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Article

Polyphenol Profile and Biological Activity Comparisons of Different Parts of Astragalus macrocephalus subsp. finitimus from Turkey

by
Cengiz Sarikurkcu
1 and
Gokhan Zengin
2,*
1
Department of Analytical Chemistry, Faculty of Pharmacy, Afyonkarahisar Health Sciences University, Afyonkarahisar 03030, Turkey
2
Department of Biology, Science Faculty, Selcuk University, Campus, Konya 42130, Turkey
*
Author to whom correspondence should be addressed.
Biology 2020, 9(8), 231; https://doi.org/10.3390/biology9080231
Submission received: 5 August 2020 / Accepted: 11 August 2020 / Published: 17 August 2020
(This article belongs to the Special Issue Bioactivity of Medicinal Plants and Extracts)
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Abstract

:
The members of the genus Astragalus have great interest as traditional drugs in several folk systems including Turkey. In this sense, the present paper was aimed to explore the biological properties and chemical profiles of different parts (aerial parts, leaves, flowers, stems, and roots) of A. macrocephalus subsp. finitimus. Antioxidant (radical quenching, reducing power, and metal chelating) and enzyme inhibitory (α-amylase and tyrosinase) effects were investigated for biological properties. Regarding chemical profiles, individual phenolic compounds were detected by LC-MS, as well as total amounts. The leaves extract exhibited the strongest antioxidant abilities when compared with other parts. However, flowers extract had the best metal chelating ability. Hyperoside, apigenin, p-coumaric, and ferulic acids were identified as main compounds in the tested parts. Regarding enzyme inhibitory properties, tyrosinase inhibitory effects varied from IC50: 1.02 to 1.41 mg/mL. In addition, the best amylase inhibition effect was observed by leaves (3.36 mg/mL), followed by aerial parts, roots, stems, and flowers. As a result, from multivariate analysis, the tested parts were classified in three cluster. Summing up the results, it can be concluded that A. macrocephalus subsp. finitimus could be a precious source of natural bioactive agents in pharmaceutical, nutraceutical, and cosmeceutical applications.

1. Introduction

Since the beginning of the last century, scientists have been focused on the biological and chemical properties of plants with ethnobotanical evidence [1,2,3]. From their studies, several important compounds have been introduced. As a springboard, the ethnobotanical records in ancient times indicated that Artemisia annua had great potential against malaria. In the light of this information, Japanese and Chinese scientist have isolated one sesquiterpene (artemisinin) from this plant to combat malaria, which they won the Nobel Prize for in 2015 [4,5]. In this sense, traditional and scientific data have to combine for further applications. Turkey has significant ethnobotanical data, with remarkable floristic features (about 12,000 plants) [6]. However, most of them have been scarcely investigated. Thus, the uninvestigated plants could be considered a treasure for pharmaceutical and medicinal applications.
In the last decade, plant secondary metabolites, especially phenolic compounds, have been gaining interest in the scientific platform. These compounds contain one or more hydroxyl groups and they have good hydrogen/electron donating abilities. Thus, these compounds are considered as main contributors to antioxidant properties. Additionally, these compounds have a broad spectrum of biological activities such as antimicrobial, anti-inflammatory, and anti-cancer [7,8].
The genus Astragalus is one of the biggest genera in the family Fabaceae and is represented by more than 2500 species [9]. The genus also contains 478 taxa in Turkey and it has many endemic species (202, endemism ratio: 42%) to Turkey [10]. Regarding folk medicinal uses, the genus is traditionally used for several purposes. For example, A. gumnifer and A. longifolius roots are used to treat diabetes mellitus [11]. Additionally, A. aureus and A. brachylcalyx are used against stomachache and sore throat [12]. In addition, A. lamarckii for ulcer [13]; A. cephalotes var. brevicalyx for wound healing [14] and A. tmoleus for abdominal pain and toothache [15]. From the light of these ethnobotanical records, several biological and chemical studies were performed on the members of the genus [16,17,18,19,20,21,22]. In the chemical studies, some biologically-active compounds, including hyperoside, apigenin, kaempferol, and naringenin, were detected [9]. However, to the authors best knowledge, very few publications can be found biological properties of Astragalus microcephalus [23,24,25]. A. microcephalus is a stout and erect perennial plant (50–100 cm). Leaves are lanceolate and narrowly elliptic. Inflorescence is 3.5–5 mm diameter and contains 30–50 sessile flowers. Calyx is 15–18 mm and tubular-campanulate. Corolla is 18–35 mm and deep yellow [26]. In the current work, we aimed to examine biological properties (antioxidant and enzyme inhibitory effect) and chemical composition (total and individual phenolic compounds) of different parts (aerial parts, leaves, flowers, stems and roots) of A. macrocephalus subsp. finitimus.

