Next Article in Journal
Genetic Diversity and Population Structure of Rhododendron rex Subsp. rex Inferred from Microsatellite Markers and Chloroplast DNA Sequences
Previous Article in Journal
Genome-Wide Identification and Expression Profile Analysis of the NF-Y Transcription Factor Gene Family in Petunia hybrida
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 9
Issue 3
10.3390/plants9030337
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Composition, Antioxidant Potential, and Antimicrobial Activity of Helichrysum plicatum DC. Various Extracts

by
Bojan Vujić
1,
Vera Vidaković
2,
Milka Jadranin
3,
Irena Novaković
3,
Snežana Trifunović
1,
Vele Tešević
1 and
Boris Mandić
1,*
1
University of Belgrade-Faculty of Chemistry, Studentski trg 12-16, 11000 Belgrade, Serbia
2
Department of Ecology, Institute for Biological Research “Siniša Stanković”-National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade, Serbia
3
Institute of Chemistry, Technology and Metallurgy, National Institute, University of Belgrade, Studentski trg 12-16, 11000 Belgrade, Serbia
*
Author to whom correspondence should be addressed.
Plants 2020, 9(3), 337; https://doi.org/10.3390/plants9030337
Submission received: 11 February 2020 / Revised: 23 February 2020 / Accepted: 26 February 2020 / Published: 6 March 2020
(This article belongs to the Section Phytochemistry)
Browse Figures
Versions Notes

Abstract

:
Helichrysum plicatum DC. is widely used in folk medicine in treating a variety of health disorders. The aim of this study was to examine the influence of different extraction solvents on the chemical composition, antioxidant potential, and antimicrobial activities of H. plicatum. Aerial parts were separately extracted with ethanol, dichloromethane, and sunflower oil. The oil extract (OE) was re-extracted with acetonitrile. A total of 142 compounds were tentatively identified in ethanolic (EE), dichloromethane (DCME), and acetonitrile (ACNE) extracts using HPLC-DAD/ESI-ToF-MS. The dominant compound class in all extracts were α-pyrones, alongside flavonoids in EE, terpenoids in DCME and ACNE, and phloroglucinols in DCME. The antioxidant potential of the extracts was assessed by the 2,2-diphenyl-1-picrylhydrazyl radical (DPPH) assay. EE and DCME possessed the most potent radical scavenging capacity. Antimicrobial activity was investigated on eight bacterial, two yeast, and one fungal species. All extracts exhibited high antifungal and notable antibacterial activities compared to control substances, with DCME being the most potent. DCME exhibited stronger antimicrobial activity against P. aeruginosa than the standard chloramphenicol.

1. Introduction

The genus Helichrysum Miller (Asteraceae) comprises about 600 species of perennial or annual herbs or shrublets distributed in Europe, Asia, and Africa, the plant parts of which have been traditionally used as infusions or decoctions in the treatment of diverse ailments [1,2]. Interest in phytochemical and pharmacological studies of this genus has increased in recent years. Helichrysum species represent an abundant source of secondary metabolites, such as flavonoids, chalcones, phenolic acids, phthalides, coumarins, pyrones, and terpenes [1]. Plant extracts and their chemical constituents exhibit a range of biological activities, including antioxidant, anti-inflammatory, wound-healing, antimicrobial, photoprotective, anticarcinogenic, etc. [3,4,5,6,7,8,9,10,11,12].
Helichrysum plicatum DC. is a herbaceous perennial plant, which is native to the Balkan and Anatolian Peninsulas and Iran [13]. It has been used in folk medicine for wound-healing and the treatment of gastric and hepatic disorders, diabetes, and kidney stones [14,15,16]. Chemically, this species was mostly studied for its phenolic, mainly flavonoid content, which is thought to be responsible for the therapeutic effects of the plant. H. plicatum polar extracts are reported to possess antimicrobial, antidiabetic, spasmolytic, nephroprotective, and antimutagenic activities [13,17,18,19,20,21].
It is apparent that extracts from the same plant will differ in their composition of bioactive compounds depending on the extraction solvent. Since, with the exception of the essential oil, only the phenolic composition of polar extractives has been investigated in H. plicatum to date, the aim of this study was to perform a more detailed chemical analysis of the plant and to examine the influence of solvents of different polarity on the extraction yield, composition of extracts, antioxidant potential, and antimicrobial activities.

2. Results

2.1. Phytochemical Profile

Aerial parts of wild H. plicatum at the full blooming stage were extracted with solvents of different polarity. The yields were 7.14%, 2.88%, and 0.62% for ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extracts, respectively. The phytochemical content of the extracts was assessed by HPLC-DAD/ESI-ToF-MS. The peaks in chromatograms were tentatively identified on the basis of the exact molecular masses and formulas, UV spectra, and literature data (Tables S1–S3, Supplementary Material). The total ion chromatograms (TIC) in the positive (for EE and DCME) and negative (for EE, DCME and ACNE) modes and HPLC-DAD chromatograms of the investigated extracts are shown in the Supplementary Material (Figures S1–S3).
A total of 142 compounds were identified in H. plicatum aerial parts. Their distribution in the different extracts is presented in Table 1. The indicated structures are in agreement with the literature on Helichrysum species and/or the Asteraceae family [4,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106] (Figure 1). All the extracts were characterized by α-pyrones. Simple α-pyrones (such as micropyrone and compound 1), homodimers (helipyrone, bisnorhelipyrone), as well as heterodimers of α-pyrones and phloroglucinols (arenol, arzanol, heliarzanol, auricepyrone, etc.) were found. The prevailing compounds in EE were flavonoids. Four classes of flavonoids were identified: flavones, flavanones, flavonols, and chalcones. Compared to DCME and ACNE, only EE contained glycosylated flavonoids (compounds 43, 44, 58–60, 63–65, 67, 68, 70–72). Being more hydrophilic than their aglycone counterparts because of the presence of sugar moieties, glycosides are easily extracted with polar protic solvents. α-Pyrones and terpenoids were predominant in both ACNE and DCME, while DCME also possessed phloroglucinols as dominant compounds (Table 1). An interesting feature of nonpolar DCM and ACN extracts is the presence of (poly)methoxylated flavones, i.e. dimethoxy- (49, 53) and pentamethoxyflavones in DCME (46, 47) and methoxy- (51, 52), dimethoxy- (50), and triethoxy-dimethoxy flavones in ACNE (54, 55, 57).

2.2. Antioxidant Potential

The antioxidant activity of H. plicatum extracts was assessed by the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical assay (Table 2). EE, DCME, and ACNE demonstrated significant DPPH scavenging activity. The analysed extracts could not be compared since the polar extract (EE) was analysed by the polar DPPH method (DPPH in methanol) and nonpolar extracts (DCME, ACNE, and OE) were analysed by the nonpolar DPPH method (DPPH in toluene). However, after comparison with standards analysed by the same method, we concluded that the DCME extract exhibited a stronger antioxidant potential than the BHT standard (toluene), while EE exhibited slightly lower activity than BHT (methanol) and Trolox.

2.3. Antimicrobial Activity

The antimicrobial activity of H. plicatum was investigated against five Gram-negative bacteria (Escherichia coli, Pseudomonas aeruginosa, Proteus hauseri, Klebsiella pneumoniae, Salmonella enterica subsp. enterica), three Gram-positive bacteria (Staphylococcus aureus, Bacillus subtilis, Clostridium sporogenes), two yeasts (Candida albicans, Saccharomyces cerevisiae), and one fungal strain (Aspergillus brasiliensis) (Table 3, Table 4 and Table 5). All the extracts displayed notable antibacterial activity in the range of 0.157–2.5 mg/mL. DCME was more active than the chloramphenicol standard against Pseudomonas aeruginosa. In addition, DCME demonstrated the best antibacterial activity among the extracts, as indicated by the lowest minimal inhibitory concentration (MIC) values. The tested extracts exhibited better or the same antifungal activity as compared to the commercial drug nystatin. Once more, DCME had the lowest MIC values.

3. Discussion

3.1. Phytochemical Profile

The predominant compounds in EE were flavonoids and their glycosylated derivatives. Luteolin (compound 45, Table 1), naringenin (62), apigenin (48), quercetin (66), kaempferol (69), as well as naringenin-, apigenin-, and kaempferol- glucosides (58–60, 43, 44, 64) have been previously reported in H. plicatum [14,107]. These compounds are probably the main contributors to the therapeutic effects of the plant, which are used for treating hepatic and gastric disorders. In addition, the same flavonoids found in H. arenarium, which are reported to exhibit choleretic, cholagogue, hepatoprotective, and detoxifying activities, are also present in H. plicatum [107]. Furthermore, the phenolic-rich extracts of H. plicatum, with the glycosides of naringenin, apigenin, quercetin, and kaempferol as the main compounds, followed by their aglycones and chlorogenic acid, exhibited potent cytotoxic activities against human cancer cell lines [108]. Flavonoids and other phenolic constituents of water and ethanol extracts are also thought to be responsible for the antidiabetic and spasmolytic effects of this plant [17,18].
DCME and ACNE were characterized by the presence of α-pyrones. Numerous diverse pyrones were isolated from Helichrysum spp., although they were poorly analysed in H. plicatum. Plicatipyrone (10) was previously isolated from this species [22]. Akaberi et al. [1] listed several different groups of α-pyrone derivatives that are distributed in Helichrysum spp., namely monomers, glycosylated forms, homo-, and heterodimers. The α-pyrone profile tentatively determined in H. plicatum in the present study corresponds to α-pyrones found in other Helichrysum species. Vrkoč et al. [27] characterized the yellow pigment from the flowers of H. arenarium as a mixture of two heterodimers—phloroglucinyl α-pyrones arenol (11) and homoarenol (later named arzanol [109], 13). Arzanol is probably the most investigated α-pyrone from Helichrysum spp. It has been reported to possess a variety of pharmacological activities, including antioxidant, anti-inflammatory, and anti-HIV [109,110,111].
Several alkoxy-flavone derivatives were detected in DCME and ACNE. O-alkylation increases the lipophilicity and bioavailability of these natural products. To the best of the authors’ knowledge, there are no previous records of these derivatives in H. plicatum, probably because this species was mostly studied for the phenolic content of more polar extracts [4,86,112,113]. Methoxylated flavones were, however, reported in other Helichrysum species, such as H. viscosum var. bracteatum [43], H. decumbens [29], H. foetidum [114], H. italicum [115], H. kraussii [116], H. melaleucum [102], H. nitens [42], H. odoratissimum [116], and H. picardii [115].

