Skip to main content
Log in

Growth, physiological, biochemical and ionic responses of pistachio seedlings to mild and high salinity

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Depending on salt concentrations, different mechanisms are involved in the tolerance of pistachio and an acclimation to salinity conditions occurs in the leaves that develop in the presence of salt.

Abstract

Pistachio (Pistacia vera L.) is a salt tolerant species that is considered an alternative crop for cultivation in salinzied orchard soils. In this work, 12-week-old pistachio seedlings cultivated in soil under greenhouse conditions were treated with five levels of salinity including control (0.63 dSm−1), low (2 and 4 dSm−1) and high (8 and 10 dSm−1) salt concentrations for further 12 weeks. Plant growth parameters were not affected by mild salinity; a significant reduction was only observed from 8 dSm−1. Considerable differences were observed between the young and mature leaves regarding osmotic and ionic stress effects of salt. Main compatible solutes were proline in mature leaves, proline and soluble sugars in young leaves, and soluble sugars and amino acids, other than proline, in roots. Concentration and content of Na in the leaves were not significantly increased at low levels of salinity and the K:Na and Ca:Na ratio of leaves were affected only by higher salt concentrations. Using the sequential extraction procedure for cell wall isolation, we observed that both absolute and relative amounts of Na in the cell wall fraction increased under low salinity, while decreased under higher levels of salt supply. Stable water relations, photochemistry and CO2 assimilation rates particularly of young leaves, as well as ion homeostasis were mechanisms for maintenance of plants growth under mild salinity. Under severe saline conditions, the impaired ability of mature leaves for synthesis of assimilates, preferent allocation of carbohydrates to roots for maintenance of osmotic homeostasis and finally, reduction of protein synthesis caused growth inhibition in pistachio.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Banakar MH, Ranjbar GH (2010) Evaluation of salt tolerance of pistachio cultivars at seedling stage. Am-Eurasian J Agric Environ Sci 9:115–120

    Google Scholar 

  • Bastam N, Baninasab B, Ghobadi C (2013) Improving salt tolerance by exogenous application of salicylic acid in seedlings of pistachio. Plant Growth Regul 69:275–284

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendia AM, Massart A, Poschenrieder C, Hariadi Y, Shabala S (2014) Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. Plant Cell Environ 37:589–600

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitative titration of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cabot C, Sibole JV, Barceló J, Poschenrieder C (2009) Sodium-calcium interactions with growth, water, and photosynthetic parameters in salt-stressed beans. J Plant Nutr Soil Sci 172:637–643

    Article  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chelli-Chaabouni A, Ben Mosbah A, Maalej M, Gargouri K, Gargouri-Bouzid R, Drira N (2010) In vitro salinity tolerance of two pistachio rootstocks: pistacia vera L. and P. atlantica Desf. Environ Exp Bot 69:302–312

    Article  CAS  Google Scholar 

  • Eimanifar A, Mohebbi F (2007) Urmia Lake (Northwest Iran): a brief review. Saline Syst 3:5. doi:10.1186/1746-1448-3-5

    Article  PubMed Central  PubMed  Google Scholar 

  • FAO (2012) http://faostat3.fao.org/faostat-gateway/go/to/download/Q/QC/E

  • FAO (2013) http://faostat3.fao.org/faostat-gateway/go/to/download/RL/*/E

  • FAO-Iran (2013) http://www.fao.org/countryprofiles/index/en/?iso3=IRN

  • Ferguson L, Poss JA, Grattan SR, Grieve CM, Wang D, Wilson C, Donovan TJ, Chao CT (2002) Pistachio rootstocks influence scion growth and ion relations under salinity and boron stress. J Am Soc Hortic Sci 127:194–199

    CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA, Yeo AR (1991) Ion accumulation in the cell walls of rice plants growing under saline conditions: evidence for Oertli hypothesis. Plant Cell Environ 14:319–325

