1 Introduction

Prangosis a perennial genus of the Apiaceae family distinguished by its winged fruits (Davis, 1972). It consists of about 30 world wide species with a diversity center being situated in the Irano-Turanian phytogeographic region (Duran et al., 2005). Prangos species have been commonly used in traditional medicine in East Mediterranean and Middle Eastern countries. Numerous studies have cited Prangos species as carminative, wound healing, haemostasis, antiflatulent, antihaemorrhoidal, anthelmintic, antispasmodic and antimicrobial in a wide range of diseases (Ulubelen et al., 1995; Shikishima et al., 2001; Tada et al., 2002; Uzel et al., 2006; Massumi et al., 2007; Razavi et al., 2010; Sadraei et al., 2012). Prangos species are also indicated in the treatment of leucoplakia and digestive disorders and to have anti-HIV and antioxidant activities (Shikishima et al., 2001; Dokovic et al., 2004; Coruh et al., 2007). Similarly to Ferula and Ferulago, the roots have aphrodisiac properties (Baytop et al., 1994; Kilic et al., 2007). More recently, insecticidal properties against Mediterranean flour moth (Ephestia kuehniella) found in stored food products, such as cereals are also displayed (Ercan et al., 2013).

Recent phytochemical investigations on different species have led to the isolation of coumarins, flavonoids, alkaloids, terpenoids and other compounds from the different plant parts which have attracted considerable attention due to their pharmacological properties supporting the traditional use (Baser et al., 2000; Ozcan et al., 2000; Shikishima et al., 2001; Tada et al., 2002; Ozek et al., 2006; Nazemiyeh et al., 2007a; Nazemiyeh et al., 2007b; Razavi et al., 2008; Kilic et al., 2010; Sajjadi et al., 2011; Kafash-Farkhad et al., 2013; Akhlaghi, 2015).

Prangos asperula Boiss., commonly known as Frash Al Dabe’e, is the only native Prangos species that grows wild in the upper mountainous regions of Lebanon (Tannourine, Dahr el Baydar, Ehden, Shouf, Kefraya, Rachaiya). P. asperula has been traditionally used as remedy of skin diseases, wounds infections and as carminative against aerocoly and in the treatment of diabetes (Loizzo et al., 2008a). Studies on the plants growing wild in Lebanon have reported a remarkable antimicrobial activity of aerial parts against some Gram-positive and Gram-negative bacteria and interesting antiproliferative effects of leaves essential oil on renal adenocarcinoma cell line (Bouaoun et al., 2007; Loizzo et al., 2008b).

Forty-two terpenes were identified in P. asperula essential oil, representing 92.1% of total oil. Sabinene (20.6%), β-phellandrene (19.0%), γ-terpinene (9.0%), α-pinene (8.4%), and α-phellandrene (6.1%) were the most representative constituents. Other interesting oil components were δ-3-carene, p-cymene and α-bisabolol. Sabinene, α-pinene, α-phellandrene and δ-3-carene were tested for their cytotoxic activity on tumor cell in vitro models. None of the compounds was found active. It was concluded that major and minor constituents may act in synergy with the other cytotoxic components of the essential oils (Loizzo et al., 2008). Other investigations on the fruit oil of the plant from Iran demonstrated that δ-3-carene, β-phellandrene, α-pinene, α-humulene, germacrene D and δ-cadinenewere the major components of the essential oil of fruits (Sajjadi and Mehregan, 2003), while δ-3-carene, α-terpinolene, α-pinene, limonene, 2, 3, 6-trimethyl benzaldehyde, bornyl acetate, osthol and cis-chrysanthenyl acetate were the most representative constituents of the aerial parts essential oil (Mirzaei and Ramezani, 2008; Sajjadi et al., 2009). In the latter study, investigators were also able to isolate in the hexane extract of the fruits the prenylated coumarin osthol recognized to be effective in the prevention of atherosclerosis, suppression of hepatic lipids, as antitumor and anti-inflammatory among its major bioactivities.

