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Composition of Essential Oils from Roots and Aerial Parts of Carpesium Cernuum and Their Antibacterial and Cytotoxic Activities

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Composition of Essential Oils from Roots and Aerial Parts of Carpesium Cernuum and Their Antibacterial and Cytotoxic Activities molecules Article Composition of Essential Oils from Roots and Aerial Parts of Carpesium cernuum and Their Antibacterial and Cytotoxic Activities Anna Wajs-Bonikowska 1 , Janusz Malarz 2 , Łukasz Szoka 3, Paweł Kwiatkowski 4 and Anna Stojakowska 2,* 1 Institute of General Food Chemistry, Faculty of Biotechnology and Food Sciences, Łód´zUniversity of Technology, Stefanowskiego Street 4/10, 90-924 Łód´z,Poland; [email protected] 2 Maj Institute of Pharmacology, Polish Academy of Sciences, Sm˛etnaStreet 12, 31-343 Kraków, Poland; [email protected] 3 Department of Medicinal Chemistry, Faculty of Pharmacy with the Division of Laboratory Medicine, Medical University of Białystok, Mickiewicza Street 2D, 15-222 Białystok, Poland; [email protected] 4 Department of Diagnostic Immunology, Chair of Microbiology, Immunology and Laboratory Medicine, Pomeranian Medical University in Szczecin, Powsta´nców Wielkopolskich Street 72, 70-111 Szczecin, Poland; [email protected] * Correspondence: [email protected]; Tel.: +481-26-623-254 Abstract: Carpesium cernuum L., one of the two Carpesium species occurring in Europe, in the Far East and India, found use as a vegetable and a traditional medicinal remedy for several ailments. In the present study, compositions of essential oils distilled from roots and shoots of C. cernuum plants, cultivated in the open field, have been studied by GC-MS-FID supported by NMR spectroscopy. The analyses led to the identification of 120 compounds in total, of which 115 were found in aerial parts Citation: Wajs-Bonikowska, A.; and 37 in roots of the plants. The major constituents found in the oil from shoots were: α-pinene (35%) Malarz, J.; Szoka, Ł.; Kwiatkowski, P.; and 2,5-dimethoxy-p-cymene (thymohydroquinone dimethyl ether, 12%), whereas 2,5-dimethoxy-p- Stojakowska, A. Composition of Essential Oils from Roots and Aerial cymene (55%), thymyl isobutyrate (9%) and thymol methyl ether (8%) predominated in the essential Parts of Carpesium cernuum and Their oil obtained from the roots. Antibacterial and cytotoxic activities of the essential oils distilled from Antibacterial and Cytotoxic Activities. C. cernuum were also tested. The essential oil from aerial parts of the plant demonstrated good Molecules 2021, 26, 1883. https:// inhibitory activity against Staphylococcus aureus ATCC 29213 and Escherichia coli ATCC 25922 (MIC: doi.org/10.3390/molecules26071883 15.6 µL/mL). Academic Editor: Laura De Martino Keywords: alpha-pinene; Carpesium cernuum; 2,5-dimethoxy-p-cymene; Inuleae; monoterpenoids; thymohydroquinone dimethyl ether; thymol derivatives Received: 26 February 2021 Accepted: 23 March 2021 Published: 26 March 2021 1. Introduction Publisher’s Note: MDPI stays neutral Although plants of the genus Carpesium (Compositae, subtribe: Inuleae-Inulinae), with regard to jurisdictional claims in have a long history of use as traditional herbal remedies and seasonal food in the Far published maps and institutional affil- iations. East [1–3], they have