Antioxidant and antimicrobial responses associated with in vitro salt stress of in vitro and in vivo grown Pistacia khinjuk stocks

Emine AYAZ TİLKAT; Nesrin HAŞİMİ; İbrahim S. KURU; Veysel SÜZERER

doi:10.15835/nbha48412016

Emine AYAZ TİLKAT Batman University, Science & Literature Faculty, Department of Biology, Batman (TR)
Nesrin HAŞİMİ Batman University, Science & Literature Faculty, Department of Biology, Batman (TR)
İbrahim S. KURU Batman University, Science & Literature Faculty, Department of Biology, Batman (TR)
Veysel SÜZERER Batman University, Sason Vocational School, Department of Crop and Animal Production, Batman; Bingöl University, Vocational School of Health Services, Department of Pharmacy Services-Bingöl (TR)

DOI: https://doi.org/10.15835/nbha48412016

Keywords: antimicrobial; antioxidant; P. khinjuk Stocks; salt stress

Abstract

P. khinjuk Stocks, known as Bıttım or Buttum in Turkey, is a member of the Anacardiaceae family. The essential oil of khinjuk pistachio has been used to treat various illnesses because of their anti-inflammatory, anticancer, antipyretic, antibacterial, anthelmintic, antiviral effects in various folk medicines. At the same time, fruits of khinjuk pistachio are used as edible wild fruits. In this study, it was aimed to determine and compare the antibacterial, antioxidant activities and total phenolic and flavonoid amounts of different parts (root, stem and leaf explants) of in vivo (grown naturally) and in vitro derived khinjuk pistachio plants under salt (NaCl) stress. Ethanol extracted explants were used for performing biological and chemical parameters. According to the results, generally, in vivo samples shows higher antioxidant and antimicrobial activity besides the higher number of phenolic compounds than their counterparts in vitro. We have also determined that the biological activity of in vitro salt elicited explants was higher than in vitro control explants. Generally, both female and male in vivo samples have higher antioxidants (DPPH, ABTS, CUPRAC) and antimicrobial activities than in vitro samples. The various plant parts (root, stem, leaf) belonging to both in vivo and in vitro samples have different biological activity level. In terms of antimicrobial activity, female plant extracts are more active than all other tested extracts. As a result, although increased salinity values significantly reduced antimicrobial activity, it is determined that 100 mM NaCl applications to in vitro leaf extracts exhibited moderate antimicrobial activity against S. aureus and C. albicans.

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References

Ahmed ABA, Magesh J, Idris SN, Mubarak EN, Taha RM (2018). Chemical constituents and antimicrobial activity of essential oils from micropropagation and field grown plants of Wedelia biflora L. Journal of Essential Oil-Bearing Plants 21(6):1712-1724. https://doi.org/10.1080/0972060X.2018.1538819

Ahmed S, Saeed-Ul-Hassan S, Islam M, Qureshi F, Waheed I, Munawar I (2017). Anti-oxidant activity of Pistachia khinjuk supported by phytochemical investigation. Acta Poloniae Pharmaceutica 74:173-78.

Apak R, Güclü K, Özyürek M, Karademir SE (2004). A novel total antioxidant capacity index for dietary polyphenols, vitamin C and E, using their cupric ion reducing capability in the presence of neocuproine: The CUPRAC method. Journal of Agriculture Food Chemistry 52:7970-7981. https://doi.org/10.1021/jf048741x

Apel K, Hirt H (2004). Reactive oxygen species: Metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology 55:373-399. https://doi.org/10.1146/annurev.arplant.55.031903.141701

Arzani A, Ashraf, M (2016). Smart engineering of genetic resources for enhanced salinity tolerance in crop plants. Critical Review Plant Science 35:146-189. https://doi.org/10.1080/07352689.2016.1245056

Assimopoulou AN, Papageorgiou VP (2005). GC-MS analysis of penta- and tetra-cyclic triterpenes from resins of Pistacia species. Part II. Pistacia terebinthus var. chia. Biomedical Chromatography 19:586-605. https://doi.org.10.1002/bmc.484

