Skip to main content
PMC home page
Plants logoLink to Plants
. 2021 Mar 4;10(3):482. doi: 10.3390/plants10030482

The Volatile Phytochemistry of Monarda Species Growing in South Alabama

Sims K Lawson 1, Prabodh Satyal 2, William N Setzer 2,3,*
Editors: Jésus Palá-Pául, Joseph Brophy, Laura Cornara
PMCID: PMC8000036  PMID: 33806521

Abstract

The genus Monarda (family Lamiaceae) contains 22 species of which three are native to southern Alabama, M. citriodora, M. fistulosa, and M. punctata. Several species of Monarda have been used in traditional medicines of Native Americans, and this present study is part of an ongoing project to add to our understanding of Native American pharmacopeia. Plant material from M. citriodora, M. fistulosa, and M. punctata was collected in south Alabama and the essential oils obtained by hydrodistillation. The essential oils were analyzed by gas chromatographic techniques to determine the chemical compositions as well as enantiomeric distributions. The compounds thymol, carvacrol, p-cymene, and their derivatives were the primary terpenoid components found in the essential oils. The known biological activities of these compounds are consistent with the traditional uses of Monarda species to treat wounds, skin infections, colds, and fevers.

Keywords: Monarda citriodora, Monarda fistulosa, Monarda punctata, essential oil, thymol, carvacrol, p-cymene

1. Introduction

The Plant List [1] shows 22 different Monarda L. (Lamiaceae) species, 18 of which occur in the United States [2]. There are three Monarda species native to south Alabama, namely Monarda citriodora Cerv. ex Lag., Monarda fistulosa L., and Monarda punctata L. (see Figure 1) [2].

Figure 1.

Figure 1

Open in a new tab

Monarda species discussed in this work (photographs by S. K. L).

Several Monarda species have been used by Native Americans as medicinal plants [3]. For example, M. fistulosa was used by the Blackfoot, Navajo, Lakota, and Winnebago people to treat boils, cuts and wounds; the Cherokee, Chippewa, Flathead, Ojibwa, and Tewa used the plant to treat colds, fever, and influenza; the Crow, Lakota, Menominee, and Ojibwa used the plant for coughs, catarrh, and other respiratory problems. Monarda punctata was used by the Delaware, Mohegan Nanticoke, and Navajo tribes to treat colds, fever coughs, and catarrh.

Both M. citriodora and M. fistulosa are popular ornamentals and have been introduced to temperate locations around the world [4,5,6]. Geographical location likely plays an important role in the phytochemistry of Monarda species. To our knowledge, however, there have been no previous examinations of M. citriodora, M. fistulosa, or M. punctata growing in their native range of south Alabama. In this work, we have examined the chemical compositions and enantiomeric distributions of essential oils of the three Monarda species from south Alabama.

2. Results

2.1. Monarda Citriodora

The M. citriodora essential oils were obtained as clear orange oils. The essential oil yields for M. citriodora aerial parts essential oil were 1.59% and 1.79% for samples #1 and #2, respectively, while the root essential oil was obtained in 0.879% yield. The chemical compositions of the essential oils from the aerial parts and the roots of M. citriodora cultivated in south Alabama are summarized in Table 1. The essential oils were dominated by the phenolic monoterpenoids thymol (RIdb = 1289) and carvacrol (RIdb = 1296). The other major components were p-cymene (RIdb = 1024) and thymol methyl ether (RIdb = 1239).

Table 1.

Essential oil compositions of Monarda citriodora cultivated in south Alabama.

Aerial Parts Essential Oil Root Essential Oil
RIcalc RIdb Compound #1, % ED, (+):(−) #2, % ED, (+):(−) #2, % ED, (+):(−)
923 925 α-Thujene 1.0 69.0:31.0 0.8 66.6:33.4 0.5 64.2:35.8
930 932 α-Pinene 0.3 84.2:15.8 0.3 62.8:37.2 0.2 74.5:25.5
947 950 Camphene tr tr tr
970 971 Sabinene tr tr ---
975 978 β-Pinene 0.1 64.5:35.5 0.1 0.1
976 974 1-Octen-3-ol 0.7 0.7 0.5
983 984 3-Octanone 0.1 0.2 0.3
987 989 Myrcene 0.7 0.4 0.3
995 996 3-Octanol 0.2 0.3 0.3
1002 1004 Octanal tr tr ---
1003 1004 p-Mentha-1(7),8-diene tr --- ---
1005 1006 α-Phellandrene 0.1 95.1:4.9 0.1 100:0 tr 100:0
1007 1008 δ-3-Carene 0.1 100:0 0.1 100:0 0.1 100:0
1015 1017 α-Terpinene 1.8 100:0 1.1 100:0 0.7 100:0
1016 1022 m-Cymene tr tr ---
1023 1024 p-Cymene 7.8 6.4 7.2
1027 1030 Limonene 0.5 26.7:73.3 0.4 63.3:36.7 0.3 57.3:42.7
1028 1029 β-Phellandrene 0.2 0:100 0.1 0:100 0.1 0:100
1030 1033 Benzyl alcohol --- --- 0.4
1030 1030 1,8-Cineole 0.2 0.3 0.2
1055 1057 γ-Terpinene 1.7 0.5 0.2
1067 1069 cis-Sabinene hydrate 0.8 95.3:4.7 1.0 89.5:10.5 0.9 90.7:9.3
1083 1086 Terpinolene tr tr tr
1084 1086 trans-Linalool oxide (furanoid) --- tr 0.1
1087 1093 p-Cymenene --- --- tr
1098 1099 Linalool 0.1 71.9:28.1 0.1 49.7:50.3 0.3 50.1:49.9
1099 1099 trans-Sabinene hydrate tr 76.5:23.5 0.3 71.1:28.9 0.3 66.8:33.2
1165 1167 exo-Acetoxycamphene --- --- 0.1
1169 1170 Borneol 0.1 0:100 0.1 0:100 0.3 0:100
1178 1180 Terpinen-4-ol 0.4 60.2:39.8 0.4 58.5:41.5 1.9 20.9:79.1
1183 1186 p-Cymen-8-ol --- --- 0.1
1187 1190 Methyl salicylate tr --- ---
1195 1195 α-Terpineol 0.1 100:0 0.1 100:0 0.2 100:0
1196 1197 Methyl chavicol (= Estragole) --- 1.5 ---
1236 1239 Thymol methyl ether 4.4 5.6 11.3
1252 1252 Thymoquinone 0.2 0.7 1.3
1253 1246 Carvone tr 39.9:60.1 --- ---
1290 1289 Thymol 38.2 37.0 29.0
1297 1296 Carvacrol 38.3 39.9 38.3
1305 1309 4-Vinylguaiacol --- --- 0.1
1306 1306 iso-Ascaridole tr tr ---
1342 1345 Thymyl acetate 0.3 0.2 0.3
1347 1356 Eugenol tr --- 0.3
1361 1365 Carvacryl acetate 0.8 0.5 1.0
1372 1375 α-Copaene tr 100:0 tr 0.1 100:0
1380 1382 β-Bourbonene tr tr 0.1
1389 1392 (Z)-Jasmone tr tr tr
1398 1398 Cyperene --- --- 0.2
1404 1408 Decyl acetate tr --- ---
1415 1417 (E)-β-Caryophyllene 0.3 100:0 0.4 100:0 0.5 100:0
1426 1430 β-Copaene tr tr tr
1451 1453 α-Humulene tr tr tr
1457 1457 Rotundene --- --- 0.1
1471 1475 γ-Muurolene tr 0.1 0.1
1473 1481 (E)-β-Ionone --- --- tr
1477 1480 Germacrene D 0.1 100:0 0.1 100:0 0.1
1481 1485 γ-Thujaplicin tr --- 0.1
1483 1489 β-Selinene tr --- ---
1487 1490 γ-Amorphene tr --- ---
1491 1497 α-Selinene tr tr 0.1
1494 1497 α-Muurolene tr tr tr
1509 1512 γ-Cadinene tr tr 0.1
1514 1518 δ-Cadinene 0.1 0.1 0.1 0:100
1548 1549 Thymohydroquinone 0.3 0.1 0.1
1577 1577 Caryophyllene oxide tr 0.1 0.1
1649 1655 α-Cadinol --- --- 0.1
1689 1691 Cyperotundone --- --- 0.2
1835 1841 Phytone --- --- 0.1
Monoterpene hydrocarbons 14.3 10.2 9.6
Oxygenated monoterpenoids 84.0 86.3 86.0
Sesquiterpene hydrocarbons 0.5 0.7 1.4
Oxygenated sesquiterpenoids tr 0.1 0.4
Benzenoid aromatics tr 1.5 0.8
Others 1.0 1.2 1.2
Total identified 99.8 99.8 99.3
Open in a new tab

