Ameliorating Effect of Salicylic Acid on Physiological and Biochemical Characteristics of Satureja spicigera (C. Koch) Boiss. under NaCl Stress

Document Type : Original Article

Authors

Department of Biology, Faculty of Science, Bu-Ali Sina University, Hamedan, Iran

Abstract

Creeping savory is a wild plant that is used for comestible consumption, preparation of beverages, and production of sanitary ware and herbal drugs. To investigate the effects of salinity stress and salicylic acid on antioxidant enzymes, photosynthetic pigments, relative water content, proline, and soluble protein content in S. spicigera a factorial experiment was conducted based on a Completely Randomized Design (CRD) and three replications. The experiment was implemented at the greenhouse of Agriculture and Natural Resources Research and Education Center of Kermanshah, Iran (2019). Experimental treatments were four levels of salinity (0-50-100-150 mM NaCl) and two levels of salicylic acid (0 and 2 mM). Results showed that increasing salinity levels caused a significant reduction in relative water content, leaf fresh weight, leaf dry weight, chlorophyll a, chlorophyll b, total chlorophyll, and carotenoid content. Salinity drastically enhanced the antioxidant activities (SOD, POD, and CAT), and cell proline content. Salicylic acid considerably decreased proline content under salt stress conditions, but improved antioxidant activities of SOD, POD, and CAT, and enhanced chlorophyll a, chlorophyll b, total chlorophyll, carotenoid content, protein content, relative water content, and leaf fresh weight under salt stress. Salicylic acid reduced the destructive effect of salinity on some morphological, physiological, and biochemical characteristics in creeping savory.

Graphical Abstract

Ameliorating Effect of Salicylic Acid on Physiological and Biochemical Characteristics of Satureja spicigera (C. Koch) Boiss. under NaCl Stress

Highlights

  • 100 and 150 mM NaCl significantly induced oxidative stress in S. spicigera.
  • 100 and 150 mM NaCl significantly reduced photosynthesis and plant growth.
  • SOD, POD, and CAT activity increased up to 150 mM NaCl.
  • Exogenous 2 mM SA enhanced antioxidant activity, photosynthetic pigments, RWC, protein content, and plant growth under salinity stress.

