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Article

Volatile Compositions and Antifungal Activities of Native American Medicinal Plants: Focus on the Asteraceae

by
Sims K. Lawson
1,
Layla G. Sharp
1,
Chelsea N. Powers
1,
Robert L. McFeeters
1,
Prabodh Satyal
2 and
William N. Setzer
1,2,*
1
Department of Chemistry, University of Alabama in Huntsville, Huntsville, AL 35899, USA
2
Aromatic Plant Research Center, 230 N 1200 E, Suite 100, Lehi, UT 84043, USA
*
Author to whom correspondence should be addressed.
Plants 2020, 9(1), 126; https://doi.org/10.3390/plants9010126
Submission received: 26 December 2019 / Revised: 11 January 2020 / Accepted: 16 January 2020 / Published: 19 January 2020
(This article belongs to the Special Issue Applications of Plant-Borne Essential Oils from Lamiaceae, Asteraceae and Apiaceae)
Versions Notes

Abstract

:
In the past, Native Americans of North America had an abundant traditional herbal legacy for treating illnesses, disorders, and wounds. Unfortunately, much of the ethnopharmacological knowledge of North American Indians has been lost due to population destruction and displacement from their native lands by European-based settlers. However, there are some sources of Native American ethnobotany remaining. In this work, we have consulted the ethnobotanical literature for members of the Asteraceae used in Cherokee and other Native American traditional medicines that are native to the southeastern United States. The aerial parts of Eupatorium serotinum, Eurybia macrophylla, Eutrochium purpureum, Polymnia canadensis, Rudbeckia laciniata, Silphium integrifolium, Smallanthus uvedalia, Solidago altissima, and Xanthium strumarium were collected from wild-growing plants in north Alabama. The plants were hydrodistilled to obtain the essential oils and the chemical compositions of the essential oils were determined by gas chromatography–mass spectrometry. The essential oils were tested for in-vitro antifungal activity against Aspergillus niger, Candida albicans, and Cryptococcus neoformans. The essential oil of E. serotinum showed noteworthy activity against C. neoformans with a minimum inhibitory concentration (MIC) value of 78 μg/mL, which can be attributed to the high concentration of cyclocolorenone in the essential oil.

1. Introduction

Many aspects of modern medicine have relied on the traditional knowledge of native cultures, including, for example, traditional Indian medicine (Ayurveda) [1], traditional Chinese medicine (TCM) [2], and traditional Islamic medicine [3]. Unfortunately, many of the traditional uses of medicinal plants are being lost due to several reasons. Recent generations are less interested in traditional knowledge, and habitat destruction and forced migration have reduced access to medicinal plants. The Native Americans of North America also had rich traditions of medicinal plant use. However, much of this knowledge has been lost due to population declines and displacement from native lands. Nevertheless, there are still some existing references to the ethnobotanical uses of medicinal plants by Native Americans [4].
Eupatorium serotinum Michx., “late boneset”, is native to eastern North America and ranges from Texas, Oklahoma, and Kansas, to the Atlantic coast and from the Gulf of Mexico north to Wisconsin and Michigan [5]. The Houma people of Louisiana used a decoction of the flowers to treat typhoid fever [6]. Extracts of the aerial parts of E. serotinum have yielded germacranolide sesquiterpenoids [7,8].
Eurybia macrophylla (L.) Cass. (syn. Aster macrophyllus L.), “bigleaf aster”, is native to southeastern Canada and northeastern United States, as far south as north Alabama and north Georgia [9]. The Iroquois used a decoction of the roots as a blood medicine and to treat venereal disease; the Ojibwa people ate the leaves of E. macrophylla as a medicine and food [6].
Eutrochium purpureum (L.) E.E. Lamont (syn. Eupatorium purpureum L.), “purple Joe-Pye weed”, ranges from central to eastern North America, from the Great Lakes region south to the Gulf of Mexico [10]. The Cherokee used the roots as a treatment for rheumatism, for kidney problems, and for “female problems”; the Chippewa inhaled the vapors from an infusion of the plant for colds; the Navajo used the plant as an antidote for poison; and the Potawatomi people applied a poultice of the leaves on burns [6].
Polymnia canadensis L., “white flower leafcup”, is found in eastern North America from Alabama and Georgia north to Ontario, and from Kansas and Oklahoma east to the Appalachians and New York [11]. The Houma people applied a poultice of the crushed leaves to swellings; the Iroquois used the plant to relieve toothache [6]. Extracts of the aerial parts of P. canadensis have yielded diterpenoid carboxylic acids and germacranolides [12].
Rudbeckia laciniata L., “cutleaf coneflower”, is widespread in the United States and Canada [13]. There are eight varieties of R. laciniata, namely ampla, bipinnata, digitata, gaspereauensis, heterophylla, hortensia, humilis, and laciniata [14]; R. laciniata var. laciniata is the common variety found in eastern North America [15]. The Cherokee ate the cooked greens to “keep well”, while the Chippewa applied a poultice of the flowers to treat burns [6]. Several lignans, flavonoid glycosides, and quinic acid derivatives have been isolated from the aerial parts of R. laciniata, and sesquiterpenoids have been isolated from root extracts [4].
Silphium integrifolium Michx., “whole-leaf rosinweed”, ranges from Wisconsin and Michigan, south through Alabama and Mississippi, and west as far as New Mexico [16]. An infusion of the leaves of S. integrifolium was taken by the Meskwaki people for “bladder troubles” [6]. Flavonoids, oleanolic acid glycosides, and phenolic acids have been identified in the aerial parts of S. integrifolium [17].
Smallanthus uvedalia (L.) Mack. (syn. Polymnia uvedalia (L.) L.), “yellow flower leafcup”, is found in the southeastern United States from Virginia to Florida, west to eastern Texas and Oklahoma [18]. The Cherokee used the bruised roots on burns and cuts; the Iroquois took an infusion of the shoots and roots to treat back pain and vomiting [6]. The plant is the source of several germacranolide sesquiterpenoids and ent-kaurane diterpenoids [4].
Solidago altissima L. (syn. Solidago canadensis L.), “Canada goldenrod”, ranges across most of North America from Canada to northern Mexico [19]. The Okanagan-Colville and the Thompson tribes used an infusion of the roots and shoots of S. altissima to treat fevers [6], and the Cherokee took an infusion of Solidago spp. to treat fevers. The phytochemistry of S. canadensis has been extensively studied and found to contain saponins [20,21], flavonoids [22,23,24], polyacetylenes [25,26], diterpenoids [27], and triterpenoids [28].
Xanthium strumarium L., “rough cocklebur”, ranges throughout North America and is considered a noxious weed in the southeastern United States [29]. The White Mountain Apache tribe took a root decoction to treat fevers; the Mahuma people of Southern California used the plant to treat rheumatism, tuberculosis, and gonorrhea [6]. The aerial parts of X. strumarium contain alkaloids, sesquiterpene lactones (guaianolides, germacranolides, and elemanolides), phenolic compounds, and the toxic carboxylic acid atractyloside, a kaurene glycoside [30].
We have had an interest in the volatile chemistry and biological activity of Native American medicinal plants [31,32,33,34,35,36,37,38,39,40,41,42], including members of the Asteraceae [43,44,45]. As part of our continuing investigations, the purpose of this work was to seek out additional species of Asteraceae important in Native American traditional medicine growing wild in northern Alabama and to obtain the essential oils by hydrodistillation of the aerial parts. As a test for biological activity, the essential oils were then screened for antifungal activity against three potentially pathogenic fungal strains. Aspergillus niger, Candida albicans, and Cryptococcus neoformans are the causative agents of opportunistic Aspergillus lung disease, candidiasis, and cryptococcosis, respectively.

2. Results and Discussion

The essential oils from E. serotinum, E. macrophylla, E. purpureum, P. canadensis, R. laciniata, S. integrifolium, S. uvedalia, S. altissima, and X. strumarium were obtained from the fresh aerial parts of the plants by hydrodistillation, generally in low yield. The essential oils were analyzed by GC and GC–MS (Tables 1, 3–9, and 11).