RIcalc = Retention indices determined with respect to a homologous series of n-alkanes on a ZB-5ms column. RIdb = Retention indices from the databases [7,8,9,10]. #1 = Plant sample #1. #2 = Plant sample #2. --- = Not observed. ED = Enantiomeric distribution (dextrorotatory enantiomer: levorotatory enantiomer). tr = Trace (< 0.05%).

Chiral gas chromatography–mass spectrometry (GC-MS) analysis of the M. citriodora essential oils revealed the (+)-enantiomers to be the major stereoisomers for α-thujene, α-pinene, β-pinene, α-phellandrene, δ-3-carene, α-terpinene, cis-sabinene hydrate, trans-sabinene hydrate, α-terpineol, α-copaene, (E)-β-caryophyllene, and germacrene D. On the other hand, the (−)-enantiomer was dominant for β-phellandrene, borneol, carvone, and δ-cadinene. Limonene showed variation in the enantiomeric distributions with (+)-limonene in 26.7%, 63.3%, and 57.3% for aerial parts #1, #2, and roots essential oils, respectively. Likewise, linalool also showed variation with (+)-linalool of 71.9%, 49.7%, and 50.1%. (+)-Terpinen-4-ol was the predominant enantiomer in the aerial parts essential oils (60.2% and 58.5%), but (−)-terpinen-4-ol (79.1%) was dominant in the root essential oil.

2.2. Monarda Fistulosa

Monarda fistulosa essential oils were obtained in 2.66–4.83% yields as bright orange oils. The chemical compositions of the essential oils from the aerial parts of M. fistulosa are summarized in Table 2. In samples #1 and #2, thymol (RIdb = 1289) dominated the compositions (54.3% and 62.2%, respectively) with lesser quantities of p-cymene (RIdb = 1024, 12.1% and 10.2%), limonene (RIdb = 1030, 6.1% and 3.7%), carvacrol (RIdb = 1296, 5.9% and 6.6%), and thymoquinone (RIdb = 1252, 8.4% and 2.3%). Curiously, sample #3, although qualitatively similar, had a very different quantitative composition with thymoquinone as the most abundant constituent (41.3%) followed by p-cymene (21.9%), but with lower concentrations of thymol (8.9%) and carvacrol (1.6%).

Table 2.

Chemical composition of Monarda fistulosa essential oils cultivated in south Alabama.

