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Essential oil composition of two Scutellaria species from Iran
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Journal of Traditional Chinese Medical Sciences xxx (xxxx) xxx
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Essential oil composition of two Scutellaria species from Iran Zahra Gharari a, Khadijeh Bagheri a, Hossein Danafar b, Ali Sharafi c,d,* a Department of Plant Production and Genetics, Faculty of Agriculture, University of Zanjan, Zanjan, Iran b School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran c Zanjan Applied Pharmacology Research Center, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran d Zanjan Pharmaceutical Biotechnology Research Center, Zanjan University of Medical Sciences, Zanjan, Iran
Received 4 February 2019; received in revised form 29 July 2019; accepted 30 July 2019
Available online - - -
KEYWORDS 14-b-H-Pregna; GC/MS; a-himachalene; a-Longipinene; Scutellaria
Abstract Objective: Medicinal plants Scutellaria multicaulis and Scutellaria bornmuelleri belong to the Scutellaria genus and Lamiaceae family, and are widely used in traditional Iranian medicine. This study aims to characterize promising bioactive phytochemicals found in the aerial parts of S. multicaulis and S. bornmuelleri. Methods: Accordingly, volatile oils were obtained by hydrodistillation of S. multicaulis and S. bornmuelleri leaves and stems, and then analyzed by gas chromatographyemass spectrometry (GC/MS). Results: A total of 88 components, representing 92.4% of the oil (oil yield determined to be 0.53%, v/w), were identified in the essential oils of S. multicaulis. The main group was sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%), a-longipinene (6.8%), and a-copaene (3.2%) as the main components. A total of 89 chemicals, representing 83.2% of the essential oil (oil yield determined to be 0.31%, v/w), were detected in the essential oil of S. bornmuelleri. The main components were steroids, such as 14-b-H-pregna (32.9%), hydrocarbons (22.5%), sesquiterpenes (11.4%), and monoterpenes (4.6%), which were considered minor constituents. The contents of sesquiterpene and monoterpene hydrocarbons present in S. multicaulis and S. bornmuelleri were 24% and 7.1%, respectively. However, the contribution of oxygenated monoterpenes (4%) and sesquiterpenes (4.3%) in both species was less than 5%. Conclusion: As the first report on the chemical composition of S. multicaulis and S. bornmuelleri, this study showed that the major compounds were steroids and sesquiterpenes.
* Corresponding author. Zanjan Applied Pharmacology Research Center, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran. Fax: þ024 33473639. E-mail addresses: [email protected] (Z. Gharari), [email protected] (K. Bagheri), [email protected] (H. Danafar), [email protected] (A. Sharafi). Peer review under responsibility of Beijing University of Chinese Medicine. https://doi.org/10.1016/j.jtcms.2019.07.003 2095-7548/ª 2019 Beijing University of Chinese Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Z. Gharari et al. ª 2019 Beijing University of Chinese Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/ by-nc-nd/4.0/).
Introduction
Extraction of essential oils
Iran is a vast country with different geographical and climatic features, which has made the wide distribution of medicinal plant species possible. In recent years, the identification of medicinal plant secondary metabolites and their roles in disease treatment and prevention has led to an increase in their use in the pharmaceutical industry and in the preparation of colors, foods, and perfumes. Skullcaps belonging to the Lamiaceae family, which consists of about 360 species of annual or perennial herbs.1 Extracts of this genus are used as traditional herbal medicines worldwide, especially in China.2 Scutellaria baicalensis (Georgi.) is the most famous plant of this genus, and possesses significant health benefits due to its antiviral,3 antioxidant,4 anticonvulsant,5 anti-inflammatory,6 and hepatoprotective7 effects. In Iran, this genus is represented by 20 species and two hybrids, of which 10 species and two hybrids are endemic.8 Two of these endemic species, S. bornmuelleri and S. multicaulis are powerful medicinal herbs that have been popularly used in Iran for thousands of years to prepare various traditional medicines that treat constipation, wounds, and stress.9 These species have also been used in alternative medicine as anti-inflammatory, antispasmodic, and sedative treatments.9 S. multicaulis subsp. multicaulis Boiss is a perennial herb distributed in Tabriz, Iran, that grows on steep westand southwest-facing slopes 1400e1800 m above sea level with an annual rainfall of 230e2700 mm. S. bornmuelleri Hausskn. ex Bornm. ssp. mianensis Rech.f. is an annual herb native to Mianeh city, East Azerbaijan Province, Iran, that grows in light soils and on steep land with south to southwest-facing slopes 1000e1500 m above sea level and an annual rainfall of 200e250 mm. To our knowledge, the odor components of the essential oils of these plants have yet to be reported. Therefore, this study aimed to collect S. bornmuelleri and S. multicaulis plants from their wild habitats in Tabriz, Iran, and analyze the volatile components of their essential oils by GC/MS analysis of the fresh stems and leaves from the plants.
The plant leaves and stems were dried in the shade using an air drying technique, and then powdered with a grinder for use as the crude source. Essential oils were isolated by hydrodistillation in a Clevenger-type apparatus for 3 h. About 100 g (fresh weight) of the ground S. multicaulis and S. bornmuelleri plants was used. After collecting the essential oils, they were dried with anhydrous sodium sulfate (Na2SO4) and stored in dark glass vials at 4 C for later use.
Materials and methods Plant material Aerial parts, comprising the leaves and stems, of S. multicaulis and S. bornmuelleri were collected from Tabriz Province, Iran, during the flowering period (July, 2018). The taxonomic identity of the plants was confirmed by the Biology Department of Tabriz University, Iran.
GC/MS analysis The essential oils was qualitatively analyzed by GC/MS. GC/ MS analysis was performed using a Hewlett-Packard (HP, Palo Alto, CA) HP 7890A system equipped with a UV detector and HP-5 capillary column (HP-5MS, 30 m 0.25 mm i.d.; film thickness, 0.25 mm). Helium (99.999%) was used as the carrier gas at a flow rate of 1 mL/min. The injection port temperature was set to 240 C. The column temperature was initially kept at 40 C for 1 min, followed by a further 5 min at 40 C, and then increased to 240 C at a rate of 3 C/min. The other conditions were as follows: Ionization potential, 70 eV; ion source temperature, 250 C; ionization current, 1000 mA; resolution, 1000; and mass range, 40e300 u.
Compound identification The chemical components of S. bornmuelleri and S. multicaulis were identified based on their mass spectra compared with those in the GC/MS library (WILEY 7n D. 04.00 and NIST08) and by comparison of their relative retention times with those of authentic samples on the HP5 MS capillary column. To determine the retention indices (Kovats indices) of the components, a mixture of alkenes (C6eC24) was added to the essential oils under the same conditions before injecting into the GC/MS system.10
Results Hydrodistillation of the dried aerial parts of S. multicaulis and S. bornmuelleri yielded essential oils (0.31% and 0.53%, respectively) with a golden-yellow color and pleasant aroma. The resulting essential oil constituents were analyzed by GC/MS. The active chemical constituents, and their retention indices (RI), molecular formulas (MF), percentage compositions of the essential oil (%), and molecular weights (MW) from S. multicaulis and S. bornmuelleri are
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species Table 1
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Compounds identified in the essential oil of S. multicaulis by GC/MS.