Keywords

Main Subjects

References

Aazami M.A., Maleki M., Rasouli F., Gohari G. 2023. Protective effects of chitosan based salicylic acid nanocomposite (CS-SA NCs) in grape (Vitis vinifera cv. ‘Sultana’) under salinity stress. Scientific Reports 13(1): 883. https://doi.org/10.1038/s41598-023-27618-z
Abdolmohammadi S., Omidi J. 2017. The effect of salicylic acid on some morphological and physiological traits under salinity stress (Catharanthus roseus). Research in Agriculture 9(3): 28-39. (In Farsi).
Afridi M.S., Mahmood T., Salam A., Mukhtar T., Mehmood S., Ali J., Khatoon Z., Bibi M., Javed M.T., Sultan T., Chaudhary H.J. 2019. Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiology and Biochemistry 139: 569-577. https://doi.org/10.1016/j.plaphy.2019.03.041
Alam P., Balawi T.A., Faizan M. 2022. Salicylic acid's impact on growth, photosynthesis, and antioxidant enzyme activity of Triticum aestivum when exposed to salt. Molecules 28(1): 100. https://doi.org/10.3390/molecules28010100
Andalibi L., Ghorbani A., Moameri M., Hazbavi Z., Nothdurft A., Jafari R., Dadjou F. 2021. Leaf area index variations in ecoregions of Ardabil province, Iran. Remote Sensing 13(15): 2879. https://doi.org/10.3390/rs13152879
Anjum N.A., Gill S.S., Gill R. 2014. Plant adaptation to environmental change: significance of amino acids and their derivatives, CABI. https://doi.org/10.1079/9781780642734.0317
Ashraf M. 2009. Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances 27(1): 84-93. https://doi.org/10.1016/j.biotechadv.2008.09.003
Ashraf M., Harris P.J.C. 2013. Photosynthesis under stressful environments: An overview. Photosynthetica 51(2): 163-190. https://doi.org/10.1007/s11099-013-0021-6
Athar H.U., Zulfiqar F., Moosa A., Ashraf M., Zafar Z.U., Zhang L., Ahmed N., Kalaji H.M., Nafees M., Hossain M.A., Islam M.S. 2022. Salt stress proteins in plants: An overview. Frontiers in Plant Science 13: 999058. https://doi.org/10.3389/fpls.2022.999058
Balti H., Abassi M., Dietz K.J., Kumar V. 2021. Differences in ionic, enzymatic, and photosynthetic features characterize distinct salt tolerance in Eucalyptus Species. Plants 10(7): 1401. https://doi.org/10.3390/plants10071401
Bates L., Waldren R., Teare I. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil 39: 205-207. https://doi.org/10.1007/BF00018060
Beauchamp C., Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry 44(1): 276-287. https://doi.org/10.1016/0003-2697(71)90370-8
Bian S., Jiang Y. 2009. Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae 120(2): 264-270. https://doi.org/10.1016/j.scienta.2008.10.014
Bishnoi S.K., Kumar B., Rani C., Datta K.S., Kumari P., Sheoran I.S., Angrish R. 2006. Changes in protein profile of pigeonpea genotypes in response to NaCl and boron stress. Biologia Plantarum 50: 135-137. https://doi.org/10.1007/s10535-005-0088-4
Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1-2): 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
Chance B., Maehly A.C. 1955. Assay of catalase and peroxidase. Methods in Enzymology 2: 764-775. http://dx.doi.org/10.1016/S0076-6879(55)02300-8
Chowdhury S., Basu A., Kundu S. 2017. Overexpression of a new osmotic-like protein gene (SindOLP) confers tolerance against biotic and abiotic stresses in sesame. Frontiers in Plant Science 8: 410. https://doi.org/10.3389/fpls.2017.00410
Davis P. 1982. Flora of turkey (S. spicigera (C. Koch) Boiss.), Edinburgh University Press, Scotland, UK (pp. 320-321).
Dehestani Ardakani M., Ghatei P., Gholamnezhad J., Momenpour A., Fakharipour Charkhabi Z. 2021. Improving growth and physiological characteristics in salt stressed lantana (Lantana camara Linn.) by application of exogenous salicylic acid. Journal of Agricultural Science and Sustainable Production 31(4): 95-115. (In Farsi). https://doi.org/10.22034/saps.2021.43284.2587
Dong Y.J., Jinc S.S., Liu S., Xu L.L., Kong J. 2014. Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. Journal of Soil Science and Plant Nutrition 14(1): 1-13. http://dx.doi.org/10.4067/S0718-95162014005000001
Dubey S., Bhargava A., Fuentes F., Shukla S., Srivastava S. 2020. Effect of salinity stress on yield and quality parameters in flax (Linum usitatissimum L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca 48(2): 954-966. http://dx.doi.org/10.15835/nbha48211861
Fabriki Ourang S., Mehrabad Pourbenab S. 2016. The effects of drought and salt stresses on some morphological and biochemical parameters of savory (Satureja hortensis L.). Eco-phytochemical Journal of Medical Plants 4(3 (15)): 23-35. SID. https://sid.ir/paper/247790/en
Ghanbari F., Bag-Nazari M., Azizi A. 2023. Exogenous application of selenium and nano-selenium alleviates salt stress and improves secondary metabolites in Lemon verbena under salinity stress. Scientific Reports 13: 5352. https://doi.org/10.1038/s41598-023-32436-4
Harati E., Kashefi B., Matinzadeh M. 2015. Investigation reducing detrimental effects of salt stress on morphological and physiological traits of (Thymus vulgaris) by application of salicylic acid. Iranian Journal of Plant Physiology 5(3): 1383-1391.
