Effects of salt stress on plant water status, leaf gas exchanges and chlorophyll fluorescence of Pistacia atlantica Desf. versus Pistacia vera L.

Paper Details

Research Paper 01/12/2014
Views (230) Download (6)

Effects of salt stress on plant water status, leaf gas exchanges and chlorophyll fluorescence of Pistacia atlantica Desf. versus Pistacia vera L.

Lefi E, Ben Hamed S
Int. J. Agron. Agri. Res.5( 6), 64-77, December 2014.
Certificate: IJAAR 2014 [Generate Certificate]


The productivity of agricultural systems and the ecological distribution of plants are strongly influenced by salinity in arid and semi-arid regions. In this context, two pistachio species, Pistacia vera L. (P. vera) and Pistacia atlantica Desf. (P. atlantica), have been exposed to NaCl (between 0 and 80 mM) to study the effect of salinity on plant water status, chlorophyll fluorescence and leaf gas exchanges. A specific pattern of response to salinity has highlighted different mechanisms of tolerance. Reductions in stomatal conductance (gs), photosynthesis (A) and total chlorophyll content (TCC) are similar to reductions in the relative water content (RWC) for both species and the NaCl treatments. The shape of the multiphasic fluorescence kinetics curves (OJIP) varies according to the severity of stress, indicating an earlier effect upon addition of NaCl for P. vera, but later in P. atlantica. The dynamic functioning of PSII depends on the toxicity by NaCl, altering plant water status, light conversion and CO2 assimilation by the mesophyll. The impact of salinity is clear at J and especially at I and P, which greatly increases for high NaCl concentrations, reflecting a decrease in the photochemical efficiency of PSII and electron transport. The chlorophyll fluorescence in P. atlantica reflects a lower sensitivity to salinity due to the maintenance of higher cell turgor, chlorophyll content and assimilation of CO2 than P. vera, explaining the agricultural practice based on its use as rootstock for P. vera for a better rusticity.


Abbaspour H, Afshari  H, Abdel-Wahhab A. 2012. Influence of salt stress on growth, pigments, soluble sugars and ion accumulation in three pistachio cultivars. Journal of Medicinal Plant Research 6, 2468- 2473.

Abbruzzese G, Beritognolo I, Muleo R, Piazzai M, Sabatti M, Mugnozza GS, Kuzminsky E. 2009. Leaf morphological plasticity and stomatal conductance in three Populus alba L. genotypes subjected to salt stress. Environmental and Experimental Botany 66, 381- 388.

Agastian P, Kingsley SJ, Vivekanandan M. 2000. Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes. Photosynthetica 38, 287- 290.

Amirjani MR. 2010. Effect of salinity stress on growth, mineral composition, proline content, antioxidant enzymes of soybean. American Journal of Plant Physiology 5, 350- 360.

Baker NR. 1991. A possible role for photosystem II in environmental perturbations of photosynthesis. Physiologia Plantarum 81, 563- 570.

Baker NR. 2008. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 659- 668.

Baker NR, Rosenqvist E. 2004. Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. Journal of Experimental Botany 55, 1607- 1621.

Ben Ahmed C, Ben Rouina B, Boukhris M. 2008. Changes in water relations, photosynthetic activity and proline accumulation in one-year-old olive trees (Olea europaea L. cv.Chemlali) in response to NaCl salinity. Acta Physiologiae Plantarum 30, 553- 560.

Benhassaini H, Fetati A, Hocine AM, Belkhodja M. 2012. Effect of salt stress on growth and accumulation of proline and soluble sugars on plantlets of Pistacia atlantica Desf. subsp. atlantica used as rootstocks. Biotechnology. Agronomy. Society and Environment 16, 159- 165.

Brugnoli E, Bjorkman O. 1992. Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. Planta 187, 335- 345.

Chelli-Chaabouni A, Ben Mosbah A, Maalej M, Gargouric K, Gargouri-Bouzid R, Drira N. 2010. In vitro salinity tolerance of two pistachio rootstocks: Pistacia vera L. and P. atlantica Desf. Environmental and Experimental Botany 69, 302- 312.

Clarke JM, MCCAIG TN. 1982. Evaluation of techniques for screening for drought resistance in wheat. Crop Science 22, 503- 506.

Dhanapackiam S, Ilyas MHM. 2010. Effect of salinity on chlorophyll and carbohydrate contents of Sesbania grandi flora seedlings. Indian Journal of Science and Technology 3, 64- 66.

