Abstract
Pistachio, one of the important tree nuts, is cultivated in arid and semi-arid regions where salinity is the most common abiotic stress encountered by this tree. However, the mechanisms underlying salinity tolerance in this plant are not well understood. In the present study, five 1-year-old pistachio rootstocks (namely Akbari, Badami, Ghazvini, Kale-Ghouchi, and UCB-1) were treated with four saline water regimes (control, 8, 12, and 16 dS m−1) for 100 days. At high salinity level, all rootstocks showed decreased relative water content (RWC), total chlorophyll content (TCHC), and carotenoids in the leaf, while ascorbic acid (AsA) and total soluble proteins (TSP) were reduced in both leaf and root organs. In addition, the total phenolic compounds (TPC), proline, glycine betaine, total soluble carbohydrate (TSC), and H2O2 content increased under salinity stress in all studied rootstocks. Three different ion exclusion strategies were observed in the studied rootstocks: (i) Na+ exclusion in UCB-1, because most of its Na+ is retained in the roots; (ii) Cl− exclusion in Badami, in which most of its Cl− remained in the roots; and (iii) similar concentrations of Na+ and Cl− were observed in the leaves and roots of Ghazvini, Akbari, and Kale-Ghouchi. Transport capacity (ST value) of K+ over Na+ from the roots to the leaves was more observable in UCB-1 and Ghazvini. Overall, the root system cooperated more effectively in UCB-1 and Badami for retaining and detoxifying an excessive amount of Na+ and Cl−. The results presented here provide important inputs to better understand the salt tolerance mechanism in a tree species for developing more salt-tolerant genotypes. Based on the results obtained here, the studied rootstocks from tolerant to susceptible are arranged as follows: UCB-1 > Badami > Ghazvini > Kale-Ghouchi > Akbari.
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Agastian P, Kingsley S, Vivekanandan M (2000) Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes. Photosynthetica 38:287–290
Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K (2009) Salt stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. Biol Plant 53:243–248
Ahmad P, Jhon R (2005) Effect of salt stress on growth and biochemical parameters of Pisum sativum L. (Einfluss von Salzstress auf Wachstum und biochemische Parameter von Pisum sativum L.) Arch Agron Soil Sci 51:665–672
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175
Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D et al (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense system. Front Plant Sci 6:868
Ahmad P, Latef AAA, Hashem A, Abd-Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347
Akram NA, Ashraf M, Al-Qurainy F (2012) Aminolevulinic acid-induced changes in some key physiological attributes and activities of antioxidant enzymes in sunflower (Helianthus annuus L.) plants under saline regimes. Sci Hortic 142:143–148
Aliakbarkhani ST, Akbari M, Hassankhah A, Talaie A, Moghadam MF (2015) Phenotypic and genotypic variation in Iranian pistachios. J Genet Eng Biotechnol 13:235–241
Aliakbarkhani ST, Farajpour M, Asadian AH, Aalifar M, Ahmadi S, Akbari M (2017) Variation of nutrients and antioxidant activity in seed and exocarp layer of some Persian pistachio genotypes. Ann Agric Sci 62:39–44
Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Athar H-u-R, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot 63:224–231
Badran EG, Abogadallah GM, Nada RM, Alla MMN (2015) Role of glycine in improving the ionic and ROS homeostasis during NaCl stress in wheat. Protoplasma 252:835–844
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bettaieb Rebey I, Bourgou S, Rahali FZ, Msaada K, Ksouri R, Marzouk B (2017) Relation between salt tolerance and biochemical changes in cumin (Cuminum cyminum L.) seeds. J Food Drug Anal 25:391–402
Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257
Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494
Chakraborty K, Bose J, Shabala L, Shabala S (2016) Difference in root K+ retention ability and reduced sensitivity of K+-permeable channels to reactive oxygen species confer differential salt tolerance in three Brassica species. J Exp Bot 67:4611–4625
