Volatile metabolites of Pistacia atlantica Desf. from Greece
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1 358 FLAVOUR O. TZAKOU AND FRAGRANCE ET AL. JOURNAL Flavour Fragr. J. 2007; 22: Published online 15 May 2007 in Wiley InterScience ( Volatile metabolites of Pistacia atlantica Desf. from Greece Olga Tzakou, 1 * Ioannis Bazos 2 and Artemios Yannitsaros 2 1 Division of Pharmacognosy and Chemistry of Natural Products, Department of Pharmacy, University of Athens, Panepistimioupoli Zographou, Athens, Greece 2 Institute of Systematic Botany, Section of Ecology and Systematics, Department of Biology, University of Athens, Panepistimioupoli Zographou, Athens, Greece Received 30 September 2006; Revised 31 January 2007; Accepted 4 February 2007 ABSTRACT: The essential oils of leaves (from male and female plants), unripe fruits and leaf-buds of different samples of Pistacia atlantica collected from Greek East Aegean islands (Kalimnos and Lesvos) were analysed by GC MS and GC. Qualitative and quantitative differences among the samples and different organs of the plant were observed. The oils were rich in monoterpenes. The main components in the leaf oil from the female plants were myrcene (17.8%, 24.8%) and terpinen-4-ol (11.6%, 6.0%) in the Kalimnos and Lesvos samples, respectively, while in the leaf oil from the male plants terpinen-4-ol (17.3% Kalimnos) and p-mentha-1(7),8-diene (41.1%, Lesvos) were the dominant constituents. The major components in unripe fruits were terpinen-4-ol (25.7%, 8.9%), myrcene (20.2%, 34.5%) and sabinene (14.9%, 19.5%). In the leaf-buds oils sabinene (52.1%) and α-pinene (11.6%) were the main constituents in the Kalimnos sample, while in the Lesvos sample the major constituent was p-mentha-1(7),8-diene (42.4%). Copyright 2007 John Wiley & Sons, Ltd. KEY WORDS: Pistacia atlantica; Anacardiaceae; essential oil; GC MS; leaves; unripe fruits; leaf-buds; female plants; male plants Introduction Pistacia is a small genus of the family Anacardiaceae, with about 10 species, which are shrubs or trees. 1,2 Pistacia atlantica Desf. is a long-living, dioecious, deciduous, variable, usually low tree, sometimes reaching 20 m height, with compound imparipinnate leaves with two to four (five) pairs of leaflets, which are variable in shape, size and colour and with a characteristic more or less winged rhachis. 1,3 5 This is a character in which it differs mainly from the somewhat similar species, P. terebinthus L. The fruits are small, also variable drupes, blue-black when they are ripe, ripening in autumn. As a result of this great variability, a number of subspecies or varieties have been described. 5 P. atlantica is a thermophilous xerophyte, which grows in dry stony or rocky hillsides, edges of fields, roadsides, near the base of dry stone walls and other similar habitats. It is considered to be an Irano-Turanian species with distribution from south-west Asia to north-west Africa (Morocco). There occur also isolated groups of stands from its compact range in Greece, Cyprus, Cyrenaica, southern Crimea and the Canary Islands. 