Aerial Parts Essential Oil
RIcalc RIdb Compound #1, % ED, (+):(−) #2, % ED, (+):(−) #3, % ED, (+):(−)
923 925 α-Thujene 1.2 72.5:27.5 0.8 72.8:27.2 0.9 71.2:28.8
930 932 α-Pinene 0.5 59.2:40.8 0.3 63.8:36.2 0.5 61.0:39.0
947 950 Camphene 0.1 100:0 0.1 100:0 0.2 100:0
971 971 Sabinene 0.2 58.4:41.6 tr 0.2 59.0:41.0
973 973 1-Octen-3-one --- --- 0.1
975 978 β-Pinene 0.2 57.3:42.7 --- 0.2 57.9:42.1
978 978 1-Octen-3-ol 3.0 3.3 3.3
982 984 3-Octanone tr 0.1 0.1
987 989 Myrcene tr 0.3 0.1
995 996 3-Octanol tr 0.1 0.1
1004 1004 p-Mentha-1(7),8-diene tr tr tr
1006 1006 α-Phellandrene 0.1 95.5:4.5 0.2 95.4:4.6 0.1 93.4:6.6
1008 1008 δ-3-Carene 0.1 100:0 0.1 100:0 0.1 100:0
1016 1017 α-Terpinene 2.1 100:0 2.3 100:0 0.8 100:0
1019 1022 m-Cymene tr tr 0.1
1024 1024 p-Cymene 12.1 10.2 21.9
1025 1026 2-Acetyl-3-methylfuran --- --- 0.5
1029 1030 Limonene 6.1 0.5:99.5 3.7 2.6:97.4 6.3 1.2:98.8
1030 1031 β-Phellandrene 0.2 0:100 0.2 0:100 0.2 0:100
1031 1030 1,8-Cineole 0.1 0.1 0.1
1056 1057 γ-Terpinene tr 0.1 tr
1069 1069 cis-Sabinene hydrate 1.2 95.8:4.2 1.3 96.3:3.7 2.4 96.5:3.5
1078 1079 1-Nonen-3-ol 0.1 0.1 0.1
1084 1086 Terpinolene tr 0.1 tr
1089 1091 p-Cymenene tr tr 0.1
1098 1099 Linalool tr 37.8:62.2 tr 37.5:62.5 tr 37.9:62.1
1099 1099 trans-Sabinene hydrate 0.2 75.9:24.1 0.3 75.0:25.0 0.5 75.3:24.7
1103 1107 Nonanal tr --- tr
1115 1112 (E)-2,4-Dimethylhepta-2,4-dienal --- --- 0.2
1121 1121 trans-p-Mentha-2,8-dien-1-ol tr tr 0.3
1123 1124 cis-p-Menth-2-en-1-ol tr tr tr
1130 1132 cis-Limonene oxide tr --- 0.1
1133 1135 2-Vinylanisole 0.1 tr tr
1134 1137 cis-p-Mentha-2,8-dien-1-ol --- --- 0.3
1135 1138 trans-Limonene oxide tr --- ---
1137 1138 trans-Sabinol --- --- tr
1138 1140 trans-Pinocarveol --- --- 0.1
1139 1141 cis-Verbenol --- --- tr
1143 1145 trans-Verbenol --- --- 0.3
1144 1145 Camphor --- --- tr
1160 1164 Pinocarvone --- --- tr
1161 1162 (Z)-iso-Citral --- --- tr
1167 1168 trans-Phellandrene epoxide --- --- 0.1
1170 1170 Borneol 0.5 0:100 0.2 0:100 0.7 0:100
1179 1180 Terpinen-4-ol 0.4 63.3:36.7 0.5 63.2:36.8 0.5
1186 1186 p-Cymen-8-ol 0.1 tr 0.6
1195 1195 α-Terpineol 0.3 100:0 0.2 100:0 0.3
1197 1198 Methylchavicol (= Estragole) --- 0.1 0.1
1197 1198 cis-Piperitol --- --- 0.2
1217 1218 trans-Carveol --- --- 0.2
1231 1232 cis-Carveol --- --- 0.1
1240 1242 Cuminaldehyde --- --- 0.1
1241 1242 Carvone --- --- 0.3
1250 1241 Pulegone --- 0.2 ---
1252 1252 Thymoquinone 8.4 2.3 41.3
1281 1282 Bornyl acetate --- --- 0.1
1284 1286 Cogeijerene 0.1 --- ---
1291 1291 p-Cymen-7-ol tr --- 0.2
1295 1293 Thymol 54.3 62.2 8.9
1300 1300 Carvacrol 5.9 6.6 1.6
1307 1306 iso-Ascaridole tr tr 0.1
1345 1346 α-Cubebene tr tr tr
1351 1356 Eugenol tr tr ---
1373 1375 α-Copaene 0.1 100:0 0.1 100:0 0.1 100:0
1382 1382 β-Bourbonene 0.1 0.1 0.1
1387 1387 trans-β-Elemene tr tr 0.1
1418 1419 β-Ylangene tr 0.1
1419 1417 (E)-β-Caryophyllene 0.3 100:0 0.3 100:0 0.2 100:0
1427 1430 β-Copaene 0.1 0.1 0.1
1452 1453 α-Humulene tr tr tr
1473 1475 γ-Muurolene 0.1 0.2 0.1
1479 1479 α-Amorphene --- tr ---
1480 1483 trans-β-Bergamotene 0.1 --- 0.1
1481 1480 Germacrene D 0.7 100:0 0.6 100:0 0.6 100:0
1484 1485 γ-Thujaplicin 0.4 0.2 1.3
1488 1490 γ-Amorphene tr --- ---
1491 1492 β-Selinene 0.1 0.1 0.1
1493 1492 trans-Muurola-4(14),5-diene --- 0.1 ---
1496 1497 epi-Cubebol --- tr ---
1497 1497 α-Selinene --- 0.1 ---
1498 1497 α-Muurolene tr 0.1 tr
1510 1512 γ-Cadinene 0.1 0.2 0.1
1511 1515 Cubebol tr --- ---
1517 1518 δ-Cadinene 0.1 0.3 0.1
1518 1519 trans-Calamenene tr tr ---
1520 1523 β-Sesquiphellandrene tr --- ---
1537 1538 α-Cadinene tr tr ---
1542 1541 α-Calacorene tr tr ---
1543 1546 α-Elemol tr --- ---
1548 1554 Thymohydroquinone 0.6 1.6 0.6
1558 1565 Eugenyl acetate tr tr tr
1559 1557 Germacrene B tr --- ---
1580 1577 Caryophyllene oxide tr tr 0.1
1638 1639 cis-Guaia-3,9-dien-11-ol 0.1 0.1 ---
1651 1655 α-Cadinol tr 0.1 tr
Monoterpene hydrocarbons 22.8 18.3 31.4
Oxygenated monoterpenoids 72.2 75.7 61.2
Sesquiterpene hydrocarbons 1.7 2.2 1.7
Oxygenated sesquiterpenoids 0.1 0.1 0.1
Benzenoid aromatics 0.1 0.1 0.1
Others 3.1 3.6 4.3
Total identified 100.0 100.0 98.7
Open in a new tab

RIcalc = Retention indices determined with respect to a homologous series of n-alkanes on a ZB-5ms column. RIdb = Retention indices from the databases [7,8,9,10]. #1 = Plant sample #1. #2 = Plant sample #2. #3 = Plant sample #3. --- = Not observed. ED = Enantiomeric distribution (dextrorotatory enantiomer: levorotatory enantiomer). tr = Trace (<0.05%).

As was observed in M. citriodora essential oils, in M. fistulosa essential oils, the (+)-enantiomer was the major for α-thujene, α-pinene, β-pinene, α-phellandrene, δ-3-carene, α-terpinene, cis-sabinene hydrate, trans-sabinene hydrate, α-terpineol, α-copaene, (E)-β-caryophyllene, and germacrene D, while the (−)-enantiomer was predominant for β-phellandrene and borneol. (−)-Limonene (97.4–99.5%) and (−)-linalool (62.1–62.5%) dominated in all three M. fistulosa samples. (+)-Camphene (100%), (+)-sabinene (58.4–59.0%), and (+)-terpinen-4-ol (63.2–63.3%) were also dominant.

2.3. Monarda Punctata

Hydrodistillation of two samples of wild-growing M. punctata aerial parts gave bright orange essential oils in 0.781% and 0.658% yield. The most abundant components in the essential oils were thymol (RIdb = 1289, 61.8% and 47.9%), p-cymene (RIdb = 1024, 15.3% and 19.8%), γ-terpinene (RIdb = 1057, 2.7% and 9.7%), and carvacrol (RIdb = 1296, 4.5% and 4.1%) (see Table 3).

Table 3.

Chemical composition of Monarda punctata essential oils growing wild in south Alabama.

