Abstract
In this study, the effects of 0.5 mM Salicylic Acid (SA) applied through the rooting medium or foliar spray (denoted SA/R and SA/F, respectively) were evaluated on the growth characteristics, nutritional behavior and some key biochemical parameters (total chlorophyll, soluble proteins, total carbohydrates, proline and lipid peroxidation) of Medicago sativa cv. Gabes plants grown in the presence of 100 mM NaCl. The exposure of alfalfa plants to salt stress conditions resulted in a reduced growth rates, associated with significant decreases in water, total chlorophyll, soluble proteins, total carbohydrates and potassium contents. However, sodium and malondialdehyde concentrations were markedly increased in salt-stressed compared to control plants. Both methods of SA application improved plant growth and increased all parameters that were reduced by NaCl treatment. Nevertheless, the mitigating effects exerted by the exogenous SA were more prominent with the SA/F method. As compared to those of salt-stressed plants, shoot and root biomass production and water contents were significantly increased with the SA/F than the SA/R method. Contrarily to the SA/R method, application of SA/F to salt-stressed alfalfa plants restored their total leaf chlorophyll content to the level of control plants. In addition, SA/F application was accompanied by a noteworthy increase in leaf and root potassium contents as compared to the SA/R method; whereas sodium contents were significantly lower in the both plant organs. As compared to salt-stressed plants, total leaf carbohydrates and proline contents were increased by 26 and 120% as well as 54 and 300% due to application of SA/R and SA/F, respectively. Similarly, total root carbohydrates and proline contents were increased by 29 and 140% as well as 93 and 350% with the SA/R and SA/F method, respectively, reflecting a higher osmotic adjustment with this latter method of SA application. Leaf MDA content was not affected by the SA/R treatment and was decreased by 33% relative to salt-stressed plants by the SA/F treatment. Likewise, root MDA content was reduced by 27 and 42% with the SA/R and SA/F method, respectively, indicating a noticeable mitigation of the salt stress-induced cell membrane damage with the SA/F method. Taken together, the findings of the present work indicate that the method of SA application is a significant factor regarding the SA ameliorating effects on salinity stress, with the SA/F being much more efficient in improving the growth of alfalfa plants in saline areas than the SA/R method.
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References
Aazami MA, Rasouli F, Ebrahimzadeh A (2021) Oxidative damage, antioxidant mechanism and gene expression in tomato responding to salinity stress under in vitro conditions and application of iron and zinc oxide nanoparticles on callus induction and plant regeneration. BMC Plant Biol 21:597. https://doi.org/10.1186/s12870-021-03379-7
Abd-Elgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:276. https://doi.org/10.3389/fpls.2016.00276
Abdi N, Van Biljon A, Steyn C, Labuschagne MT (2022) Salicylic acid improves growth and physiological attributes and salt tolerance differentially in two bread wheat cultivars. Plants 11:1853. https://doi.org/10.3390/plants11141853
Ahmad P, Jaleel CA, Sharma S (2010) Antioxidant defense system, lipid peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Rus J Plant Physiol 57:509–517. https://doi.org/10.1134/S1021443710040084
Al-Farsi SM, Nawaz A, Rehman AU, Nadaf SK et al (2020) Effects, tolerance mechanisms and management of salt stress in lucerne (Medicago sativa). Crop Pasture Sci 71:411–428. https://doi.org/10.1071/CP20033
Ardebili NO, Saadatmand S, Niknam V, Khavari-Nejad RA (2014) The alleviating effects of selenium and salicylic acid in salinity exposed soybean. Acta Physiol Plant 36:3199–3205. https://doi.org/10.1007/s11738-014-1686-6