No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
1 2 3 4 5 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
Octane Cyclohexadiene Nonyl heptafluorobutyrate Fulvene, 6-ethyl-6-methyl 1-Octen-3-ol a-Pinene Decane O-Cymene Benzeneacetaldehyde Pentadecafluorooctanoic acid Acetophenone Linalool Isopropylidene-3-methylhexa-3,5-dienal Naphthalene Diethylphenol Cinnamaldehyde p-Menth-8(10)-en-9-ol, cisa-Citral Nonanoic acid Methyl-2-furanyl)-1-buten-3-one Tridecane Azulene trans-Anethole Thymol Carvacrol a-Longipinene Isoledene Tetradecene Lyratyl acetate a -Copaene (E)-3-Methyl-2-phenyl-2-pentene Dodecanal b-cis-Caryophyllene a-Himachalene Valencene g -Muurolene Pentadecane a-Cadinene Dodecanoic acid Isoaromadendrene epoxide Calarene epoxide Hexadecane Methyl-tridecanoic acid Cyclopropane nonanoic acid Isolongifolol, methyl ether Vulgarol B Pentadecanone Heptadecane (1-Phenyl-1-Butenyl) Benzene b-Acoradienol Tetradecanoic acid Octadecene Octadecane Z-7-Hexadecenal Nonadecane Phthalic acid Methyl palmitoleate
0.1 4.4 t t t t 0.8 t t 0.1 0.5 0.6 0.9 3.2 0.3 0.3 0.4 0.7 0.8 0.3 0.5 3.9 0.2 0.1 0.8 6.8 0.6 0.6 t 3.2 0.2 0.1 2.6 7.2 0.2 0.7 0.2 2.7 0.7 4.3 0.3 0.3 0.3 0.1 1.1 0.7 2.2 0.9 0.6 0.5 0.9 0.2 2.5 0.1 1 3.8 5.6
C8H18 C6H8 C13H19F7O2 C9H12 C8H16O C10H16 C10H22 C10H14 C8H9NO C8HF15O2 C8H8O C10H18O C10H14O C10H8 C10H14O C9H8O C10H18O C10H16O C9H18O2 C9H10O2 C13H28 C10H8 C10H12O C10H14O C10H14O C15H24 C15H24 C14H28 C12H18O2 C15H24 C12H16 C12H24O C15H24 C15H24 C15H24 C15H24 C15H32 C15H24 C12H24O2 C15H24O C15H24O C16H34 C14H28O2 C12H22O2 C16H28O C15H24O C15H30O C17H36 C16H16 C15H24O C14H28O2 C18H36 C18H38 C16H30O C19H40 C8H6O4 C17H32O2
793 851 871 890 980 981 996 1012 1032 1046 1067 1098 1165 1194 1215 1268 1269 1272 1275 1286 1296 1301 1305 1310 1315 1348 1365 1382 1385 1387 1402 1412 1432 1448 1490 1497 1505 1529 1575 1580 1588 1602 1627 1629 1673 1692 1698 1700 1717 1766 1775 1789 1797 1802 1894 1913 1936
114.23 80.13 340.3 120.2 128.22 136.23 142.28 134.22 135.16 414.1 120.15 154.25 150.2 128.2 150.22 132.16 154.25 152.24 158.24 150.17 184.36 128.17 148.21 150.22 150.22 204.36 204.36 196.37 194.27 204.36 160.26 184.32 204.36 204.36 204.36 204.36 212.42 204.36 201.31 220.36 220.35 226.44 228.37 198.31 236.4 220.36 226.4 240.48 208.29 220.35 228.37 252.48 254.50 238.42 268.53 166.13 268.44
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Z. Gharari et al. Table 1 (continued ) No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88
Methylnonadecane Methyl isoheptadecanoate Eicosane 14-b -H-Pregna Heneicosane Octadecanoic acid Phytol Oleic acid cis-13-Octadecenoic acid Docosane Nonadecanoic acid 1-iodo Octadecane Methyl 18-methylnonadecanoate 1-Bromodocosane Octinoxate Octadecenamide, (Z) Tetracosane Pentacosane Tetracosane, 1-bromoDocosanoic acid Methylpentacosane Hexacosane Octacosane 1-iodo Tetracosane Triacontane 1-iodo Hexacosane Hentriacontane 1-iodo Octacosane Tetratriacontane 1-iodo Dotriacontane
0.3 0.8 1.2 0.1 1.3 0.7 0.6 3.8 1 2.9 0.1 0.6 0.3 0.2 0.1 0.4 1.9 0.8 0.6 0.2 0.1 0.5 1.3 0.2 0.6 0.7 0.9 0.3 0.1 t
C20H42 C18H36O2 C20H42 C21H36 C21H44 C18H36O2 C20H40O C18H34O2 C18H34O2 C22H46 C19H38O2 C18H37I C21H42O2 C22H45Br C18H26O3 C18H35NO C24H50 C25H52 C24H49Br C22H44O2 C26H54 C26H54 C28H58 C24H49I C30H62 C26H53I C31H64 C28H58 C34H70 C32H65I
1963 1996 2000 2071 2099 2107 2114 2145 2177 2203 2239 2240 2288 2330 2340 2377 2403 2497 2531 2567 2578 2596 2796 2836 3001 3037 3103 3230 3402 3635
282.55 284.48 282.55 288 296.58 284.48 296.54 282.46 282.46 310.61 298.51 380.39 326.56 389.50 290.40 281.47 338.66 352.69 417.56 340.59 366.71 366.71 394.77 464.55 422.82 492.61 436.85 132.20 478.93 576.76
Note: RI, Kovats retention indices determined on a HP-5 capillary column using the homologous series of n-alkanes (C6eC24); t: Trace, less than 0.05%.
shown in Tables 1 and 2, respectively. In total, 88 and 89 components were detected and characterized, representing 92.4% and 83.2% of the peak area of oil extracted from the leaves and stems of S. multicaulis and S. bornmuelleri, respectively.
S. multicaulis essential oils In the present research, 88 compounds belonging to eight main chemical groups of terpenes, hydrocarbons, alcohols, acids, aldehydes, ketones, acetates, and steroids were identified in S. multicaulis essential oil. The compounds found in the essential oil of S. multicaulis are shown in Table 1. Essential oil analysis showed that the main phytochemicals were as follows: (i) Sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%), a-longipinene (6.8%), and a-copaene (3.2%) as the main components; (ii) hydrocarbons (aliphatic, aromatic, and cyclic hydrocarbons; 24.2%), with cyclohexadiene (4.4%), docosane (2.9%), and tetracosane (1.9%) as the main components; (iii) acids (12.5%), with phthalic acid (3.8%) and oleic acid (3.8%) as the main components; (iv) monoterpene hydrocarbons (7.1%), with azulene (3.9%) and naphthalene (3.2%) as the main components; (v) acetates, with methyl palmitoleate
(5.6%) as the main component; (vi) oxygenated sesquiterpenes (4.3%), with isoaromadendrene epoxide (4.25%) as the main component; and (vii) oxygenated monoterpenes (4%), with carvacrol (0.8%) as the main component. The results also indicated that other compound group were present in low amounts, including amides (0.4%), aldehydes (0.5%), ketones (3%), alcohols (1.7%), and steroids (0.1%). In addition to the above compounds, iodine-containing compounds (1.74%), such as 1-iodo-octacosane, 1-iodo-octadecane, 1-iodohexacosane, 1-iodotetracosane, and 1iododotriacontane, were obtained from S. malticaulis essential oil.