2. Materials and Methods

2.1. Plant Material and Solvent Extraction

Astragalus macrocephalus Willd. subsp. finitimus (Bunge) Chamberlein (Fabaceae) were collected from Sucati village, Gurun, Sivas-Turkey on 23 June, 2019 (1351 m, 38°43′15.06” N 37°21′43.22” E), authenticated by Olcay Ceylan, and deposited (AD-1518) at the Department of Biology, Mugla Sıtkı Koçman University (Mugla, Aegean, Turkey). The plant was collected in the flowering season and the aerial parts do not contain fruit and seeds. The plant was firstly divided into different parts (aerial parts (as mix leaves, flowers, and stems) roots, leaves, flowers, and stems). The plant materials were dried in a shaded and well-ventilated environment (about 10 days) and were powdered in a laboratory mill. After powdering process, the plant materials were used to obtain extracts in the same week.
The methanol extracts from different parts of A. macrocephalus subsp. finitimus were prepared by maceration for 24 h. Five grams of different parts (aerial parts, roots, leaves, flowers, and stems) were mixed with 100 mL of solvent (the ratio of solid/solvent: 1:20) and agitation was set to 150 rpm in dark environment at room temperature. All of the extracts were stored at +4 °C until analyzed after concentrating the methanol extracts under reduced pressure. Extraction yields were given in Table 1.

2.2. Total Flavonoid and Phenolic Contents

To obtain total level of phenolic (TPC) and flavonoid content (TFC) in the extracts, colorimetric assays were used as described in our previous paper [27]. Gallic acid (GAE) and quercetin (QE) were used as standards, respectively. Please see the Supplementary Materials for the details.

2.3. Liquid Chromatography–Electrospray Tandem Mass Spectrometry (LC–ESI–MS/MS) Analysis

To determine chemical compositions in the extracts, we used an Agilent Technologies 1260 Infinity liquid chromatography system (Santa Clara, CA, USA) hyphenated to a 6420 Triple Quad mass spectrometer on which a chromatographic separation on a Poroshell 120 EC-C18 (100 mm × 4.6 mm I.D., 2.7 μm) column [28]. All analytical and chromatographic details are given in the Supplementary Materials. The different analytes were identified by means of their retention times, mass spectra, and tandem mass spectra. Specifically, quantitative analyses were performed using a specific MRM transition for each analyte. Analytical parameters and chromatograms are given in supplemental materials (Table S1 and Figure S1).

2.4. Biological Activity

Antioxidant properties of these extracts were detected by several assays including DPPH radical [29] ABTS+ free radical scavenging [30], cupric ion (CUPRAC) and ferric ion (FRAP) reducing power [31,32], phosphomolybdenum method [33] and ferrous ion chelating [34]. The antioxidant properties were evaluated by IC50 values (the half inhibitory concentration). The IC50 values were calculated from the graph of percentage (ABTS+, DPPH and metal chelating) against the concentration of the extracts. IC50 values for other assays (reducing power and phosphomolybdenum) reflect that the concentration at which absorbance is 0.5. For this purpose, we used the graph of absorbance against the concentration of the extracts. Trolox (TE) and Ethylenediaminetetraacetic acid (disodium salt) (EDTA)) were used as positive controls. In addition, the results were expressed as equivalents of these standards.
The key enzymes inhibition activity of the extracts against tyrosinase, and α-amylase were measured using the protocols as published by [35]. The enzyme inhibition abilities were evaluated by IC50 values. IC50 values calculated as antioxidant assays and we used a graph between concentration and percentage of enzyme inhibition. Standard enzyme inhibitors (Kojic acid (KAE) for tyrosinase and acarbose (ACE) for α-amylase) were used as positive control and also, the results were expressed as equivalents of these standards. The details for experimental methods are given in the Supplementary Materials.