Chartzoulakis K (2005) Salinity and olive: growth, salt tolerance, photosynthesis and yield. Agric Water Manag 78:108–121
FAO (2014) www.faostat.fao.org
Fayez KA, Bazaid SA (2014) Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J Saudi Soc Agric Sci 13:45–55
Ferguson L, Poss J, Grattan S, Grieve C, Wang D, Wilson C, Donovan T, Chao C-T (2002) Pistachio rootstocks influence scion growth and ion relations under salinity and boron stress. J Am Soc Hortic Sci 127:194–199
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431
Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14:296–302
Gil R, Boscaiu M, Lull C, Bautista I, Lidón A, Vicente O (2013) Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct Plant Biol 40:805–818
Guo Q, Meng L, Mao P-C, Tian X-X (2015) Salt tolerance in two tall wheatgrass species is associated with selective capacity for K+ over Na+. Acta Physiol Plant 37:1–9
Hajiboland R, Norouzi F, Poschenrieder C (2014) Growth, physiological, biochemical and ionic responses of pistachio seedlings to mild and high salinity. Trees 28:1065–1078
Hamouda I, Badri M, Mejri M, Cruz C, Siddique K, Hessini K (2015) Salt tolerance of Beta macrocarpa is associated with efficient osmotic adjustment and increased apoplastic water content. Plant Biol 18:369–375
Hichem H, Mounir D, Naceur EA (2009) Differential responses of two maize (Zea mays L.) varieties to salt stress: changes on polyphenols composition of foliage and oxidative damages. Ind Crop Prod 30:144–151
Kamiab F, Talaie A, Khezri M, Javanshah A (2014) Exogenous application of free polyamines enhance salt tolerance of pistachio (Pistacia vera L.) seedlings. Plant Growth Regul 72:257–268
Karimi HR, Nasrolahpour-Moghadam S (2016) Study of sex-related differences in growth indices and eco-physiological parameters of pistachio seedlings (Pistacia vera cv. Badami-Riz-e-Zarand) under salinity stress. Sci Hortic 202:165–172
Katare DP, Nabi G, Azooz M, Aeri V, Ahmad P (2012) Biochemical modifications and enhancement of psoralen content in salt-stressed seedlings of Psoralea corylifolia Linn. J Funct Environ Bot 2:65–74
Kchaou H, Larbi A, Gargouri K, Chaieb M, Morales F, Msallem M (2010) Assessment of tolerance to NaCl salinity of five olive cultivars, based on growth characteristics and Na+ and Cl− exclusion mechanisms. Sci Hortic 124:306–315
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487
Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218
Khoyerdi FF, Shamshiri MH, Estaji A (2016) Changes in some physiological and osmotic parameters of several pistachio genotypes under drought stress. Sci Hortic 198:44–51
Kim H-J, Fonseca JM, Choi J-H, Kubota C, Kwon DY (2008) Salt in irrigation water affects the nutritional and visual properties of romaine lettuce (Lactuca sativa L.) J Agric Food Chem 56:3772–3776
Kordrostami M, Rabiei B, Hassani Kumleh H (2017) Biochemical, physiological and molecular evaluation of rice cultivars differing in salt tolerance at the seedling stage. Physiol Mol Biol Plants 23:529–544
Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251:899–912
Li C, Sun X, Chang C, Jia D, Wei Z, Li C, Ma F (2015) Dopamine alleviates salt-induced stress in Malus hupehensis. Physiol Plant 153:584–602
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy, current protocols in food analytical chemistry, Wiley, New York
Lim J-H, Park K-J, Kim B-K, Jeong J-W, Kim H-J (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem 135:1065–1070
López-Berenguer C, Martínez-Ballesta MadC, Moreno DA, Carvajal M, García-Viguera C (2009) Growing hardier crops for better health: salinity tolerance and the nutritional value of broccoli. J Agric Food Chem 57:572–578
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26
Mukherjee S, Choudhuri M (1985) Implication of hydrogen peroxide–ascorbate system on membrane permeability of water stressed Vigna seedlings. New Phytol 99:355–360