Ashraf M, Arfan M (2005) Gas exchange characteristics and water relations in two cultivars of Hibiscus esculentus under waterlogging. Biol Plant 49:459–462. https://doi.org/10.1007/s10535-005-0029-2
Ashrafi E, Razmjoo J, Zahedi M (2018) Effect of salt stress on growth and ion accumulation of alfalfa (Medicago sativa L.) cultivars. J Plant Nutr 41:818–831. https://doi.org/10.1080/01904167.2018.1426017
Barkosky RR, Einhellig FA (1993) Effects of salicylic acid on plant-water relationships. J Chem Ecol 19:237–247. https://doi.org/10.1007/BF00993692
Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Ben-Laouane R, Meddich A, Bechtaoui N, Oufdou K, Wahbi S (2019) Effects of arbuscular mycorrhizal fungi and rhizobia symbiosis on the tolerance of Medicago sativa L. to salt stress. Gesunde Pflanz 71:135–146. https://doi.org/10.1007/s10343-019-00461-x
Ben-Laouane R, Baslam M, Ait-El-Mokhtar M et al (2020) Potential of native arbuscular mycorrhizal fungi, rhizobia, and/or green compost as alfalfa (Medicago sativa) enhancers under salinity. Microorganisms 8:1695. https://doi.org/10.3390/microorganisms8111695
Bernstein N (2019) Plants and salt: plant response and adaptations to salinity. Model ecosys extrem environ. Academic Press, Cambridge, pp 101–112
Bhattarai S, Biswas D, Fu YB, Biligetu B (2020) Morphological, physiological, and genetic responses to salt stress in alfalfa: a review. Agronomy 10:577–592. https://doi.org/10.3390/agronomy10040577
Bonnemain JL, Chollet JF, Rocher F (2013) Transport of salicylic acid and related compounds. In: Hayat S, Ahmad A, Alyemini MN (eds) Efficiency of salicylic acid application on postharvest perishable crops. Springer, Dordrecht, pp 43–59
Bouallegue A, Souissi F, Nouairi I, Souibgui M, Abbes Z, Mhadhbi H (2017) Salicylic acid and hydrogen peroxide pretreatments alleviate salt stress in faba bean (Vicia faba) seeds during germination. Seed Sci Technol 45:675–690. https://doi.org/10.15258/sst.2017.45.3.07
Bouallegue A, Souissi F, Nouairi I, Souibgui M, Abbes Z, Mhadhbi H (2019) Physiological and biochemicals mechanisms modulated by seeds priming of lentil (Lens culinaris L) under salt stress at germination stage. Acta Sci Polon Hort Cult 18:27–38. https://doi.org/10.24326/asphc.2019.5.3
Boughanmi N, Michonneau P, Verdus MC, Piton F, Ferjani E, Bizid E, Fleurat-Lessard P (2003) Structural changes induced by NaCl in companion and transfer cells of Medicago sativa blades. Protoplasma 220:179–187. https://doi.org/10.1007/s00709-002-0043-6
Boughanmi N, Michonneau P, Daghfous D, Fleurat-Lessard P (2005) Adaptation of Medicago sativa cv. Gabès to long-term NaCl stress. J Plant Nutr Soil Sci 168:262–268. https://doi.org/10.1002/jpln.200420439
Bradford MM (1976) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brahim N, Karbout N, Dhaouadi L, Bouajila A (2021) Global landscape of organic carbon and total nitrogen in the soils of oasis ecosystems in Southern Tunisia. Agronomy 11:1903. https://doi.org/10.3390/agronomy11101903
Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822. https://doi.org/10.1111/j.1365-313X.2004.02086.x
Cornacchione MV, Suarez DL (2017) Evaluation of alfalfa (Medicago sativa L.) populations’ response to salinity stress. Crop Sci 57:137–150. https://doi.org/10.2135/cropsci2016.05.0371
Dasgan HY, Aktas H, Abak K, Cakmak I (2002) Determination of screening techniques to salinity tolerance in tomatoes and investigation of genotype responses. Plant Sci 163:695–703. https://doi.org/10.1016/S0168-9452(02)00091-2
Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591. https://doi.org/10.1074/jbc.M103081200
El-Moukhtari A, Cabassa-Hourton C, Farissi M, Savouré A (2020) How does proline treatment promote salt stress tolerance during crop plant development? Front Plant Sci 11:1127–1143. https://doi.org/10.3389/fpls.2020.01127
El-Taher AM, Abd El-Raouf HS, Osman NA, Azoz SN, Omar MA, Elkelish A, Abd El-Hady MAM (2022) Effect of salt stress and foliar application of salicylic acid on morphological, biochemical, anatomical, and productivity characteristics of cowpea (Vigna unguiculata L.) plants. Plants (Basel) 11:115. https://doi.org/10.3390/plants11010115