3.2. Antioxidant Potential

The results obtained in this work are in agreement with literature data indicating that the methanolic and ethanolic extracts of H. plicatum exhibit dose-dependent antioxidant activity. Antioxidant activity was attributed to the phenolic content of the extracts, mostly phenolic acids and flavonoids [87,108]. These compounds act by inhibiting enzymes or chelating trace elements involved in reactive oxygen species generation or by reducing highly-oxidizing free radicals through hydrogen atom donation [117,118]. The phenolic radicals generated in the process of free radical scavenging can be stabilized via intramolecular hydrogen bonds and by electron delocalization in the aromatic ring.
Comparison of the EC50 values with literature data obtained by different protocols and DPPH concentrations is not consistent. Kadifkova Panovska and Kulevanova [119] reported EC50 values in the range 6–11 mg/mL for H. plicatum methanol and ethanol extracts with 100 mM DPPH, while 37–88 µg/mL EC50 values with 0.08 mM DPPH were reported by Bigović et al. [108] and 235–918 µg/mL with 0.1 mM DPPH by Acet et al. [120]. Even though 0.1 mM DPPH was used in the present study, the results are still difficult to compare with Acet et al. because of the different mixing volumes of extracts and DPPH solutions, as well as the different incubation times. Nevertheless, compared to Trolox, the results presented herein are similar to the results from a previous study [108], whereas compared to BHT, the extracts from the present study (EE, DCME, and ACNE) were more potent in radical scavenging than the methanol and ethanol extracts of H. plicatum investigated by Kadifkova Panovska and Kulevanova [119].
The most potent radical scavenging capacity in the present study was exhibited by EE and DCME, which are both rich in α-pyrones. Rosa et al. [110] showed that the α-pyrones arzanol and helipyrone achieved remarkable efficacy in scavenging lipid peroxyl radicals. Since arzanol (Figure 2) showed powerful scavenging activity against linoleic acid peroxyl radicals in the linoleic acid autoxidation test and methylarzanol was only slightly active, the authors concluded that the α-pyrone enolic hydroxyl, which can mimic a phenolic hydroxyl in assays of antioxidant activity, is responsible for the observed radical scavenging properties [110]. Furthermore, arzanol exhibited antioxidant properties at non-cytotoxic concentrations [121], which qualifies it as a candidate for investigation as a possible food additive. The presence of flavonoids probably also contributed to the significant antioxidant potential of EE.

3.3. Antimicrobial Activity

There are several studies on H. plicatum antimicrobial activity, which was ascribed to the phenolic and flavonoid contents [13,120,122]. Fungi were more sensitive to H. plicatum extracts than bacteria, which corroborates our findings. In previous studies, Gram-positive bacteria were more sensitive to the tested extracts than Gram-negative bacteria, although this pattern was not observed in the present study. In general, polyphenols have been widely investigated for their antimicrobial activities, which can be attributed to both direct action against microorganisms as well as the suppression of microbial virulence factors [123]. In this study, all extracts contained a variety of phenolic compounds. Furthermore, ACNE and DCME were characterized by the presence of (poly)methoxylated flavones. Methoxylated flavones from H. nitens displayed antifungal activity against Cladosporium cucumerinum [42]. This group of compounds is reported to exhibit mild antibacterial but potent fungicidal properties [124,125]. They are externally located on leaf and stem surfaces where they presumably play a role in antimicrobial defence. Methylation decreases the antioxidant potential but increases the stability of flavones, their lipophilicity, and, consequently, the ability to permeate membranes [126]. The presence of polymethoxylated flavonoids was confirmed herein in DCME, and it can be assumed that nonpolar flavonoids were responsible for the pronounced antifungal activity of this extract.
The main compounds of DCME, the most active extract in the antimicrobial tests, were α-pyrones, terpenoids, and phloroglucinols. The terpenoid components from H. italicum, along with flavonoids, were responsible for the antimicrobial properties of the plant [127]. Antimicrobial activity of α-pyrones from Helichrysum species has also been demonstrated. Four heterodimeric (italipyrone, plicatipyrone, arenol, and arzanol) and three homodimeric (helipyrone and two related compounds) α-pyrones from H. stoechas, which were identified in the H. plicatum investigated herein, displayed high activities against Gram-positive bacteria [26]. In another study, arzanol showed outstanding action against multidrug-resistant Staphylococcus aureus isolates, making it a good choice for further studies of suppression of antibiotic-resistant bacterial strains [23], while phloroglucinyl α-pyrones from H. decumbens displayed significant antifungal activity against Cladosporium herbarum [29].
The variety of compounds identified in H. plicatum most probably exert synergistic effects. Antioxidants and antimicrobials from natural sources have gained popularity over synthetic ones in the last twenty years because they most likely exhibit fewer side effects. Arenarin, which represents a mixture of phenolic antibiotics from H. arenarium, a plant with a similar phytochemical content to H. plicatum, is used as a skin and eye antibacterial agent in Russia [23]. Owing to the important biological activities of H. plicatum extracts and isolated compounds, they could be considered for use in the pharmaceutical, cosmetic, and food industries.

4. Materials and Methods

4.1. Plant Material

A commercial sample of wild-growing plant material was obtained from the Institute for Medicinal Plants Research “Dr. Josif Pancić”, Belgrade, Serbia. Wild-growing plant material was collected during the full-blooming stage in Macedonia in 2017.

4.2. Extraction Procedure

The dried and powdered plant material was extracted with 96% ethanol, dichloromethane, and sunflower oil in the dark for seven days. After filtration, solvent was removed from ethanol and dichloromethane extracts. In order to avoid ionization difficulties with the oil matrix, prior to HPLC-DAD/ESI-ToF-MS analyses, the oil extract was re-extracted with acetonitrile by overhead rotary mixer for 18 h.

4.3. HPLC-DAD/ESI-ToF-MS Analyses

Prior to injection, the test samples were dissolved in methanol (c ≈ 10 mg/mL) and filtered through a 0.45-μm filter.
An HPLC apparatus (Agilent 1100 Series, Agilent Technologies) with a degasser, autosampler, LiChrospher 100 RP18e column (250 × 4.0 mm i.d.; 5 μm), and a DAD detector in combination with a 6210 Time-of-Flight LC/MS system (Agilent Technologies) was used to analyse the chemical content of the tested samples. A mixture of solvents A (0.2% formic acid solution in water) and B (acetonitrile) with programmed isocratic and gradient elution was used as the mobile phase: 0–5 min 10–20% B, 5–10 min 20% B, 10–20 min 20–30% B, 20–30 min 30–70% B, 30–35 min 70–100% B, 35–40 min 100% B, 40–41 min 100–10% B, 41–45 min 10% B at a flow rate of 1.00 mL/min. The injection volume was 10 μL and the column temperature was 25°C. A DA detector was used to detect signals in the 190–550 nm wavelength range. The charged molecular ions were obtained by electrospray ionization (ESI) at atmospheric pressure: the eluted compounds were mixed with nitrogen in the heated interface and the polarity was set to negative, with the following ES parameters: capillary voltage, 4000 V; gas temperature, 350°C; drying gas flow rate, 12 L/min; nebulizer pressure, 45 psig (310.26 Pa); fragmentation voltage, 140 V, and masses were measured in the range 100–2500 m/z. MassHunter Workstation software was used for data recording and processing.

4.4. Antioxidant Assay

The antioxidant activity of the plant extracts was evaluated by the 2,2-diphenyl-1-picrylhydrazil (DPPH) assay [128], which is based on the depletion of the colour of the stable free radical DPPH in a reaction with potential antioxidants and measured by the decrease of absorbance at 517 nm. Concentrations of the extracts were in the range from 0.1 to 1.75 mg/mL. A volume of 200 µL was mixed with 1800 µL of a methanolic solution of DPPH (0.1 mM). The reaction mixture was shaken and then incubated in the dark for 30 min. After this period, the absorbance of the remaining DPPH radical was measured at 517 nm (Asample). Blank probes were done in the same way, using 200 µL of methanol instead of the extract solution to obtain Ablank. All determinations were performed in triplicate. The percentage of inhibition of the DPPH radical, I(%), by each sample was calculated according to the equation:
I ( % ) = A b l a n k − A s a m p l e A b l a n k × 100 .
The EC50 (concentration of an extract that reduces the absorption of DPPH solution by 50%) was calculated from the curve of the dependence of I(%) from the concentration of each extract. DPPH scavenging activity was also determined for Trolox and butylated hydroxytoluene (BHT), which are known artificial antioxidants that were used as positive probes. Tests were performed in triplicate.
The same procedure was undertaken for the determination of the radical scavenging capacity of oil extracts, except that toluene instead of methanol was used as a solvent, and BHT dissolved in toluene as a positive probe.

4.5. Antimicrobial Assay

Antimicrobial activity was tested against a panel of microorganisms, including: Gram-negative bacteria Escherichia coli (ATCC 25922), Pseudomonas aeruginosa (ATCC 9027), Proteus hauseri (ATCC 13315), Klebsiella pneumoniae (ATCC 10031), Salmonella enterica subsp. enterica serovar Enteritidis (ATCC 13076), Gram-positive bacteria Staphylococcus aureus (ATCC 6538), Bacillus subtilis (ATCC 6633), Clostridium sporogenes (ATCC 19404), yeasts Candida albicans (ATCC 10231), Saccharomyces cerevisiae (ATCC 9763), and fungal strain Aspergillus brasiliensis (ATCC 16404).
Antimicrobial activity was evaluated using the broth microdilution method according to the National Committee for Clinical Laboratory Standards [129]. The 96-well plates were prepared by dispensing 100 μL of Mueller-Hinton broth for bacteria and Sabouraud dextrose broth for yeasts and fungi into each well. Test extracts were dissolved in DMSO to a stock concentration of 20 mg/mL, then 100 μL from the stock solution of the tested extracts were added to the first row of the plate and double-diluted in the broth. The direct colony method was used in preparing the suspension of bacteria and yeasts in sterile 0.9% saline, while preparation of the suspension of fungal spores included gentle stripping of spores from agar slants with growing Aspergilli into sterile 0.9% saline. Suspension turbidity was conducted by comparison with 0.5 McFarland standard. After measuring the optical density OD600, the colony count was also checked after a series of dilutions of initial suspensions. Due to the visual detection of growth inhibition, the maximum concentrations of microorganisms were used. Ten µL of bacterial or yeast suspension or suspension of spores were added to each well to give a final concentration of 106 CFU/mL for bacteria and 105 CFU/mL for yeasts and fungi. In order to compare the activity of an extract with already existing, commercially available antimicrobial agents, broad-spectrum compounds commonly used in such assays served as positive controls [130]. Chloramphenicol served as the positive control for bacteria, while nystatin served as the positive control for yeasts and fungi. The inoculated plates were incubated at 37°C for 24 h for bacteria and at 28°C for 48 h for the yeasts and fungi. The MIC was determined as the lowest concentration that inhibited visible microbial growth.
Minimum bactericidal (MBC) and minimum fungicidal concentrations (MFC) were determined by plating 10 μL of samples from wells where no colony growth was observed onto nutrient agar medium for bacteria and Sabouraud dextrose agar for yeasts and fungi. After the incubation period, the lowest concentration with no visible growth (no colony) was defined as the minimum microbicidal concentration.