Aerial Parts Essential Oil
RIcalc RIdb Compound #1, % ED, (+):(−) #2, % ED, (+):(−)
923 925 α-Thujene 0.1 100:0 0.7 68.5:31.5
930 932 α-Pinene tr 0.2 83.8:16.2
945 950 Camphene --- 0.1 100:0
957 959 Benzaldehyde --- tr
970 971 Sabinene tr tr
974 978 β-Pinene tr 0.1 62.7:37.3
975 974 1-Octen-3-ol 1.8 1.8
980 983 3-Octanone --- tr
986 989 Myrcene 0.3 1.1
995 996 3-Octanol 0.1 0.1
1001 1004 p-Mentha-1(7),8-diene --- tr
1004 1006 α-Phellandrene 0.1 100:0 0.2 94.6:5.4
1006 1008 δ-3-Carene tr 0.1 100:0
1014 1017 α-Terpinene 1.3 100:0 3.0 100:0
1016 1022 m-Cymene --- tr
1024 1024 p-Cymene 15.3 19.8
1025 1026 2-Acetyl-3-methylfuran --- tr
1026 1030 Limonene 0.4 50.2:49.8 0.5 0:100
1027 1029 β-Phellandrene 0.2 0.2 0:100
1028 1030 1,8-Cineole 0.4 0.1
1039 1043 Phenylacetaldehyde --- tr
1055 1057 γ-Terpinene 2.0 9.7
1066 1069 cis-Sabinene hydrate 0.6 100:0 0.7 97.9:2.1
1076 1079 1-Nonen-3-ol --- tr
1082 1086 Terpinolene 0.1 0.1
1087 1091 p-Cymenene 0.1 0.1
1095 1099 Linalool --- tr 70.1:29.9
1098 1101 trans-Sabinene hydrate 0.2 100:0 0.1 83.2:16.8
1100 1104 Nonanal --- 0.1
1104 1107 1-Octen-3-yl acetate 0.2 0.4
1145 1145 trans-Verbenol --- tr
1161 1158 Menthone 0.3 ---
1168 1170 Borneol 0.1 0:100 tr 0:100
1177 1180 Terpinen-4-ol 0.8 58.7:41.3 0.6 66.1:33.9
1182 1183 m-Cymen-8-ol --- 0.1
1184 1186 p-Cymen-8-ol 0.5 0.5
1191 1197 Methyl chavicol (= Estragole) 0.8 ---
1193 1195 α-Terpineol --- 0.1 100:0
1202 1206 Decanal --- 0.1
1224 1224 Thymol methyl ether --- tr
1235 1238 Carvacrol methyl ether 1.1 1.0
1239 1242 Cumin aldehyde --- 0.1
1247 1250 Thymoquinone 2.0 0.2
1289 1289 Thymol 61.8 47.9
1293 1291 p-Cymen-7-ol --- 0.2
1296 1296 Carvacrol 4.5 4.1
1306 1309 4-Vinylguaicol --- tr
1347 1356 Eugenol 0.7 0.3
1370 1375 α-Copaene --- tr
1378 1382 β-Bourbonene --- tr
1384 1390 trans-β-Elemene --- tr
1415 1417 (E)-β-Caryophyllene 1.6 100:0 1.2 100:0
1424 1430 β-Copaene --- tr
1427 1430 trans-α-Bergamotene 1.2 0.7
1449 1453 α-Humulene --- tr
1469 1475 γ-Muurolene --- 0.1
1476 1480 Germacrene D 0.7 100:0 0.4 100:0
1479 1483 trans-β-Bergamotene 0.2 0.1
1480 1485 γ-Thujaplicin --- 0.1
1482 1489 β-Selinene --- tr
1489 1492 α-Selinene --- tr
1492 1497 α-Muurolene --- tr
1506 1512 γ-Cadinene --- tr
1512 1518 δ-Cadinene --- 0.1
1517 1523 β-Sesquiphellandrene --- 0.1
1546 1549 Thymohydroquinone 0.3 2.5
1576 1577 Caryophyllene oxide 0.2 0.2
1633 1639 cis-Guaia-3,9-dien-11-ol 0.2 0.1
1648 1655 α-Cadinol --- tr
1834 1841 Phytone --- tr
Monoterpene hydrocarbons 19.9 35.7
Oxygenated monoterpenoids 72.5 58.3
Sesquiterpene hydrocarbons 3.7 2.7
Oxygenated sesquiterpenoids 0.4 0.4
Benzenoid aromatics 1.5 0.3
Others 2.1 2.4
Total identified 100.0 99.8
Open in a new tab

RIcalc = Retention indices determined with respect to a homologous series of n-alkanes on a ZB-5ms column. RIdb = Retention indices from the databases [7,8,9,10]. #1 = Plant sample #1. #2 = Plant sample #2. --- = Not observed. ED = Enantiomeric distribution (dextrorotatory enantiomer: levorotatory enantiomer). tr = Trace (<0.05%).

The enantiomeric distributions of terpenoids in M. punctata essential oils were analogous to those observed for M. citriodora and M. fistulosa oils with the exception of limonene, which was virtually racemic in sample #1, but 100% (−)-limonene in sample #2.

3. Discussion

Monarda citriodora and M. fistulosa have been introduced throughout temperate regions of the world as popular herbal medicines as well as ornamentals [4,5,6]. The volatile phytochemistry has shown wide variation depending on geographical location (Table 4). The essential oils of M. citriodora in the present study were rich in both thymol and carvacrol, whereas essential oils from Europe and Asia were dominated by thymol with much lower concentrations of carvacrol. Monarda fistulosa, in particular, showed wide variation with at least three different chemotypes (carvacrol-rich, thymol-rich, and geraniol-rich, see Table 4). The essential oils of M. fistulosa (samples #1 and #2) in this study fit into the thymol-rich chemotype. Interestingly, there was a high concentration of thymoquinone in M. fistulosa sample #3, with concomitant lower concentrations of thymol and carvacrol. Thymol was reported as the major component of M. punctata in two old reports [11,12]. Consistent with these reports, a floral essential oil of M. punctata from China was rich in thymol (75.2%), which is in agreement with the aerial parts essential oils from Alabama.

Table 4.

Major essential oil components of Monarda species from geographical locations around the world.