Dodd IC, Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. Journal of Experimental Botany 63, 3415- 3428.

Duarte B, Santos D, Marques JC, Caçador I. 2013. Ecophysiological adaptations of two halophytes to salt stress: Photosynthesis, PS II photochemistry and anti-oxidant feedback. Implications for resilience in climate change. Plant Physiology and Biochemistry 67,178- 188.

Escalante-Pérez M, Lautner S, Nehls U et al. 2009. Salt stress affects xylem differentiation of grey poplar (Populus x canescens ). Planta 229, 299- 309.

Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH. 1994. Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiology 106, 281- 292.

Flowers TJ. 2004. Improving crop salt tolerance. Journal of Experimental Botany 55, 307- 319.

Gijón MC, Gimenez C, Perez-López D, Guerrero J, Couceiro JF, Moriana A. 2010. Rootstock influences the response of pistachio (Pistacia vera L. cv. Kerman) to water stress and rehydration. Scientia Horticulturae 125, 666- 671.

Govindjee, Spilotro P. 2002. An Arabidopsis thaliana mutant, altered in the y-subunit of ATP synthase, has a different pattern of intensity-dependent changes in non photochemical quenching and kinetics of P-to-S fluorescence decay. Functional Plant Biology 29, 425- 434.

Govindjee. 1995. Sixty-three years since Kautsky: chlorophyll a fluorescence. Australian Journal of Plant Physiology 22, 131- 160.

Hernandez JA, Campillo A, Jimenez A, Alacon JJ, Sevilla F. 1999. Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytologist 141, 241- 251.

Jamil M, Rehman S, Jae Lee K, KimM, Kim HS, Rha ES. 2007. Salinity reduced growth ps2 photochemistry and chlorophyll content in radish. Scientia Agricola. (Piracicaba, Braz.) 64, 111- 118.

Jones OP. 1971. Effects of rootstocks and interstock on the xylem sap composition in apple trees: effects of nitrogen, phosphorus and potassium content. Annals of Botany 35, 825- 836.

Kalaji MH, Govindjee, Bosa K, Kościelniak J, Żuk-Gołaszewska K. 2011. Effects of salt stress on Photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany 73, 64- 72.

Kamel M, El-Tayeb MA. 2004. K+/Na+ soil-plant interactions during low salt stress and their role in osmotic adjustment in faba beans. Spanish Journal of Agricultural Research 2, 257- 265.

Karimi S, Rahemi M, Maftoun M, Eshghi and Tavallali V. 2009. Effects of Long-term Salinity on Growth and Performance of Two Pistachio (Pistacia L.) Rootstocks. Australian Journal of Basic and Applied Sciences 3, 1630- 1639.

Kchaou H, Larbib A, Chaieb M, Sagardoy R, Msallem M, Morales F. 2013. Genotypic differentiation in the stomatal response to salinity and contrasting photosynthetic and photoprotection responses in five olive (Olea europaea L.) cultivars. Scientia Horticulturae 160, 129- 138.

Lazár D. 1999. Chlorophyll a fluorescence induction. Biochimica et Biophysica Acta, 1412, 1- 28.

Lu CM, Vonshak A. 1999. Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytologist 141, 231- 239.

Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659- 668.

Mishra  SK,  Subrahmanyam  D,  Singhal  GS. 1991. Interrelationship between salt and light stress on primary processes of photosynthesis. Journal of Plant Physiology 138, 92- 96.

Misra AN, Srivastava A, Strasser RJ. 2001. Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings. Journal of Plant Physiology 158, 1173- 1181.

Morales F, Abadia A, Gomez-Aparis J, Abadia J. 1992. Effects of combined NaCl and CaCl2 salinity on photosynthetic parameters of barley grown in nutrient solution. Physiologia Plantarum 86, 419- 426.

Mousavi A, Lessani H, Babalar M, Talaei AR, Fallahi E. 2008. Influence of salinity on chlorophyll, leaf water potential, total soluble sugars, and mineral nutrients in two young olive cultivars. Journal of Plant Nutrition 31, 1906- 1916.

Munns R, Richard AJ, Lauchli A. 2006. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025- 1043.

Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell and Environment. 25, 239- 250.

Nazarbeygi E, Yazdi HL, Naseri R, Soleimani R. 2011. The effects of different levels of salinity on proline and A, Bchlorophylls in canola. American-Eurasian Journal of Agriculture & Environmental Science 10, 70- 74.

