimi S, Rahemi M, Maftoun M, Tavallali V (2009) Effects of long-term salinity on growth and performance of two pistachio (Pistacia vera L.) rootstocks. Aust J Basic Appl Sci 3:1630–1639Google Scholar
  26. Khezri M, Talaie A, Javanshah A, Hadavi F (2010) Effect of exogenous application of free polyamines on physiological disorders and yield of ‘Kaleh-Ghoochi’ pistachio shoots (Pistacia vera L.). Sci Hortic 125:270–276CrossRefGoogle Scholar
  27. Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155CrossRefGoogle Scholar
  28. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–369PubMedCrossRefGoogle Scholar
  29. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate–peroxidase in spinach chloroplast. Plant Cell Physiol 22:867–880Google Scholar
  30. Neumann P (1997) Salinity resistance and plant growth revisited. Plant Cell Environ 20:1193–1198CrossRefGoogle Scholar
  31. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  32. Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species. Plant Physiol Biochem 40:141–150CrossRefGoogle Scholar
  33. Rhoades JD (1982) Soluble salts. In: Page AL (ed) Methods of soil analysis, 2nd edn. ASA, Madison, pp 167–178Google Scholar
  34. Sepaskhah AR, Maftoun M (1988) Relative salt tolerance of pistachio cultivars. J Hortic Sci 63:157–162Google Scholar
  35. Sharma P, Dubey RS (2010) Protein synthesis by plants under stressful conditions. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press, Boca Raton, pp 465–518CrossRefGoogle Scholar
  36. Smogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–29PubMedGoogle Scholar
  37. Tang W, Newton RJ (2005) Polyamines reduce salt-induced-oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43CrossRefGoogle Scholar
  38. Tavallali V, Rahemi M, Eshghi S, Kholdebarin B, Ramezanian A (2010) Zinc alleviates salt stress and increases antioxidant enzyme activity in the leaves of pistachio (Pistacia vera L.) seedlings. Turk J Agri 34:349–359Google Scholar
  39. Upchurch RG (2008) Fatty acid unsaturation, mobilization and regulation in response of stress to plants. Biotechnol Lett 30:967–977PubMedCrossRefGoogle Scholar
  40. Velikova V, Yordancv I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Sci 151:59–66CrossRefGoogle Scholar
  41. Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 62:669–677CrossRefGoogle Scholar
  42. Williams S, Twine N (1960) Flame photometric method for sodium, potassium and calcium in modern methods of plant analysis. In: Peach K, Tracey MV (eds). Springer, BerlinGoogle Scholar
  43. Yildirim E, Karlidag H, Turan M (2009) Mitigation of salt stress in strawberry by foliar K, Ca and Mg nutrient supply. Plant Soil Environ 55:213–221Google Scholar
  44. Zhu JK (2001) Plant salt tolerance. Trend Plant Sci 6:66–71CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Fereshteh Kamiab
    • 1
  • Alireza Talaie
    • 2
  • Masood Khezri
    • 3
  • Amanallah Javanshah
    • 4
  1. 1.Department of Horticulture, Rafsanjan BranchIslamic Azad UniversityRafsanjanIran
  2. 2.Department of Horticulture, University College of Agriculture and Natural ResourcesUniversity of TehranKarajIran
  3. 3.Horticultural Research InstituteShahid Bahonar University of KermanKermanIran
  4. 4.Iran’s Pistachio Research InstituteRafsanjanIran

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