2.1. Eupatorium serotinum Michx.

The essential oil from the aerial parts of E. serotinum was rich in sesquiterpenoids, with cyclocolorenone (23.38%), germacrene D (6.58%), and palustrol (5.32%), along with an unidentified sesquiterpenoid (5.72%) as the major components (Table 1).
To our knowledge, there have been no previous reports on the essential oil composition of E. serotinum. The phytochemistry of the genus Eupatorium has been reviewed [46] and there have been numerous reports on the essential oil compositions from other species of the genus (Table 2). There is much variability in the essential oil compositions of Eupatorium species, both between species and within species. Nevertheless, sesquiterpenoids often dominate the essential oils of Eupatorium species.

2.2. Eurybia macrophylla (L.) Cass.

Monoterpene hydrocarbons, limonene (28.66%), β-pinene (8.57%), and terpinolene (5.35%), and germacrane sesquiterpenes, germacrene D (19.81%), and germacrene B (7.07%), were the major components in the essential oil of E. macrophylla (Table 3). To our knowledge, there are no reports on essential oil compositions of any Eurybia species.

2.3. Eutrochium purpureum (L.) E.E. Lamont (syn. Eupatorium purpureum L.)

The major components in the essential oil of E. purpureum were the green leaf volatiles (2E)-hexenal (60.59%) and hexanal (6.78%), along with the aromatic compounds eugenol (11.68%) and methyl salicylate (10.31%; Table 4). There have apparently been no previous reports on the essential oil composition of E. purpureum or any other Eutrochium species. There are numerous reports on Eupatorium essential oils, however (see above).

2.4. Polymnia canadensis L.

α-Phellandrene (28.30%), α-pinene (19.71%), and germacrene D (11.42%) were the major components in the essential oil from the aerial parts of P. canadensis (Table 5). The volatile chemical profile of P. canadensis in this current work is in marked contrast to our previous report on this species [45]. Previous samples were rich in the sesquiterpene hydrocarbons germacrene D (63.6% and 44.5%) and β-caryophyllene (15.9% and 14.8%). The differences in compositions are likely due to seasonal variation (the current sample was collected in July, 2018, while the previous samples were collected in September, 2015, and December, 2016, respectively). We cannot rule out, however, chemical profile differences attributable to environmental differences or biotic differences (e.g., genetics, herbivory, or pathogen stress).

2.5. Rudbeckia laciniata L.

Monoterpene hydrocarbons dominated the essential oil of R. laciniata (Table 6). The major components were limonene (58.07%), α-pinene (10.18%), β-pinene (9.21%), and myrcene (5.26%). While R. laciniata essential oil was rich in monoterpene hydrocarbons, the essential oils of R. fulgida and R. hirta were rich in sesquiterpene hydrocarbons [43]. The major components in R. fulgida essential oil were germacrene D (30.1%), δ-cadinene (17.8%), β-caryophyllene (10.0%), and γ-muurolene (8.9%), along with (E)-β-ocimene (6.2%) and (2E)-hexenal (6.0%). Similarly, the major components of R. hirta essential oil were germacrene D (23.6%), δ-cadinene (16.2%), β-caryophyllene (4.7%), γ-muurolene (8.1%), as well as (E)-β-ocimene (15.2%) and (2E)-hexenal (20.2%) [43]. The leaf essential oil of Rudbeckia triloba, collected in Bucharest, Romania, was rich in monoterpene hydrocarbons, α-pinene (46.0%), sabinene (9.6%), and β-phellandrene (24.6%), along with germacrene D (6.1%), but devoid of limonene [73]. Thus, there do not seem to be any consistent chemical markers for the Rudbeckia genus.

2.6. Silphium integrifolium Michx.

The major components in the essential oil from the aerial parts of S. integrifolium were α-pinene (58.59%) and β-pinene (14.69%), followed by myrcene (9.70%; Table 7). Kowalski has extensively examined the essential oils of S. integrifolium as well as S. trifoliatum cultivated in Poland [74,75,76,77,78]. The leaf essential oil of S. integrifolium from Poland had α-pinene (7.3–9.8%), germacrene D (4.0–28.4%), allo-aromadendrene (3.7–8.5%), caryophyllene oxide (6.1–12.4%), and silphiperfol-6-en-5-one (3.7–5.1%) [74,75]; while the floral essential oil was made up of α-pinene (13.4–14.0%), camphene (5.3–5.7%), trans-verbenol (5.2–6.3%), bornyl acetate (6.5–7.0%), and allo-aromadendrene (5.6–6.1%) [74,77]. Thus, there are major qualitative and quantitative differences between the samples from Alabama and from Poland.

2.7. Smallanthus uvedalia (L.) Mack.

Monoterpene hydrocarbons dominated the essential oil of S. uvedalia (Table 8). α-Pinene (62.56%) was the major component, followed by limonene (11.43%) and β-pinene (6.00%). The chemical composition of this monoterpene-rich essential oil is very different from the compositions collected previously by us [45]. The previous samples, collected in February 2016, were dominated by β-caryophyllene (24.5% and 16.5%) and caryophyllene oxide (19.8% and 14.2%). The sample of S. uvedalia in this present work was collected in September 2018. The differences in composition may be due to seasonal variation, genetic differences, or environmental stresses. Nevertheless, α-pinene has dominated the essential oil compositions of other Smallanthus species. For example, α-pinene was the major component in the essential oil of S. maculatus from Costa Rica (32.9% α-pinene), which was also rich in camphene (5.4%), β-pinene (7.1%), β-caryophyllene (10.7%), germacrene D (13.7%), and bicyclogermacrene (6.6%) [79]. Likewise, the essential oil of S. quichensis from Costa Rica was also dominated by α-pinene (35.5–64.5%) with lesser concentrations of α-phellandrene (0.1–9.0%), p-cymene (0.1–11.5%), limonene (2.1–5.8%), β-phellandrene (up to 9.2%), and 1,8-cineole (up to 9.7%) [80]. In contrast, S. sonchifolia essential oil, grown in Sichuan, China, was made up of β-phellandrene (26.3%), β-bourbonene (10.2%), β-caryophyllene (14.0%), and β-cubebene (17.6%) [81].

2.8. Solidago altissima L. (syn. Solidago canadensis L.)

The major components in the essential oil from the aerial parts of S. altissima (syn. S. canadensis) from Alabama were α-pinene (13.91%), sabinene (14.25%), myrcene (20.29%), bornyl acetate (14.44%), and germacrene D (10.67%; Table 9). Previous examinations of S. canadensis essential oils have shown germacrene D to be one of the most abundant components (Table 10). However, Weyerstahl and co-workers [82] found curlone (23.5%) to be a major component of S. canadensis from Poland, Schmidt and co-workers [83] found cyclocolorenone (38%) to be a major component in S. canadensis from northern Germany, and Kasali and co-workers [84] found 6-epi-β-cubebene to be a major component (20.5%) in S. canadensis essential oil from Poland. Interestingly, none of these compounds was detected in the sample of S. altissima essential oil from Alabama.

2.9. Xanthium strumarium L.

The major volatile components from the aerial parts of X. strumarium were limonene (48.23%), myrcene (14.31%), germacrene D (13.92%), (2E)-hexenal (5.79%), and sabinene (4.89%; Table 11). The compositions of Xanthium strumarium essential oils from the Middle East have been reported, including Iran [93,94] and Pakistan [95]. The leaf essential oil from Khoramabad, Iran, was composed largely of limonene (24.7%), borneol (10.6%), bornyl acetate (5.9%), and β-cubebene (6.3%) [93]. The leaf essential oil from Zabol, Iran, was qualitatively similar, limonene (20.3%), borneol (11.6%), bornyl acetate (4.5%), and β-cubebene (3.8%), but also contained a large concentration of cis-β-guaiene (34.2%), which was not observed in any other X. strumarium essential oils [94]. The leaf essential oil of X. strumarium from Lahore, Pakistan, contained limonene (5.7%), β-caryophyllene (17.5%), spathulenol (6.1%), and α-cadinol (6.7%) as major components [95]. The differences in chemical compositions may be related to different genetic factors as well as geographical location; Tropicos® currently lists 13 subordinate taxa for X. strumarium [14].