Olien, WC, Lakso AN. 1986. Effect of rootstock on apple (Malus domestica) tree water relations. Physiologia Plantarum.. 67, 421- 430.

Papageorgiou GC, Govindjee. 2004. Chlorophyll a Fluorescence: A Signature of Photosynthesis, Advances in Photosynthesis and Respiration, vol. 19, Springer, Dordrecht, The Netherlands, 818 pp.

Parida AK, Das AB, Mittra B. 2003. Effects of NaCl stress on the structure, pigment complex composition and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts. Photosynthetica 41, 191- 200.

Parida AK, Das AB. 2005. Salt tolerance and salinity effects on plants: A review. Ecotoxicology and Environnemental Safety 60, 324- 349.

Porcel R, Aroca R, Ruiz-Lozano JM. 2012. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agronomy for Sustainable Development 32, 181- 200.

Qiu N, Lu O, Lu C. 2003. Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex central asiatica. New Phytologist 159, 479- 486.

Ranjbar A, Damme PV, Samson R, Lemeur R. 2002. Leaf water status and photosynthetic gas exchange of Pistacia khinjuk and Pistacia mutica exposed to osmotic drought stress. Acta Horticulturae 591, 423- 428.

Sairam RK, Veerabhadra Rao K, Srivastava GC. 2002. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science 163, 1037- 1046.

Shannon MC, Grieve CM, Francois LE. 1994. Whole-plant response to salinity. In: Wilkinson RE, ed. Plant-Environment Interactions. New York, USA: Marcel Dekker, 199- 244.

Stirbet A, Govindjee. 2011. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology 104, 236- 257.

Strasser RJ, Govindjee. 1991. The Fo and the O-J-I-P fluorescence rise in higher plants and algae. In: J.H. Argyroudi-Akoyunoglou, Ed. Regulation of Chloroplast Biogenesis Plenum Press. New York, 423-426.

Strasser RJ, Govindjee. 1992. On the O-J-I-P fluorescence transients in leaves and D1 mutants of Chlamydomonas reinhardtii. In: N. Murata, Ed. Research in Photosynthesis, vol. II, Kluwer Academic Publishers, Dordrecht. The Netherlands, 39- 42.

Tabatabaei SJ. 2006. Effects of salinity and N on the growth, photosynthesis and N status of olive (Olea europaea L.) trees. Scientia Horticulturae. 108, 432- 438.

Tattini M, Traversi ML. 2009. On the mechanism of salt tolerance in olive (Olea europaea L.) under low -or high- Ca2+ supply. Environmental and Experimental Botany 65, 72- 81.

Tattini M, Traversi ML, Castelli S, Biricolti S, Guidi L, Massai R. 2009. Contrasting response mechanisms to root-zone salinity in three co-occurring Mediterranean woody evergreens: A physiological and biochemical study. Functional Plant Biology 36, 551- 563.

Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK. 2011. Additive effects of Na + and Cl ions on barley growth under salinity stress. Journal of Experimental Botany 62, 2189- 2203.

Tavallali V, Rahemi M, Panahi B. 2008. Calcium induces salinity tolerance in pistachio rootstocks. Fruits 63, 285- 296.

Tiwari BS, Bose A, Ghosh B. 1997. Photosynthesis in rice under salt stress. Photosynthetica 34, 303- 306.

Tomaino A, Martorana M, Arcoraci T, Monteleone D, Giovinazzo C, Saija A. 2010. Antioxidatif activity and phenolic profile of pistachio (Pistacia vera L, variety Bronte) seeds and skins. Biochimie 92, 1115- 1122.

Türkan I, Demiral T. 2009. Recent developments in understanding salinity tolerance, uptake of three pecan rootstock cultivars. Agronomie Journal 77, 383- 388.

Wilkinson S. and Davis WJ. 2002. ABA-based chemical signaling: the coordination of responses to stress on plants. Plant Cell and Environnement 25, 195- 210.

Zhu C, Schraut D, Hartung W, Schaffner AR. 2005. Differential responses of maize MIP genes to salt stress and ABA. Journal of Experimental Botany 56, 2971- 2981.

Zorb C, Geilfus CM, Muhling KH, Ludwig-Muller J. 2013. The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. Journal of Plant Physiology 170, 220- 224.

Zorrig W, Attia H, Msilini N, Ouhibi C, Lachaâl M and Ouergh Z. 2013. Photosynthetic behaviour of Arabidopsis thaliana (Pa-1 accession) under salt stress. African journal of biotechnology. 12, 4594-4 602.