Ayaz Tilkat E, Kaplan A, Hoşer A, Tilkat E (2017). In vitro şartlarda yetiştirilen Buttum (Pistacia khinjuk Stocks)’da çözünür karbonhidrat değerleri ile antioksidan peroksidaz aktivitesi üzerine tuz stresinin etkileri. Batman Üniversitesi Yaşam Bilimleri Dergisi 7(2):90-97. https://hdl.handle.net/20.500.12402/1769

Ayaz Tilkat E, Kaplan A, Tilkat E, Bağlamış G, Onay A (2019). Effects of salt stress on morpho-physiological and biochemical characters of Lentisk (P. lentiscus L.). International Journal of Nature and Life Sciences 3(1):20-31. https://dergipark.org.tr/tr/pub/ijnls/issue/43966/533316

Benmahioul B, Daguin F, Kaid-Harche M (2009) Effects of salt stress on germination and in vitro growth of pistachio (Pistacia vera L.). Comptes Rendus Biologies 332(8):752-8. https://doi.org/10.1016/j.crvi.2009.03.008

Blois MS (1958). Antioxidant determinations by the use of a stable free radical. Nature 181:1199-1200. https://doi.org/10.1038/1811199a0

Brewer MS (2011). Natural antioxidants: Sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety 10:221-247.

https://doi.org/10.1111/j.1541-4337.2011.00156.x

Chelli-Chaabouni A, Mosbah AB, Maalej M, Gargouri 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(3):302-312. https://doi.org/10.1016/j.envexpbot.2010.05.010

Cuce M, Bekircan T, Laghari AH, Sökmen M, Sökmen A, Önay Uçar E, Kılıç AO (2017). Antioxidant phenolic constituents, antimicrobial and cytotoxic properties of Stachys annua L. from both natural resources and micropropagated plantlets. Indian Journal of Traditional Knowledge 16(3):407-416.

Delaquis PJ, Stanich K, Girard B, Mazza G (2002). Antimicrobial activity of individual and mixed fractions of dill, citaro, coriander and eucalyptus essential oils. International Journal of Food Microbiology 74:101-109. https://doi.org/10.1016/s0168-1605(01)00734-6

Dorman HJD, Deans SG (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology 88:308-316. https://doi.org/10.1046/j.1365-2672.2000. 00969.x

Esmaeili AK, Taha RM, Mohajer S, Banisalam B (2015). Antioxidant activity and total phenolic and flavonoid content of various solvent extracts from in vivo and in vitro grown Trifolium pratense L. (Red Clover). BioMed Research International 643285:11. https://doi.org/10.1155/2015/643285

Esmat A, Al-Abbasi FA, Algandaby MM, Moussa AY, Labib RM, Ayoub NA, Abdel-Naim AB (2012). Anti-inflammatory activity of Pistacia khinjuk in different experimental models: Isolation and characterization of its flavonoids and galloylated sugars. Journal of Medicinal Food 15(3):278-287. https://doi.org/10.1089/jmf.2011.0099

Falleh H, Jalleli I, Ksouri R, Boulaaba M, Guyot S, Magné C, Abdelly C (2012). Effect of salt treatment on phenolic compounds and antioxidant activity of two Mesembryanthemum edule provenances. Plant Physiology and Biochemistry 52:1-8. https://doi.org/10.1016/j.plaphy.2011.11.001

Giaginis C, Theocharis S (2011). Current evidence on the anticancer potential of Chios mastic gum. Nutrition Cancer 63(8):1174-84. https://doi.org/10.1080/01635581.2011.607546

Golkar P, Taghizadeh M (2018). In vitro evaluation of phenolic and osmolyte compounds, ionic content, and antioxidant activity in safflower (Carthamus tinctorius L.) under salinity stress. Plant Cell Tissue Organ Culture 134:357-368. https://doi.org/10.1007/s11240-018-1427-4

Golkar P, Taghizadeh M, Yousefian Z (2019) The effects of chitosan and salicylic acid on elicitation of secondary metabolites and antioxidant activity of safflower under in vitro salinity stress. Plant Cell, Tissue and Organ Culture 137:575-585. https://doi.org/10.1007/s11240-019-01592-9

Hacibekiroglu I, Yılmaz-Köseoglu P, Nesrin N, Ersin K, Veysel T, Ufuk K (2015). In vitro biological activities and fatty acid profiles of Pistacia terebinthus fruits and Pistacia khinjuk seeds. Natural Product Research 29(5):444-446. https://doi.org/10.1080/14786419.2014.947492