2.5. Statistical Analysis

Obtained results were given as mean ± standard deviation (SD) and the results were evaluated by ANOVA assay (with Tukey’s test, significant value: p < 0.05). Principal component analysis (PCA) and hierarchical clustered analysis (HCA) were applied to the experimental data under FactoMineR (Factor Analysis and Data Mining with R) package (R Core Team, Vienna, Austria). The antioxidant activities of the extracts were analyzed using various methods. As is well known, each of the antioxidant activity methods has a different mechanism of action on the extracts. Therefore, it is not possible to directly compare the results obtained with each other. Relative antioxidant capacity (RACI) index values were calculated to make the results comparable, and the correlation between the results obtained from each test and RACI values were presented separately [36]. The RACI values of the samples were determined for each test by dividing into standard deviation after subtracting these mean values from the raw data. Total RACI values were calculated by averaging the RACI values obtained from all antioxidant tests of the relevant sample (including phenolic and flavonoid).

3. Results and Discussion

3.1. Phytochemical Composition

The amounts of total phenolics and flavonoids in the tested extracts were affected by plant parts used. As shown in Table 1, the highest levels of phenolics and flavonoids were determined in the leaves extract (37.68 mg GAE/g and 39.23 mg QE/g). Flowers (6.96 mg GAE/g) and roots (6.03 mg QE/g) had the lowest level of total phenolics and flavonoids, respectively. Several studies reported different levels of these compounds in the members of the genus Astragalus [16,37,38,39]. Observed differences may be linked with geographical, environmental, and climatic conditions as well as plant parts [37,40,41,42]. In addition, recent studies indicated that the colorimetric methods had several drawbacks and these methods could not reflect accurate levels of these compounds in plant extracts [43,44]. Hence, chromatographic methods such as HPLC or LC-MS are required to provide certain data. In this context, the extracts were analyzed by LC-MS and the results are given in Table 2. Hyperoside, p-coumaric and ferulic acids and apigenin were identified as main compounds in the tested extracts. The level of hyperoside varied from 2.90 (in roots) to 1828.94 (in leaves) µg/g extract. The highest level of p-coumaric acid was detected in flowers extract with 146.78 µg/g extract. The main compounds in the extracts exhibited significant biological activities in earlier studies. For example, hyperoside is a main compound in the genus Hypericum and this compound exhibits promising biological abilities [45,46,47]. Additionally, similar properties were also reported for p-coumaric acid [48], apigenin [49] and ferulic acid [50,51]. From this point, observed biological activities of A. macrocephalus subsp. finitimus extracts might be linked to the presence of these compounds.

3.2. Antioxidant Properties

Oxidative stress is the main etiological factor for the progression of several chronic and degenerative diseases such as Alzheimer’s disease, cancer, and cardiovascular diseases. Thus, the balance between the production of free radicals and the endogenous antioxidant defense system plays a pivotal role in healthy physiological function [52]. At this point, we need to support the defense system with dietary antioxidants. Plants are the main sources of the dietary antioxidants and several studies have reported a negative association between the consumption of plants and the frequency of these diseases [53,54,55]. In the present study, to evaluate the antioxidant effects of A. macrocephalus subsp. finitumus extracts, several chemical methods were performed, and their results are shown in Table 3. We used IC50 values and standard equivalents (trolox (TE) and EDTA (EDTAE)) to express antioxidant abilities. Based on Table 3, the strongest antioxidant abilities were detected in leaves extracts. For example, the lowest IC50 values were detected in the leaves extract for radical scavenging (ABTS and DPPH) and to reduce power (FRAP, CUPRAC and phosphomolybdenum). Observed antioxidant effects for leaves extract could be explained with the high level of phenolics and we obtained a good correlation between these parameters Table 4. In accordance with our findings, several researchers reported a positive correlation between total phenolic content and antioxidant properties. Interestingly, the metal chelating abilities of the tested extracts can be ranked as flowers>stems>roots>aerial parts>leaves. In addition, a negative relationship was observed between total bioactive compounds (phenolics and flavonoids) and metal chelating ability. Taken together, we could imply that observed findings could be linked with the presence of non-phenolic chelators such as peptides, polysaccharides, and ascorbic acid. In earlier studies, several authors reported antioxidant properties of some Astagalus species such as A. ponticus [16], A. lagurus [56], A. spruneri [57], A. membranaceus [58,59]. With this in mind, the members of the genus Astragalus could be considered as valuable sources of natural antioxidants.
Several researchers suggested that only one method is not enough to evaluate antioxidant abilities of plant extracts and thus, multiple methods including different mechanisms are required to obtain a full antioxidant picture. [52,60]. However, different expression methods have been observed in these different methods. With this fact, any comparison between results might be unreasonable and sometimes impossible. Thus, relative antioxidant capacity index (RACI) has been developed by some researchers to obtain an accurate comparison between studies [36,61]. In the present study, we calculated the relative antioxidant capacity index for each part in Figure 1 and each method in Figure 2. Clearly, among the tested plant parts, the leaves had the strongest antioxidant ability, followed by aerial parts, stems, flowers and, roots. As shown in Figure 2, with one exception (metal chelation), the leaves exhibited the best ability in the methods performed. This fact also was confirmed by correlation analysis. The contradictory results from metal chelating assays might be explained with the presence of non-phenolic chelators such as polysaccharides, peptides, and sulphates. This approach was observed in earlier studies [62,63].