2.10. Antifungal Screening

Depending on material available, the essential oils were screened for antifungal activity against the opportunistic fungal pathogens Aspergillus niger, Candida albicans, and Cryptococcus neoformans using the microbroth dilution technique (Table 12). The essential oil of E. serotinum showed promising antifungal activity against C. neoformans with a minimum inhibitory concentration (MIC) value of 78 μg/mL. The high concentration of cyclocolorenone in E. serotinum is likely responsible for the observed antifungal activity of this essential oil. Cyclocolorenone had been previously reported to show antifungal activity against Curvularia lunata, Chaetomium cochliodes, and Chaetomium spinusum [96]. Germacrene D may also contribute to the antifungal activity of E. serotinum essential oil as well as essential oils of E. macrophylla, P. canadensis, and R. laciniata. Germacrene D has shown antifungal activity against Aspergillus niger with MIC of 39 μg/mL [97].
The modest antifungal activity of E. purpureum is somewhat surprising. The major components were hexanal, (2E)-hexenal, methyl salicylate, and eugenol. Hexanal [98] and (2E)-hexenal [99,100] are both known to be antifungal to plant pathogenic fungi. Methyl salicylate is only weakly antifungal against A. niger, C. albicans, or C. neoformans, but eugenol is somewhat active (see Table 13). Monoterpene hydrocarbons such as α-pinene, β-pinene, limonene, or myrcene show only weak antifungal activity (Table 13) and are not expected to contribute to the antifungal activities of the essential oils unless there are synergistic effects of these components (see, for example [101,102]). The mechanisms of antifungal activity of essential oils are poorly understood. However, it has been suggested that essential oils and their components, being lipophilic, can disrupt the membranes of fungi causing membrane permeability [103].

3. Materials and Methods

3.1. Plant Material

Aerial parts of each plant were collected from various sites in north Alabama (Table 14). Plants were identified by S.K. Lawson and voucher specimens were deposited in the University of Alabama in Huntsville herbarium (HALA). The fresh plant material (aerial parts) were chopped and hydrodistilled using a Likens–Nickerson apparatus with continuous extraction with CH2Cl2 for three hours. The solvent was evaporated to give pale yellow essential oils (Table 14).

3.2. Gas Chromatography–Mass Spectrometry

The Asteraceae essential oils were analyzed by GC–MS using a Shimadzu GC–MS-QP2010 Ultra fitted with a Phenomenex ZB-5ms column as previously described [104]. Identification of the essential oil components was determined by comparison of their retention indices, determined with respect to a homologous series of n-alkanes and their mass spectral fragmentation patters with those from available databases (Adams [105], NIST17 [106], and FFNSC 3 [107]) or in our in-house library [108].

3.3. Gas Chromatography–Flame Ionization Detection

Quantification of the essential oils was determined by GC–FID using a Shimadzu GC 2010 instrument fitted with a ZB-5 column [104], using the same parameters that were used for the GC–MS. The concentrations (average of three measurements ± standard deviations) are based on peak integration without standardization.

3.4. Antifungal Screening

The essential oils were screened for antifungal activity against Aspergillus niger (ATCC 16888), Candida albicans (ATCC 18804), and Cryptococcus neoformans (ATCC 24607) using the microbroth dilution method as previously described [109]. Amphotericin B was used as the positive control and RPMI medium was used as the negative control. The antifungal assays were carried out in triplicate.

4. Conclusions

There is much intraspecific variation in essential oil compositions of these members of the Asteraceae. Much of the variation can be attributed to geographical location or seasonal variation. Eupatorium serotinum essential oil showed notable antifungal activity against Cryptococcus neoformans. However, the yield of this essential oil (0.013%) is too low to be considered as pharmacologically useful. If suitable sources of the major component cyclocolorenone can be identified, then this compound may serve as important antifungal template for further elaboration.

Author Contributions

Conceptualization, S.K.L. and W.N.S.; methodology, W.N.S., R.L.M., and P.S.; software, P.S.; validation, W.N.S.; formal analysis, W.N.S.; investigation, S.K.L., L.G.S., C.N.P., and P.S.; resources, R.L.M., 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., L.G.S., C.N.P., R.L.M., P.S., and W.N.S.; supervision, W.N.S. and R.L.M.; project administration, W.N.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

P.S. and W.N.S. participated in the project as part of the activities of the Aromatic Plant Research Center (APRC, https://aromaticplant.org/).

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Chemical composition of the essential oil of Eupatorium serotinum Michx.
Table 1. Chemical composition of the essential oil of Eupatorium serotinum Michx.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
802801Hexanal0.16 ± 0.0215311533trans-Cadina-1,4-diene0.20 ± 0.07
8107962-Hexanol0.92 ± 0.011540---Unidentified e1.28 ± 0.05
850846(2E)-Hexenal0.86 ± 0.1115421539α-Copaen-11-ol7.89 ± 0.13
932932α-Pinene0.17 ± 0.011548---Unidentified f1.76 ± 0.04
949946Camphene1.78 ± 0.021550---Unidentified g0.75 ± 0.03
977974β-Pinene0.18 ± 0.0215581559Germacrene B0.44 ± 0.03
9991001δ-2-Carene0.15 ± 0.011562---Eudesmenol h0.32 ± 0.09
10291024Limonene0.26 ± 0.0115691567Palustrol5.32 ± 0.12
12831287Bornyl acetate4.72 ± 0.0715751574Germacra-1(10),5-dien-4β-ol0.91 ± 1.10
1326---Unidentified c0.93 ± 0.0315811577Spathulenol1.58 ± 0.83
13461345α-Cubebene0.59 ± 0.0115881590Globulol0.58 ± 0.03
13751374α-Copaene0.11 ± 0.0515931592Viridiflorol1.12 ± 0.09
13831387β-Bourbonene0.06 ± 0.011596---Unidentified i1.20 ± 0.02
13971387β-Cubebene3.65 ± 0.0916031602Ledol2.80 ± 0.03
14061409α-Gurjunene0.74 ± 0.0216201611Germacra-1(10),5-dien-4α-ol1.44 ± 0.13
14171419β-Ylangene0.09 ± 0.0316221624Selina-6-en-4β-ol0.31 ± 0.03
14181417β-Caryophyllene0.96 ± 0.01162716271-epi-Cubenol0.61 ± 0.10
14281434γ-Elemene0.28 ± 0.0516381639cis-Guaia-3,9-dien-11-ol0.12 ± 0.01
14481448cis-Muurola-3,5-diene0.07 ± 0.0316421638τ-Cadinol0.80 ± 0.03
14551452α-Humulene0.41 ± 0.0416421640τ-Muurolol0.62 ± 0.08
14711475trans-Cadina-1(6),4-diene0.25 ± 0.0316461644α-Muurolol (=δ-Cadinol)0.69 ± 0.07
14801484Germacrene D6.58 ± 0.0916481646Agarospirol II1.10 ± 0.04
14861488δ-Selinene0.27 ± 0.0216541652α-Cadinol2.31 ± 0.04
14881489β-Selinene0.17 ± 0.011668---Unidentifiedj5.72 ± 0.14
14911493trans-Muurola-4(14),5-diene0.69 ± 0.0317511759Cyclocolorenone23.38 ± 0.43
14941493epi-Cubebol1.81 ± 0.03 Green leaf volatiles1.94
14971500α-Muurolene0.34 ± 0.02 Monoterpene hydrocarbons2.53
1502---Unidentified d1.30 ± 0.02 Oxygenated monoterpenoids4.72
15121513γ-Cadinene0.21 ± 0.00 Sesquiterpene hydrocarbons19.14
15141514Cubebol4.18 ± 0.11 Oxygenated sesquiterpenoids57.90
15171522δ-Cadinene3.02 ± 0.25 Total Identified86.23
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c MS(EI) (mass spectrum (electron impact)): 162(84%), 147(96%), 133(20%), 120(32%), 119(41%), 108(35%), 105(100%), 91(63%), 79(29%), 77(22%), 55(11%), 53(12%), 41(14%). d MS(EI): 202(7%), 187(9%), 162(68%), 159(31%), 147(50%), 145(32%), 132(49%), 119(66%), 105(89%), 91(48%), 81(18%), 79(20%), 77(16%), 59(100%), 43(20%), 41(20%). e MS(EI): 202(4%), 187(13%), 162(56%), 159(59%), 147(39%), 145(40%), 132(73%), 131(39%), 119(73%), 106(48%), 105(88%), 91(47%), 81(16%), 79(25%), 77(19%), 59(100%), 55(18%), 43(19%), 41(20%). f MS(EI): 220(24%), 205(17%), 163(19%), 120(35%), 110(100%), 105(20%), 95(35%), 69(44%), 55(20%), 41(24%). g MS(EI): 220(47%), 163(25%), 161(32%), 121(100%), 108(42%), 93(42%), 81(59%), 69(17%), 55(15%), 41(18%). h Correct isomer not identified. i MS(EI): 220(49%), 205(7%), 163(33%), 161(28%), 121(100%), 108(40%), 93(35%), 81(80%), 69(20%), 55(17%), 41(19%). j MS(EI): 202(46%), 187(67%), 174(40%), 162(60%), 159(100%), 147(89%), 134(30%), 131(23%), 119(62%), 105(71%), 91(50%), 59(61%), 43(20%), 41(22%).
Table
Table 2. Major components and biological activities of Eupatorium essential oils.
Table 2. Major components and biological activities of Eupatorium essential oils.
Eupatorium spp. Essential OilLocationMajor ComponentsBiological ActivityRef.
E. adenophorum (aerial parts)Nainital, Indiacamphene (8.9%), p-cymene (16.6%), bornyl acetate (15.6%), amorph-4-en-7-ol (9.6%), α-cadinol (6.2%), amorpha-4,7(11)-dien-8-one (7.8%)none reported[47]
E. adenophorum (leaves)Palampur, Indiabornyl acetate (9.0%), germacrene D (5.7%), β-bisabolene (6.2%), 1-naphthalenol (17.5%), α-bisabolol (9.5%)Antibacterial (Rhodococcus rhodochrous, MBC 12.5 μL/mL)[48]
E. adenophorum (twigs)Uttar Pradesh, Indiacamphene (12.1%), α-phellandrene (8.6%), α-terpinene (6.5%), p-cymene (11.6%), bornyl acetate (10.6%), acoradiene (10.1%), α-bisabolol (5.3%)Antibacterial (Erwinia herbicola, MIC 0.25 μL/mL; Pseudomonas putida, MIC 2.0 μL/mL)[49]
E. adenophorum (inflorescence)Palampur, Indiabornyl acetate (6.3%), β-caryophyllene (5.4%), γ-muurolene (11.7%), γ-curcumene (5.7%), γ-cadinene (18.4%), 3-acetoxyamorpha-4,7(11)-dien-8-one (7.4%)Antifungal (Macrophomina phaseolina, EC50 0.076 μL/mL; Rhizoctonia solani, EC50 0.094 μL/mL; Fusarium oxysporum, EC50 0.120 μL/mL)[50]
E. amygdalinum (aerial parts)Amapá, Brazilβ-cubebene (5.7%), β-caryophyllene (12.3%), germacrene D (15.5%), δ-cadinene (5.8%), caryophyllene oxide (17.4%)none reported[51]
E. argentinum (leaves)Córdoba, Argentinaα-pinene (17.0%), β-pinene (6.1%), p-cymene (12.5%), thymyl acetate (9.7%), β-caryophyllene (7.2%)none reported[52]
E. arnottianum (aerial parts)Córdoba, Argentinaα-pinene (13.7%), p-cymene (30.0%), β-ocimene (5.3%), thymyl acetate (12.3%), β-caryophyllene (11.7%)none reported[53]
E. arnottianum (aerial parts)Córdoba, Argentinalimonene (32.7%), piperitenone (21.2%), trans-dihydrocarvone (10.2%), camphor (6.8%), cis-dihydrocarvone (6.7%)Antiviral (HSV-1, IC50 52.1 μg/mL; DENV-2, IC50 38.2 μg/mL)[54]
E. arnottii (aerial parts)San Luis, Argentinaβ-caryophyllene (7.9%), γ-elemene (5.9%), germacrene D (9.8%), cadinene (5.8%), spathulenol (10.6%), phytol (8.1%)Insecticidal (Tribolium castaneum, ED50 0.15 mg/cm2)[55]
E. ballotaefolium (aerial parts)Ceará, Brazilα-pinene (6.2%), sabinene (6.5%), β-pinene (5.4%), myrcene (7.3%), limonene (15.3%), (E)-β-ocimene (10.5%), β-caryophyllene (7.5%)none reported[56]
E. betonicaeforme (leaves)Ceará, Brazilβ-caryophyllene (36.1%), α-humulene (13.3%), γ-muurolene (20.3%), bicyclogermacrene (15.0%)Larvicidal (Aedes aegypti, LC50 129 μg/mL)[57]
E. buniifolium (aerial parts)Canelones, Uruguayα-pinene (14.7%), β-elemene (12.2%), germacrene D (11.5%), trans-β-guaiene (6.5%)none reported[58]
E. buniifolium (aerial parts)San Luis, Argentinaα-pinene (51.0%), sabinene (7.5%), limonene (9.6%), β-caryophyllene (5.2%)Insecticidal (Tribolium castaneum, ED50 0.15 mg/cm2)[55]
E. buniifolium (leaves)Canelones, Uruguayα-pinene (8.2%), germacrene D (11.1%), trans-β-guaiene (7.4%)Varroacide (Varroa destructor, LD99 0.3 mg/mL)[59]