no tradition of medicinal use in Europe. Majority of the species that belong to the genus are native to China, Japan and Korea, and some are endemic to China. Carpesium cernuum L. is a species native to Eurasia and is currently distributed in Europe, Asia and Australia [4–7]. The plant is a perennial herb, 20–80 cm tall, with an erect branched stem and solitary capitula (15–18 mm), without ray florets, which are subtended by many Copyright: © 2021 by the authors. linear-lanceolate leaves. C. cernuum inhabits waste fields and mountain slopes below Licensee MDPI, Basel, Switzerland. 3000 m [4,5]. The whole plant is medicinally utilized [1]. Recently, anti-inflammatory and This article is an open access article a tumor migration inhibitory effects of extracts from C. cernuum have been described [8,9]. distributed under the terms and conditions of the Creative Commons As a member of the Inuleae-Inulinae subtribe, the genus Carpesium is a close rela- Attribution (CC BY) license (https:// tive to such essential oil-bearing plants as Inula helenium L. and Telekia speciosa (Schreb.) creativecommons.org/licenses/by/ Baumg. [10]. Although many studies on isolation of mono- and sesquiterpenoids from 4.0/). C. cernuum have been published before [1,11–13], data on composition of essential oils Molecules 2021, 26, 1883. https://doi.org/10.3390/molecules26071883 https://www.mdpi.com/journal/molecules Molecules 2021, 26, 1883 2 of 13 produced by the plant are not available. Essential oil from the herb of Carpesium abrotanoides L. was shown to induce apoptosis in hepatocellular carcinoma cells in vitro [14]. However, only 16 components of the examined oil were identified, and the established composition was significantly different from that described earlier [15]. A detailed analysis of essential oils from roots and aerial parts of Carpesium divaricatum Sieb. & Zucc. has been published recently [16], revealing the presence of numerous thymol derivatives, especially in the oil from roots of the plant. The objective of the present study was to examine hitherto unknown chemical compo- sition and biological activity of essential oils from roots and aerial parts of C. cernuum of European origin. Antibacterial activity of the essential oils against both Gram-positive and Gram-negative bacteria has been assessed, as well as cytotoxic activity towards normal and cancer cell lines. 2. Results Though yields of the essential oil produced by aerial parts of C. cernuum were low (0.015 ± 0.002%; see Table1), 115 components of the oil, distilled from shoots of the plant collected at the beginning of flowering time, were identified by GC-MS. The identification was supported by NMR spectra analysis of the corresponding components isolated from the C. cernuum root essential oil. The identified compounds constituted 97.7% of the analyzed oil. Three compounds: α-pinene—the predominant constituent (35%, 3), 2,5- dimethoxy-p-cymene (thymohydroquinone dimethyl ether, 12%, 80) and linalool (4%, 30) (see Figure1) made up about 50% of the essential oil distilled from aerial parts of the plant. Eleven structurally diverse thymol derivatives (55, 80, 88, 89, 114, 115, 120, 121, 126, 127 and 129) composed about 20% of the oil. Structures of six constituents of the essential oil remained unknown. The constituents could not be isolated and spectroscopically