Hatamnia AA, Rostamzad A, Malekzadeh P, Darvishzadeh R, Abbaspour N, Hosseini M, Nourollahi K, Mehr RS. 2016). Antioxidant activity of different parts of Pistacia khinjuk Stocks fruit and its correlation to phenolic composition. Natural Product Research 30(12):1445-1450. https://doi.org/10.1080/14786419.2015.1060593

Hazrati S, Govahi M, Ebadi MT, Habibzadeh F (2020). Comparison and evaluation of oil content, composition and antioxidant properties of Pistacia atlantica and Pistacia khinjuk grown as wild. International Journal of Horticultural Science and Technology 7(2):165-174. https://doi.org/10.22059/ijhst.2020.287550.316

Hernandez JA, Almansa MS (2002). Short‐term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiologia Plantarum 115(2):251-257. https://doi.org/10.1034/j.1399-3054.2002.1150211.x

Holley RA, Patel D (2005). Improvement in shelf-life and safety of perishable foods by plant essential oils and smoke antimicrobials. Food Microbiology 22:273-292. Https://doi.org/10.1016/j.fm.2004.08.006

Hosseinzadeh H, Sajadi Tabassi SA, Milani Moghadam N, Rashedinia M, Mehri S (2012). Antioxidant activity of Pistacia vera fruits, leaves and gum extracts. Iranian Journal of Pharmaceutical Research 11(3):879-887.

Javed R, Gurel E (2019). Salt stress by NaCl alters the physiology and biochemistry of tissue culture-grown Stevia rebaudiana Bertoni, Turkish Journal of Agriculture Forestry 43:11-20. https://doi.org/10.3906/tar-1711-71

Kaliora AC, Mylona A, Chiou A, Petsios DG, Andrikopoulos NK (2004). Detection and identification of simple phenolics in Pistacia lentiscus resin. Journal of Liquid Chromatography Relation Technology 27:289-300. https://doi.org/10.1081/JLC-120027100

Ksouri R, Megdiche W, Debez A, Falleh M, Grignon C, Abdelly C (2007). Salinity effect on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiology and Biochemistry 45:244-248. https://doi.org/10.1016/j.plaphy.2007.02.001

Mazari K, Bendimerad N, Bekhechi C, Fernandez X (2010). Chemical composition and antimicrobial activity of essential oils isolated from Algerian Juniperus phoenicea L. and Cupressus sempervirens L. Journal of Medicinal Plant Research 4:959-964. http://www.academicjournals.org/JMPR

Mirian M, Behrooeian M, Gahanadian M, Dana N, Sadeghi-Aliabadi H (2014). Cytotoxity and antiangiogenic effects of Rhus coriaria, Pistacia vera and Pistacia khinjuk oleoresin methanol extracts. Research in Pharmaceutical Sciences 10(3):233-240.

Mohagheghzadeh A, Faridi P, Ghasemi Y (2010). Analysis of mount atlas mastic smoke: A potential food preservative. Fitoterapia 81:577-580. https://doi.org/10.1016/j.fitote.2010.01.022

Moreno MIN, Isla MI, Sampietro AR, Vattuone MA (2000). Comparison of the free radical-scavenging activity of propolis from several regions of Argentina. Journal of Ethnopharmacology 71(1-2):109-114. https://doi.org/10.1016/s0378-8741(99)00189-0

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiology 15:473-497. https://doi.org.10.1111/j.1399-3054.1962.tb08052.x

National Committee for Clinical and Laboratory Standard (2009). Performance Standards for Antimicrobial Susceptibility Testing; 20th Informational Supplement. CLSI document M100-S19. CLSI, Wayne, PA: NCCSL.

National Committee for Clinical Laboratory Standards (1997). Performance standards for antimicrobial disk susceptibility tests. Approved standard M2-A6. Wayne, PA: NCCLS.

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 Chemistry 96:66-73. https://doi.org/10.1016/j.foodchem.2005.01.057

Ongphimai N (2013). Phenolic acids content and antioxidant capacity of fruit extracts from Thailand. Chiang Mai Journal of Science 40(4):636-642.