5. Conclusions

In this study, the influence of three extraction solvents (ethanol, dichloromethane, and sunflower oil) on the composition, antioxidant, and antimicrobial activities of Helichrysum plicatum was investigated. The extracts comprised very diverse groups of secondary metabolites, including terpenoids and a myriad of (poly)phenolic compounds, flavonoids, α-pyrones, phloroglucinols, phenolic acids, acetophenones, phthalides, and other phenolic derivatives. EE and DCME, both rich in α-pyrones, possessed a marked antioxidant potential. DCME demonstrated the best antibacterial activity among the extracts. All extracts displayed significant antifungal capabilities, with MIC values lower than or equivalent to the MICs of the commercial antifungal agent nystatin. DCME had the lowest MIC values, which could be a consequence of the presence of nonpolar polymethoxylated flavonoids. Based on the results from this study, H. plicatum extracts could be considered for use as natural additives in food and cosmetic industries.

Supplementary Materials

The following are available online at https://www.mdpi.com/2223-7747/9/3/337/s1, Figure S1: The total ion and HPLC-DAD chromatograms of Helichrysum plicatum ethanol extract (EE), Figure S2: The total ion and HPLC-DAD chromatograms of Helichrysum plicatum dichloromethane extract (DCME), Figure S3: The total ion and HPLC-DAD chromatograms of Helichrysum plicatum acetonitrile oil extract (ACNE), Table S1: Tentative analysis of Helichrysum plicatum ethanol extract (EE), Table S2: Tentative analysis of Helichrysum plicatum dichloromethane extract (DCME), Table S3: Tentative analysis of Helichrysum plicatum acetonitrile oil extract (ACNE).

Author Contributions

Conceptualization, B.M.; formal analysis, B.V., M.J., S.T., and I.N.; resources, V.T. and B.M.; data curation, M.J., V.V., I.N., and B.M.; writing—original draft preparation, V.V., M.J., S.T., and I.N.; writing—review and editing, V.T. and B.M.; visualization, V.V.; supervision, B.M.; funding acquisition, V.T. and B.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Ministry of Education and Science of the Republic of Serbia (Projects: 172053 and 173011).