3.3. Inhibitory Effects on Amylase and Tyrosinase

Enzyme inhibition theory is one of the most important strategies to combat global health problems including Alzheimer’s disease and diabetes. In theory, some enzymes are targets to alleviate observed symptoms in the diseases [64]. For example, amylase is one of the main enzymes in the carbohydrate catabolism and it hydrolyzes α (1,4) glycosidic bonds in the starch. Thus, the inhibition of amylase can control the postprandial blood glucose level [65]. Additionally, tyrosinase is a key enzyme in the synthesis of melanin and its inhibition can reduce the symptoms of hyperpigmentation problems [66]. Thus, several compounds (acarbose for amylase and kojic acid for tyrosinase) have been developed as enzyme inhibitors in pharmaceutical industries. However, most of them have serious side effects such as gastrointestinal disorders and toxicity [67,68,69]. In this sense, natural substances prefer as enzyme inhibitors against synthetic ones.
Amylase and tyrosinase inhibition of A. macrocephalus subsp. finitimus extracts were investigated and the results are reported in Table 5. Similar to antioxidant assays results, the best inhibitory ability was detected in leaves extract (IC50: 3.36 mg/mL for amylase and 1.02 mg/mL for tyrosinase). In addition, the flowers exhibited the weakest inhibitory activities (IC50: 4.94 mg/mL for amylase and 1.41 mg/mL for tyrosinase). The findings could be related with chemical profiles of the tested extracts and some compounds in extracts such as hyperoside [70,71], ferulic acid [72,73], and apigenin [74,75] have been reported as inhibitory agents in earlier studies. A moderate positive correlation was also observed between total phenolic content and the enzyme inhibitory abilities Table 4. As far as we know, no information on the enzyme inhibitory effect of A. macrocephalus is present. Therefore, our results could provide new information on the biological activity poof for the genus Astragalus. At this point, A. microcephalus could be considered as a valuable source of natural enzyme inhibitors to combat global health problems including diabetes mellitus and skin disorders.

3.4. Principal Component Analysis

Unsupervised principal component analysis and hierarchical clustered analysis were applied to assess the connections between plant parts used on their biological activities. The outcomes are shown in Figure 3. With the percentage of variance of 79.1 and 9% respectively; the first two dimensions that represented a cumulative percentage of 88.1% of variance, seemed sufficient to cover the most information in the dataset. The main dominant biological activities of PC1 were FRAP, DPPH, CUPRAC, Ferrous ion chelating and phosphomolydbdenum while PC2 was dominated by alpha amylase inhibition Figure 3A. Regarding the loading plot, it can be seen that many biological activities were linked with each other Figure 3B. In fact, the greatest positive correlation occurred among tyrosinase and antioxidant properties. The existence of an interesting relationship between antioxidant defense systems and melanogenesis is well documented [76]. In fact, by reacting with toxic ROS result in the restriction of radical chain propagation, eventually preventing the skin from damage. Besides, the cytoprotective antioxidants can be increased by antioxidant molecules thanks to the nuclear accumulation of Nrf2, which is a main transcription factor for the oxidative stress regulation in human skin tissues such as melanocyte, keratinocytes, and dermal fibroblasts [76].
Further, it can be noted the involvement of polyphenols namely hyperoside, (−)-epicatechin, caffeic acid and 2,5 dihydroxybenzoic acid in these activities. Caffeic acid, an important members of hydroxycinnamic acid, (−)-epicatechin and 2,5 dihydroxybenzoic acid are reported to be a good antioxidant with an excellent tyrosinase inhibition properties [77,78,79,80]. In fact, the assays performed on the B16 melanoma cell line showed that caffeic acid can inhibit melanin production by suppressing casein kinase 2 induced phosphorylation of tyrosinase in dose dependent [81]. In addition, a flavanol glycoside, hyperoside is found to be a useful therapeutic agent in the vitiligo management and in the prevention of the oxidative stress induced by reactive oxygen species [82,83]. Regarding the ferrous ion chelating ability it might be predominantly related to the presence of syringic acid, 4-hydroxybenzoic acid, luteolin and eriodictyol.
Looking at the samples plot, a separation between the organs was achieved along PCs, with the leaves and flowers very distant from the three other organs (roots, aerial parts, and stem) (Figure 3C). Afterwards, the hierarchical analysis done on the basis of PCA result, brought out three clusters (Figure 3D). The results obtained in the current study, demonstrate that biological activities of plant differ dramatically from one organ to another. Among the analyzed organs of A. macrocephanus, leaves were found to be a promising source, enclosing biomolecules responsible for antioxidant properties and melanoma management ability. This is the result of the difference in quantity and quality of phytocompounds synthesizes in those organs. This quantitative and qualitative difference of phytocompounds is due to the anatomical and morphological structure as well as in several physiological processes that occur in the different organs [84].

