Skip to main content
SpringerLink
Log in

Methanolic extracts of Zataria multiflora and Satureja bachtiarica improved physio-chemical parameters and salinity tolerance of Salvia officinalis

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

In order to reduce salinity stress damages in Salvia officinalis, a factorial experiment was designed and implemented based on a randomized complete block with three replications. The first factor was included 0, 10%, and 15% methanolic extracts of Zataria multiflora and Satureja bachtiarica, and the second was different salinity stress levels (0, 100, and 200 mM NaCl). The results showed that the best plant growth traits, anthocyanin concentration, and ascorbate peroxidase activity were obtained by 10% S. bachtiarica extract under normal condition. The highest leaf area, relative water content, antioxidant activity, protein, and catalase activity, and the lowest amount of electrolyte leakage, malondialdehyde (MDA), proline, and superoxide dismutase activity were recorded by 10% Z. multiflora application at the absence of salinity stress. Parameters such as fresh and dry weight of leaves, net photosynthetic rate, and carotenoids were higher in 15% Z. multiflora treatment at non-stress situation. Best results of phenols and flavonoid concentrations were obtained at 100 mM NaCl, and the highest concentration of flavanols, MDA, and proline were observed in salt-affected plants (200 mM NaCl) without using extracts. Considering that various concentrations of the tested methanolic extracts have improved the physio-chemical traits, these extracts (especially 10% S. bachtiarica) can be presented as an effective natural plant biostimulant to ameliorate growth parameters and salinity tolerance in S. officinalis, thus limiting water, soil, and environmental pollution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • 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(3):161–175

    Article  CAS  PubMed  Google Scholar 

  • Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77

    Article  CAS  PubMed  Google Scholar 

  • Arzani A (2008) Improving salinity tolerance in crop plants: a biotechnological view. In Vitro Cell Dev Biol-Plant 44(5):373–383

    Article  CAS  Google Scholar 

  • Arzani A (2018) Engineering programmed cell death pathways for enhancing salinity tolerance in crops. In: Kumar V, Wani SH, Suprasanna P, Tran LPS (eds) Salinity responses and tolerance in plants, vol 2. Springer, Berlin

    Google Scholar 

  • Arzani A, Ashraf M (2016) Smart engineering of genetic resources for enhanced salinity tolerance in crop plants. Crit Rev Plant Sci 35(3):146–189

    Article  CAS  Google Scholar 

  • Ashrafi N, Nejad AR (2018) Lisianthus response to salinity stress. Photosynthetica 56(2):487–494

    Article  CAS  Google Scholar 

  • Bates L (1973) Rapid determination of free poline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Benjamin JJ, Lucini L, Jothiramshekar S, Parida A (2019) Metabolomic insights into the mechanisms underlying tolerance to salinity in different halophytes. Plant Physiol Biochem 135:528–545

    Article  CAS  PubMed  Google Scholar 

  • Betzen BM, Smart CM, Maricle KL, MariCle BR (2019) Effects of increasing salinity on photosynthesis and plant water potential in Kansas salt marsh species. Trans Kans Acad Sci 122(1–2):49–58

    Article  Google Scholar 

  • Bistgani ZE, Siadat SA, Bakhshandeh A, Pirbalouti AG, Hashemi M (2017) Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis Celak. Crop J 5(5):407–415

    Article  Google Scholar 

  • Bonesi M, Loizzo MR, Acquaviva R, Malfa GA, Aiello F, Tundis R (2017) Anti-inflammatory and antioxidant agents from Salvia genus (Lamiaceae): an assessment of the current state of knowledge. AIAAMC 16(2):70–86

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Chun OK, Kim DO, Lee CY (2003) Superoxide radical scavenging activity of the major polyphenols in fresh plums. J Agric Food Chem 51(27):8067–8072

    Article  CAS  PubMed  Google Scholar 

  • Cunha JR, Neto MCL, Carvalho FE, Martins MO, Jardim-Messeder D, Margis-Pinheiro M, Silveira JA (2016) Salinity and osmotic stress trigger different antioxidant responses related to cytosolic ascorbate peroxidase knockdown in rice roots. Environ Exp Bot 131:58–67