Acknowledgments

The authors thank Nebojša Menković from the Institute for Medicinal Plants Research Josif Pancić, Belgrade, Serbia for providing the plant material sample.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of the data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Akaberi, M.; Sahebkar, A.; Azizi, N.; Emami, S.A. Everlasting flowers: Phytochemistry and pharmacology of the genus Helichrysum. Ind. Crops Prod. 2019, 138, 111471. [Google Scholar] [CrossRef]
  2. Bayer, R.J.; Breitwieser, I.; Ward, J.; Puttock, C. Tribe Gnaphalieae (Cass.) Lecoq & Juillet (1831). In Flowering Plants Eudicots: Asterales; Kadereit, J.W., Jeffrey, C., Eds.; The Families and Genera of Vascular Plants; Springer: Berlin, Heidelberg, Germany, 2007; Volume 8, pp. 246–284. [Google Scholar] [CrossRef]
  3. Asong, J.A.; Amoo, S.O.; McGaw, L.J.; Nkadimeng, S.M.; Aremu, A.O.; Otang-Mbeng, W. Antimicrobial Activity, Antioxidant Potential, Cytotoxicity and Phytochemical Profiling of Four Plants Locally Used against Skin Diseases. Plants 2019, 8, 350. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Jarzycka, A.; Lewińska, A.; Gancarz, R.; Wilk, K.A. Assessment of extracts of Helichrysum arenarium, Crataegus monogyna, Sambucus nigra in photoprotective UVA and UVB; photostability in cosmetic emulsions. J. Photochem. Photobiol. B 2013, 128, 50–57. [Google Scholar] [CrossRef] [PubMed]
  5. Barroso, M.R.; Barros, L.; Dueñas, M.; Carvalho, A.M.; Santos-Buelga, C.; Fernandes, I.P.; Barreiro, M.F.; Ferreira, I.C.F.R. Exploring the antioxidant potential of Helichrysum stoechas (L.) Moench phenolic compounds for cosmetic applications: Chemical characterization, microencapsulation and incorporation into a moisturizer. Ind. Crops Prod. 2014, 53, 330–336. [Google Scholar] [CrossRef] [Green Version]
  6. Lourens, A.C.U.; Reddy, D.; Başer, K.H.C.; Viljoen, A.M.; Van Vuuren, S.F. In vitro biological activity and essential oil composition of four indigenous South African Helichrysum species. J. Ethnopharmacol. 2004, 95, 253–258. [Google Scholar] [CrossRef]
  7. Süntar, I.; Küpeli Akkol, E.; Keles, H.; Yesilada, E.; Sarker, S.D. Exploration of the wound healing potential of Helichrysum graveolens (Bieb.) Sweet: Isolation of apigenin as an active component. J. Ethnopharmacol. 2013, 149, 103–110. [Google Scholar] [CrossRef]
  8. Yagura, T.; Motomiya, T.; Ito, M.; Honda, G.; Iida, A.; Kiuchi, F.; Tokuda, H.; Nishino, H. Anticarcinogenic compounds in the Uzbek medicinal plant, Helichrysum maracandicum. J. Nat. Med. 2008, 62, 174. [Google Scholar] [CrossRef]
  9. Liu, Y.-J.; Zhang, J.-L.; Li, C.; Mu, X.-G.; Liu, X.-L.; Wang, L.; Zhao, Y.-C.; Zhang, P.; Li, X.-D.; Zhang, X.-X. Antimicrobial Secondary Metabolites from the Seawater-Derived Fungus Aspergillus sydowii SW9. Molecules 2019, 24, 4596. [Google Scholar] [CrossRef] [Green Version]
  10. Munekata, P.E.S.; Alcántara, C.; Collado, M.C.; Garcia-Perez, J.V.; Saraiva, J.A.; Lopes, R.P.; Barba, F.J.; do Prado Silva, L.; Sant’Ana, A.S.; Fierro, E.M.; et al. Ethnopharmacology, phytochemistry and biological activity of Erodium species: A review. Food Res. Int. 2019, 126, 108659. [Google Scholar] [CrossRef]
  11. Donkor, S.; Larbie, C.; Komlaga, G.; Emikpe, B.O. Phytochemical, Antimicrobial, and Antioxidant Profiles of Duranta erecta L. Parts. Biochem. Res. Int. 2019, 2019, 8731595. [Google Scholar] [CrossRef] [Green Version]
  12. Casciaro, B.; Calcaterra, A.; Cappiello, F.; Mori, M.; Loffredo, M.R.; Ghirga, F.; Mangoni, M.L.; Botta, B.; Quaglio, D. Nigritanine as a New Potential Antimicrobial Alkaloid for the Treatment of Staphylococcus aureus-Induced Infections. Toxins 2019, 11, 511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Bigović, D.J.; Stević, T.R.; Janković, T.R.; Noveski, N.B.; Radanović, D.S.; Pljevljakušić, D.S.; Djurić, Z.R. Antimicrobial activity of Helichrysum plicatum DC. Hem. Ind. 2017, 71, 337–342. [Google Scholar] [CrossRef]
  14. Kulevanova, S.; Stefova, M.; Stafilov, T. HPLC identification and determination of flavone aglycones in Helichrysum plicatum DC. (Asteraceae). Pharmazie 2000, 55, 391–392. [Google Scholar] [PubMed]
  15. Polat, R.; Cakilcioglu, U.; Satıl, F. Traditional uses of medicinal plants in Solhan (Bingöl—Turkey). J. Ethnopharmacol. 2013, 148, 951–963. [Google Scholar] [CrossRef] [PubMed]
  16. Tetik, F.; Civelek, S.; Cakilcioglu, U. Traditional uses of some medicinal plants in Malatya (Turkey). J. Ethnopharmacol. 2013, 146, 331–346. [Google Scholar] [CrossRef]
  17. Bigovic, D.; Brankovic, S.; Kitic, D.; Radenkovic, M.; Jankovic, T.; Savikin, K.; Zivanovic, S. Relaxant Effect of the Ethanol Extract of Helichrysum plicatum (Asteraceae) on Isolated Rat Ileum Contractions. Molecules 2010, 15, 3391–3401. [Google Scholar] [CrossRef] [Green Version]
  18. Aslan, M.; Deliorman Orhan, D.; Orhan, N.; Sezik, E.; Yesilada, E. In vivo antidiabetic and antioxidant potential of Helichrysum plicatum ssp. plicatum capitulums in streptozotocin-induced-diabetic rats. J. Ethnopharmacol. 2007, 109, 54–59. [Google Scholar] [CrossRef]
  19. Bayir, Y.; Halici, Z.; Keles, M.S.; Colak, S.; Cakir, A.; Kaya, Y.; Akçay, F. Helichrysum plicatum DC. subsp. plicatum extract as a preventive agent in experimentally induced urolithiasis model. J. Ethnopharmacol. 2011, 138, 408–414. [Google Scholar] [CrossRef]
  20. Ozbek, T.; Gulluce, M.; Adiguzel, A.; Ozkan, H.; Sahin, F.; Orhan, F. Antimutagenic Activity of the Methanol Extract of Helichrysum plicatum ssp. plicatum. Asian J. Chem. 2009, 21, 2705–2710. [Google Scholar]
  21. Apaydin Yildirim, B.; Kordali, S.; Terim Kapakin, K.A.; Yildirim, F.; Aktas Senocak, E.; Altun, S. Effect of Helichrysum plicatum DC. subsp. plicatum ethanol extract on gentamicin-induced nephrotoxicity in rats. J. Zhejiang Univ. Sci. B 2017, 18, 501–511. [Google Scholar] [CrossRef] [Green Version]
  22. Hänsel, R.; Cybulski, E.-M.; Çubukçu, B.; Meriçli, A.H.; Bohlmann, F.; Zdero, C. Neue pyron-derivate aus Helichrysum-arten. Phytochemistry 1980, 19, 639–644. [Google Scholar] [CrossRef]
  23. Taglialatela-Scafati, O.; Pollastro, F.; Chianese, G.; Minassi, A.; Gibbons, S.; Arunotayanun, W.; Mabebie, B.; Ballero, M.; Appendino, G. Antimicrobial Phenolics and Unusual Glycerides from Helichrysum italicum subsp. microphyllum. J. Nat. Prod. 2013, 76, 346–353. [Google Scholar] [CrossRef] [PubMed]
  24. Akaberi, M.; Danton, O.; Tayarani-Najaran, Z.; Asili, J.; Iranshahi, M.; Emami, S.A.; Hamburger, M. HPLC-Based Activity Profiling for Antiprotozoal Compounds in the Endemic Iranian Medicinal Plant Helichrysum oocephalum. J. Nat. Prod. 2019, 82, 958–969. [Google Scholar] [CrossRef]
  25. Vrkoč, J.; Dolejš, L.; Buděšínský, M. Methylene-bis-2H-pyran-2-ones and phenolic constituents from the root of Helichrysum arenarium. Phytochemistry 1975, 14, 1383–1384. [Google Scholar] [CrossRef]
  26. Rios, J.L.; Recio, M.C.; Villar, A. Isolation and identification of the antibacterial compounds from Helichrysum stoechas. J. Ethnopharmacol. 1991, 33, 51–55. [Google Scholar] [CrossRef]
  27. Vrkoč, J.; Dolejš, L.; Sedmera, P.; Vašíčková, S.; Šorm, F. The structure of arenol and homoarenol, α-pyrone derivatives from Helichrysum arenarium (L.) Moench. Tetrahedron Lett. 1971, 12, 247–250. [Google Scholar] [CrossRef]
  28. Bohlmann, F.; Misra, L.N.; Jakupovic, J. Weitere Phloroglucin- und α-Pyron-Derivate aus Helichrysum-Arten. Planta Med. 1984, 50, 174–176. [Google Scholar] [CrossRef]
  29. Tomás-Lorente, F.; Iniesta-Sanmartín, E.; Tomás-Barberán, F.A.; Trowitzsch-Kienast, W.; Wray, V. Antifungal phloroglucinol derivatives and lipophilic flavonoids from Helichrysum decumbens. Phytochemistry 1989, 28, 1613–1615. [Google Scholar] [CrossRef]
  30. Jakupovic, J.; Kuhnke, J.; Schuster, A.; Metwally, M.A.; Bohlmann, F. Phloroglucinol derivatives and other constituents from South African Helichrysum species. Phytochemistry 1986, 25, 1133–1142. [Google Scholar] [CrossRef]
  31. Kanlayavattanakul, M.; Ruangrungsi, N.; Watanabe, T.; Ishikawa, T. Chemical Constituents of Pterocaulon redolens. Heterocycles 2003, 61, 183. [Google Scholar] [CrossRef]
  32. Rumbero, A.; Arriaga-Giner, F.J.; Wollenweber, E. A New Oxyprenyl Coumarin and Highly Methylated Flavones from the Exudate of Ozothamnus lycopodioides (Asteraceae). Z. Für Nat. C 2014, 55, 1–4. [Google Scholar] [CrossRef] [PubMed]
  33. He, F.; Wang, M.; Gao, M.; Zhao, M.; Bai, Y.; Zhao, C. Chemical composition and biological activities of Gerbera anandria. Molecules 2014, 19, 4046–4057. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Maes, D.; Syngel, K.V.; Debenedetti, S.; De Kimpe, N. Synthesis of purpurasol, a highly oxygenated coumarin from Pterocaulon purpurascens. Tetrahedron 2006, 62, 4426–4429. [Google Scholar] [CrossRef]
  35. Medeiros-Neves, B.; De Barros, F.M.C.; Von Poser, G.L.; Teixeira, H.F. Quantification of Coumarins in Aqueous Extract of Pterocaulon balansae (Asteraceae) and Characterization of a New Compound. Molecules 2015, 20, 18083–18094. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Bohlmann, F.; Zdero, C. Neue obliquin-derivate aus Helichrysum serpyllifolium. Phytochemistry 1980, 19, 331–332. [Google Scholar] [CrossRef]
  37. Bohlmann, F.; Zdero, C. Neue phloroglucin-derivate aus Helichrysum-arten. Phytochemistry 1980, 19, 153–155. [Google Scholar] [CrossRef]
  38. Bohlmann, F.; Zdero, C. Flavanones from Helichrysum thapsus. Phytochemistry 1983, 22, 2877–2878. [Google Scholar] [CrossRef]
  39. Bohlmann, F.; Zdero, C. Neue phloroglucin-derivate aus Helichrysum natalitium und Helichrysum bellum. Phytochemistry 1979, 18, 641–644. [Google Scholar] [CrossRef]
  40. Grinev, V.S.; Shirokov, A.A.; Navolokin, N.A.; Polukonova, N.V.; Kurchatova, M.N.; Durnova, N.A.; Bucharskaya, A.B.; Maslyakova, G.N. Polyphenolic compounds of a new biologically active extract from immortelle sandy flowers (Helichrysum arenarium (L.) Moench.). Russ. J. Bioorganic Chem. 2016, 42, 770–776. [Google Scholar] [CrossRef]
  41. Mao, Z.; Gan, C.; Zhu, J.; Ma, N.; Wu, L.; Wang, L.; Wang, X. Anti-atherosclerotic activities of flavonoids from the flowers of Helichrysum arenarium L. MOENCH through the pathway of anti-inflammation. Bioorg. Med. Chem. Lett. 2017, 27, 2812–2817. [Google Scholar] [CrossRef]
  42. Tomas-Barberán, F.A.; Msonthi, J.D.; Hostettmann, K. Antifungal epicuticular methylated flavonoids from Helichrysum nitens. Phytochemistry 1988, 27, 753–755. [Google Scholar] [CrossRef]
  43. Geissman, T.A.; Mukherjee, R.; Sim, K.Y. Constituents of Helichrysum viscosum var. bracteatum DC. Phytochemistry 1967, 6, 1575–1581. [Google Scholar] [CrossRef]
  44. Cubukcu, B. Studies on lipophilic flavonoids of Helichrysum species growing in Anatolia. Doga Bilim Derg. Seri Temel Bilim. 1982, 6, 83–90. [Google Scholar]
  45. Lv, H.; Li, Q.; Zhong, J.; Liao, L.-X.; Haji Akber, A. Studies on flavonoids from Helichrysum arenarium. Chin. Pharm. J. 2008, 43, 11–13. [Google Scholar]