4. Conclusions

Analysis of phenolic components, and biological potential using antioxidant and enzyme inhibitory assays of A. macrocephalus subsp. finitimus extracts were conducted for the first time. Twenty-four compounds were identified and quantified in the tested extracts. The levels of these compounds were dependent on the plant parts used. Hyperoside, apigenin, p-coumaric, and ferulic acids were dominant compounds in the extracts. In the connect with chemical profiles, different results were observed for each part in the biological activity assays. Except for metal chelating ability, the extract from leaves exhibited the best biological activities in the performed assays. To sum up, our observations suggest that A. macrocephalus subsp. finitimus could serve as a prominent source of bioactive agents to combat global health problems caused by oxidative stress. However, further studies are needed to understand the toxic profile, the type of enzyme inhibition and bioavailability of the tested extracts.

Supplementary Materials

The following are available online at https://www.mdpi.com/2079-7737/9/8/231/s1. In section S.1 was given analytical methods applied for phenolic composition, antioxidant and enzyme inhibitory activities; Table S1: ESI–MS/MS Parameters and analytical characteristics for the Analysis of Target Analytes by MRM Negative and Positive Ionization Mode; Figure S1: LC-ESI-MS/MS chromatograms of the methanol extracts from aerial parts (A), flowers (B), leaves (C), roots (D), and stems (E) of A. macrocephalus subsp. finitimus.