This study concerns a comparative analysis of essential oils composition from different aerial plant parts of P. asperula growing wild in Lebanon and assessment of their antimicrobial activity.

2 Material and Methods

2.1 Plant material

Aerial parts of the wild growing P. asperula were collected at random from Tannourine in the North of Lebanon in July 2014, at 1750 meters. The species identification was performed using the determination keys of the New Flora of Lebanon and Syria (Mouterde, 1970). A voucher specimen (RCED 2015-295) was deposited at the herbarium of the Research Center for Environment and Development, Beirut, Arab University, Lebanon.

2.2 Essential oil isolation

The essential oils from fresh leaves and stems, flowers and fruits of P. asperula were hydrodistillled by Clevenger-type apparatus for three hours (European, 2008). The volatile oils were dried using anhydrous sodium sulphate and then stored in sterile sealed vials in the dark at 4ºC until analysis. The yield percentages of oils were calculated based on fresh weight of plant parts.

2.3 Bacterial and fungal strains

Certified bacterial and fungal strains (Medi Mark, Europe) were used. They were two pathogenic Gram positive bacteria: Enterococcus faecalis (ATCC 29212), Staphylococcus aureus (ATCC 25923); two Gram negative bacteria: Escherichia coli (ATCC 8739), Salmonella enteritidis (ATCC 13076); two fungal strains: filamentous Aspergillus fumigatus (ATCC 1022), dermatophyte Trichophyton mentagrophytes (ATCC 9533); and the yeast Candida albicans (ATCC 10231).

2.4 GC and GC-MS analyses

Gas chromatography with mass spectrometry (GC-MS) were used to identify essential oils compounds. The analysis was performed by Agilent Technologies 7890 gas chromatography equipped with a Flame Ionization Detector (FID) and a HP-5 MS 5% capillary column (30 m x 0.25 mm x 0.25 μm film thickness). Mass spectra were recorded at 70 eV of electron energy and a mass range of 50-550 m/z. The carrier gas was Helium at a flow of 0.8 ml/min. The initial column temperature was 60ºC programmed to increase to 280ºC at a rate of 4ºC/min. The split ration was 1:40. The injector temperature was set at 300ºC. The purity of helium gas was 99.99%. A sample of 1 ml was injected manually in the split mode. Components identification was based on retention indices and comparison with mass spectral data of authentic standards and computer matching with Wiley 229, NIST 107, NIST 21 libraries as well as by comparing the fragmentation patterns of the mass spectra with those reported in the literature.

2.5 Antimicrobial activity by Disc diffusion method

The antibacterial and antifungal activity of total essential oil was carried out by disc diffusion method using 100 μl of suspension containing 10⁶ CFU/ml of bacteria spread on Mueller-Hinton agar medium (Merck). Sterile 6 mm diameter filter paper discs (Whatman No.3) were impregnated with 10 μL of essential oil and were placed on the agar. Standard reference discs of the antibiotics Norfloxacin (10 µg) and Nystatin (10 µg) were used as standard antibacterial or antifungal agents and positive controls. Each test was run in triplicate and the mean values were considered. A blank disc was used as a negative control. The bacterial cultures were incubated at 37^oC for 24 hrs. Whereas Candida albicans and Trichophyton mentagrophytes were incubated at 27ºC for 48 hrs and 5 days, respectively. The diameters (mm) of growth inhibition zones around discs were measured using a caliper.

2.6 Minimum inhibitory concentration (MIC) by agar dilution method

MICs were determined by agar dilution method approved by NCCLS (1997). A series of four concentrations of oil (5, 10, 25 and 50 µL) with 0·5% (v/v) Tween-20 were added to a one ml of microbial suspension containing approximately 10⁶ CFU/ml of each organism in Mueller Hinton broth. Tween-20 (Sigma) was used to enhance the solubility of essential oil in broth. 100 μl of each mixture was spread on Mueller Hinton agar plates. The plates inoculated with bacteria were incubated at 37°C for 24 hrs. MICs determined as the lowest concentration of oil inhibiting the visible growth of each microorganism on agar plates were determined. All tests were performed in triplicates.

