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. 2020 Jul 14;58(4):1313–1318. doi: 10.1007/s13197-020-04640-x

Chemical composition of essential oil and antifungal activity of Artemisia persica Boiss. from Iran

Reza Dehghani Bidgoli 1,✉
PMCID: PMC7925796  PMID: 33746259

Abstract

Artemisia is the largest and most diverse genus from the Asteraceae family that named locally "Dermaneh" in Iran. This study was conducted to determine, the chemical compounds of Artemisia persica Boiss essential oil and its antifungal effect, toward six toxigenic fungal strains in vitro. The yield of essential oil from the aerial parts of this plant species, using hydrodistillation method obtained 0.18% (v/w). The results of GC/MS analysis identified 31 components in the essential oil that laciniata furanone E (17.1%), artedouglasia oxide C (13.2%), Trans-pinocarveol (10.2%), pinocarvone (8.5%), and α-pinene (5.8%) were the major compounds. The results of the antifungal activity showed that the most sensitive fungal strains to A. persica Boiss. essential oil were Aspergillus ochraceus and Aspergillus parasiticus with lower minimal fungicidal concentration (MFC) of 1.25 μl/ml (v/v). Also the strong fungicidal effect was observed against Aspergillus flavus and Aspergillus nidulans at a MFC value of 2.5 μl/ml, while the fungicidal activity against Aspergillus fumigatus and Aspergillus niger observed in the 10 μl/ml oil concentration. According to the results A. persica Boiss essential oil has a acceptable antifungal activity against Aspergillus strains and can be used to prevent food crops from fungal contaminations.

Keywords: Artemisia, Aspergillus, α-Pinene, GC/MS, Natural products

Introduction

Artemisia is the largest and most diverse genus from the Asteraceae family and has been scattered in the wide rangeland with moderate climates of earth. (Southern Europe, North Africa, North America, and Iran). Thirty four species of this genus with the shape of shrubs growing in different parts of Iran that named locally "Dermaneh" (Ghahraman 1977; Mozafarian 1988). There are different species of this genus product the biological active compounds such as terpenes and phenolic compounds that their toxicity and allelopathic properties had been confirmed, that from these compounds can be mention to artemisinin, camphor, bornyl acetate and cineol (Mesdaghi 1993). These species, in addition to the allelopathic feature have anti-malarial, antifungal, antimicrobial, anticancer and antioxidant properties (Ulubelen et al. 2001; Mirjalili et al. 2006).

Until the discovery of antibiotics, Artemisia was a frequent component of herbal tea mixtures, recommended to patients with tuberculosis to prevent sudation and was found to be an active ingredient in combined plant preparations for the treatment of chronic bronchitis. Also, it has been used as medication against perspiration, fever, rheumatism, and in treating mental and nervous conditions as well as an insecticidal (Babakhanlo et al. 1998; Rasooli et al. 2003)

One of the threats to human and animal health is the mycotoxin-producing fungi, especially within Aspergillus species that which are one of the largest and most diverse fungal groups and are notable destroyers and contaminants of natural products, and lead to significant agricultural and economic losses.

The Aspergillus family is an opportunistic fungus causing invasive and allergic syndromes. For example, Aspergillosis is a fungal disease caused by different species of the genus Aspergillus. These fungi in the Ascomycota branch and family of Trichocomaceae and Aspergillus species (Khongkhunthian and Reichart 2001). Aspergillus genus consists of about 180 species, and now, 30 species of fungi infectious diseases have been isolated. The most commonly fungi infectious that isolated and reported including Aspergillus fumigatus, Aspergillus flavus, Aspergillus nidulans and Aspergillus niger (Hinrikson et al. 2005). Due to the medical and biological importance Aspergillosis, and the different drug allergy patterns in different species, the exact identification of these species can be important for the purpose of Aspergillosis treatments (Kanafani and Perfect 2008).

Essential oils, in addition to its medicine value, are important for food industry which, in addition to improving the taste of food, leads to high shelf life and preventing their corruption (Rechinger 1998; Bora and Sharma 2013). Some of studies indicated that the essential oil of Artemisia species has antimicrobial activities such as anti-bactericidal and antifungal (Essawi and Srour 2000; Gulluce et al. 2004).

The antibiotics are considered the almost universal solution to serious infections, but drug efficacy is decreasing. Bacteria, viruses, and fungus have become gradually adapted to resist medications and their increasing prescription (Moore et al. 2000). The Medical Associated Plants are plants that have grown or have been picked in their natural environment for their medicinal properties and they have many functions, such as in the field of therapeutics, food, cosmetics, industries, etc. Herbs can play an important role in conserving biodiversity.