S. bornmuelleri essential oils The compounds identified in the essential oil of S. multicaulis are shown in Table 2. The main compounds found in the essential oil from the leaves and stems of S. bornmuelleri were as follows: (i) Steroids, with 14-b-H-pregna (32.9%) as the main component; (ii) hydrocarbons (aliphatic, aromatic, and cyclic hydrocarbons; 22.5%); (iii) sesquiterpenes (11.4%); (iv) acids (5.4%); (v) monoterpenes (4.6%); and (vi) ketones (3.5%). Among the identified sesquiterpene and monoterpene compounds, hydrocarbon
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species Table 2
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Compounds identified in the essential oil of S. bornmuelleri by GCeMS.
No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
1 2 3 4 5 6 7 8 9 10 11 12 13
Cyclopropane Hexane 3-Buten-2-one Octane 1,3-Cycloheptadiene Nonane 1-Octen-3-ol a-Pinene Decane d 3-Carene Limonene Acetophenone (3S)-3,3a,4,5-Tetrahydro3aa-methyl-2H-benz[e]inden-3a-ol Undecane Linalool 3-Cyclohexene-1-carbinol a-Isophorone Cyclohexane, 1,2,4,5-tetraethyl 1-Dodecene Naphthalene a-Terpineol Dodecane Decanal 4-n-Hexylthiane, S,S-dioxide 1-Naphthalenamine, 4-bromoZ-Citral Azulene Tridecane Carvacrol 1,5,5-Trimethyl-6-methylene-cyclohexene a-Longipinene Cyclosativene a-Copaene Tetradecane Isocaryophyllene 4,6-Dimethyl-2-(2-methylcyclohexyl) phenol b -Bourbonene Calarene Aromadendrene trans-Geranylacetone trans-Caryophyllene b-Chamigrene 2-Oxabicyclo[4.4.0]dec-9-en-8-one, 1,3,7, 7-tetramethyl-, ()-(1R,3S,6R)Ledene Pentadecane Germacrene D (þ)-cuparene Bicyclo[4.4.0]dec-1-ene, 2-isopropyl-5-methyl-9-methyleneCadala 1,4,9-triene d-Cadinene Cis-Alpha-bisabolene b -Cubebene 1,5-epoxysalvial-4(14)-ene Isoaromadendrene epoxide
0.1 0.1 0.2 0.3 t t 0.3 t 0.8 1.5 0.1 1.3 0.1
C3H6 C6H14 C4H6O C8H18 C7H10 C9H20 C8H16O C10H16 C10H22 C10H16 C10H16 C8H8O C14H16O
350 600 643 794 850 900 981 982 998 1021 1035 1067 1076
42.081 86.178 70.091 114.23 94.16 128.26 128.22 136.24 142.29 136.24 136.24 120.15 200.27
0.1 0.8 0.1 t 0.4 0.1 0.9 t 0.2 0.1 0.3 0.1 t 1.2 0.1 0.1 0.3 0.4 t 0.3 0.2 0.1 0.1 0.2 0.5 0.3 0.2 t 0.1 0.2
C11H24 C10H18O C7H12O C9H14O C14H28 C12H24 C10H8 C10H18O C12H26 C10H20O C11H22O2S C10H8BrN C10H16O C10H8 C13H28 C10H14O C10H16 C15H24 C15H24 C15H24 C14H30 C15H24 C15H22O C15H24 C15H24 C15H24 C13H22O C15H24 C15H24 C13H20O2
1098 1100 1108 1119 1137 1190 1192 1198 1202 1204 1231 1254 1270 1299 1304 1317 1331 1347 1369 1389 1398 1411 1430 1433 1437 1440 1456 1474 1475 1481
156.31 154.25 112.17 138.21 196.38 168.32 128.17 154.25 170.34 156.27 218.36 222.09 152.24 128.17 184.37 150.22 136.24 204.36 204.36 204.36 198.39 204.36 218.34 204.36 204.36 204.36 194.32 204.36 204.36 208.3
0.4 0.3 0.8 0.2 1.7
C15H24 C15H32 C15H24 C15H22 C15H24
1492 1500 1503 1504 1510
204.36 212.42 204.36 202.34 204.36
0.3 0.3 0.2 0.9 0.2 0.1
C15H22 C15H24 C15H24 C15H24 C15H24O C15H24O
1528 1532 1538 1544 1557 1583
202.34 204.36 204.36 204.36 220.36 220.36
14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54
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Z. Gharari et al. Table 2 (continued ) No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89
Hexadecane Caryophyllene oxide phenolic acid Spathulenol Phthalic acid 1-Bromo-11-iodoundecane Tridecanoic acid 1-Pentadecene Vulgarol B Heptadecane Aristol-9-en-3-ol Murolan-3,9(11)-diene-10-peroxy Benzyl benzoate Mint sulfide b -Costol Tetradecanoic acid Octadecane Cis-Z-alpha.-Bisabolene epoxide Aniline, 2,3,4,5,6-pentachloro Phytone 1-chloro-Tetradecane Octahydro cembrene Eicosane Palmitic acid 14-b-H-Pregna Linoleic acid Bicyclo[3.3.1]nonane-2,4-dione, 9,9-dimethoxyDocosane Tricosane a-(P-Chlorobenzoyl-P-Chloro Acetophenone Tetracosane 1,2-Benzenedicarboxylic acid Hexacosane Octacosane Pentatriacontane
1.2 0.3 1 0.4 0.4 1.4 0.3 0.1 0.7 1.1 0.6 0.8 0.2 0.2 0.6 0.4 4.1 0.2 0.1 0.7 0.2 1.6 1.3 1.9 32.9 0.9 0.2 1.4 2.9 0.7 4.5 0.5 2 0.5 t
C16H34 C15H24O C7H6O3 C15H24O C8H6O4 C11H22BrI C13H26O2 C15H30 C15H24O C17H36 C15H24O C15H24O2 C14H12O2 C15H24S C15H24O C14H28O2 C18H38 C15H24O C6H2Cl5N C18H36O C14H29Cl C20H40 C20H42 C16H32O2 C21H36 C18H32O2 C11H16O4 C22H46 C23H48 C14H10CL2O C24H50 C18H26O4 C26H54 C28H58 C35H72
1601 1604 1636 1642 1646 1668 1675 1676 1693 1700 1704 1730 1734 1742 1775 1776 1796 1816 1834 1852 1872 1959 1998 2023 2068 2103 2149 2200 2299 2355 2402 2428 2608 2800 3500
226.45 220.36 138.12 220.36 166.13 361.11 214.35 210.41 220.31 240.48 220.36 236.35 212.24 236.41 220.36 228.37 254.5 220.36 265.34 268.49 232.83 280.53 282.55 256.43 288 280.45 212.25 310.61 324.64 265.13 338.66 306.40 366.71 394.77 492.96
Note: RI, Kovats retention indices determined on a HP-5 capillary column using the homologous series of n-alkanes (C6eC24); t: Trace, less than 0.05%.
sesquiterpenes (7.1%) and hydrocarbon monoterpenes (3.7%) were the major components. However, the amounts of oxygenated sesquiterpenes (4.3%) and oxygenated monoterpenes (0.9%) were low. Among the hydrocarbons obtained from S. bornmuelleri essential oil, tetracosane (4.5%), octadecane (4.1%), and tricosane (2.9%) had the highest contents. The amounts of three other groups, namely, acetates (0.2%), aldehydes (0.1%), and alcohols (0.5%), were very low. Furthermore, metal-linked compounds 1-chlorotetradecane (0.2%), 1-bromo-11-iodoundecane (1.4%), and diethylmethyl borane (2.2%) were found in S. bornmuelleri essential oil.