Hasanuzzaman M., Fujita M. 2013. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22: 584-596. https://doi.org/10.1007/s10646-013-1050-4
Hasanuzzaman M., Raihan M.R., Masud A.A., Rahman K., Nowroz F., Rahman M., Nahar K., Fujita M. 2021. Regulation of reactive oxygen species and antioxidant defense in plants under salinity. International Journal of Molecular Sciences 22(17): 9326. https://doi.org/10.3390/ijms22179326
Hernández-Adasme C., Palma-Dias R., Escalona V.H. 2023. The effect of light intensity and photoperiod on the yield and antioxidant activity of beet microgreens produced in an indoor system. Horticulturae 9(4): 493. https://doi.org/10.3390/horticulturae9040493
Husen A., Iqbal M., Sohrab S.S., Ansari M.K. 2018. Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agriculture & Food Security 7: 44. https://doi.org/10.1186/s40066-018-0194-0
Jini D., Joseph B. 2017. Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Science 24(2): 97-108. https://doi.org/10.1016/j.rsci.2016.07.007
Kamran M., Xie K., Sun J., Wang D., Shi C., Lu Y., Gu W., Xu P. 2020. Modulation of growth performance and coordinated induction of ascorbate-glutathione and methylglyoxal detoxification systems by salicylic acid mitigates salt toxicity in choysum (Brassica parachinensis L.). Ecotoxicology and Environmental Safety 188: 109877. https://doi.org/10.1016/j.ecoenv.2019.109877
Kaur G., Asthir B. 2015. Proline: a key player in plant abiotic stress tolerance. Biologia Plantarum 59: 609-619. https://doi.org/10.1007/s10535-015-0549-3
Kaya C., Ashraf M., Alyemeni M.N., Corpas F.J., Ahmad P. 2020a. Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by upregulating the ascorbate-glutathione cycle and glyoxalase system. Journal of Hazardous Materials 399: 123020. https://doi.org/10.1016/j.jhazmat.2020.123020
Kaya C., Higgs D., Ashraf M., Alyemeni M.N., Ahmad P. 2020b. Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiologia Plantarum 168(2): 256-277. https://doi.org/10.1111/ppl.12976
Khalvandi M., Siosemardeh A., Roohi E., Keramati S. 2021. Salicylic acid alleviated the effect of drought stress on photosynthetic characteristics and leaf protein patterns in winter wheat. Heliyon 7: e05908. https://doi.org/10.1016/j.heliyon.2021.e05908
Khan M.I.R., Asgher M., Khan N.A. 2014. Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycine betaine and ethylene in mungbean (Vigna radiata L.). Plant Physiology and Biochemistry 80: 67-74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khoshbakht D., Asgharei M. 2015. Influence of foliar-applied salicylic acid on growth, gas-exchange characteristics, and chlorophyll fluorescence in Citrus under saline conditions. Photosynthetica 53: 410-418. https://doi.org/10.1007/s11099-015-0109-2
Kohli S.K., Bali S., Tejpal R., Bhalla V., Verma V., Bhardwaj R., Alqarawi A., Abd_Allah E.F., Ahmad P. 2019. In-situ localization and biochemical analysis of bio-molecules reveals Pb-stress amelioration in Brassica juncea L. by co-application of 24-epibrassinolide and salicylic acid. Scientific Reports 9: 1-15. https://doi.org/10.1038/s41598-019-39712-2
Kumar S., Ahanger M.A., Alshaya H., Latief Jan B., Yerramilli V. 2022. Salicylic acid mitigates salt induced toxicity through the modifications of biochemical attributes and some key antioxidants in capsicum annuum. Saudi Journal of Biological Sciences 29(3): 1337-1347. https://doi.org/10.1016/j.sjbs.2022.01.028
Kwon E.H., Adhikari A., Imran M., Lee D.S., Lee C.Y., Kang S.M., Lee I.J. 2023. Exogenous SA applications alleviate salinity stress via physiological and biochemical changes in St john’s wort plants. Plants 12(2): 310. https://doi.org/10.3390/plants12020310
Lichtenthaler H., Wellburn A.R. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11(5): 591-592. https://doi.org/10.1042/bst0110591
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. Frontiers Plant Science 8: 600. https://doi.org/10.3389/fpls.2017.00600 
Mady E., Abd El-Wahed A.H., Awad A.H., Asar T.O., Al-Farga A., Abd El-Raouf H.S., Randhir R., Alnuzaili E.S., El-Taher A.M., Randhir T.O., Hamada F.A. 2023. Evaluation of salicylic acid effects on growth, biochemical, yield, and anatomical characteristics of eggplant (Solanum melongena L.) plants under salt stress conditions. Agronomy 13(9): 2213. https://doi.org/10.3390/agronomy13092213
Menezes R.V., Azevedo Neto A.D., Oliveira Ribeiro M., Watanabe Cova A.M. 2017. Growth and contents of organic and inorganic solutes in amaranth under salt stress. Agropecuária Tropical Goiania 47(1): 22-30. https://doi.org/10.1590/1983-40632016v4742580
Mohammadi H., Hazrati S., Parviz L. 2017. Morphophysiological and biochemical response of savory medicinal plant using silicon under salt stress. InAnnales Universitatis Mariae Curie-Sklodowska, sectio C–Biologia 72(2): 29-40. http://dx.doi.org/10.17951/c.2017.72.2.29-40
Moustafa-Farag M., Mohamed H.I., Mahmoud A., Elkelish A., Misra A.N., Guy K.M., Kamran M., Ai S., Zhang M. 2020. Salicylic acid stimulates antioxidant defense and osmolyte metabolism to alleviate oxidative stress in watermelons under excess boron. Plants 9(6): 724. https://doi.org/10.3390/plants9060724