Author Contributions

Conceptualization C.S. and G.Z.; Methodology, C.S.; Software, C.S. and G.Z.; Validation C.S., G.Z.; Formal analysis, G.Z.; Investigation. C.S.; Resources C.S.; Data curation, C.S.; Writing—original draft preparation, C.S. and G.Z.; Writing—review and editing, G.Z.; Visualization, G.Z.; Supervision, C.S.; Project administration, G.Z.; Funding acquisition, C.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. De la Parra, J.; Quave, C.L. Ethnophytotechnology: Harnessing the Power of Ethnobotany with Biotechnology. Trends Biotechnol. 2017, 35, 802–806. [Google Scholar] [CrossRef] [PubMed]
  2. McClatchey, W.C.; Mahady, G.B.; Bennett, B.C.; Shiels, L.; Savo, V. Ethnobotany as a pharmacological research tool and recent developments in CNS-active natural products from ethnobotanical sources. Pharmacol. Ther. 2009, 123, 239–254. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Popović, Z.; Matić, R.; Bojović, S.; Stefanović, M.; Vidaković, V. Ethnobotany and herbal medicine in modern complementary and alternative medicine: An overview of publications in the field of I&C medicine 2001–2013. J. Ethnopharmacol. 2016, 181, 182–192. [Google Scholar] [PubMed]
  4. Krungkrai, J.; Krungkrai, S.R. Antimalarial qinghaosu/artemisinin: The therapy worthy of a Nobel Prize. Asian Pac. J. Trop. Biomed. 2016, 6, 371–375. [Google Scholar] [CrossRef]
  5. Weathers, P.J.; Cambra, H.M.; Desrosiers, M.R.; Rassias, D.; Towler, M.J. Artemisinin the Nobel Molecule: From Plant to Patient. In Studies in Natural Products Chemistry; Atta ur, R., Ed.; Elvesier: Amsterdam, The Netherlands, 2017; Volume 52, pp. 193–229. [Google Scholar]
  6. Güner, A.; Aslan, S.; Babaç, M.T.; Vural, M.; Ekim, T. Türkiye Bitkileri Listesi (Damarlı Bitkiler); Nezahat Gökyiğit Botanik Bahçesi: Istanbul, Turkey, 2012; pp. 1–1290. [Google Scholar]
  7. Minatel, I.O.; Borges, C.V.; Ferreira, M.I.; Gomez, H.A.G.; Chen, C.-Y.O.; Lima, G.P.P. Phenolic Compounds: Functional Properties, Impact of Processing and Bioavailability; InTech: Rijeka, Croatia, 2017; pp. 1–24. [Google Scholar]
  8. Shahidi, F.; Ambigaipalan, P. Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects—A review. J. Funct. Foods 2015, 18, 820–897. [Google Scholar] [CrossRef]
  9. Bratkov, V.M.; Shkondrov, A.M.; Zdraveva, P.K.; Krasteva, I.N. Flavonoids from the genus Astragalus: Phytochemistry and biological activity. Pharmacogn. Rev. 2016, 10, 11. [Google Scholar]
  10. Çeçen, Ö.; Aytac, Z.; Misirdali, H. Astragalus unalii (Fabaceae), a new species from Turkey. Turk. J. Bot. 2016, 40, 81–86. [Google Scholar] [CrossRef]
  11. Mükemre, M.; Behçet, L.; Çakılcıoğlu, U. Ethnobotanical study on medicinal plants in villages of Çatak (Van-Turkey). J. Ethnopharmacol. 2015, 166, 361–374. [Google Scholar] [CrossRef]
  12. Altundag, E.; Ozturk, M. Ethnomedicinal studies on the plant resources of east Anatolia, Turkey. Procedia Soc. Behav. Sci. 2011, 19, 756–777. [Google Scholar] [CrossRef] [Green Version]
  13. Polat, R.; Cakilcioglu, U.; Satıl, F. Traditional uses of medicinal plants in Solhan (Bingöl—Turkey). J. Ethnopharmacol. 2013, 148, 951–963. [Google Scholar] [CrossRef]
  14. Tetik, F.; Civelek, S.; Cakilcioglu, U. Traditional uses of some medicinal plants in Malatya (Turkey). J. Ethnopharmacol. 2013, 146, 331–346. [Google Scholar] [CrossRef] [PubMed]
  15. Sargin, S.A. Ethnobotanical survey of medicinal plants in Bozyazı district of Mersin, Turkey. J. Ethnopharmacol. 2015, 173, 105–126. [Google Scholar] [CrossRef] [PubMed]
  16. Arumugam, R.; Kirkan, B.; Sarikurkcu, C. Phenolic profile, antioxidant and enzyme inhibitory potential of methanolic extracts from different parts of Astragalus ponticus Pall. S. Afr. J. Bot. 2019, 120, 268–273. [Google Scholar] [CrossRef]