3 Results and Discussion

Table 1 indicates the qualitative and quantitative composition of oils and retention times of constituents. The yields of oils of stems and leaves, flowers and fruits were 0.09%, 0.22% and 0.21%, respectively.42 compounds were identified in the oil from leaves and stems representing 75.5% of the total, 46 compounds in the flowers oil representing 86.9% of total and 4 compounds in the fruits oil representing 99.8% of total. The main components of stems and leaves oil were nerolidol (15.2%), p-menth-3-ene (13.3%), β-myrcene (9.2%), β-farnesene (4.8%), cis-β-ocimene (3.5%), α-farnesene (3.4%), α-phellandrene (3.2%), α-bisabolol (3.1%), α-caryophyllene (3%), neo-allo-ocimene (1.9%), α-bergamotene (1.8%), cis-α-bisabolene (1.3%), o-ocymol (1.2%), 2-thujene (1.1%) and safranal (1.1). Hydrogenated monoterpenes dominated the chemical composition (34.1%), followed by oxygenated sesquiterpenes (19.4%) and hydrogenated sesquiterpenes (19.1), while oxygenated monoterpenes (2.9) formed a minor share of this oil.

The main components of flowers oil were p-menth-3-ene (14.9%), nerolidol (14.7%), β-phellandrene (7.9%), α-caryophyllene (5.1%), β-farnesene (5.1%), neo-allo-ocimene (5.1%), α-phellandrene (4.3%), α-farnesene (4.2%), β-trans-ocimene (3.9%), α-bisabolol (2.7%), α-terpinene (2.7%), α-bergamotene (1.6%), α-terpinolene (1.4%), IR-α-pinene (1.2%), cis-β-ocimene (1.2%), α-cedrene (1.1%) and (+)-4-carene (1.1%). Similarly to the stems and leaves, hydrogenated monoterpenes formed the major share of constituents (44.7%) followed by hydrogenated sesquiterpenes (22.3%), oxygenated sesquiterpenes (18.7) and oxygenated monoterpenes (1.2%). Finally the major components of fruits were sabinene (43.5%), β-phellandrene (36.1%), α-phellandrene (11.9%) and α-terpinene (8.3%). Absolute dominance of hydrogenated monoterpenes is detected forming the sole group of identified compounds (99.8%), while oxygenated monoterpenes, hydrogenated sesquiterpenes and oxygenated sesquiterpenes were completely absent in the fruits oil (Table 1).

These findings strongly illustrate that major differences exist between the composition of essential oils from different aerial parts of P. asperula. The oil of fresh fruits appears as a major source for both sabinene (43.5%), and β-phellandrene (36.1%), while aerial parts (stems, leaves and flowers) may together be considered as moderate sources for nerolidol (15.2% and 14.7%, respectively) and p-menth-3-ene (13.3% and 14.9%, respectively). It is interesting to note that β-myrcene (9.2%) seems to characterize the oil of stems and leaves only.

Although, a direct comparison between the composition of combined stems and leaves oils in this study with that reported of leaves is not legitimate (Loizzo et al., 2008b), the most representative constituents of leaves oil in the later study were sabinene (20.6%), and β-phellandrene (19.0%) with no presence of nerolidol or p-menth-3-ene which were the major constituents of our oil (15.2%, 13.3%, respectively). Moreover, only β-phellandrene as the second dominant constituent of the fresh fruit oil herein (36.1%) was also reported among the most representative compounds of the dry fruit of the plant growing in Iran (14.7 %) (Sajjadi et al., 2009). No presence of sabinene which was the major component of our fresh fruits oil (43.5%) was noted.