  46. Wollenweber, E.; Roitman, J.N. New reports on surface flavonoids from Chamaebatiaria (Rosaceae), Dodonaea (Sapindaceae), Elsholtzia (Lamiaceae), and Silphium (Asteraceae). Nat. Prod. Commun. 2007, 2, 385–389. [Google Scholar] [CrossRef]
  47. Jakupovic, J.; Zdero, C.; Grenz, M.; Tsichritzis, F.; Lehmann, L.; Hashemi-Nejad, S.M.; Bohlmann, F. Twenty-one acylphloroglucinol derivatives and further constituents from south african Helichrysum species. Phytochemistry 1989, 28, 1119–1131. [Google Scholar] [CrossRef]
  48. Czinner, E.; Kursinszki, L.; Baumann, D.; Hamburger, M.; Kéry, Á.; Szöke, É.; Lemberkovics, É. Phytochemical Study of Phenolic Compounds from Helichrysi flos by LC-DAD-MS. In Natural Products in the New Millennium: Prospects and Industrial Application; Rauter, A.P., Palma, F.B., Justino, J., Araújo, M.E., dos Santos, S.P., Eds.; Proceedings of the Phytochemical Society of Europe; Springer: Dordrecht, The Netherlands, 2002; Volume 47, pp. 99–109. ISBN 978-94-015-9876-7. [Google Scholar] [CrossRef]
  49. Albayrak, S.; Aksoy, A.; Sagdic, O.; Hamzaoglu, E. Compositions, antioxidant and antimicrobial activities of Helichrysum (Asteraceae) species collected from Turkey. Food Chem. 2010, 119, 114–122. [Google Scholar] [CrossRef]
  50. Wang, L.-B.; Toshio, M.; Gao, H.-Y.; Huang, J.; Masayuki, Y.; Wu, L.-J. Isolation and identification of chemical constituents of flavones from Flos Helichrysi Arenarii. J. Shenyang Pharm. Univ. 2009, 792–795. [Google Scholar]
  51. D’Abrosca, B.; Buommino, E.; Caputo, P.; Scognamiglio, M.; Chambery, A.; Donnarumma, G.; Fiorentino, A. Phytochemical study of Helichrysum italicum (Roth) G. Don: Spectroscopic elucidation of unusual amino-phlorogucinols and antimicrobial assessment of secondary metabolites from medium-polar extract. Phytochemistry 2016, 132, 86–94. [Google Scholar] [CrossRef]
  52. Szadowska, A. Pharmacology of galenic preparations and flavonoids isolated from Helichrysum arenarium. Acta Pol. Pharm. 1962, 19, 465–479. [Google Scholar]
  53. Morikawa, T.; Ninomiya, K.; Akaki, J.; Kakihara, N.; Kuramoto, H.; Matsumoto, Y.; Hayakawa, T.; Muraoka, O.; Wang, L.-B.; Wu, L.-J.; et al. Dipeptidyl peptidase-IV inhibitory activity of dimeric dihydrochalcone glycosides from flowers of Helichrysum arenarium. J. Nat. Med. 2015, 69, 494–506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Bohlmann, F.; Ziesche, J.; Mahanta, P.K. Neue chalkon-derivate und humulon-ähnliche verbindungen aus Helichrysum-arten. Phytochemistry 1979, 18, 1033–1036. [Google Scholar] [CrossRef]
  55. Spring, O.; Zipper, R.; Reeb, S.; Vogler, B.; Da Costa, F.B. Sesquiterpene lactones and a myoinositol from glandular trichomes of Viguiera quinqueremis (Heliantheae; Asteraceae). Phytochemistry 2001, 57, 267–272. [Google Scholar] [CrossRef]
  56. Sakamoto, H.T.; Laudares, E.P.; Crotti, A.E.M.; Lopes, N.P.; Vichnewski, W.; Lopes, J.L.C.; Heleno, V.C.G. Sesquiterpenes lactones and flavonoids from Eremanthus argenteus (Asteraceae). Nat. Prod. Commun. 2010, 5, 681–684. [Google Scholar] [CrossRef] [Green Version]
  57. Gousiadou, C.; Skaltsa, H. Secondary metabolites from Centaurea orphanidea. Biochem. Syst. Ecol. 2003, 31, 389–396. [Google Scholar] [CrossRef]
  58. Özçelik, B.; Gürbüz, I.; Karaoglu, T.; Yeşilada, E. Antiviral and antimicrobial activities of three sesquiterpene lactones from Centaurea solstitialis L. ssp. solstitialis. Microbiol. Res. 2009, 164, 545–552. [Google Scholar] [CrossRef] [PubMed]
  59. Atrrog, A.A.B.; Natić, M.; Tosti, T.; Milojković-Opsenica, D.; Đorđević, I.; Tešević, V.; Jadranin, M.; Milosavljević, S.; Lazić, M.; Radulović, S.; et al. Lipophilicity of some guaianolides isolated from two endemic subspecies of Amphoricarpos neumayeri (Asteraceae) from Montenegro. Biomed. Chromatogr. 2009, 23, 250–256. [Google Scholar] [CrossRef] [PubMed]
  60. Bai, L.; Liu, Q.; Cen, Y.; Huang, J.; Zhang, X.; Guo, S.; Zhang, L.; Guo, T.; Ho, C.-T.; Bai, N. A new sesquiterpene lactone glucoside and other constituents from Inula salsoloides with insecticidal activities on striped flea beetle (Phyllotreta striolata Fabricius). Nat. Prod. Res. 2018, 32, 552–557. [Google Scholar] [CrossRef] [PubMed]
  61. Perry, D.L.; Fischer, N.H. New germacranolide sesquiterpene dilactones from the genus Melampodium (Compositae). J. Org. Chem. 1975, 40, 3480–3486. [Google Scholar] [CrossRef]
  62. Siedle, B.; García-Piñeres, A.J.; Murillo, R.; Schulte-Mönting, J.; Castro, V.; Rüngeler, P.; Klaas, C.A.; Da Costa, F.B.; Kisiel, W.; Merfort, I. Quantitative Structure−Activity Relationship of Sesquiterpene Lactones as Inhibitors of the Transcription Factor NF-κB. J. Med. Chem. 2004, 47, 6042–6054. [Google Scholar] [CrossRef]
  63. Kimani, N.M.; Matasyoh, J.C.; Kaiser, M.; Brun, R.; Schmidt, T.J. Anti-Trypanosomatid Elemanolide Sesquiterpene Lactones from Vernonia lasiopus O. Hoffm. Molecules 2017, 22, 597. [Google Scholar] [CrossRef] [Green Version]
  64. Erasto, P.; Grierson, D.S.; Afolayan, A.J. Antioxidant Constituents in Vernonia amygdalina Leaves. Pharm. Biol. 2007, 45, 195–199. [Google Scholar] [CrossRef] [Green Version]
  65. Ono, M.; Masuoka, C.; Odake, Y.; Ito, Y.; Nohara, T. Eudesmane derivatives from Tessaria integrifolia. Phytochemistry 2000, 53, 479–484. [Google Scholar] [CrossRef]
  66. Yamada, M.; Matsuura, N.; Suzuki, H.; Kurosaka, C.; Hasegawa, N.; Ubukata, M.; Tanaka, T.; Iinuma, M. Germacranolides from Calea urticifolia. Phytochemistry 2004, 65, 3107–3111. [Google Scholar] [CrossRef]
  67. Torrenegra, R.D.; Tellez, A.N. Chemotaxonomic value of melampolides in Espeletia species (Asteraceae). Biochem. Syst. Ecol. 1995, 23, 449–450. [Google Scholar] [CrossRef]
  68. Schorr, K.; Merfort, I.; Costa, F.B.D. A Novel Dimeric Melampolide and Further Terpenoids from Smallanthus sonchifolius (Asteraceae) and the Inhibition of the Transcription Factor NF-κB. Nat. Prod. Commun. 2019. [Google Scholar] [CrossRef] [Green Version]
  69. Miyase, T.; Ozaki, H.; Ueno, A. Sesquiterpene Glycosides from Ainsliaea cordifolia FRANCH. et SAV. Chem. Pharm. Bull. (Tokyo) 1991, 39, 937–938. [Google Scholar] [CrossRef] [Green Version]
  70. Ramseyer, J.; Thuerig, B.; De Mieri, M.; Schärer, H.-J.; Oberhänsli, T.; Gupta, M.P.; Tamm, L.; Hamburger, M.; Potterat, O. Eudesmane Sesquiterpenes from Verbesina lanata with Inhibitory Activity against Grapevine Downy Mildew. J. Nat. Prod. 2017, 80, 3296–3304. [Google Scholar] [CrossRef] [PubMed]
  71. Pan, E.; Gorka, A.P.; Alumasa, J.N.; Slebodnick, C.; Harinantenaina, L.; Brodie, P.J.; Roepe, P.D.; Randrianaivo, R.; Birkinshaw, C.; Kingston, D.G.I. Antiplasmodial and Antiproliferative Pseudoguaianolides of Athroisma proteiforme from the Madagascar Dry Forest. J. Nat. Prod. 2011, 74, 2174–2180. [Google Scholar] [CrossRef] [Green Version]
  72. Jakupovic, J.; Schuster, A.; Bohlmann, F.; Ganzer, U.; King, R.M.; Robinson, H. Diterpenes and other constituents from Australian Helichrysum and related species. Phytochemistry 1989, 28, 543–551. [Google Scholar] [CrossRef]
  73. Coll Aráoz, M.V.; Mercado, M.I.; Grau, A.; Catalán, C.A.N. Ent-kaurane derivatives from the root cortex of yacon and other three Smallanthus species (Heliantheae, Asteraceae). Biochem. Syst. Ecol. 2010, 38, 1042–1048. [Google Scholar] [CrossRef]
  74. Miyakado, M.; Ohno, N.; Yoshioka, H.; Mabry, T.J.; Whiffin, T. Gymnospermin: A new labdan triol from Gymnosperma glutinosa. Phytochemistry 1974, 13, 189–190. [Google Scholar] [CrossRef]
  75. Yang, Y.; Chen, H.; Lei, J.; Yu, J. Biological activity of extracts and active compounds isolated from Siegesbeckia orientalis L. Ind. Crops Prod. 2016, 94, 288–293. [Google Scholar] [CrossRef]
  76. Cruz, F.G.; Roque, N.F. Relative stereochemistry determination of pimaradienes through oxidative products. Quím. Nova 1997, 20, 261–266. [Google Scholar] [CrossRef]
  77. Jakupovic, J.; Baruah, R.N.; Zdero, C.; Eid, F.; Pathak, V.P.; Chau-thi, T.V.; Bohlmann, F.; King, R.M.; Robinson, H. Further diterpenes from plants of the Compositae, subtribe Solidagininae. Phytochemistry 1986, 25, 1873–1881. [Google Scholar] [CrossRef]
  78. Bohlmann, F.; Ziesche, J. Neue diterpene aus Gnaphalium-arten. Phytochemistry 1980, 19, 71–74. [Google Scholar] [CrossRef]
  79. Bohlmann, F.; Suwita, A. Weitere phloroglucin-derivate aus Helichrysum-arten. Phytochemistry 1979, 18, 2046–2049. [Google Scholar] [CrossRef]
  80. Bohlmann, F.; Zdero, C.; Ziesche, J. Neue flavone und phloroglucin-derivate aus Helichrysum herbaceum und Helichrysum chrysargyrum. Phytochemistry 1979, 18, 1375–1378. [Google Scholar] [CrossRef]
  81. Bohlmann, F.; Zdero, C. Neue geranylphloroglucin-derivate aus Helichrysum monticola. Phytochemistry 1980, 19, 683–684. [Google Scholar] [CrossRef]
  82. Wang, L.-B.; Liu, F.-Z.; Gan, C.-L.; Dong, N.-W.; Hou, Y.-L.; Wang, C. Isolation and identification of chemical constituents in the lipid-lowering fraction of Flos Helichrysum arenarium(Ⅱ). J. Shenyang Pharm. Univ. 2012, 109–112, 125. [Google Scholar]
  83. Vrkoč, J.; Herout, V.; Šorm, F. Über pflanzenstoffe X. Isolierung der kristallinen bestandteile der sandstrohblume (Helichrysum arenarium MCH). Collect. Czechoslov. Chem. Commun. 1959, 24, 3938–3954. [Google Scholar] [CrossRef]
  84. Kurkina, A.V.; Ryzhov, V.M.; Avdeeva, E.V. Assay of isosalipurposide in raw material and drugs from the dwarf everlast (Helichrysum arenarium). Pharm. Chem. J. 2012, 46, 171–176. [Google Scholar] [CrossRef]
  85. Vrkoč, J.; Buděšínský, M.; Dolejš, L.; Vašíčková, S. Arenophthalide A: A new phthalide glycoside from Helichrysum arenarium roots. Phytochemistry 1975, 14, 1845–1848. [Google Scholar] [CrossRef]
  86. Babotă, M.; Mocan, A.; Vlase, L.; Crișan, O.; Ielciu, I.; Gheldiu, A.-M.; Vodnar, D.C.; Crișan, G.; Păltinean, R. Phytochemical Analysis, Antioxidant and Antimicrobial Activities of Helichrysum arenarium (L.) Moench. and Antennaria dioica (L.) Gaertn. Flowers. Molecules 2018, 23, 409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Albayrak, S.; Aksoy, A.; Sağdiç, O.; Budak, Ü. Phenolic compounds and antioxidant and antimicrobial properties of Helichrysum species collected from eastern Anatolia, Turkey. Turk. J. Biol. 2010, 34, 463–473. [Google Scholar] [CrossRef]
  88. Morikawa, T.; Wang, L.-B.; Ninomiya, K.; Nakamura, S.; Matsuda, H.; Muraoka, O.; Wu, L.-J.; Yoshikawa, M. Medicinal Flowers. XXX. Eight New Glycosides, Everlastosides F—M, from the Flowers of Helichrysum arenarium. Chem. Pharm. Bull. (Tokyo) 2009, 57, 853–859. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Yong, F.; Aisa, H.A.; Mukhamatkhanova, R.F.; Shamyanov, I.D.; Levkovich, M.G. New flavanone and other constituents of Helichrysum arenarium indigenous to China. Chem. Nat. Compd. 2011, 46, 872–875. [Google Scholar] [CrossRef]
  90. Jakupovic, J.; Pathak, V.P.; Bohlmann, F.; King, R.M.; Robinson, H. Obliquin derivatives and other constituents from Australian Helichrysum species. Phytochemistry 1987, 26, 803–807. [Google Scholar] [CrossRef]