5 In Greece it occurs on some of the Aegean Islands (Thasos, Limnos, * Correspondence to: O. Tzakou, University of Athens, Department of Pharmacy, Division of Pharmacognosy and Chemistry of Natural Products, Panepistimioupoli Zographou, Athens, Greece. tzakou@pharm.uoa.gr Lesvos, Chios, Patmos, Kalimnos, Kos, Chalki, Simi, Tilos, Rodos, Milos) 6 and in a single locality on the mainland (E. Peloponnisos), 7 but the status of the species in most cases is not clear because there are also cultivated individuals as a shade tree. 5,6 The fruits of P. atlantica smell like mastic and are sometimes used on Lesvos island in the distillation of grapes to flavour the alcoholic drink called raki. These fruits in Lesvos are called tsikuda and are also occasionally chewed by the local people (for mouth flavouring). The fruits of P. atlantica are also used for tanning 3 and as fodder for cattle. 5 They contain oil, which is used for soap making. 3 From the bark of the wood, a resin is collected for laquer production and it is also used in popular medicine (as an antiseptic to wounds, etc.). 3,5 In Iran, the oleoresin of P. atlantica var. mutica is a popular naturally occurring chewing gum and has been used traditionally in the treatment of peptic ulcers. 8 In Morocco, P. atlantica is important because it is the source of mastic gum, an exudate which strengthens gums, deodorizes breath and combats coughs, chills and stomach diseases. 9 In Jordan, P. atlantica is one of the plants widely recommended by herbalists and used for its hypoglycaemic activity. 10 Previous studies on P. atlantica deal with fatty acids and sterols from the fruit oil, 11 and the chemical composition of the oleoresin of P. atlantica var. mutica from Iran 8 and oil analyses of the leaves, fruits and resin from Morocco. 9 In our continuing research on the essential oils of aromatic Greek species herein, the composition of the
2 VOLATILE METABOLITES OF PISTACIA ATLANTICA 359 essential oil of leaves (from male and female plants), unripe fruits and leaf-buds of P. atlantica is reported, using GC and GC MS analyses. Materials and Methods Plant Material Fresh leaves, unripe fruits and leaf-buds of P. atlantica plants (female and male), growing spontaneously on the East Aegean islands of Kalimnos and Lesvos, were collected during Representative samples from several individuals in each locality were transported in paper bags in small freezer to the laboratory. Voucher specimens are deposited in the Herbarium of the University of Athens (ATHU) and the samples were as follows: 1. Kalimnos, Arginonta, leaves of female plants and unripe fruits (Bazos 4243). 2. Kalimnos, Arginonta, leaves and leaf buds of male plants (Bazos 4243a). 3. Lesvos, NNW of Vrisa, leaves of female plants and unripe fruits (Bazos 4275). 4. Lesvos, between Mesotopos and Tavari, leaves and leaf buds of male plants (Bazos 4283). Reference Compounds Authentic reference chemicals were purchased from Sigma Chemical Co (St Louis, MO, USA). Recovery of Essential Oils The fresh plant material was cut in small pieces (<0.5 cm) and the essential oils were isolated twice for each sample by hydrodistillation for 3 h using a modified Clevenger-type apparatus. The obtained oils were dried over anhydrous sodium sulphate and stored under a nitrogen atmosphere in amber vials at 4 6 C until they were submitted to GC MS analysis. All oils were analysed within 24 h of their production. Based on the estimated obtained volume of essential oil, the corresponding amount of capillary GC grade pentane was added to afford an appropriate concentration of 10 µl/ml. Gas Chromatography Mass Spectrometry (GC MS) The chemical composition of the oils was analysed using GC and GC MS. GC MS analyses were carried out using a Hewlett Packard GC MS system operating in the EI mode at 70 ev, equipped with a split/splitless injector (200 C). The transfer line temperature was 250 C. Helium was used as carrier gas (1 ml/min) and the capillary column used was HP 5MS (30 m 0.25 mm; film thickness 0.25 µm). The initial temperature of the column was 60 C and was raised to 280 C at a 3 C/min rate. Split ratio was 1:10. The injected volume was 1 µl. Gas Chromatography GC analyses were carried out using a SRI 8610C GC-FID system, equipped with DB-5 capillary column (30 m 0.32 mm i.d., film thickness 0.25 µm) and connected to a FID detector. The injector and detector temperatures were set to 280 C. The carrier gas was helium at a flow rate of 1.2 ml/min. The thermal program was the same as that used for the GC MS analyses. Each analysis was made at least twice. Relative percentage amounts were calculated on the basis of peak areas. Identification of the Components The identification of the chemical constituents was based on comparison of their relative retention indices (RRI), retention times (RT) and mass spectra with those obtained from authentic samples and/or the NIST/NBS, Wiley libraries and the literature. 12 Results and Discussion Sixty-seven components were identified, accounting for % of the total essential oils. The components of the essential oils are listed in Table 1 in order of their experimental relative retention indices (RRI) from the HP 5MS column and the percentage contribution is the mean value of two analyses. All the essential oils exhibited a light yellow to yellow-green colour and a strong odour. The oil yields, calculated from fresh material, were % for leaves, % for unripe fruits (v/w) and traces for leaf-bud oils. In the female plants, the essential oils of the leaves consisted mainly of monoterpenes. Among the monoterpenes the hydrocarbons predominated (44.3% Kalimnos, 52.2% Lesvos), with myrcene (17.8%, 24.8%), sabinene (7.8%, 5.2%) and terpinen-4-ol (11.6%, 6.0%) being the main components. In unripe fruits monoterpenes accounted for 85.6% (Kalimnos) and 82.2% (Lesvos) of the entire essential oil. The components characterizing unripe fruit oils were sabinene (14.9% Kalimnos, 19.5% Lesvos), myrcene (10.2% Kalimnos, 34.5% Lesvos), terpinen-4-ol (25.7% Kalimnos, 8.9% Lesvos) and p-cymene (10.0% Kalimnos).
3 360 O. TZAKOU ET AL. Table 1. Percentage composition of the essential oils of Pistacia atlantica Components RRI a RI b Kalimnos collections Lesvos collections Identification KLeaves KUfruits KLeaves KLbuds LLeaves LUfruits LLeaves LLbuds Tricyclene t t t t t t t MS, Co GC α-thujene t t MS, Co GC α-pinene MS, Co GC Camphene t t 2.5 t t t t MS Sabinene t t MS, Co GC β-pinene t t 2.9 t t t t t MS, Co GC Myrcene t t MS, Co GC α-phellandrene t t t t MS, Co GC p-mentha-1(7),8-diene t t t t t MS α-terpinene t t MS p-cymene t t t t MS, Co GC β-phellendrene MS (Z)-β-Ocimene t t t t MS Benzene acetaldehyde t MS (E)-β-Ocimene t 1.0 t t t t t MS γ-terpinene t t MS, Co GC cis-sabinene hydrate t t MS Terpinolene MS, Co GC p-cymenene t MS trans-sabinene hydrate t t MS Nonanal t t t t MS 1,3,8-p-Menthatriene t t t MS endo-fenchol t t MS cis-p-menth-2-en-1-ol t t t t MS Camphor t t MS, Co GC Terpinen-4-ol t t MS, Co GC p-cymen-8-ol MS α-terpineol t 0.7 t 0.9 t MS, Co GC cis-piperitol t 0.5 t t t MS trans-piperitol t t t t t MS endo-fenchyl acetate t MS cis-sabinene hydrate acetate t MS Bornyl acetate t t t 0.9 t t MS α-cubebene t t MS, Co GC α-longipinene t t MS α-ylangene t MS α-copaene t t t t t t MS β-bourbonene t t t t t t t MS β-cubebene t t t t MS α-gurjunene t t t t MS (E)-Caryophyllene MS, Co GC β-ylangene MS β-gurjunene t t t t t t t MS cis-muurola-3,5-diene t t MS trans-muurola-3,5-diene t t t MS α-humulene t 1.3 t 0.9 t t t MS allo-aromadendrene t 0.4 t 1.2 MS trans-cadina-1(6),4-diene t t MS Germacrene D MS trans-muurola-4(14),5-diene t t 0.4 t t MS epi-cubebol t t MS Bicyclogermacrene t t t t t t t MS α-muurolene t t t t t t MS (E,E)-α-Farnesene t 1.9 t 2.5 t MS γ-cadinene t t t t t t t MS, Co GC Cubebol t 0.6 t 1.7 MS δ-cadinene t 1.7 t MS, Co GC Zonarene t t t t MS trans-cadina-1(2),4-diene t MS α-cadinene t t t t t t MS Germacrene D-4-ol t 1.5 MS 1,10-di-epi-Cubenol t 0.8 t 1.1 t MS 10-epi-γ-Eudesmol t t MS epi-α-cadinol t t t MS epi-α-muurolol t t t MS
4 VOLATILE METABOLITES OF PISTACIA ATLANTICA 361 Table 1. (Continued) Components RRI a RI b Kalimnos collections Lesvos collections Identification KLeaves KUfruits KLeaves KLbuds LLeaves LUfruits LLeaves LLbuds α-muurolol t t t t 1.2 t MS α-cadinol t 1.9 t t MS Identified components (%) Grouped components Monoterpene hydrocarbons Oxygenated monoterpenes t t Sesquiterpene hydrocarbons Oxygenated sesquiterpenes 3.6 t 1.9 t a RRI, relative retention indices calculated against C 9 C 24 n-alkanes on the HP 5MS column. b RI, retention indices reported in the literature. 12 KLeaves and LLeaves, leaves from female plants; KLeaves and LLeaves, leaves from male plants; KUfruits and LUfruits, unripe fruits; KLbuds, LLbuds, male leaf-buds; t, concentration <0.1%; MS, identification by RRI and comparison with mass spectra; Co GC, retention time identical to authentic compounds. In the male plants, the major components of the Kalimnos leaf oil were sabinene (7.5%), α-pinene (5.1%) and terpinen-4-ol (17.3%), whereas in the Lesvos leaf oil p-mentha-1(7),8-diene was the predominant monoterpene (41.1%). The essential oils of leaf-buds were characterized also by the abundance of monoterpenes. The main constituents in the Kalimnos sample were sabinene (52.1%), α-pinene (11.6%) and terpinen-4-ol (10.1%), while in the Lesvos sample p-mentha-1(7),8-diene (42.4%) was the dominant component. It is interesting that in the Lesvos leaf-bud oil sesquiterpenes amounted to 47.6% with germacrene D (20.3%) being the main component, whereas in the Kalimnos leaf-bud oil sesquiterpenes were present in low amount. The most predominant differences between the samples were observed in the leaf-bud oils and in the leaf oils from male plants. All the essential oils were characterized by high percentages of monoterpenes, mainly hydrocarbon derivatives, except in the Kalimnos leaf oil from male plants and the Lesvos leaf-bud oil, in which monoterpenes and sesquiterpenes were present in equal amounts. It is interesting to note that the leaf oil (probably from female plants) of P. atlantica from Morocco was rich in sesquiterpene compounds (41.1%), with elemol and β-eudesmol being the major constituents, compounds not detected in our corresponding oils. 9 The oil of the Moroccan fruits was determined to be rich in oxygenated monoterpenes, with bornyl acetate being the most predominant compound (21.5%), whereas in the studied fruit oils this was detected only in traces. 