In general terms, neither of our oils displayed the presence of 2,3,6-trimethyl benzaldehyde or δ-3-carene which were reported as the major constituents in the aerial parts oil of the plant from Iran (18.4% and 18.0%, respectively) (Sajjadi et al., 2009). Comparisons with previous studies on the essential oils of other Prangos species showed considerable quantitative and qualitative variations in yield and composition. In the oils of the flowers/umbels of several other species, the main compounds reported were: β-pinene (35.58%); α-pinene (22.13%) and β-phellandrene (12.54%) in P. peucedanifolia (Brusotti et al., 2013), α-pinene (33.87%) in P. pabularia (Razavi, 2012), epi-globulol (21.1%) and β-elemene (19.7%) in P. scabra (Nazemiyeh et al., 2007a), α-pinene (31.78%) and β-bourbonene (15.9%) in P. uloptera (Nazmiyeh et al., 2007b).

Substantial differences were even also found in three different studies on flowers/umbels oil of P. ferulacea from Iran: β-pinene (20.6 %) (Taherkhani et al., 2012), linalool (19.0%); lavandulyl acetate (16.0%); 1,8-cineole (14.5%); α-pinene (12.4%) and geranyl isobutyrate (12.2%) (Akbari et al., 2010), α-pinene (42.2%) and cis-ocimene (36.3%) (Razavi et al., 2010).

Thus, both the major constituents of the flowers/umbels oil of P. asperula in this present study, p-menth-3-ene (14.9%) and nerolidol (14.7%),which were not previously reported in any of the above mentioned species seem to be distinctive to our plant.

In the fruits oil, similarly to our results sabinene (26.1%) was reported as a major constituent in P. denticulata (Kilic et al., 2010). On the contrary, α-pinene representing the main constituent of P. ferulacea; P. pabularia and P. uloptera (63.1%, 21.46%, 14.98%, respectively) was absent in our plant (Razavi et al., 2010; Razavi, 2012; Nazemiyeh et al., 2007b). In addition, neither of the following reported major constituents was noted in our results: chrysanthenyl acetate (26.53%), limonene (19.59%), α-pinene (19.50%) in P. ferulacea (Massumi et al., 2007); β-elemene (19.9%), β-farnesene (16.2%) in P. scabra (Nazemiyeh et al., 2007a), α-humulene (16.6%); bicyclogermacrene (16.1%); spathulenol (10.6%) in P. pabularia (Özek et al., 2007), germacrene-D-4-ol (42.8%);  α-cadinol (18.5%) in P. bornmuelleri (Başer et al., 1999), γ-terpinene (30.22% and 33.27%), α-pinene (16.71% and 12.83%) in crushed and whole fruits yielded oils of P. ferulacea, respectively (Baser et al., 1996), β-bisabolenal (53.3%) and β-bisabolenol (14.6%) in P. heynlae (Başer et al., 2000), and p-cymene (10.9%) in P. uechtritzii (Özcan et al., 2000).

In conclusion, the above mentioned variability in oil composition from different species cited and P. asperula, sufficient to allow distinction of different chemotypes, are the result of an adaptive process of the plant to a particular ecological conditions (geographical regions, climatic conditions, period of collection, plant part, state of plant- dry or fresh- and extraction methods).