  17. Gülcemal, D.; Masullo, M.; Napolitano, A.; Karayıldırım, T.; Bedir, E.; Alankuş-Çalışkan, Ö.; Piacente, S. Oleanane glycosides from Astragalus tauricolus: Isolation and structural elucidation based on a preliminary liquid chromatography-electrospray ionization tandem mass spectrometry profiling. Phytochemistry 2013, 86, 184–194. [Google Scholar] [CrossRef]
  18. Liu, Y.; Liu, J.; Wu, K.-X.; Guo, X.-R.; Tang, Z.-H. A rapid method for sensitive profiling of bioactive triterpene and flavonoid from Astragalus mongholicus and Astragalus membranaceus by ultra-pressure liquid chromatography with tandem mass spectrometry. J. Chromatogr. B 2018, 1085, 110–118. [Google Scholar] [CrossRef] [PubMed]
  19. Nalbantsoy, A.; Nesil, T.; Yılmaz-Dilsiz, Ö.; Aksu, G.; Khan, S.; Bedir, E. Evaluation of the immunomodulatory properties in mice and in vitro anti-inflammatory activity of cycloartane type saponins from Astragalus species. J. Ethnopharmacol. 2012, 139, 574–581. [Google Scholar] [CrossRef] [PubMed]
  20. Sevimli-Gür, C.; Onbaşılar, İ.; Atilla, P.; Genç, R.; Çakar, N.; Deliloğlu-Gürhan, İ.; Bedir, E. In vitro growth stimulatory and in vivo wound healing studies on cycloartane-type saponins of Astragalus genus. J. Ethnopharmacol. 2011, 134, 844–850. [Google Scholar] [CrossRef]
  21. Yesilada, E.; Bedir, E.; Çalış, İ.; Takaishi, Y.; Ohmoto, Y. Effects of triterpene saponins from Astragalus species on in vitro cytokine release. J. Ethnopharmacol. 2005, 96, 71–77. [Google Scholar] [CrossRef]
  22. Zhang, Y.; Jiang, W.; Xia, Q.; Qi, J.; Cao, M. Pharmacological mechanism of Astragalus and Angelica in the treatment of idiopathic pulmonary fibrosis based on network pharmacology. Eur. J. Integr. Med. 2019, 32, 101003. [Google Scholar] [CrossRef]
  23. Adigüzel, A.; Soekmen, M.; Oezkan, H.; Ağar, G.; Guelluece, M.; Şahin, F. In vitro antimicrobial and antioxidant activities of methanol and hexane extract of Astragalus species growing in the eastern Anatolia region of Turkey. Turk. J. Biol. 2009, 33, 65–71. [Google Scholar]
  24. Gulluce, M.; Agar, G.; Baris, O.; Karadayi, M.; Orhan, F.; Sahin, F. Mutagenic and antimutagenic effects of hexane extract of some Astragalus species grown in the eastern Anatolia region of Turkey. Phytother. Res. 2010, 24, 1014–1018. [Google Scholar] [PubMed]
  25. Sokmen, M.; Gulluce, M.; Agar, G.; Sengul, M.; Sahin, F.; Baris, O. Antioxidant activities of methanol extract of some astragalus species wildly growing in Erzurum. Acta Hortic. 2009, 59. [Google Scholar] [CrossRef]
  26. Davis, P.H. Flora of Turkey and the East Aegean Islands; Edinburgh University Press: Edinburgh, Scotland, 1970; Volume 3. [Google Scholar]
  27. Zengin, G.; Sarikurkcu, C.; Aktumsek, A.; Ceylan, R. Sideritis galatica Bornm.: A source of multifunctional agents for the management of oxidative damage, Alzheimer’s and diabetes mellitus. J. Funct. Foods 2014, 11, 538–547. [Google Scholar] [CrossRef]
  28. Cittan, M.; Çelik, A. Development and validation of an analytical methodology based on liquid chromatography–electrospray tandem mass spectrometry for the simultaneous determination of phenolic compounds in Olive leaf extract. J. Chromatogr. Sci. 2018, 56, 336–343. [Google Scholar] [CrossRef]
  29. Odabas Kose, E.; Aktaş, O.; Deniz, I.G.; Sarikürkçü, C. Chemical composition, antimicrobial and antioxidant activity of essential oil of endemic Ferula lycia Boiss. J. Med. Plants Res. 2010, 4, 1698–1703. [Google Scholar]
  30. Zengin, G.; Sarikurkcu, C.; Uyar, P.; Aktumsek, A.; Uysal, S.; Kocak, M.S.; Ceylan, R. Crepis foetida L. subsp rhoeadifolia (Bleb.) Celak. as a source of multifunctional agents: Cytotoxic and phytochemical evaluation. J. Funct. Foods 2015, 17, 698–708. [Google Scholar] [CrossRef]