Monarda spp. Plant Tissue Collection Site Composition (Major Components) Ref.
M. citriodora Aerial parts Jammu, India (cultivated) Thymol (82.3%), carvacrol (4.8%) [13]
M. citriodora Aerial parts Imola (BO) Italy (cultivated) Thymol (19.6%), p-cymene (15.6%), γ-terpinene (13.5%), carvacrol (9.3%), α-terpinene (9.2%), myrcene (5.7%) [14]
M. citriodora Not reported Commercial (India) (E)-β-Caryophyllene (19.2%), citral a (13.3%), limonene (11.8%), cis-verbenol (11.4%), geraniol (7.6%), citronellal (5.6%) [15]
M. citriodora var. citriodora Leaves Liverpool, UK (cultivated) Thymol (50.7%), p-cymene (22.8%), carvacrol (3.6%) [16]
M. citriodora var. citriodora Flowers Liverpool, UK (cultivated) Thymol (61.8%), γ-terpinene (13.3%), p-cymene (4.2%), carvacrol (3.8%) [16]
M. citriodora var. citriodora Aerial parts Liverpool, UK (cultivated) Thymol (56.9%), p-cymene (13.0%), α-terpinene (10.0%), carvacrol (4.3%) [17]
M. citriodora var. citriodora Aerial parts Commercial (unknown) Thymol (70.6%), p-cymene (10.6%), carvacrol (6.1%) [18]
M. fistulosa Aerial parts Krasnodarsk Krai, Russia (introduced, wild) p-Cymene (32.5%), carvacrol (23.9%), thymol (12.6%), carvacrol methyl ether (5.5%), unidentified aliphatic aldehyde (6.3%) [19]
M. fistulosa Aerial parts Casola Valsenio, Italy (cultivated) Thymol (26.5%), β-phellandrene (17.0%), α-phellandrene (13.7%), p-cymene (13.5%), myrcene (8.1%) [20]
M. fistulosa Aerial parts Saint-Jean-sur-Richelieu, QC, Canada (cultivated) Geraniol (61.8%), geranyl formate (16.6%), geranial (10.6%), neral (6.6%) [21]
M. fistulosa Aerial parts Poplarville, MS, USA (cultivated) Carvacrol (39.1%), p-cymene (35.4%), (−)-1-octen-3-ol [22]
M. fistulosa Aerial parts Imola (BO) Italy (cultivated) Thymol (31.6%), β-phellandrene (18.1%), α-phellandrene (14.2%), p-cymene (13.1%), myrcene (8.8%) [23]
M. fistulosa Aerial parts Imola (BO) Italy (cultivated) Thymol (28.4%), β-phellandrene (16.9%), α-phellandrene (13.7%), p-cymene (13.3%), myrcene (8.7%) [24]
M. fistulosa Aerial parts Imola (BO) Italy (cultivated) Thymol (33.4%), β-phellandrene (18.0%), α-phellandrene (14.0%), p-cymene (13.2%), myrcene (8.6%) [24]
M. fistulosa Aerial parts Ravenna, Italy (cultivated) γ-Terpinene (25.2%), carvacrol (24.3%), p-cymene (11.0%; reported as o-cymene), thymol (8.4%), α-terpinene (5.0%), thymol methyl ether (4.7%) [25]
M. fistulosa Aerial parts Chişinău, Republic of Moldova (cultivated) Carvacrol (54.8%), p-cymene (23.2%), carvacrol methyl ether (5.9%) [26]
M. fistulosa Flowers Gallatin Valley, MT, USA (wild) Carvacrol (45.7%), p-cymene (25.6%), γ-terpinen (6.8%), thymol (3.1%) [27]
M. fistulosa Leaves Gallatin Valley, MT, USA (wild) Carvacrol (71.5%), p-cymene (13.1%), γ-terpinen (2.5%), thymol (3.3%) [27]
M. fistulosa Aerial parts Moscow, Russia (cultivated) α-Terpineol (37.7%), 1-octen-3-ol (10.5%), geraniol (10.4%), thymol (9.3%), p-cymene (4.9%) [28]
M. fistulosa cv. Fortuna Aerial parts Kherson, Ukraine (cultivated) Thymol (77.3%), carvacrol methyl ether (4.9%), carvacrol (3.8%) [6]
M. fistulosa cv. Premiera Aerial parts Kherson, Ukraine (cultivated) Thymol (78.3%), carvacrol methyl ether (4.8%), carvacrol (3.6%) [6]
M. fistulosa var. menthifolia Aerial parts Morden, Manitoba, Canada (cultivated) Geraniol (86.8%) [29]
M. punctata Flowers Xi’an, China (cultivated?) Thymol (75.2%), p-cymene (6.7%), limonene (5.4%), carvacrol (3.5%) [30]
Open in a new tab

a Isomer not indicated.

The high concentrations of thymol, carvacrol, and p-cymene are consistent with the traditional uses of Monarda spp. to treat skin infections, wounds, fevers, and respiratory problems. Thymol [31], carvacrol [32], and p-cymene [33] have demonstrated antibacterial and antifungal activities [34,35], as well as wound-healing activity [36]. Thymol [37] and carvacrol [38], in addition to thymoquinone [39], have shown antitussive effects. Thymoquinone has also shown wound-healing properties [40]. Furthermore, both thymol [41] and carvacrol [32] have shown analgesic and anti-inflammatory activities [42].

As far as we are aware, this work presents the first chiral analysis of terpenoid constituents of Monarda species. Several investigations on the enantiomeric distributions in other members of the Lamiaceae have been reported in the literature, however. There seems to be much variation in the enantiomeric distribution of monoterpenoids across the family. Consistent with what was observed in Monarda essential oils, (+)-α-pinene was the major enantiomer found in Coridothymus capitatus [43], Rosmarinus officinalis [44], Lepechinia heteromorpha [45], Ocimum canum, and Ocimum kilimandscharicum [46]. Likewise, (+)-β-pinene predominates over (−)-β-pinene in C. capitatus [43] as well as the Monarda essential oils. On the other hand, (−)-β-pinene dominates in R. officinalis [44] and Lepechinia mutica [47]. The essential oils of peppermint (Mentha × piperita) and spearmint (Mentha spicata) have shown nearly racemic mixtures of α- and β-pinenes [48]. (+)-α-Phellandrene and (−)-β-phellandrene were the dominant enantiomers in the Monarda essential oils. In marked contrast, however, (−)-α-phellandrene and (+)-β-phellandrene predominated in L. mutica essential oil [47]. (−)-Limonene predominates in M. fistulosa essential oil, peppermint (M. piperita) and spearmint (M. spicata) essential oils [48] whereas (+)-limonene is the major enantiomer in C. capitatus [43], O. canum, and O. kilimandscharicum [46], and a nearly racemic mixture was found in rosemary (R. officinalis) essential oil [44]. (+)-Linalool was the predominant enantiomer in C. capitatus [43], Salvia schimperi [49], Pycnanthemum incanum [50], O. canum, and O. kilimandscharicum [46], whereas (−)-linalool was the major stereoisomer in Lavandula angustifolia [51] and R. officinalis [44].

4. Materials and Methods

4.1. Plant Material

Monarda citriodora was cultivated in Kirkland Gardens, Newville, AL, USA (31°26′27″ N, 85°21′31″ W) from seeds (Outsidepride Seed Source, Independence, OR, USA). The cultivated Monarda spp. were grown in loamy clayey-sand and fertilized with chicken manure, kelp meal, and bone meal at planting in full sun. The aerial parts of M. citriodora were collected from separate plants on separate occasions (plant #1, collected on 20 June 2020; plant #2 collected on 1 August 2020). The roots of M. citriodora were obtained from plant #2.

Monarda fistulosa was cultivated in Kirkland Gardens, Newville, AL, USA (31°26′27″ N, 85°21′31″ W) from seedlings (Home Depot, Dothan, AL, USA) as above. The aerial parts of three different plant samples were collected on 25 June 2020.