3.1 Antimicrobial activity

The antimicrobial activity of the total essential oil evaluated by the disc diffusion method revealed variable levels of susceptibility in the tested bacteria and fungi (Table 2). S. aureus displayed the highest sensitivity (15.06 mm) which was also more effective than the antibiotic Norfloxacine (9.30 mm). The susceptibility of E. coli came in second place (11.80 mm) followed by A. fumigatus (9.16 mm), T. mentagrophytes (7.3 mm), S. enteritidis (3.8 mm) and C. albicans (1.96) being the least sensitive among the responsive microorganisms. The oil failed to show any response on E. faecalis which was completely resistant to the volatile oil. It may be of a high importance to note that the relatively substantial susceptibility of T. mentagrophytes (7.3 mm) to the oil which was completely resistant to the antifungal Nystatine (10 µg). The MIC/MIF values determined by mean of agar dilution method were 5.0 µl in S. aureus followed by E. coli and A. fumigatus (10 µl), S. enteritidis and T. mentagrophytes (25 µl) and C. albicans (50 µl). Our results are in line with the findings of a previous study testing the oil of the plant from Lebanon against several microorganisms all of which exhibited remarkable activity supporting the traditional use of plant in the treatment of wide range of diseases and confirming its promising potential of the antibacterial properties of this plant oil (Bouaoun et al., 2007). Some of the main compounds are reported to possess antimicrobial activities. In particular, nerolidol, β-phellandrene, sabinene are reported to possess antibacterial and antifungal activity (Togashi et al., 2008; Park et al., 2009; Krist et al., 2015).The findings can further underline the importance of the ethnobotanical approach to select plants that contain new antimicrobial substances, particularly when considering the increased development of resistance of bacteria, fungi and yeast to antibiotics.

Table 2 The mean ± SD growth inhibition zone and MIC/MFC values of the essential oil of Prangos asperula Boiss. growing wild in Lebanon

The strong inhibitory activity of the oils, particularly on S. aureus and T. mentagrophytes, may be related to hydrogenated monoterpene components which constituted 34.1%, 44.7%, 99.8% of the oil of stems and leaves, flowers and fruits, respectively. However, it is difficult to attribute the activity of a complex mixture to a single or group of constituents especially when some evidence that minor components have a critical part to play in antimicrobial activity, possibly by producing a synergistic effect with various components (Cox et al., 2000; Loizzo et al., 2008; Zouari et al., 2010).

4 Conclusion

P. asperula is one of Lebanese indigenous plants which possess many medicinal properties. The study presents for the first time knowledge on the composition of the oils of stems and leaves, flowers and fruits which appear as unique and substantially different from previously reported oils. The antimicrobial activity suggests a potentiality for a new source of antimicrobial compounds to be applied in pharmaceutical industry. Further studies are needed for a better understanding of the biological properties of the oils and their constituents.

References

Akbari M.T., Esmaeili A., Zarea A.H., Saad N., and Bagheri F., 2010, Chemical composition and antibacterial activity of essential oil from leaves, stems and flowers of Prangos ferulacea (L.) Lindl. grown in Iran. Bulgarian Chemical Communications, 42(1): 36-39

Akhlaghi H, 2015, GC/MS Analysis of the Essential Oils from Aerial parts of Prangos latiloba Korov. collected in Northeast Iran. Natural Products Chemistry and Research, 3(158): 2

http://dx.doi.org/10.4172/2329-6836.1000158

Baser K.H.C., Ermin N., Adigüzel N., and Aytac Z., 1996, Composition of the essential oil of Prangos ferulacea (L.) Lindl. Journal of Essential Oil Research, 8(3): 297-298

http://dx.doi.org/10.1080/10412905.1996.9700617

Baser K.H.C., Kürkçüoglu M., and Duman H., 1999, Steam volatiles of the fruits of Prangos bornmuelleri Hub.-Mor. et Reese. Journal of Essential Oil Research, 11(2): 151-152

http://dx.doi.org/10.1080/10412905.1999.9701096

Başer K.H.C., Özek T., Demirci B., and Duman H., 2000, Composition of the essential oil of Prangos heynlae H. Dumanet MF Watson, a new endemic from Turkey. Flavour and Fragrance Journal, 15(1): 47-49

http://dx.doi.org/10.1002/(SICI)1099-1026(200001/02)15:1<47::AID-FFJ869>3.0.CO;2-9

Baytop T., 1999, Tiirkiye’de Bitkiler ile Tedavi-G e 9 mi§- ten Bugüne (Therapy with Medicinal Plants in Turkey-Past and Present). 2nd Ed, Nobel Tip Basimevi, Istanbul, pp.348-349