Nazar R., Umar S., Khan N., Sareer O. 2015. Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. South African Journal of Botany 98: 84-94. https://doi.org/10.1016/j.sajb.2015.02.005
Palma F., López-Gómez M., Tejera N.A., Lluch C. 2013. Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Science 208: 75-82. https://doi.org/10.1016/j.plantsci.2013.03.015
Panahyan Kivi M., Alami M., Abbasi A. 2020. Some physiological changes and oil yield of common purslane (Portulaca oleracea) under water deficiet in response to salicylic acid and abscisic acid. Iranian Journal of Field Crop Science 51(2): 49-61. (In Farsi). https://doi.org/10.22059/ijfcs.2019.270023.654550
Peltzer D., Dreyer E., Polle A. 2002. Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiology Biochemistry 40(2): 141-150. https://doi.org/10.1016/S0981-9428(01)01352-3
Polash M.A.S., Sakil M., Hossain M.A. 2019. Plants responses and their physiological and biochemical defense mechanisms against salinity: a review. Tropical Plant Research 6(2): 250-274. https://doi.org/10.22271/tpr.2019.v6.i2.035
Qasim M., Ashraf M., Ashraf M.Y., Rehman S.U., Rha E.S. 2003. Salt-induced changes in two canola cultivars differing in salt tolerance. Biologia Plantarum 46: 629-632. https://doi.org/10.1023/A:1024844402000
Ramachandra Reddy A., Chaitanya K.V., Jutur P.P., Sumithra K. 2004. Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environmental and Experimental Botany 52(1): 33-42. https://doi.org/10.1016/j.envexpbot.2004.01.002
Rostami M. 2018. Effect of salinity stress and salicylic acid on physiological characteristics of Lallemantia royleana. Journal of Plant Research (Iranian Journal of Biology) 31(2): 208-220. (In Farsi).
Saadatfar A., Hossein Jafari S. 2022. The effect of methyl jasmonate on morpho-physiological and biochemical parameters and mineral contents in Satureja khuzistanica Jamzad under salinity stress. Journal of Medicinal Plants 21(84): 87-99. http://dx.doi.org/10.52547/jmp.21.84.87
Sarker U., Oba S. 2020. The response of salinity stress-induced A. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. Frontiers Plant Science 11: 559876. https://doi.org/10.3389/fpls.2020.559876
Sinha A.K. 1972. Colorimetric assay of catalase. Analytical biochemistry 47(2): 389-394. https://doi.org/10.1016/0003-2697(72)90132-7
Souri M.K., Tohidloo G. 2019. Effectiveness of different methods of salicylic acid application on growth characteristics of tomato seedlings under salinity. Chemical and Biological Technologies in Agriculture 6: 26. https://doi.org/10.1186/s40538-019-0169-9
Tahjib-Ul-Arif M., Siddiqui M.N., Sohag A.A., Sakil M.A., Rahman M.M., Polash M.A., Mostofa M.G., Tran L.S. 2018. Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. Journal of Plant Growth Regulation 37: 1318-1330. https://doi.org/10.1007/s00344-018-9867-y
Wang L., Pan D., Li J., Tan F., Hoffmann-Benning S., Liang W., Chen W. 2015. Proteomic analysis of changes in the Kandelia candel chloroplast proteins reveals pathways associated with salt tolerance. Plant Science 231: 159-72. https://doi.org/10.1016/j.plantsci.2014.11.013
Wang Y., Ma W., Fu H., Li L., Ruan X., Zhang X. 2023. Effects of salinity stress on growth and physiological parameters and related gene expression in different ecotypes of Sesuvium portulacastrum on Hainan Island. Genes 14(7): 1336. https://doi.org/10.3390/genes14071336
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(8): 1920. https://doi.org/10.3390/agronomy12081920
Yousefi B., Sefidkon F., Safari H. 2023. Evaluation of essential oil in Satureja spicigera (C. Koch) Boiss. in dry farming under the effect of different organic fertilizers and plant densities. International Journal of Horticultural Science and Technology 10(3): 319-332.
Zarei B., Fazeli A., Tahmasebi Z. 2019. Salicylic acid in reducing effect of salinity on some growth parameters of black cumin (Nigella sativa). Plant Process and Function 8(29): 287-298. (In Farsi). http://jispp.iut.ac.ir/article-1-833-en.html
Zhang L., Zhao H.X., Fan X., Wang M., Ding C., Yang R.W., Yin Z.Q., Xie X.L., Zhou Y.H., Wan D.G. 2012. Genetic diversity among Salvia miltiorrhiza Bunge and related species inferred from nrDNA ITS sequences. Turkish Journal of Biology 36(3): 319-326. https://doi.org/10.3906/biy-1104-1
Zhang M., Fang Y., Ji Y., Jiang Z., Wang L. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. South African Journal of Botany 85: 1-9. https://doi.org/10.1016/j.sajb.2012.11.005
Zhang W.P., Jiang B., Lou L.N., Lu M.H., Yang M., Chen J.F. 2011. Impact of salicylic acid on the antioxidant enzyme system and hydrogen peroxide production in Cucumis sativus under chilling stress. Zeitschrift für Naturforschung C Bioscience 66(7-8): 413-422. https://doi.org/10.1515/znc-2011-7-814  
Agrotechniques in Industrial Crops

Articles in Press, Accepted Manuscript
Available Online from 20 April 2024

Files

Share

How to cite

Statistics