Monarda punctata was collected from wild-growing plants near Newville, AL, USA (31°27′23″ N, 85°22′17″ W); the edge of a planted pine forest, disturbed grassland, full/partial sun, sandy-clay soil that had been intentionally burned (prescribed burn) 1.5 years before collection. The aerial parts of two different plants were collected on 1 June 2020.

Plants were identified by S.K. Lawson and a voucher specimen of each plant was deposited in the University of Alabama in Huntsville Herbarium (HALA); voucher numbers for M. citriodora (SKL61820), M. fistulosa (SKL72020), and M. punctata (SKL9620). The Monarda plant materials were allowed to dry in the shade for several days, the air-dried plant materials were pulverized and subjected to hydrodistillation using a Likens-Nickerson apparatus with continuous extraction with dichloromethane (Table 5).

Table 5.

Hydrodistillation details of Monarda species collected or cultivated in south Alabama.

Monarda spp. Mass Plant Material Yield Essential Oil (EO)
Monarda citriodora #1 25.57 g dried aerial parts 406.2 mg orange EO
Monarda citriodora #2 37.81 g dried aerial parts 675.6 mg orange EO
Monarda citriodora #2 17.47 g dried roots 153.6 mg yellow EO
Monarda fistulosa #1 9.60 g dried aerial parts 364.0 mg bright orange EO
Monarda fistulosa #2 7.58 g dried aerial parts 366.2 mg bright orange EO
Monarda fistulosa #3 8.98 g dried aerial parts 238.9 mg bright orange EO
Monarda punctata #1 39.09 g dried aerial parts 305.6 mg bright orange EO
Monarda punctata #2 62.62 g dried aerial parts 411.9 mg bright orange EO
Open in a new tab

4.2. Gas Chromatographic Analysis

The essential oils were analyzed by gas chromatography–mass spectrometry (GC-MS), gas chromatography with flame ionization detection (GC-FID), and chiral GC-MS as previously reported [52].

4.2.1. Gas Chromatography–Mass Spectrometry

Shimadzu GCMS-QP2010 Ultra, ZB-5ms GC column, GC oven temperature 50 °C–260 °C (2 °C/min), 1-μL injection of 5% solution of EO in dichloromethane (split mode, 30:1). Retention indices (RIs) were determined with reference to a homologous series of n-alkanes. Compounds identified by comparison of the MS fragmentation and retention indices with those in the databases [7,8,9,10].

4.2.2. Gas Chromatography–Flame Ionization Detection

Shimadzu GC 2010, FID detector, ZB-5 GC column, GC oven temperature 50 °C–260 °C (2.0 °C/min). The percent compositions were determined from raw peak areas without standardization.

4.2.3. Chiral Gas Chromatography–Mass Spectrometry

Shimadzu GCMS-QP2010S, Restek B-Dex 325 column, GC oven temperature 50 °C–120 °C (1.5 °C/min) then 120 °C–200 °C (2.0 °C/min), 0.1 μL injection of 5% solution of EO in dichloromethane (split mode, 45:1). The enantiomeric distributions were determined by comparison of retention times with authentic samples obtained from Sigma-Aldrich (Milwaukee, WI, USA). Relative enantiomer percentages were calculated from peak areas.

5. Conclusions

This study presents, for the first time, analyses of the essential oils of three species of Monarda growing in south Alabama. In addition, the enantiomeric distribution of terpenoids was also carried out. This work illustrates the wide variation in essential oil compositions based on geographical location as well as variations in enantiomeric distribution. It would be interesting to compare enantiomeric distributions for Monarda essential oils from other geographical locations and for other Monarda species. Nevertheless, the phenolic monoterpenoids thymol and/or carvacrol were found to dominate the compositions of M. citriodora, M. fistulosa, and M. punctata and support the traditional medicinal uses of these plants.

Acknowledgments

P.S. and W.N.S. participated in this work as part of the activities of the Aromatic Plant Research Center (APRC, https://aromaticplant.org/, accessed on 9 February 2021).