El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. J Plant Growth Regul 45:215–224. https://doi.org/10.1007/s10725-005-4928-1
Fahad S, Bano A (2012) Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pak J Bot 44:1433–1438
Fatemi H, Carvajal M, José Rios J (2020) Foliar application of Zn alleviates salt stress symptoms of pakchoi plants by activating water relations and glucosinolate synthesis. Agronomy 10:1528–1549. https://doi.org/10.3390/agronomy10101528
Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyper accumulators. Plant Physiol 137:1082–1091. https://doi.org/10.1104/pp.104.055293
Fu J, Huang B (2001) Involvement of antioxidant and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114. https://doi.org/10.1016/S0098-8472(00)00084-8
Ghaleb W, Ahmed LQ, Escobar-Gutiérrez AJ, Julier B (2021) The history of domestication and selection of lucerne: a new perspective from the genetic diversity for seed germination in response to temperature and scarification. Front Plant Sci 11:578121. https://doi.org/10.3389/fpls.2020.578121
Gharbi E, Martínez JP, Ben Ahmed H, Fauconnier ML, Lutts S, Quinet M (2016) Salicylic acid differently impacts ethylene and polyamine synthesis in the glycophyte Solanum lycopersicum and the wild-related halophyte Solanum chilense exposed to mild salt stress. Physiol Plant 158:152–167. https://doi.org/10.1111/ppl.12458
Gharbi E, Martínez JP, Benahmed H, Hichri I, Dobrev PI, Motyka V, Quinet M, Lutts S (2017) Phytohormone profiling in relation to osmotic adjustment in NaCl-treated plants of the halophyte tomato wild relative species Solanum chilense comparatively to the cultivated glycophyte Solanum lycopersicum. Plant Sci 258:77–89. https://doi.org/10.1016/j.plantsci.2017.02.006
Gharbi E, Lutts S, Dailly H, Quinet M (2018) Comparison between the impacts of two different modes of salicylic acid application on tomato (Solanum lycopersicum) responses to salinity. Plant Signal Behav 13:1–9. https://doi.org/10.1080/15592324.2018.1469361
Gondor OK, Janda T, Soós V, Pál M, Majláth I, Adak MK, Balázs E, Szalai G (2016) Salicylic acid induction of flavonoid biosynthesis pathways in wheat varies by treatment. Front Plant Sci 7:1447. https://doi.org/10.3389/fpls.2016.01447
Guiza M, Benabdelrahim MA, Brini F, Haddad M, Saibi W (2022) Assessment of alfalfa (Medicago sativa L.) cultivars for salt tolerance based on yield, growth, physiological, and biochemical traits. J Plant Growth Regul 41:3117–3126. https://doi.org/10.1007/s00344-021-10499-9
Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736. https://doi.org/10.1016/j.jplph.2005.12.009
Hafsi C, Lakhdhar A, Rabhi M, Debez A, Abdelly C, Ouerghi Z (2007) Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum. J Plant Nutr Soil Sci 170:469–473. https://doi.org/10.1002/jpln.200625203
Hameed A, Ahmed MZ, Hussain T, Aziz I et al (2021) Effects of salinity stress on chloroplast structure and function. Cells 10:2023. https://doi.org/10.3390/cells10082023
Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787. https://doi.org/10.3389/fpls.2016.01787
Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25. https://doi.org/10.1016/j.envexpbot.2009.08.005
Horchani F, Aschi-Smiti S (2010) Prolonged root hypoxia effects on enzymes involved in nitrogen assimilation pathway in tomato plants. Plant Signal Behav 5:1583–1589. https://doi.org/10.4161/psb.5.12.13820
Horchani F, Aloui A, Brouquisse R, Aschi-Smiti S (2008b) Physiological responses of tomato plants (Solanum lycopersicum) as affected by root hypoxia. J Agron Crop Sci 194:297–303. https://doi.org/10.1111/j.1439-037X.2008.00313.x
Horchani F, Gallusci P, Baldet P, Cabasson C, Maucourt M, Rolin D, Aschi-Smiti S, Raymond P (2008a) Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J Plant Physiol 165:1352–1359. https://doi.org/10.1016/j.jplph.2007.10.016