Bouaoun D., Hilan C., Garabeth F., and Sfeir R., 2007, Antimicrobial activity of the essential oil of the wild plant, Prangos asperula Boiss. Phytotherapie, 5: 129-134

http://dx.doi.org/10.1007/s10298-007-0238-2

Brusotti G., Ibrahim M.F., Dentamaro A., Gilardoni G., Tosi S., Grisoli P., and Vidari G., 2013, Chemical composition and antimicrobial activity of the volatile fractions from leaves and flowers of the wild Iraqi Kurdish plant Prangos peucedanifolia Fenzl. Chemistry & Biodiversity, 10(2): 274-280

http://dx.doi.org/10.1002/cbdv.201200202

European Directorate for the Quality of Medicines, 2008, European Pharmacopoeia 6th Edition

Cox S.D., Mann C.M., Markham J.L., Bell H.C., Gustafson J.E., Warmington J.R., and Wyllie S.G., 2000, The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). Journal of Applied Microbiology, 88(1): 170-175

http://dx.doi.org/10.1046/j.1365-2672.2000.00943.x

Coruh N., Sagdicoglu Celep A.G., and Ozgokce F., 2007, Antioxidant properties of Prangos ferulacea (L.) Lindl., Chaerophyllum macropodum Boiss. and Heracleum persicum Desf. from Apiaceae family used as food in Eastern Anatolia and their inhibitory effects on glutathione-S-transferase. Food Chemistry, 100(3): 1237-1242

http://dx.doi.org/10.1016/j.foodchem.2005.12.006

Davis P.H., 1988, Flora of Turkey and the East Aegean islands (Vol. 10). Edinburgh University Press

Doković D.D., Bulatović V.M., Bozić B.D., Kataranovski M.V., Zrakić T.M., and Kovacević N.N., 2004, 3,5-Nonadiyne isolated from the rhizome of Cachrys ferulacea inhibits endogenous nitric oxide release by rat peritoneal macrophages. Chemical and Pharmaceutical Bulletin, 52(7): 853-854

http://dx.doi.org/10.1248/cpb.52.853

Duran A., Sağıroğlu M., and Duman H., 2005 January, Prangos turcica (Apiaceae), a new species from South Anatolia, Turkey. Finnish Zoological and Botanical Publishing Board, In Annales Botanici Fennici, pp.67-72

Ercan F.S., Hatice B.A.Ş., Murat K.O.Ç., Pandir D., and Öztemiz S., 2013, Insecticidal activity of essential oil of Prangosferulacea (Umbelliferae) against Ephestia kuehniella (Lepidoptera: Pyralidae) and Trichogramma embryophagum (Hymenoptera: Trichogrammatidae). Turkish Journal of Agriculture and Forestry, 37(6): 719-725

http://dx.doi.org/10.3906/tar-1211-15

Grassi P., Novak J., Steinlesberger H., and Franz C., 2004, A direct liquid, non-equilibrium solid-phase micro-extraction application for analysing chemical variation of single peltatetrichomes on leaves of Salvia officinalis. Phytochemical Analysis,15(3): 198-203

http://dx.doi.org/10.1002/pca.769

Kafash-Farkhad N., Asadi-Samani M., and Rafieian-Kopaei M., 2013, A review on phytochemistry and pharmacological effects of Prangos ferulacea (L.) Lindl. Life Science Journal, 10(8s): 360-367

Kılıç C.S., Coşkun M., Duman H., Demirci B., and Başer K.H., 2010, Comparison of the essential oils from fruits and roots of Prangos denticulata Fisch. et Mey. growing in Turkey. Journal of Essential Oil Research, 22(2): 170-173

http://dx.doi.org/10.1080/10412905.2010.9700294

Krist S., Banovac D., Tabanca N., Wedge D.E., Gochev V.K., Wanner J., and Jirovetz L., 2015, Antimicrobial activity of nerolidol and its derivatives against airborne microbes and further biological activities. Natural Product Communications, 10(1): 143-148