Parsaeimehr A, Sargsyan E, Javidnia K (2010). A comparative study of the antibacterial, antifungal and antioxidant activity and total content of phenolic compounds of cell cultures and wild plants of three endemic species of Ephedra. Molecules 15(3):1668-1678. https://doi.org/10.3390/molecules15031668

Rahneshan Z, Nasibi F, Moghadam AA (2018). Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks, Journal of Plant Interactions 13(1)7:73-82. https://doi.org/10.1080/17429145.2018.1424355

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice EC (1999). Antioxidant activity applying an improved ABTS radical cation decolourization assay. Free Radical Biology and Medicine 26:1231-1237. https://doi.org/10.1016/s0891-5849(98)00315-3

Sacchetti G, Maietti S, Muzzoli M, Scaglianti M, Manfredini S, Radice M, Bruni R (2005). Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chemistry 91:621-632. https://doi.org/10.1016/j.foodchem.2004.06.031

Salem MZM, Salem AZM, Camacha LM Ali HM (2013). Antimicrobial activities and phytochemical composition of extracts of Ficus species: An over view. African Journal of Microbiology Research 7(33):4207-4219. https://doi.org/10.5897/AJMR2013.5570

Salem N, Msaada K, Dhifi W, Limam F, Marzouk B (2014). Effect of salinity on plant growth and biological activities of Carthamus tinctorius L. extracts at two flowering stages. Acta Physiologiae Plantarum 36(2):433-445. https://doi.org/10.1007/s11738-013-1424-5

Slinkard K, Singleton VL (1977). Total phenol analyses: Automation and comparison with manual methods. American Journal of Enology and Viticulture 28:49-55.

Taghizadeh SF, Davarynejad G, Asili J, Riahi-Zanjani B, Nemati SH, Karimi G (2018). Chemical composition, antibacterial, antioxidant and cytotoxic evaluation of the essential oil from pistachio (Pistacia khinjuk) hull. Microbial Pathogenesis 124:76-81. https://doi.org/10.1016/j.micpath.2018.08.039

Tahvilian R, Moradi R, Zhale H, Zangeneh MM, Zangeneh A, Yazdani H, Hajialiani M (2016). Ethnomedicinal plants: Study on antifungal activity of essential oil of Pistacia khinjuk (combined with the dominance γ-Terpinene) against Candida albicans. International Journal of Pharmaceutical and Clinical Research 8(10):1369-1373. www.ijpcr.com

Taran M, Sharifi M, Azizi E, Khanahmadi M (2010). Antimicrobial activity of the leaves of Pistacia khinjuk. Journal of Medicinal Plants 9(6):81-85.

Tilkat E, Ertaş A, Surmuş-Aşan H, Yılmaz MA, Süzerer V (2018). TÜBİTAK KBAG 114Z842 Pistacia lentiscus L.’un ın vitro sürgün, kallus ve hücre süspansiyon kültürlerinde antikanser aktivite gösteren kimyasal bileşenlerin üretilmesi. [The production of chemical components perfoming anti-anticancer activity in in vitro culture of shoots, callus and suspension of Pistacia lentiscus L.] TÜBİTAK Final Report pp 241 (In Turkish) https://app.trdizin.gov.tr/publication/project/detail/TVRjMk5UTXo=

Tilkat E, Işıkalan Ç, Onay A (2005). In vitro propagation of khinjuk pistachio (Pistacia khinjuk Stocks) through seedling apical shoot tip culture. Propagation of Ornamental Plants 5:124-128. http://www.journal-pop.org/2005_5_3_124-128.html

Topçu G, Ay M, Bilici A, Sarıkürkcü C, Öztürk M, Ulubelen A (2007). A new flavone from antioxidant extracts of Pistacia terebinthus. Food Chemistry 103(3):816-822. https://doi.org/10.1016/j.foodchem.2006.09.028

Valifard M, Mohsenzadeh S, Kholdebarina B, Rowshanb V (2014). Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South African Journal of Botany 93:92-97. https://doi.org/10.1016/j.sajb.2014.04.002

Wei T, Sun H, Zhao X, Hou J, Hou A, Zhao Q (2002). Scavenging of reactive oxygen species and prevention of oxidative neuronal cell damage by a novel gallotannin, pistafolia A. Life Sciences 70:1889-1899. https://doi.org/10.1016/S0024-3205(02)01494-7

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 Chemistry 121:1014-1019. https://doi.org/10.1016/j.foodchem.2010.01.040