Discussion In this study, essential oils from the leaves and stems of S. multicaulis and S. bornmuelleri were isolated and analyzed for the first time. However, several studies evaluating the volatile oil composition of other Scutellaria species and
subspecies have been reported.11,12 In most studies on the composition of essential oils extracted from the Scutellaria genus, the main chemical components reported were sesquiterpene hydrocarbons, with differences in the amount of each component among species. For example, the principal components of S. baicalensis and Scutellaria californica flowers from India and USA, respectively, were b-caryophyllene, germacrene D, and a-humulene.13,14 Meanwhile, b-caryophyllene has been described as the major constituent of both Scutellaria albida essential oil from Turkey and S. sieberi oil from Greece.15,16 Furthermore, analysis of the essential oil of Scutellaria luteocaerulea11 and S. pinnatifida12 from Iran and Scutellaria rubicunda from Italy17 showed that caryophyllene and germacrene-D were the major sesquiterpene hydrocarbons. However, caryophyllenes and germacrene D have not been isolated as main constituents in the essential oils of Scutellaria barbata from China,18 Scutellaria rupestris from Greece,16 Scutellaria volubilis from Ecuador,19 and S.
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species Table 3 No
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Bioactivities and structures of main components obtained from S. multicaulis and S. bornmuelleri essential oils. compound
Biological activity
Structure 29
1
Oleic acid
apoptotic activity in tumor cells
2
Phthalic acid
Insecticidal activities against oriental armyworms and diamondback moths30
3
Isoaromadendrene epoxide
Antibacterial activity31
4
Linoleic acid
Antibacterial activity,32 treat skin-related disorders related to deficiency33
5
Phytol
6
Azulene
Anxiolytic, metabolism-modulating, cytotoxic, antioxidant, autophagyand apoptosis-inducing, anti-nociceptive, anti-inflammatory, immune-modulating, and antimicrobial effects34 Cytotoxic activity against human oral tumor cell lines35
7
Acetophenone
Antifungal activity, anti-bacterial36
8
Naphthalene
Antibiotic properties with minimum toxicity37
9
copaene
Antioxidant38
10
Caryophyllene oxide
Anticancer and analgesic properties39
11
14-b-H-Pregna
It is a defense chemical and has Diabetic retinopathy prevention23
12
d 3-Carene
Anti-inflammatory activity40
13
trans-anethole
Antioxidant, anti-inflammatory,41 Anti-viral42
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Z. Gharari et al. Table 3 (continued ) No
compound
Biological activity
Structure
14
Palmitic acid
Selective cytotoxicity to human leukemic cells
15
Spathulenol
Antifungal activity44
16
Vulgarol B
Antifungal45
multicaulis and S. bornmuelleri from Iran. In the essential oil of S. multicaulis, similar to that of other Scutellaria species, the main compound group was sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%) and a-longipinene (6.8%) as the principal components. Chaudhary et al. (2014) have shown that the aryl derivatives of himachalene (isomeric mixture of a, b, and g-himachalenes from Cedrus deodara essential oil) has potential antimicrobial activity against some Gram-positive bacteria and mycotoxigenic fungi.20 a-Longipinene, a bridged sesquiterpene compound was found in large amounts in the essential oil of S. multicaulis (6.8%) compared with that of S. bornmuelleri. Derivatives of the aforementioned constituents showed antifeedant and cytotoxic activity against herbivorous insects Spodoptera littoralis, Rhopalosiphum padi, and Myzus persicae.21 Recently, Manoharan et al. (2010) reported the inhibitory activity of a-longipinene on
Table 4 Comparison of major compound groups obtained from two Scutellaria species in Iran.
43
biofilm and hyphal formation of Candida albicans. Furthermore, a-longipinene reduced the virulence of C. albicans in Caenorhabditis elegans.22 The bioactivities and structures of the main components obtained from S. multicaulis and S. bornmuelleri essential oils are shown in Table 3. The main component of the essential oil obtained from S. bornmuelleri was 14-b-H-pregna (32.9%). However, in the essential oil of S. multicaulis, the 14-b-H-pregna content was very low (0.1%). 14-b-H-Pregna was identified in Scutellaria plants for the first time in this study. The high content was probably due to the environmental impact of this region of Iran on the contents of essential oils obtained from these species. 14-b-H-Pregna is a steroid considered to be a sex pheromone specific to males, and is also a defensive chemical with diabetic retinopathy prevention and treatment effects.23 The presence of 14-b-H-pregna has been reported in the essential oils and different parts of some plants, including Urginea indica Kunth,24 Allium rotundum,25 Gundelia tournefortii L,26 Citrus limon,27 and Cenchrus biflorus.28 Dehpour et al. reported that 14-b-Hpregna was the major compound in the essential oil of flower A. rotundum, which displayed antibacterial activity at concentrations of <1/200 (v/v).25
Compound
S. multicaulis
S. bornmuelleri
Oxygenated sesquiterpene Sesquiterpene hydrocarbons Oxygenated monoterpene Monoterpene hydrocarbons Hydrocarbons Ketones Aldehydes Alcohols Acids Acetates Steroids Amides Metal-linked compounds Total
5.8%
4.3%
24%
7.1%
Conclusions
4%
0.9%
7.1%
3.7%
24.2% 3% 0.5% 1.7% 12.5% 6.8% 0.1% 0.4 2.3% 92.4%
22.5% 3.5% 0.1% 0.5% 5.4% 0.2% 32.9% e 2.1% 83.2%
Analysis of the essential oils of S. multicaulis and S. bornmuelleri showed that they contained different major constituents (Table 4). The major constituents of S. bornmuelleri essential oil were steroids (14-b-H-pregna), while those of S. multicaulis were sesquiterpene hydrocarbons (a-himachalene (7.16%) and a-longipinene (6.82%)). Therefore, based on contradictory reports on the essential oil composition, it can be suggested that this difference resulted from the effects of the genotype, environment, and soil nature on the contents of essential oil compounds. As most of the chemical compounds derived from the essential oils of these plants were biologically active compounds, these plants can be used as a herbal source of drug compounds in future pharmaceutical studies.
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species
Funding This work was supported by the University of Zanjan and the School of Pharmacy, Zanjan University of Medical Sciences.
Conflicts of interest The authors declare that there are no conflicts of interest regarding the publication of this article.
CRediT authorship contribution statement Zahra Gharari: Project administration, Investigation, Formal analysis and Writing ‒ original draft. Khadijeh Bagheri: Supervision, Conceptualization and Writing ‒ original draft. Ali Sharafi: Supervision, Resources, Funding acquisition and Writing ‒ review & editing. Hossein Danafar: Formal analysis, Methodology, Validation, Visualization and Software.
Acknowledgment The authors would like to thank the School of Pharmacy, Zanjan University of Medical Sciences, for their support.