E. cannabinum ssp. cannabinum (aerial parts)Agerola, Italyδ-2-carene (6.5%), germacrene D (33.5%), α-farnesene (12.9%)Antibacterial (Staphylococcus aureus, Streptococcus fecalis, Bacillus subtilis, Bacillus cereus, MIC 1.25 mg/mL)[60]
E. cannabinum (leaves)Tuscany, Italythymol methyl ether (7.8%), germacrene D (29.2%), spathulenol (7.3%)none reported[61]
E. cannabinum ssp. corsicum (aerial parts)Corsica, Franceα-phellandrene (19.0%), p-cymene (5.2%), germacrene D (28.5%)none reported[62]
E. cannabinum (aerial parts)Mazandaran, Iranα-terpinene (17.8%), thymol methyl ether (5.2%), germacrene D (9.1%)none reported[63]
E. cannabinum (leaves)Vilnius, Lithuaniathymol methyl ether (5.7%), neryl acetate (9.4%), germacrene D (11.3%), β-bisabolene (6.7%)none reported[64]
E. capillifolium (aerial parts)Cubap-cymene (23.7%), thymol methyl ether (8.9%), β-bisabolene (8.2%), selin-11-en-4α-ol (12.3%)none reported[65]
E. capillifolium (aerial parts)Mississippi, USAmyrcene (15.7%), α-phellandrene (6.5%), thymol methyl ether (36.3%), 2,5-dimethoxy-p-cymene (20.8%)Insecticidal (Stephanitis pyrioides, LC50 5800 μg/mL)[66]
E. catarium (aerial parts)Córdoba, Argentinaspathulenol (15.5%), β-caryophyllene (7.8%), germacrene D (5.5%), bicyclogermacrene (5.1%)Antiviral (HSV-1, IC50 47.9 μg/mL; DENV-2, IC50 57.3 μg/mL)[54]
E. conyzoides (aerial parts)Tocantins, Brazilβ-caryophyllene (7.1%), α-humulene (6.6%), germacrene D (16.8%), bicyclogermacrene (7.2%), spathulenol (8.3%)none reported[51]
E. glabratum (leaves)Michoacán, Méxicoα-pinene (29.5%), β-pinene (6.3%), α-phellandrene (19.6%)Insecticidal (Sitophilus zeamais, LC50 18.0 μL/mL)[67]
E. hecatanthum (leaves)Córdoba, Argentinaα-pinene (13.4%), β-pinene (7.8%), β-ocimene (6.2%), carvacrol (7.1%), thymyl acetate (10.6%), β-caryophyllene (8.1%)none reported[52]
E. inulaefolium (aerial parts)San Luis, Argentinalimonene (9.7%), δ-elemene (10.6%), β-caryophyllene (27.7%), α-humulene (5.9%), patchoulene (9.2%), germacrene D (13.7%), viridiflorol (9.2%)Insecticidal (Tribolium castaneum, ED50 0.15 mg/cm2)[55]
E. laevigatum (aerial parts)Roraima, Brazilgermacrene D (8.6%), selina-3,7(11)-diene (6.1%), spathulenol (5.4%), globulol (16.2%), laevigatin (23.6%)none reported[51]
E. laevigatum (leaves)Rio Grande do Sul, Brazilgermacrene D (11.7%), bicyclogermacrene (9.3%), laevigatin (59.6%)none reported[68]
E. macrophyllum (aerial parts)Chapada dos Guimarães, Brazilsabinene (46.7%), limonene (23.3%)none reported[51]
E. marginatum (aerial partsAnanindeua, Pará, Brazilar-curcumene (6.8%), α-zingiberene (57.5%), β-sesquiphellandrene (7.1%), (E)-γ-bisabolene (9.7%)none reported[51]
E. marginatum (aerial partsRoraima, Brazilα-gurjunene (19.5%), germacrene D (14.8%), α-selinene (9.0%), (E)-γ-bisabolene (5.0%)none reported[51]
E. odoratum (aerial parts)Thitsanulok, Thailandα-pinene (8.4%), β-pinene (5.6%), pregeijerene (17.6%), germacrene D (11.1%), β-caryophyllene (7.3%), vestitenone (6.5%)none reported[69]
E. odoratum (leaves)Lagos, Nigeriaα-pinene (42.2%), β-pinene (10.6%), β-caryophyllene (5.4%), germacrene D (9.7%), β-copaen-4α-ol (9.4%)Antibacterial (Bacillus cereus, MIC 39 μg/mL), antifungal (Aspergillus niger, MIC 78 μg/mL)[70]
E. odoratum (aerial parts)Western Ghats, Indiacis-sabinene hydrate (5.7%), pregeijerene (14.2%), epi-cubebol (9.8%), cubebol (8.6%)none reported[71]
E. squalidum (aerial parts)Amapá, Brazilβ-caryophyllene (6.2%), germacrene D (21.6%), bicyclogermacrene (6.0%), spathulenol (14.2%), globulol (25.1%)none reported[51]
E. squalidum (aerial parts)Tocantins, Brazillimonene (6.6%), β-caryophyllene (9.6%), germacrene D (10.4%), caryophyllene oxide (30.1%)none reported[51]
E. subhastatum (leaves)Córdoba, Argentinaα-pinene (11.0%), β-pinene (5.9%), p-cymene (24.8%), α-copaene (5.1%), α-humulene (5.1%)none reported[52]
E. triplinerve (leaves)Lucknow, Indiaδ-elemene (5.9%), β-caryophyllene (14.7%), selina-4(15),7(11)-dien-8-onenone reported[72]
E. viscidum (aerial parts)San Luis, Argentina6-methyl-5-hepten-2-one (18.2%), spathulenol (25.2%)Insecticidal (Tribolium castaneum, ED50 > 0.212 mg/cm2)[55]
Table
Table 3. Chemical composition of the essential oil of Eurybia macrophylla (L.) Cass.
Table 3. Chemical composition of the essential oil of Eurybia macrophylla (L.) Cass.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
801797(3Z)-Hexenal0.06 ± 0.0113871389β-Elemene1.48 ± 0.04
802801Hexanal0.31 ± 0.0514181417β-Caryophyllene4.60 ± 0.07
850846(2E)-Hexenal1.44 ± 0.0614271434γ-Elemene3.16 ± 0.01
8658631-Hexanol0.11 ± 0.0214311432trans-α-Bergamotene0.05 ± 0.02
924924α-Thujene0.16 ± 0.0114541452α-Humulene0.64 ± 0.01
932974α-Pinene3.12 ± 0.0414731471Massoia lactone0.35 ± 0.04
948946Camphene0.60 ± 0.0014801484Germacrene D19.81 ± 0.20
971969Sabinene0.15 ± 0.0214871489β-Selinene0.31 ± 0.05
977974β-Pinene8.57 ± 0.0714941500Bicyclogermacrene1.95 ± 0.02
988988Myrcene1.79 ± 0.0214971500α-Muurolene0.16 ± 0.03
989988Dehydro-1,8-cineole0.28 ± 0.0115161522δ-Cadinene0.19 ± 0.02
10061002α-Phellandrene0.88 ± 0.0115361537α-Cadinene0.10 ± 0.02
10161014α-Terpinene0.16 ± 0.0215571559Germacrene B7.07 ± 0.07
10241020p-Cymene0.15 ± 0.0115751577Spathulenol0.10 ± 0.01
10281024Limonene28.66 ± 0.3315811582Caryophyllene oxide0.38 ± 0.01
10301025β-Phellandrene0.75 ± 0.0315951592Viridiflorol0.23 ± 0.03
10341032(Z)-β-Ocimene0.18 ± 0.0016271629iso-Spathulenol0.08 ± 0.01
10441044(E)-β-Ocimene2.14 ± 0.0216411638τ-Cadinol0.09 ± 0.02
10571054γ-Terpinene0.37 ± 0.0116431640τ-Murrolol0.12 ± 0.03
10841086Terpinolene5.35 ± 0.0816461644α-Muurolol (=δ-Cadinol)0.10 ± 0.01
11121114(E)-4,8-Dimethylnona-1,3,7-triene0.35 ± 0.0116541652α-Cadinol0.47 ± 0.02
11241118cis-p-Menth-2-en-1-ol0.72 ± 0.0118321835Neophytadiene0.05 ± 0.02
11421136trans-p-Menth-2-en-1-ol0.44 ± 0.0118381841Phytone0.05 ± 0.02
11871179p-Cymen-8-ol0.21 ± 0.03 Green leaf volatiles1.91
11951186α-Terpineol0.06 ± 0.02 Monoterpene hydrocarbons53.03
11971195cis-Piperitol0.15 ± 0.02 Oxygenated monoterpenoids2.30
12091207trans-Piperitol0.17 ± 0.01 Sesquiterpene hydrocarbons40.03
12831287Bornyl acetate0.27 ± 0.10 Oxygenated sesquiterpenoids1.59
12921293Undecan-2-one0.05 ± 0.01 Diterpenoids0.11
13331335δ-Elemene0.50 ± 0.00 Others0.75
Total Identified99.72
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases.
Table