Loizzo M.R., Saab A.M., Tundis R., Menichini F., Bonesi M., Piccolo V., and & Menichini F., 2008, In vitro inhibitory activities of plants used in Lebanon traditional medicine against angiotensin converting enzyme (ACE) and digestive enzymes related to diabetes. Journal of Ethnopharmacology, 119(1): 109-116

http://dx.doi.org/10.1016/j.jep.2008.06.003

Loizzo M.R., Tundis R., Menichini F., Saab A.M., and Statti G.A., 2008, Antiproliferative effects of essential oils and their major constituents in human renal adenocarcinoma and amelanotic melanoma cells. Cell Proliferation, 41(6): 1002-1012

http://dx.doi.org/10.1111/j.1365-2184.2008.00561.x

Massumi M.A., Fazeli M.R., Alavi S.H.R., and Ajani Y., 2007, Chemical constituents and antibacterial activity of essential oil of Prangosferulacea (L.) Lindl. Fruits. Iranian Journal of Pharmaceutical Sciences, 3(3): 171-176

Mehregan S.E.S.I., 2003, Chemical Composition of The Essential Oil of Prangos asperula Boiss. Subsp. Haussknechtii (BOISS.) Herrnst. et Heyn Fruits. DARU Journal of Pharmaceutical Sciences, 11(2): 79-81

Mirzaei H.H., and Ramezani Z., 2008, Volatile components of the essential oil of Prangosasperula from West of Iran. Asian Journal of Chemistry, 20(5): 3763

Nazemiyeh H., Razavi S.M., Delazar A., Hajiboland R., Mozaffarian V., Nahar L., and Sarker S.D., 2007, Essential oil composition of the umbels and fruits of Prangos uloptera DC. Natural Product Communications, 2(1): 89-91

Nazemiyeh H., Razavi S.M., Hajiboland R., Delazar A., Esna-Asharii S., Bamdad R., and Sarker S.D., 2007, Composition of the essential oils of Prangosscabra fruits and inflorescence from Iran. Chemistry of Natural Compounds, 43(6): 736-737

http://dx.doi.org/10.1007/s10600-007-0251-6

Novak J., Bahoo L., Mitteregger U., and Franz C., 2006, Composition of individual essential oil glands of savory (Satureja hortensis L., Lamiaceae) from Syria. Flavour and Fragrance Journal, 21(4): 731-734

http://dx.doi.org/10.1002/ffj.1725

Özcan M., Bagci Y., Akgül A., Dural H., and Novak J., 2000, Chemical composition of the essential oil of Prangos uechtritzii Boiss. et hausskn, fruits from turkey, Journal of Essential Oil Research, 12(2): 183-185

Özek G., Özek T., Işcan G., Başer K.H.C., Hamzaoglu E., and Duran A., 2007, Comparison of hydrodistillation and microdistillation methods for the analysis of fruit volatiles of Prangos pabularia Lindl. and evaluation of its antimicrobial activity. South African Journal of Botany,73(4): 563-569

http://dx.doi.org/10.1016/j.sajb.2007.05.002

Park M.J., Gwak K.S., Yang I., Kim K.W., Jeung E.B., Chang J.W., and Choi I.G., 2009, Effect of citral, eugenol, nerolidol and α-terpineol on the ultrastructural changes of Trichophyton mentagrophytes. Fitoterapia, 80(5): 290-296

http://dx.doi.org/10.1016/j.fitote.2009.03.007

Razavi S.M., 2011, Chemical composition and some allelopathic aspects of essential oils of Prangos ferulacea L. Lindl. at different stages of growth. Journal of Agricultural Science and Technology, 14(2): 349-356

Razavi S.M., 2012, Chemical and allelopathic analyses of essential oils of Prangos pabulariaLindl. from Iran. Natural Product Research, 26(22): 2148-2151