    Article  CAS  Google Scholar 

  • D’Amelia L, Dell’Aversana E, Woodrow P, Ciarmiello LF, Carillo P (2018) Metabolomics for crop improvement against salinity stress. In: Kumar V, Wani SH, Suprasanna P, Tran L-SP (eds) Salinity responses and tolerance in plants, 2nd edn. Springer, Cham, pp 267–287

    Chapter  Google Scholar 

  • Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Hernández JA, Burgos L (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotechnol J 11(8):976–985

    Article  CAS  PubMed  Google Scholar 

  • Dutta S, Ray S (2020) Comparative assessment of total phenolic content and in vitro antioxidant activities of bark and leaf methanolic extracts of Manilkara hexandra (Roxb.) Dubard. J King Saud Univ-Sci 32(1):643–647

    Article  Google Scholar 

  • El-Kholy WM, El-Habibi EM, Mousa AT (2010) Oxidative stress in brains of rats intoxicated with aluminum and the neuromodulating effect of different forms of sage. J Am Sci 6(12):1462–1474

    Google Scholar 

  • Farouk S, Al-Huqail AA (2022) Sustainable biochar and/or melatonin improve salinity tolerance in borage plants by modulating osmotic adjustment, antioxidants, and ion homeostasis. Plants 11(6):765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galmes J, Flexas J, Savé R, Medrano H (2007) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290(1–2):139–155

    Article  CAS  Google Scholar 

  • Gharibi S, Tabatabaei BES, Saeidi G (2015) Comparison of essential oil composition, flavonoid content and antioxidant activity in eight Achillea species. J Essent Oil Bear Plants 18(6):1382–1394

    Article  CAS  Google Scholar 

  • Giannoulis KD, Skoufogianni E, Bartzialis D, Solomou AD, Danalatos NG (2021) Growth and productivity of Salvia officinalis L. under Mediterranean climatic conditions depends on biofertilizer, nitrogen fertilization, and sowing density. Ind Crops Prod 160:113136

    Article  CAS  Google Scholar 

  • Golkar P, Mosavat N, Jalali SAH (2020) Essential oils, chemical constituents, antioxidant, antibacterial and in vitro cytotoxic activity of different Thymus species and Zataria multiflora collected from Iran. S Afr J Bot 130:250–258

    Article  CAS  Google Scholar 

  • Gomes MADC, Suzuki MS, Cunha MD, Tullii CF (2011) Effect of salt stress on nutrient concentration, photosynthetic pigments, proline and foliar morphology of Salvinia auriculata Aubl. Acta Limnol Bras 23:164–176

    Article  Google Scholar 

  • Gupta DK, Palma JM, Corpas FJ (2015) Reactive oxygen species and oxidative damage in plants under stress. Springer, Heidelberg, pp 1–22

    Book  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21(2):79–102

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Anee TI, Bhuiyan TF, Nahar K, Fujita M (2019) Emerging role of osmolytes in enhancing abiotic stress tolerance in rice. In: Hasanuzzaman M, Fujita M, Nahar K, Biswas JK (eds) Advances in rice research for abiotic stress tolerance. Woodhead Publishing, Sawston, pp 677–708

    Chapter  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHM, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  CAS  PubMed  Google Scholar 

  • Hendawy SF, Khalid KA (2005) Response of sage (Salvia officinalis L.) plants to zinc application under different salinity levels. J Appl Sci Res 1(2):147–155

    Google Scholar 

  • Hughes NM, Carpenter KL, Cannon JG (2013) Estimating contribution of anthocyanin pigments to osmotic adjustment during winter leaf reddening. J Plant Physiol 170(2):230–233

    Article  CAS  PubMed  Google Scholar 

  • Jakovljević M, Jokić S, Molnar M, Jašić M, Babić J, Jukić H, Banjari I (2019) Bioactive profile of various Salvia officinalis L. preparations. Plants 8(3):55

    Article  PubMed  PubMed Central  Google Scholar 

  • Jedidi S, Aloui F, Selmi H, Rtibi K, Dallali S, Sebai CAEH (2018) Ethnobotanical survey on the traditional use of officinal sage (Salvia officinalis L.) in Tabarka and Aïn Draham (Northwestern of Tunisia). J New Sci 18:3402–3412

    Google Scholar 

  • Jedidi S, Sammari H, Selmi H, Hosni K, Rtibi K, Aloui F, Adouni O, Sebai H (2021) Strong protective effects of Salvia officinalis L. leaves decoction extract against acetic acid-induced ulcerative colitis and metabolic disorders in rat. J Funct Foods 79:104406