  91. Pereira, C.G.; Barreira, L.; Bijttebier, S.; Pieters, L.; Neves, V.; Rodrigues, M.J.; Rivas, R.; Varela, J.; Custódio, L. Chemical profiling of infusions and decoctions of Helichrysum italicum subsp. picardii by UHPLC-PDA-MS and in vitro biological activities comparatively with green tea (Camellia sinensis) and rooibos tisane (Aspalathus linearis). J. Pharm. Biomed. Anal. 2017, 145, 593–603. [Google Scholar] [CrossRef]
  92. Zhang, F.; Su, R.-N.; Wu, H.-B.; Wang, W.-S. Jacaranone Derivatives from Senecio laetus (Compositae). Plant Divers. 2013, 35, 501–504. [Google Scholar] [CrossRef]
  93. de Gomes, K.S.; Tamayose, C.I.; Ferreira, M.J.P.; Murakami, C.; Young, M.C.M.; Antar, G.M.; Camilo, F.F.; Sartorelli, P.; Lago, J.H.G.; de Gomes, K.S.; et al. Isolation of antifungal quinoid derivatives from leaves of Pentacalia desiderabilis (Vell.) Cuatre. (Asteraceae) using ionic liquid in the microwave assisted extraction. Quím. Nova 2019, 42, 156–158. [Google Scholar] [CrossRef]
  94. Jakupovic, J.; Schuster, A.; Sun, H.; Bohlmann, F.; Bhakuni, D.S. Prenylated phthalides from Anaphalis araneosa and Helichrysum platypterum. Phytochemistry 1987, 26, 580–581. [Google Scholar] [CrossRef]
  95. Yang, Y.-N.; Huang, X.-Y.; Feng, Z.-M.; Jiang, J.-S.; Zhang, P.-C. Hepatoprotective Activity of Twelve Novel 7′-Hydroxy Lignan Glucosides from Arctii Fructus. J. Agric. Food Chem. 2014, 62, 9095–9102. [Google Scholar] [CrossRef]
  96. Ruan, J.; Li, Z.; Yan, J.; Huang, P.; Yu, H.; Han, L.; Zhang, Y.; Wang, T. Bioactive Constituents from the Aerial Parts of Pluchea indica Less. Molecules 2018, 23, 2104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Wang, H.; Du, H.-B.; Zhu, F.-Y.; Shang, J.; Silafu, A. Chemical constituents from Artemisia rupestris L. J. China Pharm. Univ. 2011, 42, 310–313. [Google Scholar]
  98. Hänsel, R.; Rimpler, H.; Schwarz, R. Erstmaliger nachweis eines auronols (aroylcumaranons) im pflanzenreich. Tetrahedron Lett. 1965, 6, 1545–1548. [Google Scholar] [CrossRef]
  99. Li, X.; Gao, P.; Gjetvaj, B.; Westcott, N.; Gruber, M.Y. Analysis of the metabolome and transcriptome of Brassica carinata seedlings after lithium chloride exposure. Plant Sci. 2009, 177, 68–80. [Google Scholar] [CrossRef]
  100. Granica, S.; Lohwasser, U.; Jöhrer, K.; Zidorn, C. Qualitative and quantitative analyses of secondary metabolites in aerial and subaerial of Scorzonera hispanica L. (black salsify). Food Chem. 2015, 173, 321–331. [Google Scholar] [CrossRef] [PubMed]
  101. Powell, R.G.; Smith, C.R.; Wolff, I.A. Helichrysum seed oil. I. Separation and characterization of individual acids. J. Am. Oil Chem. Soc. 1965, 42, 165–169. [Google Scholar] [CrossRef]
  102. Gouveia, S.C.; Castilho, P.C. Characterization of phenolic compounds in Helichrysum melaleucum by high-performance liquid chromatography with on-line ultraviolet and mass spectrometry detection. Rapid Commun. Mass Spectrom. RCM 2010, 24, 1851–1868. [Google Scholar] [CrossRef]
  103. Meusel, I.; Neinhuis, C.; Markstädter, C.; Barthlott, W. Chemical Composition and Recrystallization of Epicuticular Waxes: Coiled Rodlets and Tubules. Plant Biol. 2000, 2, 462–470. [Google Scholar] [CrossRef]
  104. Popoola, O.K.; Marnewick, J.L.; Rautenbach, F.; Iwuoha, E.I.; Hussein, A.A. Acylphloroglucinol Derivatives from the South African Helichrysum niveum and Their Biological Activities. Mol. Basel Switz. 2015, 20, 17309–17324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Liu, H.; He, H.; Yang, X.; Chen, M.; Hao, X. Chemical Constituents of the Flowers of Helichrysum bracteatum. Nat. Prod. Res. Dev. 2007, 19, 423–426. [Google Scholar]
  106. Bohlmann, F.; Mahanta, P.K.; Zdero, C. Neue chalkon-derivate aus südafrikanischen Helichrysum-arten. Phytochemistry 1978, 17, 1935–1937. [Google Scholar] [CrossRef]
  107. han Çubukcu, B. Helichrysum Species as Choleretic and Cholagogue Crude Drugs. ACTA Pharm. Sci. 2002, 44, 144–150. [Google Scholar]
  108. Bigović, D.; Šavikin, K.; Janković, T.; Menković, N.; Zdunić, G.; Stanojković, T.; Djurić, Z. Antiradical and Cytotoxic Activity of Different Helichrysum plicatum Flower Extracts. Nat. Prod. Commun. 2011, 6, 1934578X1100600617. [Google Scholar] [CrossRef] [Green Version]
  109. Appendino, G.; Ottino, M.; Marquez, N.; Bianchi, F.; Giana, A.; Ballero, M.; Sterner, O.; Fiebich, B.L.; Munoz, E. Arzanol, an Anti-inflammatory and Anti-HIV-1 Phloroglucinol α-Pyrone from Helichrysum italicum ssp. microphyllum. J. Nat. Prod. 2007, 70, 608–612. [Google Scholar] [CrossRef]
  110. Rosa, A.; Deiana, M.; Atzeri, A.; Corona, G.; Incani, A.; Melis, M.P.; Appendino, G.; Dessì, M.A. Evaluation of the antioxidant and cytotoxic activity of arzanol, a prenylated α-pyrone–phloroglucinol etherodimer from Helichrysum italicum subsp. microphyllum. Chem. Biol. Interact. 2007, 165, 117–126. [Google Scholar] [CrossRef]
  111. Kothavade, P.S.; Nagmoti, D.M.; Bulani, V.D.; Juvekar, A.R. Arzanol, a Potent mPGES-1 Inhibitor: Novel Anti-Inflammatory Agent. Sci. World J. 2013, 2013, 1–9. [Google Scholar] [CrossRef] [Green Version]
  112. Czinner, E.; Kéry, Á.; Hagymási, K.; Blázovics, A.; Lugasi, A.; Szõke, É.; Lemberkovics, É. Biologically active compounds of Helichrysum arenarium (L.) Moench. Eur. J. Drug Metab. Pharm. 1999, 24, 309–313. [Google Scholar] [CrossRef]
  113. Czinner, E.; Hagymási, K.; Blázovics, A.; Kéry, A.; Szoke, E.; Lemberkovics, E. In vitro antioxidant properties of Helichrysum arenarium (L.) Moench. J. Ethnopharmacol. 2000, 73, 437–443. [Google Scholar] [CrossRef]
  114. Malolo, F.-A.E.; Bissoue Nouga, A.; Kakam, A.; Franke, K.; Ngah, L.; Flausino, O.; Mpondo Mpondo, E.; Ntie-Kang, F.; Ndom, J.C.; da Bolzani, V.S.; et al. Protease-inhibiting, molecular modeling and antimicrobial activities of extracts and constituents from Helichrysum foetidum and Helichrysum mechowianum (Compositae). Chem. Cent. J. 2015, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  115. Iniesta-Sanmartín, E.; Tomás-Barberán, F.A.; Guirado, A.; Tomás-Lorente, F. Antibacterial Flavonoids from Helichrysum picardii and H. italicum. Planta Med. 1990, 56, 648–649. [Google Scholar] [CrossRef]
  116. Legoalea, P.B.; Mashimbyeb, M.J.; van Rec, T. Antiinflammatory and antioxidant flavonoids from Helichrysum kraussii and H. odoratissimum flowers. Nat. Prod. Commun. 2013, 8, 1403–1404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Pietta, P.-G. Flavonoids as Antioxidants. J. Nat. Prod. 2000, 63, 1035–1042. [Google Scholar] [CrossRef] [PubMed]
  118. Chandrasekara, A. Phenolic Acids. In Encyclopedia of Food Chemistry; Melton, L., Shahidi, F., Varelis, P., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 535–545. [Google Scholar] [CrossRef]
  119. Kadifkova Panovska, T.; Kulevanova, S. Antioxidant potential of Helichrysum plicatum DC. (Asteraceae). Maced. Pharm. Bull. 2005, 51, 29–34. [Google Scholar] [CrossRef]
  120. Acet, T.; Ozcan, K.; Zengin, G. An assessment of phenolic profiles, fatty acid compositions, and biological activities of two Helichrysum species: H. plicatum and H. chionophilum. J. Food Biochem. 2019, 44, e13128. [Google Scholar] [CrossRef]
  121. Rosa, A.; Pollastro, F.; Atzeri, A.; Appendino, G.; Melis, M.P.; Deiana, M.; Incani, A.; Loru, D.; Dessì, M.A. Protective role of arzanol against lipid peroxidation in biological systems. Chem. Phys. Lipids 2011, 164, 24–32. [Google Scholar] [CrossRef]
  122. Demir, A.; Taban, B.M.; Aslan, M.; Yesilada, E.; Aytac, S.A. Antimicrobial effect of Helichrysum plicatum subsp. plicatum. Pharm. Biol. 2009, 47, 289–297. [Google Scholar] [CrossRef]
  123. Daglia, M. Polyphenols as antimicrobial agents. Curr. Opin. Biotechnol. 2012, 23, 174–181. [Google Scholar] [CrossRef]
  124. Almada-Ruiz, E.; Martínez-Téllez, M.Á.; Hernández-Álamos, M.M.; Vallejo, S.; Primo-Yúfera, E.; Vargas-Arispuro, I. Fungicidal potential of methoxylated flavones from citrus for in vitro control of Colletotrichum gloeosporioides, causal agent of anthracnose disease in tropical fruits. Pest Manag. Sci. 2003, 59, 1245–1249. [Google Scholar] [CrossRef] [PubMed]
  125. Ortuño, A.; Báidez, A.; Gómez, P.; Arcas, M.C.; Porras, I.; García-Lidón, A.; Río, J.A.D. Citrus paradisi and Citrus sinensis flavonoids: Their influence in the defence mechanism against Penicillium digitatum. Food Chem. 2006, 98, 351–358. [Google Scholar] [CrossRef]
  126. Berim, A.; Gang, D.R. Methoxylated flavones: Occurrence, importance, biosynthesis. Phytochem. Rev. 2016, 15, 363–390. [Google Scholar] [CrossRef]
  127. Nostro, A.; Germanò, M.P.; D’Angelo, V.; Marino, A.; Cannatelli, M.A. Extraction methods and bioautography for evaluation of medicinal plant antimicrobial activity. Lett. Appl. Microbiol. 2000, 30, 379–384. [Google Scholar] [CrossRef]
  128. Blois, M.S. Antioxidant Determinations by the Use of a Stable Free Radical. Nature 1958, 181, 1199–1200. [Google Scholar] [CrossRef]
  129. National Committee for Clinical Laboratory Standards, 5th ed.; Methods for Dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standards. NCCLS document M7-A5; NCCLS: Wayne, PA, USA, 2000.
  130. Novaković, M.; Novaković, I.; Cvetković, M.; Sladić, D.; Tešević, V. Antimicrobial activity of the diarylheptanoids from the black and green alder. Braz. J. Bot. 2015, 38, 441–446. [Google Scholar] [CrossRef]
Plants 09 00337 g001 550
Figure 1. Phenolic representatives of H. plicatum: (a) naringenin (flavanone), (b) isosalipurposide (chalcone), (c) chlorogenic acid (phenolic acid ester), (d) 5,7-dihydroxyphthalide (phthalide), (e) plicatipyrone (chromanyl α-pyrone).
Figure 1. Phenolic representatives of H. plicatum: (a) naringenin (flavanone), (b) isosalipurposide (chalcone), (c) chlorogenic acid (phenolic acid ester), (d) 5,7-dihydroxyphthalide (phthalide), (e) plicatipyrone (chromanyl α-pyrone).
Plants 09 00337 g001
Plants 09 00337 g002 550
Figure 2. Structures of arzanol (left) and methylarzanol (right).
Figure 2. Structures of arzanol (left) and methylarzanol (right).
Plants 09 00337 g002
Table
Table 1. Composition of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract analysed by HPLC-DAD/ESI-ToF.
Table 1. Composition of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract analysed by HPLC-DAD/ESI-ToF.
NoCompound Class/NameEEDCMEACNE
Pyrone
α-pyrone
16-ethyl-4-hydroxy-5-methyl-3-(3-oxopentyl)-2H-pyran-2-one [22] +
2micropyrone [23] +
3micropyrone analog [19] +
4helipyrone C [20]+++
5bisnorhelipyrone [21] +
6plicatipyrone analog [22]+
73,3’-methylenebis[4-(acetyloxy)-5,6-dimethyl-2H-pyran-2-one [21] +
8helipyrone B [20] +
93-[[3-acetyl-2,4,6-trihydroxy-5-(3-methyl-2-buten-1-yl)phenyl]methyl]-4-hydroxy-6-methyl-2H-pyran-2-one [19] +
10plicatipyrone [22]+++
11arenol [23]+++
12plicatipyrone analog [22]+
13arzanol [27]+++
14heliarzanol [23]+ +
15cycloarzanol [23]+
16helipyrone diacetate [25]++
17methylarzanol [23]+ +
183-[1-[3-acetyl-2,4,6-trihydroxy-5-(3-methyl-2-buten-1-yl)phenyl]ethyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [23]+ +