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Essential oil composition of two Scutellaria species from Iran Zahra Gharari a, Khadijeh Bagheri a, Hossein Danafar b, Ali Sharafi c,d,* a Department of Plant Production and Genetics, Faculty of Agriculture, University of Zanjan, Zanjan, Iran b School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran c Zanjan Applied Pharmacology Research Center, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran d Zanjan Pharmaceutical Biotechnology Research Center, Zanjan University of Medical Sciences, Zanjan, Iran
Received 4 February 2019; received in revised form 29 July 2019; accepted 30 July 2019
Available online - - -
KEYWORDS 14-b-H-Pregna; GC/MS; a-himachalene; a-Longipinene; Scutellaria
Abstract Objective: Medicinal plants Scutellaria multicaulis and Scutellaria bornmuelleri belong to the Scutellaria genus and Lamiaceae family, and are widely used in traditional Iranian medicine. This study aims to characterize promising bioactive phytochemicals found in the aerial parts of S. multicaulis and S. bornmuelleri. Methods: Accordingly, volatile oils were obtained by hydrodistillation of S. multicaulis and S. bornmuelleri leaves and stems, and then analyzed by gas chromatographyemass spectrometry (GC/MS). Results: A total of 88 components, representing 92.4% of the oil (oil yield determined to be 0.53%, v/w), were identified in the essential oils of S. multicaulis. The main group was sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%), a-longipinene (6.8%), and a-copaene (3.2%) as the main components. A total of 89 chemicals, representing 83.2% of the essential oil (oil yield determined to be 0.31%, v/w), were detected in the essential oil of S. bornmuelleri. The main components were steroids, such as 14-b-H-pregna (32.9%), hydrocarbons (22.5%), sesquiterpenes (11.4%), and monoterpenes (4.6%), which were considered minor constituents. The contents of sesquiterpene and monoterpene hydrocarbons present in S. multicaulis and S. bornmuelleri were 24% and 7.1%, respectively. However, the contribution of oxygenated monoterpenes (4%) and sesquiterpenes (4.3%) in both species was less than 5%. Conclusion: As the first report on the chemical composition of S. multicaulis and S. bornmuelleri, this study showed that the major compounds were steroids and sesquiterpenes.
* Corresponding author. Zanjan Applied Pharmacology Research Center, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan, Iran. Fax: þ024 33473639. E-mail addresses: [email protected] (Z. Gharari), [email protected] (K. Bagheri), [email protected] (H. Danafar), [email protected] (A. Sharafi). Peer review under responsibility of Beijing University of Chinese Medicine. https://doi.org/10.1016/j.jtcms.2019.07.003 2095-7548/ª 2019 Beijing University of Chinese Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Z. Gharari et al. ª 2019 Beijing University of Chinese Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/ by-nc-nd/4.0/).
Introduction
Extraction of essential oils
Iran is a vast country with different geographical and climatic features, which has made the wide distribution of medicinal plant species possible. In recent years, the identification of medicinal plant secondary metabolites and their roles in disease treatment and prevention has led to an increase in their use in the pharmaceutical industry and in the preparation of colors, foods, and perfumes. Skullcaps belonging to the Lamiaceae family, which consists of about 360 species of annual or perennial herbs.1 Extracts of this genus are used as traditional herbal medicines worldwide, especially in China.2 Scutellaria baicalensis (Georgi.) is the most famous plant of this genus, and possesses significant health benefits due to its antiviral,3 antioxidant,4 anticonvulsant,5 anti-inflammatory,6 and hepatoprotective7 effects. In Iran, this genus is represented by 20 species and two hybrids, of which 10 species and two hybrids are endemic.8 Two of these endemic species, S. bornmuelleri and S. multicaulis are powerful medicinal herbs that have been popularly used in Iran for thousands of years to prepare various traditional medicines that treat constipation, wounds, and stress.9 These species have also been used in alternative medicine as anti-inflammatory, antispasmodic, and sedative treatments.9 S. multicaulis subsp. multicaulis Boiss is a perennial herb distributed in Tabriz, Iran, that grows on steep westand southwest-facing slopes 1400e1800 m above sea level with an annual rainfall of 230e2700 mm. S. bornmuelleri Hausskn. ex Bornm. ssp. mianensis Rech.f. is an annual herb native to Mianeh city, East Azerbaijan Province, Iran, that grows in light soils and on steep land with south to southwest-facing slopes 1000e1500 m above sea level and an annual rainfall of 200e250 mm. To our knowledge, the odor components of the essential oils of these plants have yet to be reported. Therefore, this study aimed to collect S. bornmuelleri and S. multicaulis plants from their wild habitats in Tabriz, Iran, and analyze the volatile components of their essential oils by GC/MS analysis of the fresh stems and leaves from the plants.
The plant leaves and stems were dried in the shade using an air drying technique, and then powdered with a grinder for use as the crude source. Essential oils were isolated by hydrodistillation in a Clevenger-type apparatus for 3 h. About 100 g (fresh weight) of the ground S. multicaulis and S. bornmuelleri plants was used. After collecting the essential oils, they were dried with anhydrous sodium sulfate (Na2SO4) and stored in dark glass vials at 4 C for later use.
Materials and methods Plant material Aerial parts, comprising the leaves and stems, of S. multicaulis and S. bornmuelleri were collected from Tabriz Province, Iran, during the flowering period (July, 2018). The taxonomic identity of the plants was confirmed by the Biology Department of Tabriz University, Iran.
GC/MS analysis The essential oils was qualitatively analyzed by GC/MS. GC/ MS analysis was performed using a Hewlett-Packard (HP, Palo Alto, CA) HP 7890A system equipped with a UV detector and HP-5 capillary column (HP-5MS, 30 m 0.25 mm i.d.; film thickness, 0.25 mm). Helium (99.999%) was used as the carrier gas at a flow rate of 1 mL/min. The injection port temperature was set to 240 C. The column temperature was initially kept at 40 C for 1 min, followed by a further 5 min at 40 C, and then increased to 240 C at a rate of 3 C/min. The other conditions were as follows: Ionization potential, 70 eV; ion source temperature, 250 C; ionization current, 1000 mA; resolution, 1000; and mass range, 40e300 u.
Compound identification The chemical components of S. bornmuelleri and S. multicaulis were identified based on their mass spectra compared with those in the GC/MS library (WILEY 7n D. 04.00 and NIST08) and by comparison of their relative retention times with those of authentic samples on the HP5 MS capillary column. To determine the retention indices (Kovats indices) of the components, a mixture of alkenes (C6eC24) was added to the essential oils under the same conditions before injecting into the GC/MS system.10
Results Hydrodistillation of the dried aerial parts of S. multicaulis and S. bornmuelleri yielded essential oils (0.31% and 0.53%, respectively) with a golden-yellow color and pleasant aroma. The resulting essential oil constituents were analyzed by GC/MS. The active chemical constituents, and their retention indices (RI), molecular formulas (MF), percentage compositions of the essential oil (%), and molecular weights (MW) from S. multicaulis and S. bornmuelleri are
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species Table 1
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Compounds identified in the essential oil of S. multicaulis by GC/MS.