9 Comparison with previous studies on the most closely related species, P. terebinthus and P. palaestina, shows a variability that seems to depend on plant species and plant organ. Although P. terebinthus is morphologically closely related to P. atlantica, the composition of leaf oils was different. In Turkish P. terebinthus leaf oil the monoterpenes terpinen-4-ol (33.7%), γ-terpinene (9.3%) and α-terpineol (8.1%) were reported as the main compounds, 13 while in P. atlantica leaf oils the main compounds were myrcene and sabinene, with the exception of leaf oil from the Lesvos male plants, where p-mentha-1(7),8-diene was the dominant monoterpene. In the essential oil of unripe fruits from P. terebinthus of Turkish origin, limonene (34.2%), α-pinene (15.6%) and β-pinene (11.5%) were reported as the major constituents, 14 while in P. atlantica myrcene, sabinene and terpinen-4-ol were detected as the main compounds. In a recent study, Flamini et al. 15 reported on the chemical composition of P. palaestina (closely related to P. terebinthus, and considered by some botanists as a subspecies or variety of it); the main compounds in the leaf oil were α-pinene (63.1%) and myrcene (13.3%) and in unripe fruit oil (E)-ocimene (41.3%) and sabinene (20.3%). The vast amount of literature deals with the chemical composition of P. lentiscus essential oils, where a considerable variability in the terpene composition is also observed The common feature for the samples of P. atlantica studied, as well as for the most studied Pistacia species, is the biosynthesis of monoterpenoids as the main class of compounds in their essential oils, irrespective of the observed variability of the terpene composition of the oils. References 1. Meickle RD. Flora of Cyprus, vol. 1. The Bentham Moxon Trust, Royal Botanic Gardens: Kew, 1977; Arabatzis Th. I. Dendra ke thamnoi stin Ellada (Shrubs and Trees in Greece), vol. 2. Oikologiki Kinisi Dramas-TEI Kavalas: Drama, 2001; (In Greek). 3. Yaltirik F. Pistacia L. In Flora of Turkey and the East Aegean Islands, vol. 2, Davis PH (ed.). Edinburgh University Press: Edinburgh, 1967; Tutin TG. Pistacia L. In Flora Europaea, vol. 2, Tutin TG, Heywood VH, Burges NA et al. (eds). Cambridge University Press: Cambridge, 1968; 237.
5 362 O. TZAKOU ET AL. 5. Browicz K. Chorology of Trees and Shrubs in South-West Asia and Adjacent Regions, vol. 6. Polish Scientific Publishers: Warszawa-Poznañ, 1988; Bazos I, Yannitsaros A. Edinburgh J. Bot. 2004; 61: Rechinger KH. fil. Flora Aegaea. Akad. Wiss. Wien, Math.- Naturwiss. Kl. Denkschr. 1943; 105(1). 8. Delazar A, Reid RG, Sarker SD. Chem. Nat. Comp. 2004; 40: Barrero AF, Herrador MM, Arteaga JF et al. J. Essent. Oil Res. 2004; 17: Hamdam II, Afifi FU. J. Ethnopharm. 2004; 93: Yousfi M, Nedjmi B, Bellal R, Ben Bertal D, Palla G. J. Am. Oil Chem. Soc. 2002; 79: Adams RP. Identification of Essential Oil Components by Gas Chromatography/Quadrupole Mass Spectrometry. Allured: Carol Stream, IL, Duru ME, Cakir A, Kordali S et al. Fitoterapia 2003; 74: Couladis M, Özcan M, Tzakou O, Akgül A. J. Sci. Food Agric. 2003; 83: Flamini G, Badder A, Cioni PL, Katbeh-Bader A, Morelli I. J. Agric. Food Chem. 2004; 52: Castola V, Bighelli A, Casanova J. Biochem. Syst. Ecol. 2000; 28: Zrira S, Elamrani A, Benjilali B. Flavour Fragr. J. 2003; 18: Vidrich V, Fusi P, Graziano A et al. J. Essent. Oil Res. 2004; 16: Congiu R, Falconieri D, Marongiu B, Piras A, Porcedda S. Flavour Fragr. J. 2002; 17: Douissa FB, Hayder N, Chekir-Ghedira L et al. Flavour Fragr. J. 2005; 20: Boelens MH, Jimenez R. Flavour Fragr. J. 1991; 6: Calabro G, Curro P. Essenze Deriv. Agrum. 1974; 44: Fleisher Z, Flisher A. J. Essent. Oil Res. 1992; 4: Magiatis P, Melliou E, Skaltsounis AL, Chinou IB, Mitaku S. Planta Med. 1999; 65: Fernadez A, Camacho A, Fernadez C, Altarejos J. J. Essent. Oil Res. 2000; 12:
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