19auricepyrone [22], 23-methyl-6-O-desmethylauricepyrone [22] +
20helicerastripyrone [28] +
214-hydroxy-5,6-dimethyl-3-[[2,4,6-trihydroxy-3-(3-methyl-2-buten-1-yl)-5-(2-methyl-1-oxobutyl)phenyl]methyl]-2H-pyran-2-one [24]+
223-[[3-acetyl-5-(3,7-dimethyl-2,6-octadien-1-yl)-2,4,6-trihydroxyphenyl]methyl]-4-hydroxy-5,6-dimethyl-2H-pyran-2-one [29]+
23plicatipyrone analog [26]++
246-ethyl-4-hydroxy-5-methyl-3-[[2,4,6-trihydroxy-3-(3-methyl-2-buten-1-yl)-5-(2-methyl-1-oxopropyl)phenyl]methyl]-2H-pyran-2-one [23]+ +
25norauricepyrone [24] +
263-[[2,4-dihydroxy-6-methoxy-3-(2-methyl-1-oxobutyl)phenyl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [30] +
273-[1-[3-acetyl-2,4,6-trihydroxy-5-(3-methyl-2-buten-1-yl)phenyl]heptyl]-4-hydroxy-6-methyl-2H-pyran-2-one [23], 3-[[2,4-dihydroxy-6-methoxy-5-(3-methyl-2-buten-1-yl)-3-(2-methyl-1-oxobutyl)phenyl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [30], 3-[[2,4-dihydroxy-6-methoxy-3-(3-methyl-2-buten-1-yl)-5-(2-methyl-1-oxobutyl)phenyl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [22]+ +
283-[[3-acetyl-5-(3,7-dimethyl-2,6-octadienyl)-2,4,6-trihydroxyphenyl]methyl]-4-hydroxy-5-methyl-6-propyl-2H-pyran-2-one [29], 3-[[3-(3,7-dimethyl-2,6-octadien-1-yl)-2,4,6-trihydroxy-5-(2-methyl-1-oxopropyl)phenyl]methyl]-4-hydroxy-5,6-dimethyl-2H-pyran-2-one [24]+
293-[[3-(3,7-dimethyl-2,6-octadien-1-yl)-2,4,6-trihydroxy-5-(2-methyl-1-oxobutyl)phenyl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [24] +
303-[[3,7-dimethyl-2,6-octadien-1-yl]-2,4,6-trihydroxy-5-(2-methyl-1-oxobutyl)phenyl]methyl]-4-hydroxy-5,6-dimethyl-2H-pyran-2-one [24]+ +
313-[[2,3-dihydro-4,6-dihydroxy-2-(1-methylethenyl)-5-(2-methyl-1-oxobutyl)-7-benzofuranyl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [30], 3-[[5,7-dihydroxy-2,2-dimethyl-6-(2-methyl-1-oxobutyl)-2H-1-benzopyran-8-yl]methyl]-6-ethyl-4-hydroxy-5-methyl-2H-pyran-2-one [30] +
α-pyrone (coumarin)
322’,3’-dihydroxypuberulin [31] +
337-(2,3-dihydroxy-3-methylbutoxy)-5-hydroxy-6-methoxy-2H-1-benzopyran-2-one [32]++
34coumarin derivative [33,34] +
357-(2,3-dihydroxy-3-methylbutoxy)-5,6-dimethoxy-2H-1-benzopyran-2-one [35] +
362,3-dihydro-10-methoxy-2-(1-methylethenyl)-7H-pyrano[2,3-g]-1,4-benzodioxin-7-one [36] +
γ-pyrone
372-methoxy-3,5-dimethyl-6-(1-methylethyl)-4H-pyran-4-one [30] +
383-[[2,4-dihydroxy-6-methoxy-3-(3-methyl-2-buten-1-yl)-5-(2-methyl-1-oxobutyl)phenyl]methyl]-6-ethyl-2-methoxy-5-methyl-4H-pyran-4-one [37] +
39italipyrone [22] +
40italipyrone analog [22] +
γ-pyrone (chromone)
413-(acetyloxy)-2,3-dihydro-5,7-dihydroxy-6-(3-methyl-2-butenyl)-2-phenyl-4H-1-benzopyran-4-one [38] +
422,3-dihydro-5,7-dihydroxy-3-methyl-8-(3-methyl-2-butenyl)-2-(1-methylethyl)-4H-1-benzopyran-4-one [39]+
Flavonoid
flavone
43apigenin-7-O-glucoside [4]+
44apigenin-5-O-glucoside [40]+
45luteolin [41]+
463,5,6,7,8-pentamethoxyflavone [42] +
473’,4’,5,6,7-pentamethoxyflavone [43] +
48apigenin [40]+
49dihydroxy-dimethoxyflavone [44] +
50jaceosidin [45] +
51chrysoeriol [45] +
525,7-dihydroxy-3-methoxyflavone [44] +
535,7,4’-trihydroxy-3,6-dimethoxy-3’-prenylflavone [46] +
54TEDMF 1 [43] +
55TEDMF [43] +
566-[(6-ethyl-4-hydroxy-5-methyl-2-oxo-2H-pyran-3-yl)methyl]-2,3-dihydro-5,7-dihydroxy-8-(3-methyl-2-buten-1-yl)-2-phenyl-4H-1-benzopyran-4-one [47] +
57TEDMF [43] +
flavanone
58naringenin-5-O-glucoside [40]+
59naringenin-4′-O-glucoside [48]+
60naringenin-7-O-glucoside [40]+
61eriodictyol [49]+
62naringenin [40]++
flavonol
63quercetin-3-O-glucoside [4], hyperoside (quercetin-3-O-galactoside) [4]+
64kaempferol-3-O-glucoside [50]+
65helichrysoside [51]+
66quercetin [40]+ +
67tiliroside [52]+
68tiliroside analog [52]+
69kaempferol [41]+
chalcone
70arenariumoside V [53], arenariumoside VI [53], arenariumoside VII [53]+
71tomoroside A [53]+
72isosalipurposide [40]+
73helilupolone [54]+
Terpenoid
sesquiterpenoid
74sesquiterpene derivative [55,56,57] +
75sesquiterpene derivative [55,56,57] +
76sesquiterpene derivative [58,59,60] +
77sesquiterpene derivative [61,62] +
78sesquiterpene derivative [62,63,64] +
79eudesmane derivative [65] +
80sesquiterpene derivative [66,67,68] +
81sesquiterpene derivative [66,67,68] +
82ainsliaside E [69]+
83cinnamoyloxy-hydroxyeudesmane [70] +
84athrolide C [71] ++
85athrolide D [71] +
diterpenoid
86diterpene derivative [30,72] +
878-(acetyloxy)-3-ethenyloctahydro-10-hydroxy-3,4a,7,7,10a-pentamethyl-1H-naphtho[2,1-b]pyran-2,5(3H,4aH)-dione [72] +
88(7-ethenyl-1,2,3,4,4a,4b,5,6,7,8,10,10a-dodecahydro-1,4a,7-trimethyl-1-phenanthrenyl)methyl-butanedioic acid methyl ester [72] +
89ent-kaurane derivative [73] +
90gymnospermin [74]+
91diterpene derivative [75,76,77] +
92ent-kaurane derivative [73] +
935-(acetyloxy)-α-ethenyldecahydro-α,3a,5,7b-tetramethyl-1H-cyclopropa[a]naphthalene-4-propanol acetate [78] +
94ent-kaurane derivative [73]++
Phloroglucinol
954-[3,5-dihydroxy-4-(1-oxobutyl)phenoxy]-2-methyl-butanoic acid [47], 4-[3,5-dihydroxy-4-(2-methyl-1-oxopropyl)phenoxy]-2-methyl-butanoic acid [47], 1-[2,6-dihydroxy-4-[[4-hydroxy-3-(hydroxymethyl)-2-buten-1-yl]oxy]phenyl]-1-butanone [47] +
962,3-dihydro-4,5-dimethoxy-2,2-dimethyl-6-benzofuranol [79] +
974,5-dimethoxy-6-(2-methyl-1-propen-1-yl)-1,3-benzenediol-1,3-diacetate [79] +
981-(4,6-dihydroxy-2,3-dimethoxyphenyl)-2-methyl-1-butanone [43,79,80] +
994-[3,5-dihydroxy-4-(2-methyl-1-oxopropyl)phenoxy]-2-methyl-2-butenoic acid methyl ester [47] +
100acylphloroglucinol derivative [47]++
1012-methyl-1-[2,4,6-trihydroxy-3-(3-methyl-2-buten-1-yl)phenyl]-1-propanone [47], 1-[2,6-dihydroxy-4-[(3-methyl-2-buten-1-yl)oxy]phenyl]-2-methyl-1-propanone [47], 1-[2,6-dihydroxy-4-[(3-methyl-2-buten-1-yl)oxy]phenyl]-1-butanone [47], 1-[2,4,6-trihydroxy-3-(3-methyl-2-buten-1-yl)phenyl]-1-butanone [47], 1-(3,4-dihydro-5,7-dihydroxy-2,2-dimethyl-2H-1-benzopyran-6-yl)-2-methyl-1-propanone [30] +
102[3,4-dihydro-5,7-dihydroxy-2-(4-methyl-3-penten-1-yl)-2H-1-benzopyran-6-yl]phenyl-methanone [81]++
1032-(3,7-dimethyl-2,6-octadienyl)-3-hydroxy-5-methoxy-6-(2-methyl-1-oxopropyl)-2,5-cyclohexadiene-1,4-dione [30] +
104phenyl[2,4,6-trihydroxy-3-(3-methyl-2-buten-1-yl)phenyl]-methanone [47], [2,6-dihydroxy-4-[(3-methyl-2-buten-1-yl)oxy]phenyl]phenyl-methanone [47]+
1051-[2,3-dihydro-4,6-dihydroxy-2-(1-methylethenyl)-5-benzofuranyl]-2-methyl-1-propanone [30] +
1067-acetyl-5’-ethyl-4,6-dihydroxy-4’-methyl-5-(3-methyl-2-buten-1-yl)-spiro[benzofuran-2(3H),2’(3’H)-furan]-3’-one [24]++
1071-[2,6-bis(acetyloxy)-4-[[4-(acetyloxy)-3-[(acetyloxy)methyl]-2-buten-1-yl]oxy]phenyl]-1-butanone [47]++
1084,6-dihydroxy-4’,5’-dimethyl-5-(3-methyl-2-buten-1-yl)-7-(2-methyl-1-oxobutyl)-spiro[benzofuran-2(3H),2’(3’H)-furan]-3’-one [24], 5’-ethyl-4,6-dihydroxy-4’-methyl-5-(3-methyl-2-buten-1-yl)-7-(2-methyl-1-oxopropyl)-spiro[benzofuran-2(3H),2’(3’H)-furan]-3’-one [24] +
1092-methyl-1-[2,4,6-trihydroxy-5-[(1S)-1-(4-hydroxy-6-methoxy-1,3-benzodioxol-5-yl)-2-methylpropyl]-3-(3-methyl-2-butenyl)phenyl]-1-propanone [30] +
Phthalide
1107-(β-D-glucopyranosyloxy)-5-hydroxy-1(3H)-isobenzofuranone [82]+
1115,7-dihydroxyphthalide [83]++
1127-(β-D-glucopyranosyloxy)-5-methoxy-phthalide [83]+
1135-methoxy-7-hydroxyphthalide [84]++
1144-(4-hydroxy-3-methylbutyl)-5,7-dimethoxy-1(3H)-isobenzofuranone [85] +
Phenolic acid (derivative)
115chlorogenic acid [86]+
116caffeic acid [87]+
117everlastoside M [88]+
118syringic acid [87]+
1193’,4’-methylenedioxycinnamic acid [89] +
120di-O-caffeoylquinic acid [4]+
121di-O-caffeoylquinic acid [4]+
1224-(3-methoxy-3-oxo-1-propen-1-yl)-2-(3-methyl-2-buten-1-yl)phenyl-3-(acetyloxy)-butanoic acid ester [90]+
Acetophenone
1234’-hydroxy-3’-(3-methyl-2-butenyl)-acetophenone [26] +
1241-[2-[1-[(acetyloxy)methyl]ethenyl]-2,3-dihydro-3-hydroxy-5-benzofuranyl]ethanone [51] ++
Other
125inositol [83]+
126quinic acid [91]+
1271,6-dihydroxy-4-oxo-2-cyclohexene-1-acetic acid methyl ester [92] +
128tetrahydrojacarone [93] +
129loliolide [94] +
1302-[4-(1,3-dihydroxypropyl)-2-methoxyphenoxy]-3-hydroxy-1-(4-hydroxy-3-methoxyphenyl)-1-propanone [95] +
131pinellic acid [96], tianshic acid [97]++
132(3,4,5,6,7-pentamethoxy-2-benzofuranyl)phenylmethanone [98] +
133PUFA 2 [99,100,101]+
134pinoresinol [102]+
135PUFA [99,100,101] +
136dihydro-5-(5,8-tetradecadienyl)-2(3H)-furanone [47] +
137PUFA [99,100,101]++
138hexadecanal [103] +
Unclassified3
1394-hydroxy-3,5-dimethyl-6-(1-methylethyl)-2H-pyran-2-one [30], 2-ethyl-6-methoxy-3,5-dimethyl-4H-pyran-4-one [28] +
1403-prenyl-2,4,6-trihydroxyacetophenone [30], 4,6-dimethoxy-5-(2-methyl-1-propen-1-yl)-1,3-benzodioxole [80]+ +
141helinivene A [104], piperitol [105], 1-[6-(acetyloxy)-2,3,4-trimethoxyphenyl]-3-phenyl- 2-propen-1-one [106]+
142ent-kaurane derivative [73], eudesmane derivative [65] +
1 triethoxy-dimethoxy-flavone; 2 polyunsaturated fatty acid; 3 presumed compounds for one formula which belongs to different classes are listed as unclassified.
Table
Table 2. DPPH free radical scavenging activities of H. plicatum ethanol (EE), dichloromethane (DCME), acetonitrile oil (ACNE), and oil extracts (OE); BHT—butylated hydroxytoluene.
Table 2. DPPH free radical scavenging activities of H. plicatum ethanol (EE), dichloromethane (DCME), acetonitrile oil (ACNE), and oil extracts (OE); BHT—butylated hydroxytoluene.
EEDCMEACNEOETroloxBHT (Methanol)BHT (Toluene)
EC50 1 (mg/mL)0.45 ± 0.040.58 ± 0.021.74 ± 0.0117.61 ± 0.160.064 ± 0.010.33 ± 0.011.42 ± 0.01
1 Data are presented as mean ± standard deviation (n = 3).
Table
Table 3. Antibacterial activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract against Gram-negative bacteria.
Table 3. Antibacterial activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract against Gram-negative bacteria.
Escherichia coliPseudomonas aeruginosaProteus hauseriKlebsiella pneumoniaeSalmonella enterica subsp. enterica
MICMBCMICMBCMICMBCMICMBCMICMBC
mg/mLmg/mLmg/mLmg/mLmg/mL
EE2.5>100.6252.52.5>101.2552.55
DCME0.3132.50.15710.6250.1570.6250.1570.6251.2510
ACNE0.6252.51.2551.2550.6251.251.255
Chloramphenicol0.062 0.25 0.125 0.062 0.125
1 MIC value lower than the control.
Table
Table 4. Antibacterial activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract against Gram-positive bacteria.
Table 4. Antibacterial activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract against Gram-positive bacteria.
Staphylococcus aureusBacillus subtilisClostridium sporogenes
MICMBCMICMBCMICMBC
mg/mLmg/mLmg/mL
EE0.3132.50.3131.252.510
DCME0.1570.6250.1570.6250.3131.25
ACNE0.62552.5102.510
Chloramphenicol0.015 0.015 0.25
Table
Table 5. Antifungal activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract.
Table 5. Antifungal activity of H. plicatum ethanol (EE), dichloromethane (DCME), and acetonitrile oil (ACNE) extract.
Aspergillus brasiliensisSaccharomyces cerevisiaeCandida albicans
MICMFCMICMFCMICMFC
mg/mLmg/mLmg/mL
EE1.251>101.25102.55
DCME0.6252.51.2551.252.5
ACNE1.25101.25102.55
Nystatin2.5 1.25 2.5
1 MIC values lower than the control are bolded.