Table 4. Chemical composition of the essential oil of Eutrochium purpureum (L.) E.E. Lamont.
Table 4. Chemical composition of the essential oil of Eutrochium purpureum (L.) E.E. Lamont.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
801797(3Z)-Hexenal1.01 ± 0.1112061201Decanal0.37 ± 0.05
802801Hexanal6.78 ± 0.1713511356Eugenol11.68 ± 0.14
850946(2E)-Hexenal60.59 ± 1.0014171417β-Caryophyllene0.24 ± 0.02
8659631-Hexanol2.35 ± 0.4114791484Germacrene D0.67 ± 0.10
931932α-Pinene1.48 ± 0.0915591561(E)-Nerolidol0.50 ± 0.01
943---Unidentified c0.56 ± 0.07 Green leaf volatiles71.47
1004998Octanal0.33 ± 0.04 Monoterpene hydrocarbons2.36
10051004(3Z)-Hexenyl acetate0.72 ± 0.12 Sesquiterpene hydrocarbons0.91
10281024Limonene0.88 ± 0.07 Oxygenated sesquiterpenoids0.50
10451036Benzene acetaldehyde0.60 ± 0.03 Benzenoids22.59
11051100Nonanal0.91 ± 0.19 Fatty aldehydes1.61
11921190Methyl salicylate10.31 ± 0.18 Total Identified99.44
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c MS(EI): 208(8%), 97(100%), 96(17%), 86(9%), 69(12%), 56(22%), 55(64%), 43(18%).
Table
Table 5. Chemical composition of the essential oil of Polymnia canadensis L.
Table 5. Chemical composition of the essential oil of Polymnia canadensis L.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
802801Hexanal0.28 ± 0.0414171417β-Caryophyllene3.05 ± 0.02
8117962-Hexanol0.17 ± 0.0114281430β-Copaene0.09 ± 0.02
850850(3Z)-Hexenol4.31 ± 0.1614461453Geranyl acetone0.17 ± 0.01
861854(2E)-Hexenol0.08 ± 0.0114541452α-Humulene1.14 ± 0.00
8648631-Hexanol0.30 ± 0.0214581458allo-Aromadendrene0.17 ± 0.02
921921Tricyclene0.07 ± 0.0114791484Germacrene D11.42 ± 0.01
924924α-Thujene0.06 ± 0.0114841486Phenylethyl 2-methylbutanoate0.18 ± 0.04
932932α-Pinene19.71 ± 0.1114871489β-Selinene0.41 ± 0.03
948946Camphene0.80 ± 0.0114901490Phenylethyl 3-methylbutanoate0.09 ± 0.01
971969Sabinene1.96 ± 0.0014931500Bicyclogermacrene1.03 ± 0.00
976974β-Pinene0.87 ± 0.0114961500α-Muurolene0.12 ± 0.01
987988Myrcene0.53 ± 0.0115021509Lavandulyl 3-methylbutanoate0.76 ± 0.01
10061002α-Phellandrene28.30 ± 0.1615111513γ-Cadinene0.21 ± 0.01
10161014α-Terpinene0.09 ± 0.0115151518Bornyl 3-methylbutanoate0.39 ± 0.01
10241020p-Cymene4.42 ± 0.0215161522δ-Cadinene0.36 ± 0.01
10281024Limonene0.38 ± 0.0115271529Kessane0.59 ± 0.04
10301025β-Phellandrene0.06 ± 0.0215351534Liguloxide0.84 ± 0.01
10341032(Z)-β-Ocimene0.17 ± 0.0115591561(E)-Nerolidol1.71 ± 0.01
10441044(E)-β-Ocimene0.19 ± 0.0115651565Thymyl 2-methylbutanoate0.69 ± 0.01
10571054γ-Terpinene0.09 ± 0.0115681570Neryl 2-methylbutanoate0.76 ± 0.01
10691065cis-Sabinene hydrate0.08 ± 0.0115751574Germacrene D-4β-ol0.18 ± 0.01
10841086Terpinolene0.07 ± 0.0115811582Caryophyllene oxide0.21 ± 0.02
10991095Linalooltr c16081613Copaborneol0.18 ± 0.05
11011098trans-Sabinene hydratetr16411638τ-Cadinol0.59 ± 0.02
11411135trans-Pinocarveol0.08 ± 0.0216541652α-Cadinol0.81 ± 0.02
11451140trans-Verbenol0.14 ± 0.0116571658Selin-11-en-4α-ol0.15 ± 0.01
11631165Lavandulol0.12 ± 0.0116841685Germacra-4(15),5,10(14)-trien-1α-ol0.49 ± 0.03
11721165Borneol0.11 ± 0.01169316956-epi-Shyobunol0.20 ± 0.02
11801174Terpinen-4-ol0.26 ± 0.002227dKauran-16β-ol3.48 ± 0.01
12081204Verbenone0.06 ± 0.012243dKauran-16α-ol0.17 ± 0.02
12281232Thymol methyl ether2.89 ± 0.01 Green leaf volatiles5.13
134213457-epi-Silphiperfol-5-ene0.59 ± 0.02 Monoterpene hydrocarbons57.78
13511356Eugenol0.18 ± 0.03 Oxygenated monoterpenoids6.34
13671369Cyclosativene0.08 ± 0.01 Sesquiterpene hydrocarbons18.92
13671371Longicyclenetr Oxygenated sesquiterpenoids5.96
13721377Silphiperol-6-ene0.06 ± 0.00 Diterpenoids3.65
13741374α-Copaene0.12 ± 0.01 Benzenoids0.45
13801382Modheph-2-ene0.11 ± 0.00 Others0.17
13861387β-Cubebene0.06 ± 0.01 Total Identified98.40
13871389β-Elemene0.50 ± 0.01
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c tr = “trace” (<0.05%). d Assignment tentative; based on MS only.
Table
Table 6. Chemical composition of the essential oil of Rudbeckia laciniata L.
Table 6. Chemical composition of the essential oil of Rudbeckia laciniata L.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
802801Hexanal0.05 ± 0.0012061204Verbenone0.10 ± 0.03
8107962-Hexanol0.34 ± 0.0112181215trans-Carveol0.25 ± 0.06
922921Tricyclene0.10 ± 0.0012321226cis-Carveol0.07 ± 0.02
924924α-Thujene0.10 ± 0.0112431239Carvone0.49 ± 0.02
932932α-Pinene10.18 ± 0.0612831287Bornyl acetate2.68 ± 0.02
948946Camphene2.24 ± 0.0213491350α-Longipinene0.08 ± 0.02
971969Sabinene0.90 ± 0.0113681369Cyclosativene0.06 ± 0.02
977974β-Pinene9.21 ± 0.0513751374α-Copaene0.16 ± 0.01
988988Myrcene5.26 ± 0.0213911390Sativene0.05 ± 0.01
10041003p-Mentha-1(7),8-diene0.07 ± 0.0114171419β-Ylangenetr
10241020p-Cymene0.11 ± 0.0114181417β-Caryophyllene0.43 ± 0.03
10291024Limonene58.07 ± 0.4714281434γ-Elemene0.07 ± 0.00
10301025β-Phellandrene0.74 ± 0.0814311432trans-α-Bergamotene0.19 ± 0.02
10341032(Z)-β-Ocimene0.09 ± 0.0114541452α-Humulene0.12 ± 0.01
10441044(E)-β-Ocimene1.07 ± 0.0314731478γ-Muurolene0.05 ± 0.01
10691067cis-Linalool oxide (furanoid)0.19 ± 0.0014801484Germacrene D2.52 ± 0.02
10851084trans-Linalool oxide (furanoid)0.05 ± 0.0114821484(Z,Z)-α-Farnesene0.05 ± 0.01
11211119trans-p-Mentha-2,8-dien-1-ol0.37 ± 0.0114941500Bicyclogermacrene0.06 ± 0.01
11301131Limona ketone0.06 ± 0.0114971500α-Muurolene0.07 ± 0.01
11321132cis-Limonene oxide0.20 ± 0.0015141514Cubebol0.12 ± 0.01
11361133cis-p-Mentha-2,8-dien-1-ol0.26 ± 0.0115171522δ-Cadinene0.15 ± 0.01
11361137trans-Limonene oxide0.27 ± 0.0115751574Germacra-1(10),5-dien-4β-ol0.20 ± 0.02
11381135Nopinone0.06 ± 0.0115811582Caryophyllene oxide0.19 ± 0.03
11401135trans-Pinocarveol0.19 ± 0.0315911594Salvial-4(14)-en-1-onetr
11451140trans-Verbenol0.07 ± 0.0116011594Carotol0.18 ± 0.01
11621160Pinocarvone0.12 ± 0.0016201611Germacra-1(10),5-dien-4α-ol0.20 ± 0.01
11711165Borneol0.11 ± 0.02 Green leaf volatiles0.39
117811792-Isopropenyl-5-methyl-4-hexenal0.08 ± 0.01 Monoterpene hydrocarbons88.15
11801174Terpinen-4-ol0.11 ± 0.02 Oxygenated monoterpenoids6.18
11871183Cryptone0.10 ± 0.01 Sesquiterpene hydrocarbons4.06
11951195Myrtenal0.23 ± 0.02 Oxygenated sesquiterpenoids0.89
11971200trans-Dihydrocarvone tr c Total Identified99.67
11991195cis-Piperitol0.11 ± 0.07
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c tr = “trace” (<0.05%).
Table
Table 7. Chemical composition of the essential oil of Silphium integrifolium Michx.