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Navarro JM, Flores P, Garrido C, Martinez V (2006) Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity. Food Chem 96:66–73
Nemati I, Moradi F, Gholizadeh S, Esmaeili MA, Bihamta MR (2011) The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant Soil Environ 57:26–33
Pan Y-Q, Guo H, Wang S-M, Zhao B, Zhang J-L, Ma Q, Yin H-J, Bao A-K (2016) The photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens in response to salinity. Front Plant Sci 7:848
Parida AK, Jha B (2013) Inductive responses of some organic metabolites for osmotic homeostasis in peanut (Arachis hypogaea L.) seedlings during salt stress. Acta Physiol Plant 35:2821–2832
Parida A, Das AB, Das P (2002) NaCl stress causes changes in photosynthetic pigments, proteins, and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J Plant Biol 45:28–36
Petridis A, Therios I, Samouris G, Tananaki C (2012) Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ Exp Bot 79:37–43
Rasool S, Ahmad A, Siddiqi T, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050
Raymond MJ, Smirnoff N (2002) Proline metabolism and transport in maize seedlings at low water potential. Ann Bot 89:813–823
Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073
Saied AS, Keutgen AJ, Noga G (2005) The influence of NaCl salinity on growth, yield and fruit quality of strawberry cvs. ‘Elsanta’and ‘Korona’. Sci Hortic 103:289–303
Sandhu D, Cornacchione MV, Ferreira JF, Suarez DL (2017) Variable salinity responses of 12 alfalfa genotypes and comparative expression analyses of salt-response genes. Sci Rep 7:42958
Sayyad-Amin P, Borzouei A, Jahansooz M-R, Parsaeiyan M (2016) Root biochemical responses of grain and sweet-forage sorghum cultivars under saline conditions at vegetative and reproductive phases. Braz J Bot 39:115–122
Taïbi K, Taïbi F, Ait Abderrahim L, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312
Talebi M, Akbari M, Zamani M, Sayed-Tabatabaei BE (2016) Molecular polymorphism in Pistacia vera L. using non-coding regions of chloroplast DNA. J Genet Eng Biotechnol 14:31–37
Tang J, Camberato JJ, Yu X, Luo N, Bian S, Jiang Y (2013) Growth response, carbohydrate and ion accumulation of diverse perennial ryegrass accessions to increasing salinity. Sci Hortic 154:73–81
Tanou G, Molassiotis A, Diamantidis G (2009) Hydrogen peroxide-and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913
Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na+ and Cl− ions on barley growth under salinity stress. J Exp Bot 62:2189–2203
Tsabarducas V, Chatzistathis T, Therios I, Koukourikou-Petridou M, Tananaki C (2015) Differential tolerance of 3 self-rooted Citrus limon cultivars to NaCl stress. Plant Physiol Biochem 97:196–206
Wang S, Zheng W, Ren J, Zhang C (2002) Selectivity of various types of salt-resistant plants for K+ over Na+. J Arid Environ 52:457–472
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Yin R, Bai T, Ma F, Wang X, Li Y, Yue Z (2010) Physiological responses and relative tolerance by Chinese apple rootstocks to NaCl stress. Sci Hortic 126:247–252
Yu J, Sun L, Fan N, Yang Z, Huang B (2015) Physiological factors involved in positive effects of elevated carbon dioxide concentration on Bermudagrass tolerance to salinity stress. Environ Exp Bot 115:20–27
Yuan G, Wang X, Guo R, Wang Q (2010) Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem 121:1014–1019
Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, Kopka J, Fotopoulos V, Munnik T, Gómez-Cadenas A, Tiburcio AF, Alcázar R (2017) Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant Cell Environ 40:527–542
Zeng C-L, Liu L, Wang B-R, Wu X-M, Zhou Y (2011) Physiological effects of exogenous nitric oxide on Brassica juncea seedlings under NaCl stress. Biol Plant 55:345–348
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Akbari, M., Mahna, N., Ramesh, K. et al. Ion homeostasis, osmoregulation, and physiological changes in the roots and leaves of pistachio rootstocks in response to salinity. Protoplasma 255, 1349–1362 (2018). https://doi.org/10.1007/s00709-018-1235-z
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DOI: https://doi.org/10.1007/s00709-018-1235-z