Share and Cite

MDPI and ACS Style

Vujić, B.; Vidaković, V.; Jadranin, M.; Novaković, I.; Trifunović, S.; Tešević, V.; Mandić, B. Composition, Antioxidant Potential, and Antimicrobial Activity of Helichrysum plicatum DC. Various Extracts. Plants 2020, 9, 337. https://doi.org/10.3390/plants9030337

AMA Style

Vujić B, Vidaković V, Jadranin M, Novaković I, Trifunović S, Tešević V, Mandić B. Composition, Antioxidant Potential, and Antimicrobial Activity of Helichrysum plicatum DC. Various Extracts. Plants. 2020; 9(3):337. https://doi.org/10.3390/plants9030337

Chicago/Turabian Style

Vujić, Bojan, Vera Vidaković, Milka Jadranin, Irena Novaković, Snežana Trifunović, Vele Tešević, and Boris Mandić. 2020. "Composition, Antioxidant Potential, and Antimicrobial Activity of Helichrysum plicatum DC. Various Extracts" Plants 9, no. 3: 337. https://doi.org/10.3390/plants9030337

APA Style

Vujić, B., Vidaković, V., Jadranin, M., Novaković, I., Trifunović, S., Tešević, V., & Mandić, B. (2020). Composition, Antioxidant Potential, and Antimicrobial Activity of Helichrysum plicatum DC. Various Extracts. Plants, 9(3), 337. https://doi.org/10.3390/plants9030337

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop