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Appl. Sci. 2019, 9(15), 3179; https://doi.org/10.3390/app9153179

Article
Essential Oil Compositions and Antifungal Activity of Sunflower (Helianthus) Species Growing in North Alabama
1
Department of Biological Sciences, University of Alabama in Huntsville, Huntsville, AL 35899, USA
2
Department of Chemistry, University of Alabama in Huntsville, Huntsville, AL 35899, USA
3
Aromatic Plant Research Center, 230 N 1200 E, Suite 100, Lehi, UT 84043, USA
*
Author to whom correspondence should be addressed.
Received: 1 May 2019 / Accepted: 2 August 2019 / Published: 5 August 2019

Abstract

:
Helianthus species are North American members of the Asteraceae, several of which have been used as traditional medicines by Native Americans. The aerial parts of two cultivars of Helianthus annuus, “Chianti” and “Mammoth”, and wild-growing H. strumosus, were collected from locations in north Alabama. The essential oils were obtained by hydrodistillation and analyzed by gas chromatography—mass spectrometry. The Helianthus essential oils were dominated by monoterpene hydrocarbons, in particular α-pinene (50.65%, 48.91%, and 58.65%, respectively), sabinene (6.81%, 17.01%, and 1.91%, respectively), β-pinene (5.79%, 3.27%, and 4.52%, respectively), and limonene (7.2%, 7.1%, and 3.8%, respectively). The essential oils were screened against three opportunistic pathogenic fungal species, Aspergillus niger, Candida albicans, and Cryptococcus neoformans. The most sensitive fungus was C. neoformans with minimum inhibitory concentration (MIC) values of 78, 156, and 78 μg/mL, respectively.
Keywords:
Helianthus annuus; Helianthus strumosus; Aspergillus niger; Candida albicans; Cryptococcus neoformans; α-pinene

1. Introduction

Helianthus L., the sunflowers, is a genus in the family Asteraceae, tribe Heliantheae, made up of 51 North American species [1]. Helianthus annuus L. (common sunflower) is native to North America and the current range of wild forms of H. annuus are central and western United States, southern Canada, and northern Mexico [2]. The common sunflower is one of the earliest domesticated plants in the Americas. There is evidence that the plant was domesticated in Tabasco, Mexico, around 2600 B.C. [3], and independently in the southeastern United States around 2800 B.C. [2,4]. Several Native American tribes used H. annuus in traditional medicine [5]. For example, the White Mountain Apache used a poultice of the crushed plants to treat snakebites; the Hopi used the plant as a spider bite medicine; the Jemez applied the juice of the plant to cuts; the Pima used a decoction of the leaves to treat fevers [5]; and the Zuni natives of New Mexico used the roots to treat rattlesnake bites [6]. In addition, H. annuus is used as a traditional herbal medicine in many locations where it has been introduced. Ethiopians use H. annuus in teas to treat food poisoning [7]. In Bangladesh the seeds and/or the flowers are crushed and used for snake bites, scorpion bites, and a variety of other ailments, such as burning sensation in the vagina and worms in the ears [8].
Helianthus strumosus L. (woodland sunflower) is a rhizomatous perennial plant, growing up to two meters tall and is native to eastern North America [9,10,11]. These plants are strongly aromatic. Leaves are up to 10 cm long and cuneate to subcordate in shape. The composite flower heads can be up to 9 cm at the peduncle. The ray flowers are a dark yellow color with orange-brown disc flowers in the center. These flowers are common along roadsides and in open fields and are sometimes found in forests. The Iroquois used a decoction of the roots as an anthelmintic [5].
Invasive fungal infections are becoming increasingly common in immunocompromised patients, such as those receiving cancer chemotherapy, transplant patients receiving immunosuppressant drugs, and HIV patients [12]. The predominant fungal pathogens are Aspergillus spp. [13,14] and Candida spp. [15,16] among others [12]. Aspergillus niger is a haploid filamentous parasitic fungus that is commonly known for the disease “black mold” on fruits, vegetables, and nuts [17]. Aspergillus conidia (fungal “spores”) are environmentally widespread and inhalation can lead to opportunistic pulmonary aspergillosis, chiefly attributed to A. fumigatus, A. flavus, and A. tubingensis, as well as A. niger [18]. In immunocompromised individuals, however, the infection can progress to invasive systemic aspergillosis [19]. Candida albicans is another opportunistic pathogenic fungus that commonly colonizes the human body [20]. The organism can cause superficial infections of the mucosa, but can lead to invasive candidiasis in immunocompromised patients [21]. Cryptococcosis is a fungal infection caused by Cryptococcus neoformans [22]. The fungus is widespread in the environment and typically enters the body through inhalation where it can cause pulmonary infection [23]. However, the organism has the ability to cross the blood brain barrier and in immunocompromised patients, cryptococcosis can lead to cryptococcal meningoencephalitis with increased intracranial pressure [24,25]. As part of our continuing investigation of antifungal activity of essential oils [26] as well as essential oils from the Asteraceae growing in north Alabama [27], we have collected and analyzed the essential oils from the aerial parts of H. annuus and H. strumosus, and we have carried out in vitro antifungal screening of the essential oils against A. niger, C. albicans, and C. neoformans.

2. Materials and Methods

2.1. Plant Materials

The two cultivars of H. annuus (“Chianti” and “Mammoth”) were cultivated, grown without fertilizer or pesticides, in a rural area near Gurley in north Alabama (34°38′29″N, 86°24′39″W, elevation 199 m) and the aerial parts were collected on 4 and 6 August 2018. Aerial parts of H. strumosus were collected on 10 August 2018 from wild-growing plants near Huntsville, Alabama (34°42′42″N, 86°32′35″W, elevation 354 m). The plants were identified by S.K. Lawson. Voucher specimens have been deposited in the herbarium of the University of Alabama in Huntsville (20180729-183243 and 20190402-111732). The fresh plant materials (78.14, 80.32, and 65.47 g, respectively) were hydrodistilled using a Likens–Nickerson apparatus with continuous extraction with dichloromethane for 3 h. The dichloromethane was carefully evaporated, and the residual essential oils weighed using an analytical balance to give the essential oils (82.3, 20.3, and 24.0 mg, respectively).

2.2. Gas Chromatographic—Mass Spectral Analysis

The Helianthus essential oils were analyzed by GC-MS with a Shimadzu GCMS-QP2010 Ultra with a ZB-5 capillary column as previously described [28]. Identification of the chemical components was carried out by comparison of the retention indices, calculated with respect to a homologous series of normal alkanes using the arithmetic index [29], and by comparison of their mass spectra with those reported in the Adams [30], NIST17 [31], FFNSC 3 [32], and our own in-house library [33]. Concentrations shown in Table 1 (average of three measurements ± standard deviations) are based on peak integration without standardization.

2.3. Antifungal Screening Assays

The Helianthus essential oils were screened for antifungal activity against Aspergillus niger (ATCC 16888), Candida albicans (ATCC 18804), and Cryptococcus neoformans (ATCC 24607) using the broth dilution technique as previously described [26,34]. Antifungal screening was carried out in triplicate.

3. Results and Discussion

3.1. Essential Oil Compositions

Hydrodistillation of Helianthus aerial parts gave pale yellow essential oils in 0.105%, 0.025%, and 0.037% yield (w/w) for H. annuus “Chianti”, H. annuus “Mammoth”, and H. strumosus, respectively. The essential oil compositions for the three essential oils are compiled in Table 1. A perusal of the table reveals that the three Helianthus essential oils are qualitatively similar. The major components for H. annuus “Chianti” were α-pinene (50.65%), camphene (7.26%), limonene (7.20%), bornyl acetate (7.13%), sabinene (6.81%), and β-pinene (5.79%). The essential oil of H. annuus “Mammoth” was also dominated by α-pinene (48.91%), followed by sabinene (17.01%), limonene (7.11%), and germacrene D (6.84%). H. strumosus essential oil was also rich in α-pinene (58.65%), as well as myrcene (9.79%) and bornyl acetate (4.97%).
The compositions of H. annuus essential oils cultivated in north Alabama are very similar to those reported by Adams and co-workers for populations growing in the southern plains of the United States [35]. The essential oils of H. annuus from Pisa, Tuscany, Italy [36]; Lagos, Nigeria [37]; or from western United States [35] had much lower concentrations of α-pinene and correspondingly higher concentrations of germacrene D. In marked contrast to the essential oils of Helianthus, essential oils of Rudbeckia fulgida Aiton and Rudbeckia hirta L. (Asteraceae, Heliantheae) from north Alabama were devoid of α-pinene, but rich in sesquiterpene hydrocarbons [27].

3.2. Antifungal Activity

The Helianthus essential oils were screened for antifungal activity against three potentially pathogenic fungi, Aspergillus niger, Candida albicans, and Cryptococcus neoformans, as shown in Table 2. The most susceptible fungus was C. neoformans. Both H. annuus “Chianti” and H. strumosus essential oils showed minimum inhibitory concentration (MIC) values of 78 μg/mL. It is tempting to suggest that the major component, α-pinene, is responsible for the observed anti-Cryptococcus activity; all three Helianthus essential oils have around 50% α-pinene. Furthermore, α-pinene has shown antifungal activity against C. neoformans with an MIC around 70 μg/mL [38,39]. In addition, α-pinene-rich (46.1% α-pinene) commercial Myrtis communis essential oil showed a similar antifungal activity against C. neoformans (MIC = 78 μg/mL) [26]. Conversely, commercial Cupressus sempervirens essential oil, with 49.7% α-pinene was less active against C. neoformans (MIC = 313 μg/mL) [26]. There may be synergistic or antagonistic effects of α-pinene with minor components. Limonene [39,40] and β-pinene [39], have also shown antifungal activity against C. neoformans; camphene, however, was inactive [41]. Although we do not know which of the enantiomers is present in the Helianthus essential oils, we have screened both (+)- and (−)-α-pinene, (+)- and (−)-limonene, and (−)-β-pinene against the three fungal strains, as shown in Table 2. Consistent with previous investigations, (−)-β-pinene and (+)-limonene both showed activity against C. neoformans with MIC values of 39 and 78 μg/mL. Furthermore, both enantiomers of α-pinene were active against C. neoformans; MIC = 20 and 39 μg/mL for (+)- and (−)-α-pinene, respectively.

4. Conclusions

Helianthus essential oils have been shown to be rich in α- and β-pinenes, sabinene, and limonene, and have demonstrated poor antifungal activities against A. niger and C. albicans, but promising activity against C. neoformans (although much lower activity than the reference antifungal drug amphotericin B). These and other monoterpene-rich essential oils deserve further exploration as alternative and complementary agents to combat fungal infections; further studies against more susceptible fungi are recommended.

Author Contributions

Conceptualization, S.K.L. and W.N.S.; methodology, S.K.L., L.G.S. and C.N.P.; software, P.S.; validation, W.N.S.; formal analysis, W.N.S.; investigation, S.K.L., L.G.S. and C.N.P.; resources, R.L.M.; data curation, W.N.S.; writing—original draft preparation, S.K.L., L.G.S. and W.N.S.; writing—review and editing, all authors; project administration, W.N.S.