Horchani F, Khayati H, Raymond P, Brouquisse R, Aschi-Smiti S (2009) Contrasted effects of prolonged root hypoxia on tomato (Solanum lycopersicum) roots and fruits metabolism. J Agron Crop Sci 195:313–318. https://doi.org/10.1111/j.1439-037X.2009.00363.x
Horchani F, Hajri R, Khayati H, Brouquisse R, Aschi-Smiti S (2010) Does the source of nitrogen affect the response of subterranean clover to prolonged root hypoxia? J Plant Nutr Soil Sci 173:275–283. https://doi.org/10.1002/jpln.200900280
Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundara R, Panneerselvam R (2009) Drought stress plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105
Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala SS (2015) Salicylic acid in plant salinity stress signaling and tolerance. J Plant Growth Regul 76:25–40. https://doi.org/10.1007/s10725-015-0028-z
Jha U, Bohra A, Jha R, Parida SK (2019) Salinity stress response and ‘omics’ approaches for improving salinity stress tolerance in major grain legumes. Plant Cell Rep 38:255–277. https://doi.org/10.1007/s00299-019-02374-5
Jini D, Joseph B (2017) Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Sci 24:97–108
Kang HM, Saltveit M (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576. https://doi.org/10.1034/j.1399-3054.2002.1150411.x
Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycine betaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khedr AHA, Abbas MA, Abdel Wahid MA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritinum L. to salt stress. J Exp Bot 54:2553–2562. https://doi.org/10.1093/jxb/erg277
Korkmaz A, Uzunlu M, Demirkiran AR (2007) Treatment with acetyl salicylic acid protects muskmelon seedlings against drought stress. Acta Physiol Plant 29:503–508. https://doi.org/10.1007/s11738-007-0060-3
Kováčik J, Gruz J, Backor M, Strnad M, Repcak M (2009) Salicylic acid induced changes to growth and phenolic metabolism in Matricaria chamomilla plants. Plant Cell Rep 28:135–143. https://doi.org/10.1007/s00299-008-0627-5
Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermo-tolerance. Plant Physiol 138:882–897. https://doi.org/10.1104/pp.105.062257
Li T, Hu Y, Du X, Tang H, Shen C, Wu J (2014) Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS One 9:e109492. https://doi.org/10.1371/journal.pone.0109492
Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495:286–291. https://doi.org/10.1016/j.bbrc.2017.11.043
Lutts S, Majerus V, Kinet JM (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105:450–458. https://doi.org/10.1034/j.13993054.1999.105309.x
Ma X, Zheng J, Zhang X, Hu Q, Qian R (2017) Salicylic acid alleviates the adverse effects of salt stress on Dianthus superbus (Caryophyllaceae) by activating photosynthesis, protecting morphological structure, and enhancing the antioxidant system. Front Plant Sci 8:600. https://doi.org/10.3389/fpls.2017.00600
Ma Y, Wei Z, Liu J, Liu X, Liu F (2021) Growth and physiological responses of cotton plants to salt stress. J Agron Crop Sci 207:565–576. https://doi.org/10.1111/jac.12484
Manaa A, Gharbi E, Mimouni H, Wasti S, Aschi-Smiti S, Lutts S, Ben Ahmed H (2014) Simultaneous application of salicylic acid and calcium improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars. S Afr J Bot 95:32–39. https://doi.org/10.1016/j.sajb.2014.07.015
Mc Cready RM, Guggolz J, Silviera V, Owes HS (1950) Determination of starch and amylase in vegetables, application to peas. Anal Chem 22:1156–1158. https://doi.org/10.1021/ac60045a016
Methenni K, Abdallah MB, Nouairi I, Smaoui A, Zarrouk M, Youssef NB (2018) Salicylic acid and calcium pretreatments alleviate the toxic effect of salinity in the Oueslati olive variety. Sci Hortic 233:349–358. https://doi.org/10.1016/j.scienta.2018.01.060
Miao Y, Luo X, Gao X, Wang W, Li B, Ho L (2020) Exogenous salicylic acid alleviates salt stress by improving leaf photosynthesis and root system architecture in cucumber seedlings. Sci Hortic 272:e109577. https://doi.org/10.1016/j.scienta.2020.109577