    Article  Google Scholar 

  • Hajiboland R, Bastani S (2012) Tolerance to water stress in boron-deficient tea (Camellia sinensis) plants. Folia Hort 24:41–51

    Google Scholar 

  • Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Stat Circular 347:25–32

    Google Scholar 

  • Hwang M, Ederer GM (1975) Rapid hippurate hydrolysis method for presumptive identification of group B streptococci. J Clin Microbiol 1:114–115

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karimi HR, Ebadi A, Zamani Z, Fatahi R (2011) Effects of water salinity on growth indices and physiological parameters in some pistachio rootstocks. J Plant Nutr 34:935–944

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23

    Article  CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • Longstreth DJ, Nobel PS (1979) Salinity effects on leaf anatomy consequences for photosynthesis. Plant Physiol 63:700–703

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Magné C, Saladin G, Clément C (2006) Transient effect of the herbicide flazasulfuron on carbohydrate physiology in Vitis vinifera. Chemosphere 62:650–657

    Article  PubMed  Google Scholar 

  • Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Munns R (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ 16:15–24

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nooghi FH, Mozafari V (2012) Effects of calcium on eliminating the negative effects of salinity in pistachio (Pistacia vera L.) seedlings. Aust J Crop Sci 6(4):711–716

    Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400

    Article  CAS  PubMed  Google Scholar 

  • Pons TL, Jordi W, Kuiper D (2001) Acclimation of plants to light gradients in leaf canopies: evidence for a possible role for cytokinins transported in the transpiration stream. J Exp Bot 52:1563–1574

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues CRF, Silva EN, Ferreira-Silva SL, Voigt EL, Viégas RA, Silveira JAG (2013) High K+ supply avoids Na+ toxicity and improves photosynthesis by allowing favorable K+:Na+ ratios through the inhibition of Na+ uptake and transport to the shoots of Jatropha curcas plants. J Plant Nutr Soil Sci 176:157–164

    Article  CAS  Google Scholar 

  • Saqib M, Zörb C, Schubert S (2008) Silicon-mediated improvement in the salt resistance of wheat (Triticum aestivum) results from increased sodium exclusion and resistance to oxidative stress. Funct Plant Biol 35:633–639

    Article  CAS  Google Scholar 

  • Shannon MC, Grieve CM, Francois LE (1994) Whole-plant response to salinity. In: Wilkinson RE (ed) Plant-environment interactions. Marcel Dekker Inc, New York, pp 199–244

    Google Scholar 

  • Sheibani A (1994) Pistachio production in Iran. Acta Hort 419:14–15

    Google Scholar 

  • Shomer I, Novacky AJ, Pike SM, Yermiyahu U, Kinraide TM (2003) Electrical potentials of plant cell walls in response to the ionic environment. Plant Physiol 133:411–422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sibole OV, Cabot C, Michalke W, Poschenrieder C, Barceló J (2005) Relationship between expression of the PM H+-ATPase, growth and ion partitioning in the leaves of salt-treated Medicago species. Planta 221:557–566

    Article  CAS  PubMed  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid L. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Tattini M, Lombardini L, Gucci R (1997) The effect of NaCl stress and relief on gas exchange properties of two olive cultivars differing in tolerance to salinity. Plant Soil 197:87–93

    Article  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • Thiele A, Winter K, Krause HG (1997) Low inactivation of D1 protein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress. J Plant Physiol 151:286–292

    Article  CAS  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

  • Zohary D (1995) The genus Pistacia L. In: S. Padulosi, T. Caruso E. Barone (eds) Taxonomy, distribution, conservation and uses of Pistacia genetic resources. International Plant Genetic Resources Institute (IPGRI), Rome, p 145

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roghieh Hajiboland.

Additional information

Communicated by U. Luettge.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hajiboland, R., Norouzi, F. & Poschenrieder, C. Growth, physiological, biochemical and ionic responses of pistachio seedlings to mild and high salinity. Trees 28, 1065–1078 (2014). https://doi.org/10.1007/s00468-014-1018-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1018-x

Keywords

Navigation