Razavi S.M., Nazemiyeh H., Hajiboland R., Kumarasamy Y., Delazar A., Nahar L., and Sarker S.D., 2008, Coumarins from the aerial parts of Prangos uloptera (Apiaceae). Revista Brasileira de Farmacognosia, 18(1): 1-5

http://dx.doi.org/10.1590/S0102-695X2008000100002

Razavi S.M., Nazemiyeh H., Zarrini G., Asna-Asharii S., and Dehghan G., 2010, Chemical composition and antimicrobial activity of essential oil of Prangos ferulacea (L.) Lindl from Iran. Natural Product Research, 24(6): 530-533

http://dx.doi.org/10.1080/14786410802379539

Razavi S.M., Zarrini G., Zahri S., and Mohammadi S., 2010, Biological activity of Prangosuloptera DC roots, a medicinal plant from Iran. Natural Product Research, 24(9): 797-803

http://dx.doi.org/10.1080/14786410802588667

Sadraei H., Shokoohinia Y., Sajjadi S.E., and Ghadirian B., 2012, Antispasmodic effect of osthole and Prangos ferulacea extract on rat uterus smooth muscle motility. Research in Pharmaceutical Sciences, 7: 141–149

Sajjadi S.E., and Mehregan I., 2003, Constituents of essential oil of Prangos asperula subsp. Haussknechtii (Boiss.) Herrnst. et Heyn. fruits. DARU Journal of Pharmaceutical Sciences, 11: 72-79

Sajjadi S.E., Shokoohinia Y., and Gholamzadeh S., 2011, Chemical composition of essential oil of Prangos ferulacea (L.) Lindl. Roots. Chemija, 22(3): 178-80

Sajjadi S.E., Zeinvand H., and Shokoohinia Y., 2009, Isolation and identification of osthol from the fruits and essential oil composition of the leaves of Prangos asperula Boiss. Research in Pharmaceutical Sciences, 4(1): 19-23

Shikishima Y., Takaishi Y., Honda G., Ito M., Takeda Y., Kodzhimatov O.K., and Lee K.H., 2001, Chemical constituents of Prangos tschimganica; Structure Elucidation and Absolute Configuration of Coumarin and Furanocoumarin Derivatives with Anti-HIV Activity. Chemical and Pharmaceutical Bulletin, 49(7): 877-880

http://dx.doi.org/10.1248/cpb.49.877

Tada Y., Shikishima Y., Takaishi Y., Shibata H., Higuti T., Honda G., and Ohmoto Y., 2002, Coumarins and γ-pyrone derivatives from Prangos pabularia: antibacterial activity and inhibition of cytokine release. Phytochemistry, 59(6): 649-654

http://dx.doi.org/10.1016/S0031-9422(02)00023-7

Togashi N., Inoue Y., Hamashima H., and Takano A., 2008, Effects of two terpene alcohols on the antibacterial activity and the mode of action of farnesol against Staphylococcus aureus. Molecules, 13(12): 3069-3076

http://dx.doi.org/10.3390/molecules13123069

Ulubelen A., Topcu G., Tan N., Ölçal S., Johansson C., Üçer M., and Tamer Ş., 1995, Biological activities of a Turkish medicinal plant, Prangosplatychlaena. Journal of Ethnopharmacology, 45(3): 193-197

http://dx.doi.org/10.1016/0378-8741(94)01215-L

Uzel A., Dirmenci T., Celik A., and Arabaci T., 2006, Composition and antimicrobial activity of Prangosplatychlaena and P. Uechtritzii. Chemistry of Natural Compounds, 42(2): 169-171

http://dx.doi.org/10.1007/s10600-006-0069-7

Zouari S., Zouari N., Fakhfakh N., Bougatef A., Ayadi M.A., and Neffati M., 2010, Chemical composition and biological activities of a new essential oil chemotype of Tunisian Artemisia herbaalba Asso. Journal of Medicinal Plants Research, 4(10): 871-880