    Article  CAS  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–67

    CAS  Google Scholar 

  • Karimi A, Krähmer A, Herwig N, Schulz H, Hadian J, Meiners T (2020a) Variation of secondary metabolite profile of Zataria multiflora Boiss. populations linked to geographic, climatic, and edaphic factors. Front Plant Sci 11:969

    Article  PubMed  PubMed Central  Google Scholar 

  • Karimi S, Karami H, Vahdati K, Mokhtassi-Bidgoli A (2020b) Antioxidative responses to short-term salinity stress induce drought tolerance in walnut. Sci Hortic 267:109322

    Article  CAS  Google Scholar 

  • Kiani R, Arzani A, Mirmohammady Maibody SAM (2021) Polyphenols, flavonoids, and antioxidant activity involved in salt tolerance in wheat, Aegilops cylindrica and their amphidiploids. Front Plant Sci 12:646221

    Article  PubMed  PubMed Central  Google Scholar 

  • Kulak M, Gul F, Sekeroglu N (2020) Changes in growth parameter and essential oil composition of sage (Salvia officinalis L.) leaves in response to various salt stresses. Ind Crops Prod 145:112078

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Transac 11:591–592

    Article  CAS  Google Scholar 

  • Marchica A, Ascrizzi R, Flamini G, Cotrozzi L, Tonelli M, Lorenzini G, Nali C, Pellegrini E (2021) Ozone as eustress for enhancing secondary metabolites and bioactive properties in Salvia officinalis. Ind Crops Prod 170:113730

    Article  CAS  Google Scholar 

  • Masoudniaragh A, Oraei M, Gohari G, Akbari A, Faramarzi A (2021) Using halloysite nanotubes as carrier for proline to alleviate salt stress effects in sweet basil (Ocimum basilicum L.). Sci Hortic 285:110202

    Article  CAS  Google Scholar 

  • Masukasu H, Karin O, Kyoto H (2003) Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus) hypocotyls. Plant Sci 164(2):259–265

    Article  Google Scholar 

  • Memarzadeh SM, Pirbalouti AG, AdibNejad M (2015) Chemical composition and yield of essential oils from Bakhtiari savory (Satureja bachtiarica Bunge.) under different extraction methods. Ind Crops Prod 76:809–816

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Miliauskas G, Venskutonis PR, Van Beek TA (2004) Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chem 85(2):231–237

    Article  CAS  Google Scholar 

  • Misra N, Gupta AK (2006) Effect of salinity and different nitrogen sources on the activity of antioxidant enzymes and indole alkaloid content in Catharanthus roseus seedlings. J Plant Physiol 163(1):11–18

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Navada S, Vadstein O, Gaumet F, Tveten AK, Spanu C, Mikkelsen Ø, Kolarevic J (2020) Biofilms remember: osmotic stress priming as a microbial management strategy for improving salinity acclimation in nitrifying biofilms. Water Res 176:115732

    Article  CAS  PubMed  Google Scholar 

  • Pandey VP, Awasthi M, Singh S, Tiwari S, Dwivedi UN (2017) A comprehensive review on function and application of plant peroxidases. Biochem Anal Biochem 6(1):308

    Article  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349

    Article  CAS  PubMed  Google Scholar 

  • 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(1):28–36

    Article  CAS  Google Scholar 

  • Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73(1–3):149–156

    Article  CAS  PubMed  Google Scholar 

  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163(5):1037–1046

    Article  CAS  Google Scholar 

  • Sefidkon F, Jamzad Z (2000) Essential oil of Satureja bachtiarica Bunge. J Essent Oil Res 12(5):545–546

    Article  CAS  Google Scholar 

  • Sharma A, Zheng B (2019) Melatonin mediated regulation of drought stress: physiological and molecular aspects. Plants 8(7):190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheldon AR, Dalal RC, Kirchhof G, Kopittke PM, Menzies NW (2017) The effect of salinity on plant-available water. Plant Soil 418(1):477–491

    Article  CAS  Google Scholar 

  • Soori N, Bakhshi D, Rezaei NA, Faizian M (2019) Effect of salinity stress on some physiological characteristics and photosynthetic parameters of several Iranian commercial pomegranate genotypes. J Plant Process Funct 8:155–170