Author Contributions

Conceptualization, S.K.L. and W.N.S.; methodology, S.K.L., P.S., and W.N.S.; software, P.S.; validation, W.N.S., formal analysis, P.S. and W.N.S.; investigation, S.K.L., P.S., and W.N.S.; data curation, W.N.S.; writing—original draft preparation, W.N.S.; writing—review and editing, S.K.L., P.S., and W.N.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Royal Botanic Gardens K. The Plant List. [(accessed on 1 February 2021)]; Available online: http://www.theplantlist.org/tpl1.1/search?q=Monarda.
  • 2.Kartesz J.T. BONAP’s North American Plant Atlas. [(accessed on 1 February 2021)]; Available online: http://bonap.net/Napa/TaxonMaps/Genus/County/Monarda.
  • 3.Moerman D.E. Native American Ethnobotany. Timber Press, Inc.; Portland, OR, USA: 1998. [Google Scholar]
  • 4.Davidson C.G. Monarda, Bee-balm. In: Anderson N.O., editor. Flower Breeding and Genetics. Springer; Dordrecht, The Netherlands: 2007. pp. 756–779. [Google Scholar]
  • 5.Ciuruşniuc A.-M., Robu T. Study of the behaviour of cultivated species of the genus Monarda L. in Vaslui County, to introduce them in cultivation as medicinal, aromatic and decorative plants. Lucr. Științifice Ser. Agron. 2012;55:309–312. [Google Scholar]
  • 6.Dudchenko V.V., Svydenko L.V., Markovska O.Y., Sydiakina O.V. Morphobiological and biochemical characteristics of Monarda L. varieties under conditions of the southern steppe of Ukraine. J. Ecol. Eng. 2020;21:99–107. [Google Scholar]
  • 7.Adams R.P. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry. 4th ed. Allured Publishing; Carol Stream, IL, USA: 2007. [Google Scholar]
  • 8.Mondello L. FFNSC 3. Shimadzu Scientific Instruments; Columbia, MD, USA: 2016. [Google Scholar]
  • 9.NIST . NIST17. National Institute of Standards and Technology; Gaithersburg, MD, USA: 2017. [Google Scholar]
  • 10.Satyal P. Ph.D. Thesis. University of Alabama in Huntsville; Huntsville, AL, USA: 2015. Development of GC-MS Database of Essential Oil Components by the Analysis of Natural Essential Oils and Synthetic Compounds and Discovery of Biologically Active Novel Chemotypes in Essential Oils. [Google Scholar]
  • 11.Schroeter H.J. Analysis of the volatile oil of Monarda punctata, Linne. Am. J. Pharm. 1888;1888:113. [Google Scholar]
  • 12.Schumann W.R., Kremers E. On the chemical composition of the oil from Monarda punctata, L. Am. J. Pharm. 1896;1896:469. [Google Scholar]
  • 13.Pathania A.S., Guru S.K., Verma M.K., Sharma C., Abdullah S.T., Malik F., Chandra S., Katoch M., Bhushan S. Disruption of the PI3K/AKT/mTOR signaling cascade and induction of apoptosis in HL-60 cells by an essential oil from Monarda citriodora. Food Chem. Toxicol. 2013;62:246–254. doi: 10.1016/j.fct.2013.08.037. [DOI] [PubMed] [Google Scholar]
  • 14.Di Vito M., Bellardi M.G., Mondello F., Modesto M., Michelozzi M., Bugli F., Sanguinetti M., Sclocchi M.C., Sebastiani M.L., Biffi S., et al. Monarda citriodora hydrolate vs. essential oil comparison in several anti-microbial applications. Ind. Crops Prod. 2019;128:206–212. doi: 10.1016/j.indcrop.2018.11.007. [DOI] [Google Scholar]
  • 15.Deepika, Singh A., Chaudhari A.K., Das S., Dubey N.K. Nanoencapsulated Monarda citriodora Cerv. ex Lag. essential oil as potential antifungal and antiaflatoxigenic agent against deterioration of stored functional foods. J. Food Sci. Technol. 2020;57:2863–2876. doi: 10.1007/s13197-020-04318-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Collins J.E., Bishop C.D., Deans S.G., Svoboda K.P. Composition of the essential oil from the leaves and flowers of Monarda citriodora var. citriodora grown in the United Kingdom. J. Essent. Oil Res. 1994;6:27–29. doi: 10.1080/10412905.1994.9698320. [DOI] [Google Scholar]
  • 17.Bishop C.D., Thornton I.B. Evaluation of the antifungal activity of the essential oils of Monarda citriodora var. citriodora and Melaleuca alternifolia on post-harvest pathogens. J. Essent. Oil Res. 1997;9:77–82. doi: 10.1080/10412905.1997.9700718. [DOI] [Google Scholar]
  • 18.Dorman H.J.D., Deans S.G. Chemical composition, antimicrobial and in vitro antioxidant properties of Monarda citriodora var. citriodora, Myristica fragrans, Origanum vulgare ssp. hirtum, Pelargonium sp. and Thymus zygis oils. J. Essent. Oil Res. 2004;16:145–150. doi: 10.1080/10412905.2004.9698679. [DOI] [Google Scholar]
  • 19.Zamureenko V.A., Klyuev N.A., Bocharov B.V., Kabanov V.S., Zacharov A.M. An investigation of the component composition of the essential oil of Monarda fistulosa. Chem. Nat. Compd. 1989;25:549–551. doi: 10.1007/BF00598073. [DOI] [Google Scholar]
  • 20.Contaldo N., Bellardi M.G., Cavicchi L., Epifano F., Genovese S., Curini M., Bertaccini A. Phytochemical effects of phytoplasma infections on essential oil of Monarda fistulosa L. Bull. Insectology. 2011;64:S177–S178. [Google Scholar]
  • 21.Adebayo O., Bélanger A., Khanizadeh S. Variable inhibitory activities of essential oils of three Monarda species on the growth of Botrytis cinerea. Can. J. Plant Sci. 2013;93:987–995. doi: 10.4141/cjps2013-044. [DOI] [Google Scholar]
  • 22.Tabanca N., Bernier U.R., Ali A., Wang M., Demirci B., Blythe E.K., Khan S.I., Baser K.H.C., Khan I.A. Bioassay-guided investigation of two Monarda essential oils as repellents of yellow fever mosquito Aedes aegypti. J. Agric. Food Chem. 2013;61:8573–8580. doi: 10.1021/jf402182h. [DOI] [PubMed] [Google Scholar]
  • 23.Francati S., Gualandi G. Side effects of essential oils of Monarda fistulosa L. and M. didyma L. on the tachinid parasitoid Exorista larvarum (L.): A preliminary study. Tachinid Times. 2017;30:4–8. [Google Scholar]
  • 24.Mattarelli P., Epifano F., Minardi P., Di Vito M., Modesto M., Barbanti L., Bellardi M.G. Chemical composition and antimicrobial activity of essential oils from aerial parts of Monarda didyma and Monarda fistulosa cultivated in Italy. J. Essent. Oil-Bear. Plants. 2017;20:76–86. doi: 10.1080/0972060X.2016.1278184. [DOI] [Google Scholar]
  • 25.Laquale S., Avato P., Argentieri M.P., Bellardi M.G., D’Addabbo T. Nematotoxic activity of essential oils from Monarda species. J. Pest Sci. 2018;91:1115–1125. doi: 10.1007/s10340-018-0957-1. [DOI] [Google Scholar]
  • 26.Colţun M.B., Bogdan A.A. Aspects of the biology and the cultivation of Monarda fistulosa L. as aromatic species in the Republic Of Moldova. Оснoвні, малoпoширені і нетрадиційні види рoслин–від вивчення дo oсвoєння (сільськoгoспoдарські і біoлoгічні науки) 2020;2020:103–109. [Google Scholar]
  • 27.Ghosh M., Schepetkin I.A., Özek G., Özek T., Khlebnikov A.I., Damron D.S., Quinn M.T. Essential oils from Monarda fistulosa: Chemical composition and activation of transient receptor potential A1 (TRPA1) channels. Molecules. 2020;25:4873. doi: 10.3390/molecules25214873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Malankina E.L., Kuzmenko A.N., Zaitchik B.T., Ruzhitskiy A.O., Evgrafov A.A., Kozlovskaya L.N. Content and composition of wild bergamot (Monarda fistulosa L.) essential oil at different phenological phases. Moscow Univ. Chem. Bull. 2020;75:391–394. doi: 10.3103/S0027131420060140. [DOI] [Google Scholar]