These plants are actually very familiar to rural people who are very sensitive to their scarcity and their disappearance. Indeed, medicinal plants play an important role in the health care of the population and represent a significant source of income for many families in the countryside and cities (Menaker et al. 2004).

Our research aims to study the biological activity of extracts of Artemisa persica Boiss chosen for therapeutic characteristics in traditional medicine, therefore, the present study was carried out to determine the chemical composition of Artemisia persica Boiss. essential oil from Iran and to evaluate its antifungal effect in vitro toward six toxigenic fungal strains belonging to Aspergillus species.

Materials and methods

Plant material

The aerial parts of Artemisia persica Boiss. were collected from the natural habitat of Ghazaan in Kashan province of Iran during the flowering stage from June to July, 2017. After transferring samples to the laboratory, the samples were dried at room temperature (25 °C) and away from the sunlight, in the shade. Also the plant was confirmed by the botanists of the Research Institute of Forests and Rangelands (RIFR), Tehran, Iran.

Analysis of essential oil using GC/MS

The dried samples were exposed to hydrodistillation in a Clevenger-type device for approximately four hours (Schott Duran, Mainz, Germany), based on the British Pharmacopoeia method (British Pharmacopoeia 1990). The GC/MS system was an Agilent HP-6890 gas chromatograph and a capillary column of HP-5MS, 5% phenylmethylsiloxane (30 m × 0.25 mm, 0.25 µm film thickness) equipped with a FID detector. The temperature of oven was initially set at 80 °C for 5 min, and then increased at a rate of 3 ºC/min to 250 ºC. The temperature of injector and detector was set at 220 °C and 290 °C, respectively. Helium was used as carrier gas at a flow rate of 1 ml/min. The diluted samples (1/1000 in n-pentane, v/v) of 1.0 µl were injected in the splitless mode manually. To obtain the quantitative data, peaks area percents were used.

GC/MS analysis of the essential oil was carried out using an Agilent HP-6890 gas chromatograph (Agilent Technologies, Palo Alto, CA, USA) with a HP-5MS 5% phenylmethylsiloxane capillary column (30 m × 0.25 mm, 0.25 µm film thickness; Restek, Bellefonte, PA) equipped with an Agilent HP-5973 mass selective detector in the electron impact mode (ionization energy: 70 eV), operating under the same conditions as explained above. For all components, the retention indices were calculated using a homologous series of n-alkanes injected in conditions equal to samples ones.

To identify the oil components, the mass spectra were compared with those from NIST and Wiley libraries or reported in the literature (Adams 2007). The peak area of the chromatogram was used to calculate the relative percentage of the oil constituents using the software provided by the manufacturer. The peak areas for different compounds were all assumed proportional to their molecular concentration.

Antifungal activity

For the evaluation of the antifungal activity, the method of direct contact was adopted, in this regard, the antifungal susceptibility of Artemisia persica Boiss. essential oil, with six toxigenic Aspergillus fungi species, a broth macrodilution method M38-A (CLSI Clinical and Laboratory Standards Institute 2002) was applied. Similar to the study performed by (Houicher et al. 2018), two type Aspergillus strains were from the Agricultural Research Service (ARS) culture collection (United States Department of Agriculture, Washington, DC, USA) (Aspergillus flavus NRRL 3251, and Aspergillus ochraceus NRRL 3174). One type strain was from the Central Bureau of Fungal Cultures (CBS) culture collections of micro-organisms (Utrecht, The Netherlands) (Aspergillus parasiticus CBS 100926), and three type strains including (Aspergillus nidulans TN02A7, Aspergillus fumigatus AfS34 and Aspergillus niger KB1001) were from (FGSC Aspergillus collection), produced by the Filamentous Fungus Program Project Grant GM068087 (Han et al. 2010).

RPMI-1640 medium (Sigma Aldrich R8758, USA) adjusted to pH 7.0 with MOPS (morpholinopropane-1-sulfonic acid, Sigma No. 220299) buffer was used in all experiments. Then, according to (Roswell Park Memorial Institute medium, Sigma R6504, St. Louis, MO, USA), DMSO was used to prepare the serial doubling dilutions from 0.04 to 20 μl/ml (dimethyl sulfoxide, Merck 200-664-3). The final concentration of the DMSO was calculated to be ≤ 1%. Inoculum was prepared from 7 to 14 day cultures, adjusted to the density of a 0.5 McFarland standard at 530 nm wavelength using a spectrophotometer (HACH, DR 6000 UV/VIS, Essex, USA) f or each fungal strain. Then, it was diluted 1:100 to obtain a working suspension within the range of 0.4–5×104 CFU (colony-forming units)/ml. The test tubes were inoculated in three replicates, including two control tubes (sterile and growth) in each strain. The minimal inhibitory concentrations (MIC) were determined visually after incubation at 35 °C for 48 h/72 h. Approximately, 20 μl aliquots were transferred onto Sabouraud dextrose agar (Eur-Pharm, 1024.00 Madrid, Spain) plates from each negative tube, and after 72 h incubation at 35 °C, the minimal fungicidal concentrations (MFC) were evaluated (Houicher et al. 2018).