Table 7. Chemical composition of the essential oil of Silphium integrifolium Michx.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
800797(3Z)-Hexenaltr c13871387β-Cubebenetr
801801Hexanal0.07 ± 0.0213881389β-Elemene0.06 ± 0.01
8107962-Hexanoltr14171419β-Ylangenetr
849846(2E)-Hexenal0.33 ± 0.0214181417β-Caryophyllene2.50 ± 0.02
850844(3E)-Hexenol0.27 ± 0.0414291430β-Copaenetr
922921Tricyclene0.12 ± 0.0014321432trans-α-Bergamotene0.13 ± 0.02
925924α-Thujene0.19 ± 0.0014541452α-Humulene1.07 ± 0.02
933932α-Pinene58.59 ± 0.21146914714,5-di-epi-Aristolochene0.05 ± 0.00
947945α-Fenchenetr14731478γ-Muurolene0.06 ± 0.01
949946Camphene2.44 ± 0.0214801484Germacrene D2.95 ± 0.01
971969Sabinene1.78 ± 0.0014821484(Z,Z)-α-Farnesene0.10 ± 0.01
977974β-Pinene14.69 ± 0.0714881489β-Selinene0.15 ± 0.01
988988Myrcene9.70 ± 0.0214911493trans-Muurola-4(14),5-dienetr
10041003p-Mentha-1(7),8-dienetr14941500Bicyclogermacrene0.08 ± 0.00
10241020p-Cymenetr14971500α-Muurolenetr
10281024Limonene1.76 ± 0.0115121513γ-Cadinenetr
10301025β-Phellandrene0.31 ± 0.0315171522δ-Cadinene0.10 ± 0.02
10341032(Z)-β-Ocimene0.05 ± 0.0115751574Germacra-1(10),5-dien-4β-ol0.27 ± 0.02
10441044(E)-β-Ocimene0.44 ± 0.0315811582Caryophyllene oxide0.47 ± 0.01
10571054γ-Terpinenetr16091608Humulene epoxide II0.13 ± 0.01
10851086Terpinolenetr20192026(E,E)-Geranyl linalool0.06 ± 0.01
10991099α-Pinene oxide0.10 ± 0.01222822377α-Hydroxymanool0.16 ± 0.02
11121113(E)-4,8-Dimethylnona-1,3,7-trienetr23002300Tricosanetr
11261122α-Campholenaltr25002500Pentacosane0.16 ± 0.01
11401135trans-Pinocarveoltr27002700Heptacosane0.16 ± 0.02
11451140trans-Verbenol0.11 ± 0.02 Green leaf volatiles0.66
11621160Pinocarvonetr Monoterpene hydrocarbons90.09
11801174Terpinen-4-oltr Oxygenated monoterpenoids0.38
11951195Myrtenal0.06 ± 0.01 Sesquiterpene hydrocarbons7.37
12061204Verbenone0.10 ± 0.02 Oxygenated sesquiterpenoids1.09
13681369Cyclosativene0.06 ± 0.00 Others0.32
13751374α-Copaene0.08 ± 0.01 Total Identified99.90
13831387β-Bourbonenetr
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c tr = “trace” (<0.05%).
Table
Table 8. Chemical composition of the essential oil of Smallanthus uvedalia (L.) Mack.
Table 8. Chemical composition of the essential oil of Smallanthus uvedalia (L.) Mack.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
7958012-Methylhept-2-ene0.10 ± 0.0012071204Verbenone0.09 ± 0.01
801801Hexanal0.86 ± 0.1613461345α-Cubebene0.15 ± 0.04
850846(2E)-Hexenal1.40 ± 0.0913821387β-Bourbonene0.15 ± 0.02
8658631-Hexanol0.22 ± 0.0114181417β-Caryophyllene3.80 ± 0.07
922921Tricyclene0.08 ± 0.0014541452α-Humulene0.36 ± 0.02
924924α-Thujene1.28 ± 0.0214731478γ-Muurolene0.56 ± 0.12
932932α-Pinene62.56 ± 0.7915121513γ-Cadinene0.29 ± 0.09
948946Camphene1.35 ± 0.0115171522δ-Cadinene0.63 ± 0.03
971969Sabinene0.16 ± 0.0315361537α-Cadinene0.22 ± 0.04
977974β-Pinene6.00 ± 0.0915761577Spathulenol0.58 ± 0.11
988988Myrcene2.43 ± 0.0715811582Caryophyllene oxide1.37 ± 0.02
10241020p-Cymene0.15 ± 0.01 Green leaf volatiles2.48
10281024Limonene11.43 ± 0.11 Monoterpene hydrocarbons88.28
10301025β-Phellandrene0.70 ± 0.10 Oxygenated monoterpenoids0.74
10441044(E)-β-Ocimene1.87 ± 0.09 Sesquiterpene hydrocarbons6.16
10571054γ-Terpinene0.26 ± 0.01 Oxygenated sesquiterpenoids1.95
11261122α-Campholenal0.29 ± 0.01 Others0.10
11401135trans-Pinocarveol0.23 ± 0.04 Total Identified99.71
11451140trans-Verbenol0.14 ± 0.05
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases.
Table
Table 9. Chemical composition of the essential oil of Solidago altissima L.
Table 9. Chemical composition of the essential oil of Solidago altissima L.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
802801Hexanal0.17 ± 0.0113821387β-Bourbonenetr
850846(2E)-Hexenal1.21 ± 0.0313861387β-Cubebene0.10 ± 0.01
921921Tricyclene0.06 ± 0.0013871389β-Elemene0.18 ± 0.00
924924α-Thujene1.30 ± 0.0014161419β-Ylangene0.14 ± 0.01
931932α-Pinene13.91 ± 0.0414181417β-Caryophyllene0.50 ± 0.03
948946Camphene2.41 ± 0.0114281430β-Copaene0.14 ± 0.01
971969Sabinene14.25 ± 0.0314541452α-Humulene0.17 ± 0.00
976974β-Pinene4.62 ± 0.0214731478γ-Muurolene0.59 ± 0.03
988988Myrcene20.29 ± 0.0414771483α-Amorphene0.12 ± 0.02
10051004(3Z)-Hexenyl acetatetr c14791484Germacrene D10.67 ± 0.03
10061002α-Phellandrene2.84 ± 0.0214871489β-Selinenetr
10161014α-Terpinene0.10 ± 0.0014901495γ-Amorphene0.59 ± 0.01
10241020p-Cymene2.26 ± 0.0014941500Bicyclogermacrene0.18 ± 0.00
10281024Limonene1.27 ± 0.0114961500α-Muurolene0.14 ± 0.01
10301025β-Phellandrene0.35 ± 0.0115111513γ-Cadinene0.30 ± 0.01
10441044(E)-β-Ocimene0.08 ± 0.0115131514Cubebol0.06 ± 0.02
10571054γ-Terpinene0.38 ± 0.0015161522δ-Cadinene0.68 ± 0.02
10691065cis-Sabinene hydrate0.24 ± 0.0015351537α-Cadinene0.09 ± 0.01
10841086Terpinolene0.15 ± 0.0115471548Elemol0.06 ± 0.01
109010906,7-Epoxymyrcene0.05 ± 0.0015751574Germacra-1(10),5-dien-4β-ol0.14 ± 0.01
10991099α-Pinene oxidetr15811582Caryophyllene oxide0.06 ± 0.01
11011098trans-Sabinene hydrate0.15 ± 0.0015911594Salvial-4(14)-en-1-one0.06 ± 0.01
11051100Nonanaltr16191611Germacra-1(10),5-dien-4α-ol0.12 ± 0.01
11121113(E)-4,8-Dimethylnona-1,3,7-triene0.11 ± 0.0316271629iso-Spathulenol0.20 ± 0.01
11241124cis-p-Menth-2-en-1-ol0.05 ± 0.0016411638τ-Cadinol0.09 ± 0.02
11801174Terpinen-4-ol0.73 ± 0.0116431640τ-Murrolol0.14 ± 0.01
11951186α-Terpineol0.06 ± 0.0116451644α-Muurolol (=δ-Cadinol)0.10 ± 0.01
12031202cis-Sabinol0.50 ± 0.0116541652α-Cadinol0.41 ± 0.03
12191219cis-Sabinene hydrate acetate0.15 ± 0.01 Green leaf volatiles1.38
12831287Bornyl acetate14.44 ± 0.02 Monoterpene hydrocarbons64.26
13331335δ-Elemene0.05 ± 0.00 Oxygenated monoterpenoids16.37
13451345α-Cubebene0.12 ± 0.00 Sesquiterpene hydrocarbons14.90
13671373α-Ylangenetr Oxygenated sesquiterpenoids1.44
13681373Linalyl isobutyratetr Others0.11
13741374α-Copaene0.05 ± 0.00 Total Identified98.45
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases. c tr = “trace” (<0.05%).
Table
Table 10. Comparison of the major components in Solidago altissima (syn. S. canadensis) essential oils.
Table 10. Comparison of the major components in Solidago altissima (syn. S. canadensis) essential oils.
ComponentSource of S. altissima (S. canadensis)
Commercial (Young Living)
[85]		Bimtal, India
[86]		Bimtal, India
[87]		Slovakia
[88]		Moscow, Russia
[89]		Slovakia
[90]		Hungary
[91]		Giza, Egypt