No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
1 2 3 4 5 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
Octane Cyclohexadiene Nonyl heptafluorobutyrate Fulvene, 6-ethyl-6-methyl 1-Octen-3-ol a-Pinene Decane O-Cymene Benzeneacetaldehyde Pentadecafluorooctanoic acid Acetophenone Linalool Isopropylidene-3-methylhexa-3,5-dienal Naphthalene Diethylphenol Cinnamaldehyde p-Menth-8(10)-en-9-ol, cisa-Citral Nonanoic acid Methyl-2-furanyl)-1-buten-3-one Tridecane Azulene trans-Anethole Thymol Carvacrol a-Longipinene Isoledene Tetradecene Lyratyl acetate a -Copaene (E)-3-Methyl-2-phenyl-2-pentene Dodecanal b-cis-Caryophyllene a-Himachalene Valencene g -Muurolene Pentadecane a-Cadinene Dodecanoic acid Isoaromadendrene epoxide Calarene epoxide Hexadecane Methyl-tridecanoic acid Cyclopropane nonanoic acid Isolongifolol, methyl ether Vulgarol B Pentadecanone Heptadecane (1-Phenyl-1-Butenyl) Benzene b-Acoradienol Tetradecanoic acid Octadecene Octadecane Z-7-Hexadecenal Nonadecane Phthalic acid Methyl palmitoleate
0.1 4.4 t t t t 0.8 t t 0.1 0.5 0.6 0.9 3.2 0.3 0.3 0.4 0.7 0.8 0.3 0.5 3.9 0.2 0.1 0.8 6.8 0.6 0.6 t 3.2 0.2 0.1 2.6 7.2 0.2 0.7 0.2 2.7 0.7 4.3 0.3 0.3 0.3 0.1 1.1 0.7 2.2 0.9 0.6 0.5 0.9 0.2 2.5 0.1 1 3.8 5.6
C8H18 C6H8 C13H19F7O2 C9H12 C8H16O C10H16 C10H22 C10H14 C8H9NO C8HF15O2 C8H8O C10H18O C10H14O C10H8 C10H14O C9H8O C10H18O C10H16O C9H18O2 C9H10O2 C13H28 C10H8 C10H12O C10H14O C10H14O C15H24 C15H24 C14H28 C12H18O2 C15H24 C12H16 C12H24O C15H24 C15H24 C15H24 C15H24 C15H32 C15H24 C12H24O2 C15H24O C15H24O C16H34 C14H28O2 C12H22O2 C16H28O C15H24O C15H30O C17H36 C16H16 C15H24O C14H28O2 C18H36 C18H38 C16H30O C19H40 C8H6O4 C17H32O2
793 851 871 890 980 981 996 1012 1032 1046 1067 1098 1165 1194 1215 1268 1269 1272 1275 1286 1296 1301 1305 1310 1315 1348 1365 1382 1385 1387 1402 1412 1432 1448 1490 1497 1505 1529 1575 1580 1588 1602 1627 1629 1673 1692 1698 1700 1717 1766 1775 1789 1797 1802 1894 1913 1936
114.23 80.13 340.3 120.2 128.22 136.23 142.28 134.22 135.16 414.1 120.15 154.25 150.2 128.2 150.22 132.16 154.25 152.24 158.24 150.17 184.36 128.17 148.21 150.22 150.22 204.36 204.36 196.37 194.27 204.36 160.26 184.32 204.36 204.36 204.36 204.36 212.42 204.36 201.31 220.36 220.35 226.44 228.37 198.31 236.4 220.36 226.4 240.48 208.29 220.35 228.37 252.48 254.50 238.42 268.53 166.13 268.44
(continued on next page)
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Z. Gharari et al. Table 1 (continued ) No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88
Methylnonadecane Methyl isoheptadecanoate Eicosane 14-b -H-Pregna Heneicosane Octadecanoic acid Phytol Oleic acid cis-13-Octadecenoic acid Docosane Nonadecanoic acid 1-iodo Octadecane Methyl 18-methylnonadecanoate 1-Bromodocosane Octinoxate Octadecenamide, (Z) Tetracosane Pentacosane Tetracosane, 1-bromoDocosanoic acid Methylpentacosane Hexacosane Octacosane 1-iodo Tetracosane Triacontane 1-iodo Hexacosane Hentriacontane 1-iodo Octacosane Tetratriacontane 1-iodo Dotriacontane
0.3 0.8 1.2 0.1 1.3 0.7 0.6 3.8 1 2.9 0.1 0.6 0.3 0.2 0.1 0.4 1.9 0.8 0.6 0.2 0.1 0.5 1.3 0.2 0.6 0.7 0.9 0.3 0.1 t
C20H42 C18H36O2 C20H42 C21H36 C21H44 C18H36O2 C20H40O C18H34O2 C18H34O2 C22H46 C19H38O2 C18H37I C21H42O2 C22H45Br C18H26O3 C18H35NO C24H50 C25H52 C24H49Br C22H44O2 C26H54 C26H54 C28H58 C24H49I C30H62 C26H53I C31H64 C28H58 C34H70 C32H65I
1963 1996 2000 2071 2099 2107 2114 2145 2177 2203 2239 2240 2288 2330 2340 2377 2403 2497 2531 2567 2578 2596 2796 2836 3001 3037 3103 3230 3402 3635
282.55 284.48 282.55 288 296.58 284.48 296.54 282.46 282.46 310.61 298.51 380.39 326.56 389.50 290.40 281.47 338.66 352.69 417.56 340.59 366.71 366.71 394.77 464.55 422.82 492.61 436.85 132.20 478.93 576.76
Note: RI, Kovats retention indices determined on a HP-5 capillary column using the homologous series of n-alkanes (C6eC24); t: Trace, less than 0.05%.
shown in Tables 1 and 2, respectively. In total, 88 and 89 components were detected and characterized, representing 92.4% and 83.2% of the peak area of oil extracted from the leaves and stems of S. multicaulis and S. bornmuelleri, respectively.
S. multicaulis essential oils In the present research, 88 compounds belonging to eight main chemical groups of terpenes, hydrocarbons, alcohols, acids, aldehydes, ketones, acetates, and steroids were identified in S. multicaulis essential oil. The compounds found in the essential oil of S. multicaulis are shown in Table 1. Essential oil analysis showed that the main phytochemicals were as follows: (i) Sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%), a-longipinene (6.8%), and a-copaene (3.2%) as the main components; (ii) hydrocarbons (aliphatic, aromatic, and cyclic hydrocarbons; 24.2%), with cyclohexadiene (4.4%), docosane (2.9%), and tetracosane (1.9%) as the main components; (iii) acids (12.5%), with phthalic acid (3.8%) and oleic acid (3.8%) as the main components; (iv) monoterpene hydrocarbons (7.1%), with azulene (3.9%) and naphthalene (3.2%) as the main components; (v) acetates, with methyl palmitoleate
(5.6%) as the main component; (vi) oxygenated sesquiterpenes (4.3%), with isoaromadendrene epoxide (4.25%) as the main component; and (vii) oxygenated monoterpenes (4%), with carvacrol (0.8%) as the main component. The results also indicated that other compound group were present in low amounts, including amides (0.4%), aldehydes (0.5%), ketones (3%), alcohols (1.7%), and steroids (0.1%). In addition to the above compounds, iodine-containing compounds (1.74%), such as 1-iodo-octacosane, 1-iodo-octadecane, 1-iodohexacosane, 1-iodotetracosane, and 1iododotriacontane, were obtained from S. malticaulis essential oil.