Data analysis

The tests were performed in randomized design with three repetitions and SPSS version 18 was used for statistical analysis of data.

Results and discussion

The analysis of essential oil of Artemisia persica Boiss showed that the oil yield, obtained from the aerial parts of this plant species using hydrodistillation, was 0.18% (v/w) (Table 1). In several researches, the essential oil of different species of Artemisia has been already studied, and the chemical compounds for Artemisia persica Boiss from Iran are also reported. However, most of these studies are related to the cultivated Artemisia species, while in this the plant samples were collected from a rangeland ecosystem as a natural habitat. According to a study carried out by (Bagheri et al. 2017), the essential oil yield of Artemisia persica Boiss, cultivated in a farm at the north of Iran, was reported to be 0.81%, which was noticeably lower than that of the present study. In another study, (Habibi et al. 2004) showed that α-pinene, α-tujune and camphene were the major constituents of essential oil for A. persica Boiss., collected from a natural habitat in the west of Iran, contradicting the results of the present study. Bagheri et al. (2017) studied the effects of different levels of drought stress on the essential oil of A. persica Boiss. under greenhouse condition, the results showed that the essential oil yield of this species varied under different levels of drought stress.

Table 1.

Essential oil compounds of Artemisa persica Boiss. identified by GC/MS

No. Compounds Retention time (min)a % Composition Artemisa persica Boiss Identificationb
1 α-Pinene 12.25 5.8 MS
2 Camphene 13.45 0.5 MS
3 Thuja-2,4(10)-diene 14.18 1.6 MS
4 Sabinene 16.32 0.3 MS
5 β-Pinene 18.45 0.3 MS
6 α-Terpinene 19.66 2.4 MS
7 P-cymene 21.19 1.4 MS
8 1,8-Cineole 22.63 5.6 MS
9 γ-Terpinene 23.79 0.3 MS
10 cis-Sabinene hydrate 24.89 0.9 MS
11 trans-Arbusculone 25.66 1.8 MS
12 α-Compholenal 26.58 2.5 MS
13 trans-Pinocarveol 27.22 10.2 MS
14 trans-Verbenol 29.36 3.1 MS
15 Pinocarvone 32.66 8.5 MS
16 Borneol 34.57 1.2 MS
17 n-Nonanal 36.47 0.5 MS
18 Terpinen-4-ol 38.98 1.3 MS
19 P-cymen-8-ol 39.86 2.8 MS
20 Myrtenal 41.79 3.4 MS
21 Verbenone 43.68 0.5 MS
22 trans-Carveol 45.21 0.5 MS
23 trans-Pinocarvyl acetate 47.52 0.9 MS
24 Phenyl ethyl 3-methyl butanoate 49.36 2.7 MS
25 Artedouglasia oxide C 51.47 13.2 MS
26 Laciniata furanone G 53.78 1.3 MS
27 Laciniata furanone F 54.57 1.2 MS
28 Laciniata furanone E 55.32 17.1 MS
29 Laciniata furanone Hl 56.36 2.7 MS
30 Artedouglasia oxide D 57.35 5.2 MS
31 Artedouglasia oxide B 58.53 5.1 MS
Total identified 95.5
Monoterpenes 34.19
Oxygenatedl 15.9
Sesquiterpenes –
Hydrocarbons 21.2
Oxygenated –
Sesquiterpenes 14.6
Others 15.5
Oil yield (%) 0.18
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Bold values indicate the highest values among the essential oil components

aRetention time (min) in elution order from the SGE column

bMS, NIST and Wiley libraries, and the literature

Thirty-one components were identified using the GC/MS analysis, corresponding to more than 95.5% of the total sample. The major compounds of A. persica Boiss. essential oil were laciniata furanone E (17.1%), artedouglasia oxide C (13.2%), trans-pinocarveol (10.2%), pinocarvone (8.5%), and α-pinene (5.8%), other constituents were also identified with minor concentrations. Soylu et al. (2015) reported that the main components of A. persica Boiss. grown in Iran were 1,8-cineole(12.5%) and α-pinene(6.3%), camphene (3.9%), linalool(6.8%) and Sabinene (4.6%). The changes in the essential oil compositions could be related to the climatic, seasonal, geographical, geological differences, as mentioned by (Perry et al. 1999). According to the findings reported by (Cavar et al. 2012), pinocarvone (5.5%), and α-pinene (3.9%) were the major constituents of Artemisia annua L oil and that this finding is consistent with the result presented here, in present study.