  • 29.Mazza G., Chubey B.B., Kiehn F. Essential oil of Monarda fistulosa L. var. menthaefolia, a potential source of geraniol. Flavour Fragr. J. 1987;2:129–132. doi: 10.1002/ffj.2730020310. [DOI] [Google Scholar]
  • 30.Li H., Yang T., Li F.-Y., Yao Y., Sun Z.-M. Antibacterial activity and mechanism of action of Monarda punctata essential oil and its main components against common bacterial pathogens in respiratory tract. Int. J. Clin. Exp. Pathol. 2014;7:7389–7398. [PMC free article] [PubMed] [Google Scholar]
  • 31.Marchese A., Orhan I.E., Daglia M., Barbieri R., Di Lorenzo A., Nabavi S.F., Gortzi O., Izadi M., Nabavi S.M. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem. 2016;210:402–414. doi: 10.1016/j.foodchem.2016.04.111. [DOI] [PubMed] [Google Scholar]
  • 32.Sharifi-Rad M., Varoni E.M., Iriti M., Martorell M., Setzer W.N., del Mar Contreras M., Salehi B., Soltani-Nejad A., Rajabi S., Tajbakhsh M., et al. Carvacrol and human health: A comprehensive review. Phyther. Res. 2018;32:1675–1687. doi: 10.1002/ptr.6103. [DOI] [PubMed] [Google Scholar]
  • 33.Marchese A., Arciola C.R., Barbieri R., Silva A.S., Nabavi S.F., Sokeng A.J.T., Izadi M., Jafari N.J., Suntar I., Daglia M., et al. Update on monoterpenes as antimicrobial agents: A particular focus on p-cymene. Materials. 2017;10:947. doi: 10.3390/ma10080947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Memar M.Y., Raei P., Alizadeh N., Aghdam M.A., Kafil H.S. Carvacrol and thymol: Strong antimicrobial agents against resistant isolates. Rev. Med. Microbiol. 2017;28:63–68. doi: 10.1097/MRM.0000000000000100. [DOI] [Google Scholar]
  • 35.Aljaafari M.N., AlAli A.O., Baqais L., Alqubaisy M., AlAli M., Aidin M., Ong-Abdullah J., Abushelaibi A., Lai K.-S., Lim S.-H.E. An overview of the potential therapeutic applications of essential oils. Molecules. 2021;26:628. doi: 10.3390/molecules26030628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Costa M.F., Durço A.O., Rabelo T.K., Barreto R.d.S.S., Guimarães A.G. Effects of carvacrol, thymol and essential oils containing such monoterpenes on wound healing: A systematic review. J. Pharm. Pharmacol. 2019;71:141–155. doi: 10.1111/jphp.13054. [DOI] [PubMed] [Google Scholar]
  • 37.Gavliakova S., Biringerova Z., Buday T., Brozmanova M., Calkovsky V., Poliacek I., Plevkova J. Antitussive effects of nasal thymol challenges in healthy volunteers. Respir. Physiol. Neurobiol. 2013;187:104–107. doi: 10.1016/j.resp.2013.02.011. [DOI] [PubMed] [Google Scholar]
  • 38.Boskabady M.H., Jandaghi P., Kiani S., Hasanzadeh L. Antitussive effect of Carum copticum in guinea pigs. J. Ethnopharmacol. 2005;97:79–82. doi: 10.1016/j.jep.2004.10.016. [DOI] [PubMed] [Google Scholar]
  • 39.Hosseinzadeh H., Eskandari M., Ziaee T. Antitussive effect of thymoquinone, a constituent of Nigella sativa seeds, in Guinea pigs. Pharmacologyonline. 2008;2:480–484. [Google Scholar]
  • 40.Selçuk C.T., Durgun M., Tekin R., Yolbas L., Bozkurt M., Akçay C., Alabalk U., Basarali M.K. Evaluation of the effect of thymoquinone treatment on wound healing in a rat burn model. J. Burn Care Res. 2013;34:274–281. doi: 10.1097/BCR.0b013e31827a2be1. [DOI] [PubMed] [Google Scholar]
  • 41.Jyoti D.D., Singh D., Kumar G., Karnatak M., Chandra S., Verma V.P., Shankar R. Thymol chemistry: A medicinal toolbox. Curr. Bioact. Compd. 2018;15:454–474. doi: 10.2174/1573407214666180503120222. [DOI] [Google Scholar]
  • 42.Fachini-Queiroz F.C., Kummer R., Estevão-Silva C.F., Carvalho M.D.D.B., Cunha J.M., Grespan R., Bersani-Amado C.A., Cuman R.K.N. Effects of thymol and carvacrol, constituents of Thymus vulgaris L. essential oil, on the inflammatory response. Evid. Based Complement. Altern. Med. 2012;2012:657026. doi: 10.1155/2012/657026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Tateo F., Mariotti M., Bononi M. Essential oil composition and enantiomeric distribution of some monoterpenoid components of Coridothymus capitatus (L.) Rchb. grown on the island of Kos (Greece) J. Essent. Oil Res. 1998;10:241–244. doi: 10.1080/10412905.1998.9700895. [DOI] [Google Scholar]
  • 44.Satyal P., Jones T.H., Lopez E.M., McFeeters R.L., Ali N.A.A., Mansi I., Al-Kaf A.G., Setzer W.N. Chemotypic characterization and biological activity of Rosmarinus officinalis. Foods. 2017;6:20. doi: 10.3390/foods6030020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Gilardoni G., Ramírez J., Montalván M., Quinche W., León J., Benítez L., Morocho V., Cumbicus N., Bicchi C. Phytochemistry of three Ecuadorian Lamiaceae: Lepechinia heteromorpha (Briq.) Epling, Lepechinia radula (Benth.) Epling and Lepechinia paniculata (Kunth) Epling. Plants. 2019;8:1. doi: 10.3390/plants8010001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Pragadheesh V.S., Saroj A., Yadav A., Samad A., Chanotiya C.S. Compositions, enantiomer characterization and antifungal activity of two Ocimum essential oils. Ind. Crops Prod. 2013;50:333–337. doi: 10.1016/j.indcrop.2013.08.009. [DOI] [Google Scholar]
  • 47.Ramírez J., Gilardoni G., Ramón E., Tosi S., Picco A.M., Bicchi C., Vidari G. Phytochemical study of the Ecuadorian species Lepechinia mutica (Benth.) Epling and high antifungal activity of carnosol against Pyricularia oryzae. Pharmaceuticals. 2018;11:33. doi: 10.3390/ph11020033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Coleman W.M., Lawrence B.M. Examination of the enantiomeric distribution of certain monoterpene hydrocarbons in selected essential oils by automated solid-phase microextraction-chiral gas chromatography-mass selective detection. J. Chromatogr. Sci. 2000;38:95–99. doi: 10.1093/chromsci/38.3.95. [DOI] [PubMed] [Google Scholar]
  • 49.Endeshaw M.M., Gautun O.R., Asfaw N., Aasen A.J. Volatile oil constituents of the Ethiopian plant Salvia schimperi Benth. Flavour Fragr. J. 2000;15:27–30. doi: 10.1002/(SICI)1099-1026(200001/02)15:1&#x0003c;27::AID-FFJ868&#x0003e;3.0.CO;2-E. [DOI] [Google Scholar]
  • 50.Dein M., Munafo J.P. Characterization of key odorants in hoary mountain mint, Pycnanthemum incanum. J. Agric. Food Chem. 2019;67:2589–2597. doi: 10.1021/acs.jafc.8b06803. [DOI] [PubMed] [Google Scholar]
  • 51.Satyal P., Pappas R.S. Antique lavender essential oil from 1945, its chemical composition and enantiomeric distribution. Nat. Volatiles Essent. Oils. 2016;3:20–25. [Google Scholar]
  • 52.DeCarlo A., Johnson S., Okeke-Agulu K.I., Dosoky N.S., Wax S.J., Owolabi M.S., Setzer W.N. Compositional analysis of the essential oil of Boswellia dalzielii frankincense from West Africa reveals two major chemotypes. Phytochemistry. 2019;164:24–32. doi: 10.1016/j.phytochem.2019.04.015. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data are contained within the article.

Articles from Plants are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)

RESOURCES