S. bornmuelleri essential oils The compounds identified in the essential oil of S. multicaulis are shown in Table 2. The main compounds found in the essential oil from the leaves and stems of S. bornmuelleri were as follows: (i) Steroids, with 14-b-H-pregna (32.9%) as the main component; (ii) hydrocarbons (aliphatic, aromatic, and cyclic hydrocarbons; 22.5%); (iii) sesquiterpenes (11.4%); (iv) acids (5.4%); (v) monoterpenes (4.6%); and (vi) ketones (3.5%). Among the identified sesquiterpene and monoterpene compounds, hydrocarbon
Please cite this article as: Gharari Z et al., Essential oil composition of two Scutellaria species from Iran, Journal of Traditional Chinese Medical Sciences, https://doi.org/10.1016/j.jtcms.2019.07.003
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Essential oil composition of two Scutellaria species Table 2
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Compounds identified in the essential oil of S. bornmuelleri by GCeMS.
No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
1 2 3 4 5 6 7 8 9 10 11 12 13
Cyclopropane Hexane 3-Buten-2-one Octane 1,3-Cycloheptadiene Nonane 1-Octen-3-ol a-Pinene Decane d 3-Carene Limonene Acetophenone (3S)-3,3a,4,5-Tetrahydro3aa-methyl-2H-benz[e]inden-3a-ol Undecane Linalool 3-Cyclohexene-1-carbinol a-Isophorone Cyclohexane, 1,2,4,5-tetraethyl 1-Dodecene Naphthalene a-Terpineol Dodecane Decanal 4-n-Hexylthiane, S,S-dioxide 1-Naphthalenamine, 4-bromoZ-Citral Azulene Tridecane Carvacrol 1,5,5-Trimethyl-6-methylene-cyclohexene a-Longipinene Cyclosativene a-Copaene Tetradecane Isocaryophyllene 4,6-Dimethyl-2-(2-methylcyclohexyl) phenol b -Bourbonene Calarene Aromadendrene trans-Geranylacetone trans-Caryophyllene b-Chamigrene 2-Oxabicyclo[4.4.0]dec-9-en-8-one, 1,3,7, 7-tetramethyl-, ()-(1R,3S,6R)Ledene Pentadecane Germacrene D (þ)-cuparene Bicyclo[4.4.0]dec-1-ene, 2-isopropyl-5-methyl-9-methyleneCadala 1,4,9-triene d-Cadinene Cis-Alpha-bisabolene b -Cubebene 1,5-epoxysalvial-4(14)-ene Isoaromadendrene epoxide
0.1 0.1 0.2 0.3 t t 0.3 t 0.8 1.5 0.1 1.3 0.1
C3H6 C6H14 C4H6O C8H18 C7H10 C9H20 C8H16O C10H16 C10H22 C10H16 C10H16 C8H8O C14H16O
350 600 643 794 850 900 981 982 998 1021 1035 1067 1076
42.081 86.178 70.091 114.23 94.16 128.26 128.22 136.24 142.29 136.24 136.24 120.15 200.27
0.1 0.8 0.1 t 0.4 0.1 0.9 t 0.2 0.1 0.3 0.1 t 1.2 0.1 0.1 0.3 0.4 t 0.3 0.2 0.1 0.1 0.2 0.5 0.3 0.2 t 0.1 0.2
C11H24 C10H18O C7H12O C9H14O C14H28 C12H24 C10H8 C10H18O C12H26 C10H20O C11H22O2S C10H8BrN C10H16O C10H8 C13H28 C10H14O C10H16 C15H24 C15H24 C15H24 C14H30 C15H24 C15H22O C15H24 C15H24 C15H24 C13H22O C15H24 C15H24 C13H20O2
1098 1100 1108 1119 1137 1190 1192 1198 1202 1204 1231 1254 1270 1299 1304 1317 1331 1347 1369 1389 1398 1411 1430 1433 1437 1440 1456 1474 1475 1481
156.31 154.25 112.17 138.21 196.38 168.32 128.17 154.25 170.34 156.27 218.36 222.09 152.24 128.17 184.37 150.22 136.24 204.36 204.36 204.36 198.39 204.36 218.34 204.36 204.36 204.36 194.32 204.36 204.36 208.3
0.4 0.3 0.8 0.2 1.7
C15H24 C15H32 C15H24 C15H22 C15H24
1492 1500 1503 1504 1510
204.36 212.42 204.36 202.34 204.36
0.3 0.3 0.2 0.9 0.2 0.1
C15H22 C15H24 C15H24 C15H24 C15H24O C15H24O
1528 1532 1538 1544 1557 1583
202.34 204.36 204.36 204.36 220.36 220.36
14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54
(continued on next page)
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Z. Gharari et al. Table 2 (continued ) No
Compound
Percentage (%)
Mol. formula
RI
Mol. wt. (g/mol)
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89
Hexadecane Caryophyllene oxide phenolic acid Spathulenol Phthalic acid 1-Bromo-11-iodoundecane Tridecanoic acid 1-Pentadecene Vulgarol B Heptadecane Aristol-9-en-3-ol Murolan-3,9(11)-diene-10-peroxy Benzyl benzoate Mint sulfide b -Costol Tetradecanoic acid Octadecane Cis-Z-alpha.-Bisabolene epoxide Aniline, 2,3,4,5,6-pentachloro Phytone 1-chloro-Tetradecane Octahydro cembrene Eicosane Palmitic acid 14-b-H-Pregna Linoleic acid Bicyclo[3.3.1]nonane-2,4-dione, 9,9-dimethoxyDocosane Tricosane a-(P-Chlorobenzoyl-P-Chloro Acetophenone Tetracosane 1,2-Benzenedicarboxylic acid Hexacosane Octacosane Pentatriacontane
1.2 0.3 1 0.4 0.4 1.4 0.3 0.1 0.7 1.1 0.6 0.8 0.2 0.2 0.6 0.4 4.1 0.2 0.1 0.7 0.2 1.6 1.3 1.9 32.9 0.9 0.2 1.4 2.9 0.7 4.5 0.5 2 0.5 t
C16H34 C15H24O C7H6O3 C15H24O C8H6O4 C11H22BrI C13H26O2 C15H30 C15H24O C17H36 C15H24O C15H24O2 C14H12O2 C15H24S C15H24O C14H28O2 C18H38 C15H24O C6H2Cl5N C18H36O C14H29Cl C20H40 C20H42 C16H32O2 C21H36 C18H32O2 C11H16O4 C22H46 C23H48 C14H10CL2O C24H50 C18H26O4 C26H54 C28H58 C35H72
1601 1604 1636 1642 1646 1668 1675 1676 1693 1700 1704 1730 1734 1742 1775 1776 1796 1816 1834 1852 1872 1959 1998 2023 2068 2103 2149 2200 2299 2355 2402 2428 2608 2800 3500
226.45 220.36 138.12 220.36 166.13 361.11 214.35 210.41 220.31 240.48 220.36 236.35 212.24 236.41 220.36 228.37 254.5 220.36 265.34 268.49 232.83 280.53 282.55 256.43 288 280.45 212.25 310.61 324.64 265.13 338.66 306.40 366.71 394.77 492.96
Note: RI, Kovats retention indices determined on a HP-5 capillary column using the homologous series of n-alkanes (C6eC24); t: Trace, less than 0.05%.
sesquiterpenes (7.1%) and hydrocarbon monoterpenes (3.7%) were the major components. However, the amounts of oxygenated sesquiterpenes (4.3%) and oxygenated monoterpenes (0.9%) were low. Among the hydrocarbons obtained from S. bornmuelleri essential oil, tetracosane (4.5%), octadecane (4.1%), and tricosane (2.9%) had the highest contents. The amounts of three other groups, namely, acetates (0.2%), aldehydes (0.1%), and alcohols (0.5%), were very low. Furthermore, metal-linked compounds 1-chlorotetradecane (0.2%), 1-bromo-11-iodoundecane (1.4%), and diethylmethyl borane (2.2%) were found in S. bornmuelleri essential oil.