Table 2 shows the antifungal activity of A. persica Boiss. essential oil. According to the results, Aspergillus ochraceus and Aspergillus parasiticus, with MIC and MFC values of 1.25 μl/ml (v/v), respectively, were the most sensitive fungal strains to A. persica Boiss. essential oil. This oil showed a potent inhibitory effect against A. flavus, and A. nidulans was inhibited at a MIC value of 2.5 μl/ml (v/v). A strong fungicidal effect against A. flavus and A. nidulans was reported for the essential oil, while the oil at a concentration of 10 μl/ml (v/v) was sufficient to show a fungicidal activity against A. fumigatus and A. niger. In the previous study, essential oils and extracts of other Artemisia species have shown variable degrees of antimicrobial activities against different bacteria and fungi (Hammami et al. 2013; Selles et al. 2013; Tariq et al. 2009; Kalemba et al. 2002); however, there was no report about the A. persica Boiss. effects on the plant pathogenic fungi. It seems that several factors such as habitat conditions affect the fungicidal effects of essential oils in the plants and have significant effects on the major components of the essential oil. In present study, A. persica Boiss. essential oil is mainly composed of laciniata furanone E (17.1%) and artedouglasia oxide C (13.2%), and the antifungal activity could be associated with the predominance of the compounds studied. Laciniata furanone E was the most active components against Aspergillus fungi (Watson et al. 2002).

Table 2.

Antifungal activity of Artemisa persica Boiss. essential oil determined using a broth macrodilution method

Strain Artemisa persica Boiss
MIC (μl/ml) MFC (μl/ml)
Aspergillus ochraceus NRRL 3174 1.25 1.25
Aspergillus flavus NRRL 3251 2.5 2.5
Aspergillus parasiticus CBS 100,926 1.25 1.25
Aspergillus fumigatusAfS34 2.5 10
Aspergillus nidulans TN02A7 2.5 2.5
Aspergillus niger KB1001 5 10
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According to Msaada et al. (2015), pinocarvone and α-pinene are the potent compounds having a strong activity against plant bacteria, pathogens, and some of microorganisms. The antimicrobial efficacy of essential oils of different plants in which α-pinene is the main compound is also reported by the other authors (Ahameethunisa, and Hopper 2010; Soylu et al. 2015). In addition, artedouglasia oxide C and 1,8-cineole are the other major components of the oil with antifungal activities (Cheng et al. 2005). According to the results, the ability of essential oils to penetrate and disrupt the fungal cell wall, resulting in the malformation of important structures is also reported, leading to the cell death (Nosrati and Behbahani 2015). Aspergillus fungi species are the most resistant fungi with relatively thick cell walls, so the effectiveness of A. persica Boiss. essential oil against the fungi could be explained by the results of this study.

Conclusion

The essential oil from A. persica Boiss. is a potential alternative source of caryophyllene, germacrene D, and humulene. The volatile compounds from this plant species possess antifungal and antibacterial properties. Hence, there is a potential for using this essential oil from A. persica Boiss as disinfectants and preservatives against microorganisms. More studies are required to be focused on isolating the compounds from essential oils and to investigate their biological activities and mode of action in order to use these volatile compounds at the commercial level.

The results in this study showed the strong fungicidal activity of A. persica Boiss. essential oil against all Aspergillus strains. This effect could be related to the main compounds in this oil, produced under habitat conditions. As the essential oils are the important natural products and recognized safe for human health, the findings of this research suggested that A. persica Boiss. essential oil was a potential candidate to be used to prevent foods and agricultural products from fungal contamination. However, the antifungal efficiency of essential oils against the other fungi species and strains needs to be determined with further studies. Also, according to the results of this study and since the A. persica Boiss. essential oil has a high antifungal property, it is recommended to examine this ability e in other species of Artemisia.

Acknowledgements

The author wish to thank Dr. Zandi (Research Institute of Forests and Rangelands (RIFR) for the botanical identification of the plant material used in this study.

Abbreviations

ARS

Agricultural Research Service

CBS

Central Bureau of Fungal Cultures

CLSI

Clinical and Laboratory Standards Institute

DMSO

Dimethyl sulfoxide

GC/MS

Gas chromatography–mass spectrometry

MFC

Minimal fungicidal concentration

MIC

Minimal inhibitory concentrations

Na2SO4

Sodium sulfate

NIST

National Institute of Standards and Technology

Funding

This project supported by University of Kashan, Iran.

Compliance with ethical standards

Conflict of interest

The author declare that there are no conflicts of interest in this research study.

Ethical approval

The author is fully satisfied with this project and its publication.

Informed consent

The author agrees to publish this article.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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