    Google Scholar 

  • Suhanya P, Juzaili B, Azizi R, Ismail S, Sasidharan S, Mahsufi M (2009) Evaluation of antioxidant and antibacterial activities of aqueous, methanolic and alkaloid extracts from Mitragyna speciosa (Rubiaceae family) leaves. Molecules 14:3964–3974

    Article  Google Scholar 

  • Taarit MB, Msaada K, Hosni K, Hammami M, Kchouk ME, Marzouk B (2009) Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Ind Crops Prod 30(3):333–337

    Article  Google Scholar 

  • Tavallali V, Karimi S, Espargham O (2018) Boron enhances antioxidative defense in the leaves of salt-affected Pistacia vera seedlings. Hortic J 87(1):55–62

    Article  Google Scholar 

  • Tounekti T, Hernández I, Müller M, Khemira H, Munné-Bosch S (2011) Kinetin applications alleviate salt stress and improve the antioxidant composition of leaf extracts in Salvia officinalis. Plant Physiol Biochem 49(10):1165–1176

    Article  CAS  PubMed  Google Scholar 

  • Valentovic P, Luxova M, Kolarovic L, Gasparikova O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ 52(4):184

    Article  Google Scholar 

  • Velmurugan A, Swarnam P, Subramani T, Meena B, Kaledhonkar MJ (2020) Water demand and salinity. In: Farahani MHDA, Vatanpour V, Taheri A (eds) Desalination-challenges and opportunities. London, IntechOpen

    Google Scholar 

  • Wang S, Wan C, Wang Y, Chen H, Zhou Z, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56(3):525–539

    Article  Google Scholar 

  • Wang P, Li X, Tian L, Gu Z, Yang R (2019) Low salinity promotes the growth of broccoli sprouts by regulating hormonal homeostasis and photosynthesis. Hortic Environ Biotechnol 60(1):19–30

    Article  CAS  Google Scholar 

  • Wani AS, Ahmad A, Hayat S, Tahir I (2019) Epibrassinolide and proline alleviate the photosynthetic and yield inhibition under salt stress by acting on antioxidant system in mustard. Plant Physiol Biochem 135:385–394

    Article  CAS  PubMed  Google Scholar 

  • Xu DP, Li Y, Meng X, Zhou T, Zhou Y, Zheng J, Zhang JJ, Li HB (2017) Natural antioxidants in foods and medicinal plants: extraction, assessment and resources. Int J Mol Sci 18(1):96

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan F, Wei H, Ding Y, Li W, Liu Z, Chen L, Tang S, Ding C, Jiang Y, Li G (2021) Melatonin regulates antioxidant strategy in response to continuous salt stress in rice seedlings. Plant Physiol Biochem 165:239–250

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Dai W (2019) Plant response to salinity stress. In: Wenhao D (ed) Stress physiology of woody plants. CRC Press, Boca Raton, pp 155–173

    Chapter  Google Scholar 

  • Zorb C, Geilfus CM, Dietz KJ (2019) Salinity and crop yield. Plant Biol 21:31–38

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by a grant from Deputy of Research and Technology, Ilam University. The authors are grateful to the Head of the Research Institute of Medicinal and Aromatic Plants, Ilam University, Ilam, Iran for using and providing access to the research farm and greenhouse of their institute.

Author information

Authors and Affiliations

  1. Department of Horticultural Sciences, College of Agriculture, Ilam University, Ilam, Iran

    Majid Bagnazari

  2. Department of Horticulture, College of Agriculture, Bu-Ali-Sina University, Hamedan, Iran

    Hadis Hasanbeigi

Authors
  1. Majid Bagnazari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hadis Hasanbeigi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Dr. MB and Miss. HH performed the experiments, analysis on all samples, interpreted data, and wrote manuscript. Dr. MB supervised development of work, manuscript evaluation and acted as corresponding author.

Corresponding author

Correspondence to Majid Bagnazari.

Additional information

Communicated by F. Araniti.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bagnazari, M., Hasanbeigi, H. Methanolic extracts of Zataria multiflora and Satureja bachtiarica improved physio-chemical parameters and salinity tolerance of Salvia officinalis. Acta Physiol Plant 45, 114 (2023). https://doi.org/10.1007/s11738-023-03595-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-023-03595-8

Keywords

Search

Navigation