analyzed due to their minute amounts in the plant material. Table 1. Chemical composition of essential oils from aerial parts and roots of Carpesium cernuum L. Aerial Arts Roots No Compound RI 1 RI 2 Amount (%) 1 n-Hexanal 0.2 775 769 2 (E)-2-Hexenal 1.7 826 822 3 α-Pinene 34.7 0.1 932 932 4 Camphene 0.1 940 943 5 Thuja-2,4(10)-diene 0.3 944 957 6 Octane-2,3-dione tr 962 967 7 6-Methylhept-5-en-2-one 0.5 963 972 8 1-Octen-3-ol 0.9 964 972 9 β-Pinene 0.6 966 972 10 2-Pentylfuran 0.7 977 977 11 Myrcene 0.3 981 979 12 (E)-2-(2-Pentenyl)furan 0.2 985 983 13 m-Cymene 0.1 993 999 14 α-Terpinene 0.2 1007 1013 15 p-Cymene 0.2 1010 1015 16 1,1,3-Trimethylcyclohexan-3-one 0.2 1011 1019 17 4,6-Dimethylhept-5-en-2-one 0.3 1016 1119 18 Limonene 0.4 1019 1025 19 (Z)-β-Ocimene 0.1 1026 1029 20 2,6-Dimethylhept-5-enal 0.1 1034 1036 21 (E)-β-Ocimene 0.1 1038 1041 22 γ-Terpinene 0.3 1048 1051 23 trans-Linalooloxide (furanoid) 0.2 1057 1058 24 Non-1-en-3-ol 0.2 1068 1064 25 Camphen-6-ol 0.1 1072 1070 26 cis-Linalooloxide (furanoid) tr 1075 1072 Molecules 2021, 26, 1883 3 of 13 Table 1. Cont. Aerial Arts Roots No Compound RI 1 RI 2 Amount (%) 27 p-Cymenene tr 1076 1076 28 Terpinolene 0.1 1078 1082 29 n-Nonanal 0.3 1084 1083 30 Linalool 4.3 1088 1086 31 Oct-1-en-3-yl acetate tr 1096 1096 32 α-Cyclocitral 0.1 1097 1103 33 α-Campholenal 0.4 1104 1105 34 Perillene 0.2 1106 1109 35 + 36 Camphor + Unknown (MS: 123/86/119 M) 0.2 1120 1123 37 trans-Pinocarveol 0.4 1123 1126 38 p-Mentha-1,5-diene-8-ol tr 1125 1127 39 cis-Verbenol 0.1 1129 1132 40 trans-Verbenol 0.2 1130 1137 41 trans-Pinocamphone 0.4 1138 1140 42 + 43 β-Phellandren-8-ol + 4-Ethylbenzaldehyde 0.4 1148 1143 + 1147 α-Phellandren-8-ol + 44 + 45 0.4 5.6 1149 1150 + 1149 (2E)-4-(2-Methyl-1-cyclohexen-1-yl)-2-butenal 46 Terpinen-4-ol 0.5 1162 1164 47 Dimethylsiloxane pentamer (artifact) 0.1 1169 1169 48 α-Terpineol 1.0 1174 1176 49 Myrtenol 0.1 1181 1178 50 n-Decanal 2.2 1187 1180 51 Dihydrocarveol (Isomer 2) tr 1193 1193 52 β-Cyclocitral 0.3 1197 1195 53 trans-Carveol 0.1 1202 1200 54 Nerol 0.1 1214 1210 55 Thymol methyl ether 0.5 8.4 1216 1215 56 β-apo-8-Carotenal 0.1 1236 1236 57 Geraniol 0.5 1238 1238 58 α-Ionene 0.1 1243 1255 59 Thymol tr tr 1269 1267 60 Carvacrol 0.1 1277 1278 61 Dihydroedulan I 0.2 1280 1290 62 Dihydroedulan II 0.4 1283 1296 63 Theaspirane (Isomer 1) 0.1 1290 1299 64 + 65 Myrtenyl acetate + Theaspirane (Isomer 2) 0.2 1305 1313 + 1313 66 γ-Pyronene 0.1 1316 1336 67 cis-Edulan tr 1320 1328 68 Unknown (MS: 79/77/107 M178) 0.1 1324 69 Dehydro-ar-ionene 0.1 1337 1336 70 α-Longipinene 0.1 tr 1350 1360 3-Hydroxy-2,4,4-trimethylpentyl 71 tr 1356 1381 2-methylpropanoate 72 (E)-β-Damascenone 0.2 1363 1361 73 α-Longicyclene tr 1369 1382 74 Unknown (MS: 79/95/107/178 M204) 0.3 1370 – 75 1,2-Dihydro-1,4,6-trimethylnaphthalene 0.1 1372 1373 76 1,2-Dihydro-1,5,8-trimethylnaphthalene 0.1 1375 1376 77 1,4-Dimethoxy-2-tert-butylbenzene tr 1382 1398 78 β-Ionol 0.1 1390 1400 79 7,8-Dihydro-β-ionone 0.2 0.2 1393 1413 2,5-Dimethoxy-p-cymene 80 11.6 54.8 1405 1399 (Thymohydroquinone dimethyl ether) 3 81 2-tert-Butyl-1,4-dimethoxybenzene 0.3 1410 1400 2-tert-Butyl-1,4-dimethoxybenzene 81 + 82 0.4 1417 1400 + Unknown: (MS: 105/119/77/147 M194) 83 Unknown (MS: 123/121/179 M194) 0.1 1421 – Molecules 2021, 26, 1883 4 of 13 Table 1.
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