Mimouni H, Wasti S, Manaa A, Gharbi E, Chalh A, Vandoorne B, Lutts S, Ben Ahmed H (2016) Does salicylic acid (SA) improve tolerance to salt stress in plants? a study of SA effects on tomato plant growth, water dynamics, photosynthesis, and biochemical parameters. OMICS 20:180–190. https://doi.org/10.1089/omi.2015.0161
Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189. https://doi.org/10.1016/j.plantsci.2009.05.007
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. https://doi.org/10.1046/j.0016-8025.2001.00808.x
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nawaz A, Al-Sadi A, Rehman AU, Siddique KHM (2020) Effects, tolerance mechanisms and management of salt tolerance in lucerne (Medicago sativa L.). Crop Pasture Sci 71:411–428. https://doi.org/10.1071/CP20033
Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815. https://doi.org/10.1016/j.jplph.2010.11.001
Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10:e1003751. https://doi.org/10.1080/15592324.2014.1003751
Németh M, Janda T, Horváth E, Páldi E, Szalai G (2002) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci 162:569–574. https://doi.org/10.1016/S0168-9452(01)00593-3
Nie W, Gong B, Chen Y, Wang J, Wei M, Shi Q (2018) Photosynthetic capacity, ion homeostasis and reactive oxygen metabolism were involved in exogenous salicylic acid increasing cucumber seedlings tolerance to alkaline stress. Sci Hortic 235:413–423. https://doi.org/10.1016/j.scienta.2018.03.011
Noreen S, Ashraf M, Akram NA (2012) Does exogenous application of salicylic acid improves growth and some key physiological attributes in sunflower plants subjected to salt stress? J Appl Bot Food Qual 84:169–177
Palma F, López-Gómez M, Tejera NA, Lluch C (2013) Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci 208:75–82. https://doi.org/10.1016/j.plantsci.2013.03.015
Pang CH, Wang B (2008) Oxidative stress and salt tolerance in plants. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany, vol 69. Springer, Berlin, Heidelberg
Poór P, Gémes K, Horváth F, Szepesi A, Simon ML, Tari I (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fxation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol (Stuttg) 13:105–114. https://doi.org/10.1111/j.1438-8677.2010.00344.x
Raeeszadeh M, Beheshtipour J, Jamali R, Akbari A (2022) The antioxidant properties of alfalfa (Medicago sativa L.) and its biochemical, antioxidant, anti-inflammatory, and pathological effects on nicotine-induced oxidative stress in the rat liver. Oxid Med Cell Long. https://doi.org/10.1155/2022/2691577
Rao IM, Miles JW, Beebe SE, Horst WJ (2016) Root adaptations to soils with low fertility and aluminium toxicity. Ann Bot 118:593–605. https://doi.org/10.1093/aob/mcw073
Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: Its role in plant growth and development. J Exp Bot 62:3321–3338. https://doi.org/10.1093/jxb/err031
Sarker U, Oba S (2020) The response of salinity stress-induced a. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. Front Plant Sci 11:559876. https://doi.org/10.3389/fpls.2020.559876
Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322. https://doi.org/10.1016/S0168-9452(02)00415-6
Shao Q, Wang H, Guo H, Zhou A, Huang Y, Sun Y, Li M (2014) Effects of shade treatments on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii. PLoS One 9:e85996. https://doi.org/10.1371/journal.pone.0085996
Shen C, Hu Y, Du XH, Li T, Tang H, Wu J (2014) Salicylic acid induces physiological and biochemical changes in Torreya grandis cv. Merrillii seedlings under drought stress. Trees 28:961–970. https://doi.org/10.1007/s00468-014-1009-y
Shi S, Nan L, Smith KF (2017) The current status, problems, and prospects of alfalfa (Medicago sativa L.) breeding in China. Agronomy 7:1. https://doi.org/10.3390/agronomy7010001
Silva EN, Silveira JAG, Rodrigues CRF, Viégas RA (2015) Physiological adjustment to salt stress in Jatropha curcas is associated with accumulation of salt ions, transport and selectivity of K+, osmotic adjustment and K+/Na+ homeostasis. Plant Biol (Stuttg) 17:1023–1029. https://doi.org/10.1111/plb.12337
Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353. https://doi.org/10.1007/s11738-013-1279-9
Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447. https://doi.org/10.1093/aob/mcu239
Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilization. J Plant Growth Regul 49:77–83. https://doi.org/10.1007/s10725-006-0019-1
Szepesi A, Csiszár J, Gémes K, Horvath E (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. J Plant Physiol 166:914–925. https://doi.org/10.1016/j.jplph.2008.11.012
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. https://doi.org/10.1016/j.sajb.2016.03.011
Torabi M, Halim M (2010) Variation of root and shoot growth and free proline accumulation in Iranian alfalfa ecotypes under salt stress. J Food Agric Environ 8:323–328
Tufail A, Arfan M, Gurmani AR, Khan A, Bano A (2013) Salicylic acid induced salinity tolerance in maize (Zea mays). Pak J Bot 45:75–82
Wang Y, Zhang Z, Zhang P, Cao Y, Hu T, Yang P (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402:247–261. https://doi.org/10.1007/s11104-016-2792-6
Wang Z, Dong S, Teng K, Chang Z, Zhang X (2022) Exogenous salicylic acid optimizes photosynthesis, antioxidant metabolism, and gene expression in perennial ryegrass subjected to salt stress. Agronomy 12:1920. https://doi.org/10.3390/agronomy12081920
Wasti S, Mimouni H, Smiti S, Zid E, Ben Ahmed H (2012) Enhanced salt tolerance of tomatoes by exogenous salicylic acid applied through rooting medium. OMICS 16:200–207. https://doi.org/10.1089/omi.2011.0071
Wintermans J, Mots A (1965) Spectrophotometric characteristic of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta 109:448–453. https://doi.org/10.1016/0926-6585(65)90170-6
Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059. https://doi.org/10.1080/00103628209367332
Xu L, Chen H, Zhang T, Deng Y, Yan J, Wang L (2022) Salicylic acid improves the salt tolerance capacity of Saponaria officinalis by modulating its photosynthetic rate, osmoprotectants, antioxidant levels, and ion homeostasis. Agronomy 12:1443. https://doi.org/10.3390/agronomy12061443
Yassin M, El Sabagh A, Mekawy AM, Islam M et al (2019) Comparative performance of two bread wheat (Triticum aestivum L.) genotypes under salinity stress. Appl Ecol Environ Res 17:5029–5041. https://doi.org/10.15666/aeer/1702_50295041
Zarai B, Walter C, Michot D, Montoroi JP, Hachicha M (2022) Integrating multiple electromagnetic data to map spatiotemporal variability of soil salinity in Kairouan region, Central Tunisia. J Arid Land 14:186–202. https://doi.org/10.1007/s40333-022-0052-6
Zhang M, Liu Y, Han G, Zhang Y, Wang B, Chen M (2021) Salt tolerance mechanisms in trees: research progress. Trees 35:717–730. https://doi.org/10.1007/s00468-020-02060-0
Zhanwu G, Hui Z, Jicai G, Chunwu Y, Chunsheng M, Deli W (2011) Germination responses of Alfalfa (Medicago sativa L.) seeds to various salt-alkaline mixed stress. Afr J Agric Res 6:3793–3803. https://doi.org/10.5897/AJAR11.050
Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021) Regulation of plant responses to salt stress. Int J Mol Sci 22:4609. https://doi.org/10.3390/ijms22094609
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by F. Horchani, L. Mabrouk, M. A. Borgi and Z. Abbes. The first draft of the manuscript was written by F. Horchani and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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F. Horchani, L. Mabrouk, M. A. Borgi and Z. Abbes declare that they have no competing interests.
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Horchani, F., Mabrouk, L., Borgi, M.A. et al. Foliar Spray or Root Application: Which Method of Salicylic Acid Treatment is More Efficient in Alleviating the Adverse Effects of Salt Stress on the Growth of Alfalfa Plants, Medicago sativa L.?. Gesunde Pflanzen 75, 2697–2712 (2023). https://doi.org/10.1007/s10343-023-00867-8
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DOI: https://doi.org/10.1007/s10343-023-00867-8