Discussion In this study, essential oils from the leaves and stems of S. multicaulis and S. bornmuelleri were isolated and analyzed for the first time. However, several studies evaluating the volatile oil composition of other Scutellaria species and
subspecies have been reported.11,12 In most studies on the composition of essential oils extracted from the Scutellaria genus, the main chemical components reported were sesquiterpene hydrocarbons, with differences in the amount of each component among species. For example, the principal components of S. baicalensis and Scutellaria californica flowers from India and USA, respectively, were b-caryophyllene, germacrene D, and a-humulene.13,14 Meanwhile, b-caryophyllene has been described as the major constituent of both Scutellaria albida essential oil from Turkey and S. sieberi oil from Greece.15,16 Furthermore, analysis of the essential oil of Scutellaria luteocaerulea11 and S. pinnatifida12 from Iran and Scutellaria rubicunda from Italy17 showed that caryophyllene and germacrene-D were the major sesquiterpene hydrocarbons. However, caryophyllenes and germacrene D have not been isolated as main constituents in the essential oils of Scutellaria barbata from China,18 Scutellaria rupestris from Greece,16 Scutellaria volubilis from Ecuador,19 and S.
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Essential oil composition of two Scutellaria species Table 3 No
7
Bioactivities and structures of main components obtained from S. multicaulis and S. bornmuelleri essential oils. compound
Biological activity
Structure 29
1
Oleic acid
apoptotic activity in tumor cells
2
Phthalic acid
Insecticidal activities against oriental armyworms and diamondback moths30
3
Isoaromadendrene epoxide
Antibacterial activity31
4
Linoleic acid
Antibacterial activity,32 treat skin-related disorders related to deficiency33
5
Phytol
6
Azulene
Anxiolytic, metabolism-modulating, cytotoxic, antioxidant, autophagyand apoptosis-inducing, anti-nociceptive, anti-inflammatory, immune-modulating, and antimicrobial effects34 Cytotoxic activity against human oral tumor cell lines35
7
Acetophenone
Antifungal activity, anti-bacterial36
8
Naphthalene
Antibiotic properties with minimum toxicity37
9
copaene
Antioxidant38
10
Caryophyllene oxide
Anticancer and analgesic properties39
11
14-b-H-Pregna
It is a defense chemical and has Diabetic retinopathy prevention23
12
d 3-Carene
Anti-inflammatory activity40
13
trans-anethole
Antioxidant, anti-inflammatory,41 Anti-viral42
(continued on next page)
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Z. Gharari et al. Table 3 (continued ) No
compound
Biological activity
Structure
14
Palmitic acid
Selective cytotoxicity to human leukemic cells
15
Spathulenol
Antifungal activity44
16
Vulgarol B
Antifungal45
multicaulis and S. bornmuelleri from Iran. In the essential oil of S. multicaulis, similar to that of other Scutellaria species, the main compound group was sesquiterpene hydrocarbons (24%), with a-himachalene (7.2%) and a-longipinene (6.8%) as the principal components. Chaudhary et al. (2014) have shown that the aryl derivatives of himachalene (isomeric mixture of a, b, and g-himachalenes from Cedrus deodara essential oil) has potential antimicrobial activity against some Gram-positive bacteria and mycotoxigenic fungi.20 a-Longipinene, a bridged sesquiterpene compound was found in large amounts in the essential oil of S. multicaulis (6.8%) compared with that of S. bornmuelleri. Derivatives of the aforementioned constituents showed antifeedant and cytotoxic activity against herbivorous insects Spodoptera littoralis, Rhopalosiphum padi, and Myzus persicae.21 Recently, Manoharan et al. (2010) reported the inhibitory activity of a-longipinene on
Table 4 Comparison of major compound groups obtained from two Scutellaria species in Iran.
43
biofilm and hyphal formation of Candida albicans. Furthermore, a-longipinene reduced the virulence of C. albicans in Caenorhabditis elegans.22 The bioactivities and structures of the main components obtained from S. multicaulis and S. bornmuelleri essential oils are shown in Table 3. The main component of the essential oil obtained from S. bornmuelleri was 14-b-H-pregna (32.9%). However, in the essential oil of S. multicaulis, the 14-b-H-pregna content was very low (0.1%). 14-b-H-Pregna was identified in Scutellaria plants for the first time in this study. The high content was probably due to the environmental impact of this region of Iran on the contents of essential oils obtained from these species. 14-b-H-Pregna is a steroid considered to be a sex pheromone specific to males, and is also a defensive chemical with diabetic retinopathy prevention and treatment effects.23 The presence of 14-b-H-pregna has been reported in the essential oils and different parts of some plants, including Urginea indica Kunth,24 Allium rotundum,25 Gundelia tournefortii L,26 Citrus limon,27 and Cenchrus biflorus.28 Dehpour et al. reported that 14-b-Hpregna was the major compound in the essential oil of flower A. rotundum, which displayed antibacterial activity at concentrations of <1/200 (v/v).25
Compound
S. multicaulis
S. bornmuelleri
Oxygenated sesquiterpene Sesquiterpene hydrocarbons Oxygenated monoterpene Monoterpene hydrocarbons Hydrocarbons Ketones Aldehydes Alcohols Acids Acetates Steroids Amides Metal-linked compounds Total
5.8%
4.3%
24%
7.1%
Conclusions
4%
0.9%
7.1%
3.7%
24.2% 3% 0.5% 1.7% 12.5% 6.8% 0.1% 0.4 2.3% 92.4%
22.5% 3.5% 0.1% 0.5% 5.4% 0.2% 32.9% e 2.1% 83.2%
Analysis of the essential oils of S. multicaulis and S. bornmuelleri showed that they contained different major constituents (Table 4). The major constituents of S. bornmuelleri essential oil were steroids (14-b-H-pregna), while those of S. multicaulis were sesquiterpene hydrocarbons (a-himachalene (7.16%) and a-longipinene (6.82%)). Therefore, based on contradictory reports on the essential oil composition, it can be suggested that this difference resulted from the effects of the genotype, environment, and soil nature on the contents of essential oil compounds. As most of the chemical compounds derived from the essential oils of these plants were biologically active compounds, these plants can be used as a herbal source of drug compounds in future pharmaceutical studies.
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Essential oil composition of two Scutellaria species
Funding This work was supported by the University of Zanjan and the School of Pharmacy, Zanjan University of Medical Sciences.
Conflicts of interest The authors declare that there are no conflicts of interest regarding the publication of this article.
CRediT authorship contribution statement Zahra Gharari: Project administration, Investigation, Formal analysis and Writing ‒ original draft. Khadijeh Bagheri: Supervision, Conceptualization and Writing ‒ original draft. Ali Sharafi: Supervision, Resources, Funding acquisition and Writing ‒ review & editing. Hossein Danafar: Formal analysis, Methodology, Validation, Visualization and Software.
Acknowledgment The authors would like to thank the School of Pharmacy, Zanjan University of Medical Sciences, for their support.
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