[92]		Poland
[82]		Alabama (This Work)
α-Pinene13.35.00.41.8–36.328.111.64.629.214.713.9
Sabinene8.02.40.3---0.53.90.1---0.214.2
β-Pinene---1.20.20.5–6.52.83.11.24.81.54.6
Myrcene6.32.8------7.3---tr13.74.220.2
Limonene11.012.54.24.3-9.07.012.51.09.69.31.3
Bornyl acetate4.32.13.4---7.36.313.46.21.314.4
Germacrene D34.456.764.10.0–11.139.234.911.010.319.810.6
Table
Table 11. Chemical composition of the essential oil of Xanthium strumarium L.
Table 11. Chemical composition of the essential oil of Xanthium strumarium L.
RI aRI bCompound% ± SDRI aRI bCompound% ± SD
7937881-Octene0.09 ± 0.0114171417β-Caryophyllene0.93 ± 0.04
801797(3Z)-Hexenal0.11 ± 0.0114281430β-Copaene0.06 ± 0.01
802801Hexanal0.75 ± 0.0714541452α-Humulene0.49 ± 0.03
859846(2E)-Hexenal5.79 ± 0.0314791484Germacrene D13.92 ± 0.05
8658631-Hexanol0.12 ± 0.0114871489β-Selinene0.11 ± 0.01
921921Tricyclene0.05 ± 0.0114931500Bicyclogermacrene0.29 ± 0.01
924924α-Thujene0.08 ± 0.0314961500α-Muurolene0.13 ± 0.01
931932α-Pinene0.80 ± 0.0115111513γ-Cadinene0.19 ± 0.01
948946Camphene0.95 ± 0.0215161522δ-Cadinene0.27 ± 0.03
971969Sabinene4.89 ± 0.0215751547Germacra-1(10),5-dien-4β-ol0.21 ± 0.01
976974β-Pinene0.30 ± 0.0115811582Caryophyllene oxide0.23 ± 0.01
9789741-Octen-3-ol0.20 ± 0.0216411638τ-Cadinol0.31 ± 0.02
987988Myrcene14.31 ± 0.0416431640τ-Muurolol0.23 ± 0.02
10041003p-Mentha-1(7),8-diene0.05 ± 0.0116541652α-Cadinol0.59 ± 0.05
10161014α-Terpinene0.06 ± 0.0116631668ar-Turmerone0.10 ± 0.01
10281024Limonene48.23 ± 0.2216931688Shyobunol0.27 ± 0.03
10301025β-Phellandrene0.90 ± 0.0319321931Beyerene0.64 ± 0.02
10441044(E)-β-Ocimene0.10 ± 0.0221052106(E)-Phytol0.25 ± 0.03
10571054γ-Terpinene0.16 ± 0.01 Green leaf volatiles6.77
10691067cis-Linalool oxide (furanoid)0.06 ± 0.01 Monoterpene hydrocarbons70.87
10991095Linalool1.16 ± 0.01 Oxygenated monoterpenoids2.22
11801174Terpinen-4-ol0.39 ± 0.01 Sesquiterpene hydrocarbons16.58
12191217β-Cyclocitral0.11 ± 0.02 Oxygenated sesquiterpenoids1.95
12831287Bornyl acetate0.56 ± 0.01 Diterpenoids0.89
13511356Eugenol0.28 ± 0.03 Benzenoids0.28
13861387β-Cubebene0.10 ± 0.02 Others0.29
14161419β-Ylangene0.08 ± 0.03 Total Identified99.85
a RI = Retention index determined in reference to a homologous series of n-alkanes on a ZB-5ms column. b RI values from the databases.
Table
Table 12. Major components and antifungal activities of Asteraceae essential oils.
Table 12. Major components and antifungal activities of Asteraceae essential oils.
Plant SpeciesMajor Components (>5%) in the Essential OilAntifungal Activity, MIC, μg/mL a
Aspergillus nigerCandida albicansCryptococcus neoformans
Eupatorium serotinum Michx.germacrene D (6.6%), palustrol (5.4%), cyclocolorenone (23.5%)31362578
Eurybia macrophylla (L.) Cass.β-pinene (8.5%), limonene (28.6%), terpinolene (5.3%), germacrene D (19.7%), germacrene B (7.0%)625625156
Eutrochium purpureum (L.) E.E. Lamonthexanal (6.8%), (2E)-hexenal (59.7%), methyl salicylate (10.4%), eugenol (11.8%)625625625
Polymnia canadensis L.α-pinene (19.6%), α-phellandrene (28.2%), germacrene D (11.4%)625625156
Rudbeckia laciniata L.α-pinene (10.2%), β-pinene (9.2%), myrcene (5.3%), limonene (58.9%)6251250156
Silphium integrifolium Michx.α-pinene (58.5%), β-pinene (14.7%), myrcene (9.7%)n.t. bn.t.n.t.
Smallanthus uvedalia (L.) Mack.α-pinene (62.3%), β-pinene (6.0%), limonene (11.3%)n.t.n.t.n.t.
Solidago altissima L.α-pinene (13.9%), sabinene (14.2%), myrcene (20.2%), bornyl acetate (14.4%), germacrene D (10.6%)6251250313
Xanthium strumarium L.(2E)-hexenal (5.8%), myrcene (14.3%), limonene (48.0%), germacrene D (13.9%)6251250n.t.
a Each minimum inhibitory concentration (MIC) determination was carried out in triplicate. b n.t. = not tested due to limited availability of the essential oil.
Table
Table 13. Antifungal activities (MIC, μg/mL) of essential oil components.
Table 13. Antifungal activities (MIC, μg/mL) of essential oil components.
CompoundAspergillus nigerCandida albicansCryptococcus neoformans
α-Pinene1250625313
β-Pinene6251250625
Limonene6251250625
Myrcene625625625
Methyl salicylate625625625
Eugenol78313156
Bornyl acetate625625625
Table
Table 14. Plant collection sites and essential oil yields of Asteraceae from north Alabama.
Table 14. Plant collection sites and essential oil yields of Asteraceae from north Alabama.
PlantCollection Site, DateVoucher NumberMass of Aerial Parts (g)Yield of Essential Oil (mg)
Eupatorium serotinum Michx.34°38′29″ N, 86°24′39″ W,
elev. 199 m
13 September 2018		23375449.096.4 (0.013%)
Eurybia macrophylla (L.) Cass.34°39′25″ N, 86°24′45″ W,
elev. 241 m
15 September 2018		23311756.5610.6 (0.019%)
Eutrochium purpureum (L.) E.E. Lamont34°38′40″ N, 86°27′22″ W,
elev. 180 m
12 August 2018		09184363.4412.3 (0.019%)
Polymnia canadensis L.34°38′29″ N, 86°24′39″ W,
elev. 199 m
21 July 2018		18470052.8939.1 (0.074%)
Rudbeckia laciniata L.34°42′42″ N, 86°32′38″ W,
elev. 345 m
13 September 2018		00442654.536.0 (0.011%)
Silphium integrifolium Michx.34°42′42″ N, 86°32′38″ W,
elev. 345 m
15 September 2018		00415215.026.4 (0.043%)
Smallanthus uvedalia (L.) Mack.34°42′42″ N, 86°32′38″ W,
elev. 345 m
15 September 2018		00071456.215.9 (0.010%)
Solidago altissima L.34°38′40″ N, 86°27′22″ W,
elev. 180 m
12 August 2018		00142554.4144.9 (0.083%)
Xanthium strumarium L.34°38′49″ N, 86°24′38″ W,
elev. 200 m
15 September 2018		22472469.697.0 (0.010%)

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Lawson, S.K.; Sharp, L.G.; Powers, C.N.; McFeeters, R.L.; Satyal, P.; Setzer, W.N. Volatile Compositions and Antifungal Activities of Native American Medicinal Plants: Focus on the Asteraceae. Plants 2020, 9, 126. https://doi.org/10.3390/plants9010126

AMA Style

Lawson SK, Sharp LG, Powers CN, McFeeters RL, Satyal P, Setzer WN. Volatile Compositions and Antifungal Activities of Native American Medicinal Plants: Focus on the Asteraceae. Plants. 2020; 9(1):126. https://doi.org/10.3390/plants9010126

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Lawson, Sims K., Layla G. Sharp, Chelsea N. Powers, Robert L. McFeeters, Prabodh Satyal, and William N. Setzer. 2020. "Volatile Compositions and Antifungal Activities of Native American Medicinal Plants: Focus on the Asteraceae" Plants 9, no. 1: 126. https://doi.org/10.3390/plants9010126

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