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 1. Chemical compositions of Helianthus annuus “Chianti”, H. annuus “Mammoth”, and H. strumosus aerial parts essential oils.
Table 1. Chemical compositions of Helianthus annuus “Chianti”, H. annuus “Mammoth”, and H. strumosus aerial parts essential oils.
RI aRI bCompoundPercent Composition c
H. annuus “Chianti”H. annuus “Mammoth”H. strumosus
800797(3Z)-Hexenal0.06 ± 0.01Tr dtr
801801Hexanal0.35 ± 0.020.24 ± 0.040.41 ± 0.03
8107962-Hexanol------0.07 ± 0.00
849846(2E)-Hexenal1.13 ± 0.050.83 ± 0.051.96 ± 0.03
861854(2E)-Hexenol------tr
8648631-Hexanol------0.09 ± 0.00
921921Tricyclene0.37 ± 0.000.21 ± 0.010.18 ± 0.00
924924α-Thujene0.17 ± 0.000.23 ± 0.010.1
932932α-Pinene50.65 ± 0.3248.91 ± 0.6458.65 ± 0.14
946945α-Fenchene------tr
948946Camphene7.26 ± 0.033.72 ± 0.033.38 ± 0.02
952953Thuja-2,4(10)-diene0.05 ± 0.01---tr
971969Sabinene6.81 ± 0.0417.01 ± 0.181.91 ± 0.00
977974β-Pinene5.79 ± 0.043.27 ± 0.014.52 ± 0.02
988988Myrcene0.42 ± 0.010.30 ± 0.039.79 ± 0.03
10041003p-Mentha-1(7),8-diene------tr
10061002α-Phellandrene---0.08 ± 0.010.05 ± 0.01
10081008δ-3-Carene------tr
10161014α-Terpinene---tr---
10241020p-Cymene0.06 ± 0.030.09 ± 0.010.07 ± 0.00
10281024Limonene7.20 ± 0.037.11 ± 0.113.79 ± 0.01
10301025β-Phellandrene0.24 ± 0.000.21 ± 0.140.29 ± 0.01
103110261,8-Cineole0.06 ± 0.000.07 ± 0.02tr
10341032(Z)-β-Ocimene------tr
10441044(E)-β-Ocimene---tr0.41 ± 0.01
10571054γ-Terpinene0.10 ± 0.000.25 ± 0.01tr
10691065cis-Sabinene hydrate------tr
10841086Terpinolene0.10 ± 0.010.16 ± 0.01tr
10991099α-Pinene oxide0.10 ± 0.01---tr
11051100Nonanal------tr
11091108p-Mentha-2,8-dien-1-ol0.36 ± 0.000.10 ± 0.02tr
11121114(3E)-4,8-Dimethyl-1,3,7-nonatriene0.09 ± 0.010.13 ± 0.020.18 ± 0.00
11211124Chrysanthenone0.05 ± 0.00------
11271122α-Campholenal0.33 ± 0.010.05 ± 0.010.06 ± 0.01
11401135trans-Pinocarveol0.37 ± 0.05tr0.06 ± 0.02
11411137cis-Verbenol0.10 ± 0.01---tr
11451140trans-Verbenol1.50 ± 0.020.24 ± 0.020.26 ± 0.00
11631160Pinocarvone0.11 ± 0.01trtr
11711165Borneol0.73 ± 0.010.07 ± 0.020.12 ± 0.00
11801174Terpinen-4-ol0.09 ± 0.010.19 ± 0.01tr
11871179p-Cymen-8-ol0.05 ± 0.01------
11951186α-Terpineol---tr---
11951195Myrtenal0.29 ± 0.02tr0.10 ± 0.01
12061201Decanaltr------
12071204Verbenone0.28 ± 0.040.11 ± 0.010.07 ± 0.00
12191215trans-Carveol0.16 ± 0.00---tr
12831287Bornyl acetate7.13 ± 0.043.02 ± 0.044.97 ± 0.01
12941298trans-Pinocarvyl acetate0.08 ± 0.01trtr
13821387β-Bourbonene0.21 ± 0.020.18 ± 0.01tr
13861387β-Cubebenetrtrtr
13871389β-Elemene0.05 ± 0.010.17 ± 0.01tr
13921392(Z)-Jasmone------tr
14161419β-Ylangene0.07 ± 0.010.15 ± 0.01tr
14171417β-Caryophyllene 0.33 ± 0.030.54 ± 0.090.84 ± 0.00
14271434γ-Elemene------tr
14281431β-Gurjunene (=Calarene)0.62 ± 0.010.86 ± 0.01tr
14301432trans-α-Bergamotene0.06 ± 0.000.14 ± 0.03tr
144214426,9-Guaiadienetrtr---
14461453Geranyl acetonetrtr---
14541452α-Humulene0.19 ± 0.020.29 ± 0.010.20 ± 0.00
14791484Germacrene D3.32 ± 0.036.84 ± 0.093.68 ± 0.02
14871489β-Selinene0.12 ± 0.01trtr
14931493epi-Cubebol0.12 ± 0.04------
14941500Bicyclogermacrene---0.16 ± 0.010.07 ± 0.01
15131514Cubebol0.14 ± 0.02trtr
15161522δ-Cadinene tr0.07 ± 0.00tr
15471548Elemol---tr0.07 ± 0.01
15591561(E)-Nerolidol0.10 ± 0.020.09 ± 0.030.64 ± 0.03
15751574Germacrene D-4β-ol0.37 ± 0.020.46 ± 0.000.46 ± 0.00
15811582Caryophyllene oxide0.16 ± 0.09tr0.37 ± 0.01
16081608Humulene epoxide II------0.05 ± 0.01
16361639Caryophylla-4(12),8(13)-dien-5β-ol------tr
16381643Hedycaryol------0.10 ± 0.01
16411638τ-Cadinol0.18±0.01tr0.14 ± 0.01
16541649β-Eudesmol0.10 ± 0.02---0.16 ± 0.03
16551652α-Cadinol---trtr
16631665Intermedioltr0.56 ± 0.01---
16831685Germacra-4(15),5,10(14)-trien-1α-ol0.13 ± 0.04---0.51 ± 0.01
16861687Eudesma-4(15),7-dien-1β-ol------0.14 ± 0.00
16891690(Z)-trans-α-Bergamotol------0.12 ± 0.01
169916956-epi-Shyobunol------0.05 ± 0.01
Monoterpene hydrocarbons79.2181.5683.13
Oxygenated monoterpenoids11.803.855.64
Sesquiterpene hydrocarbons e4.979.404.79
Oxygenated sesquiterpenoids e1.391.112.79
Green leaf volatiles1.541.072.53
Others0.0910.130.18
Total Identified99.0197.1299.05
a RI = Retention index determined with reference to a homologous series of n-alkanes on a ZB-5 column. b RI values from the databases (NIST17 [31], FFNSC 3 [32], Adams [30], or Satyal [33]). c Average of three measurements ± standard deviations. d tr = “trace” (<0.05%). e Sesquiterpenoids are considered tentatively identified based on MS and RI.
Table 2. Antifungal activities (minimum inhibitory concentration (MIC), μg/mL) of Helianthus essential oils and major components a.
Table 2. Antifungal activities (minimum inhibitory concentration (MIC), μg/mL) of Helianthus essential oils and major components a.
MaterialFungal Species
Aspergillus nigerCandida albicansCryptococcus neoformans
H. annuus “Chianti”62562578
H. annuus “Mammoth”625625156
H. strumosus625125078
(+)-α-Pinene62531320
(−)-α-Pinene15662539
(−)-β-Pinene15662539
(+)-Limonene125062578
(−)-Limonene25001250313
Amphotericin B0.780.781.56
a Each MIC determination was carried out in triplicate.

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