  31. Apak, R.; Güçlü, K.; Özyürek, M.; Esin Karademir, S.; Erçaǧ, E. The cupric ion reducing antioxidant capacity and polyphenolic content of some herbal teas. Int. J. Food Sci. Nutr. 2006, 57, 292–304. [Google Scholar] [CrossRef]
  32. Kocak, M.S.; Sarikurkcu, C.; Cengiz, M.; Kocak, S.; Uren, M.C.; Tepe, B. Salvia cadmica: Phenolic composition and biological activity. Ind. Crop. Prod. 2016, 85, 204–212. [Google Scholar] [CrossRef]
  33. Zengin, G.; Sarikurkcu, C.; Gunes, E.; Uysal, A.; Ceylan, R.; Uysal, S.; Gungor, H.; Aktumsek, A. Two Ganoderma species: Profiling of phenolic compounds by HPLC-DAD, antioxidant, antimicrobial and inhibitory activities on key enzymes linked to diabetes mellitus, Alzheimer’s disease and skin disorders. Food Funct. 2015, 6, 2794–2802. [Google Scholar] [CrossRef]
  34. Tepe, B.; Sarikurkcu, C.; Berk, S.; Alim, A.; Akpulat, H.A. Chemical composition, radical scavenging and antimicrobial activity of the essential oils of Thymus boveii and Thymus hyemalis. Rec. Nat. Prod. 2011, 5, 208–220. [Google Scholar]
  35. Zengin, G.; Sarıkürkçü, C.; Aktümsek, A.; Ceylan, R. Antioxidant potential and inhibition of key enzymes linked to Alzheimer’s diseases and diabetes mellitus by monoterpene-rich essential oil from Sideritis galatica Bornm. Endemic to Turkey. Rec. Nat. Prod. 2015, 10, 195–206. [Google Scholar]
  36. Sun, T.; Tanumihardjo, S. An integrated approach to evaluate food antioxidant capacity. J. Food Sci. 2007, 72, R159–R165. [Google Scholar] [CrossRef] [PubMed]
  37. Babich, O.; Prosekov, A.; Zaushintsena, A.; Sukhikh, A.; Dyshlyuk, L.; Ivanova, S. Identification and quantification of phenolic compounds of Western Siberia Astragalus danicus in different regions. Heliyon 2019, 5, e02245. [Google Scholar] [CrossRef] [Green Version]
  38. Chen, Y.; Wang, E.; Wei, Z.; Zheng, Y.; Yan, R.; Ma, X. Phytochemical analysis, cellular antioxidant and α-glucosidase inhibitory activities of various herb plant organs. Ind. Crops Prod. 2019, 141, 111771. [Google Scholar] [CrossRef]
  39. Li, Y.; Guo, S.; Zhu, Y.; Yan, H.; Qian, D.-W.; Wang, H.-Q.; Yu, J.-Q.; Duan, J.-A. Comparative analysis of twenty-five compounds in different parts of Astragalus membranaceus var. mongholicus and Astragalus membranaceus by UPLC-MS/MS. J. Pharm. Anal. 2019, 9, 392–399. [Google Scholar] [CrossRef] [PubMed]
  40. Hazrati, S.; Ebadi, M.-T.; Mollaei, S.; Khurizadeh, S. Evaluation of volatile and phenolic compounds, and antioxidant activity of different parts of Ferulago angulata (schlecht.) Boiss. Ind. Crops Prod. 2019, 140, 111589. [Google Scholar] [CrossRef]
  41. Oldoni, T.L.C.; Merlin, N.; Karling, M.; Carpes, S.T.; Alencar, S.M.d.; Morales, R.G.F.; Silva, E.A.d.; Pilau, E.J. Bioguided extraction of phenolic compounds and UHPLC-ESI-Q-TOF-MS/MS characterization of extracts of Moringa oleifera leaves collected in Brazil. Food Res. Int. 2019, 125, 108647. [Google Scholar] [CrossRef] [PubMed]
  42. Xiang, J.; Li, W.; Ndolo, V.U.; Beta, T. A comparative study of the phenolic compounds and in vitro antioxidant capacity of finger millets from different growing regions in Malawi. J. Cereal Sci. 2019, 87, 143–149. [Google Scholar] [CrossRef]
  43. Amorati, R.; Valgimigli, L. Advantages and limitations of common testing methods for antioxidants. Free Radic. Res. 2015, 49, 633–649. [Google Scholar] [CrossRef]
  44. Sánchez-Rangel, J.C.; Benavides, J.; Heredia, J.B.; Cisneros-Zevallos, L.; Jacobo-Velázquez, D.A. The Folin–Ciocalteu assay revisited: Improvement of its specificity for total phenolic content determination. Anal. Methods 2013, 5, 5990–5999. [Google Scholar] [CrossRef]
  45. Gao, Y.; Fang, L.; Wang, X.; Lan, R.; Wang, M.; Du, G.; Guan, W.; Liu, J.; Brennan, M.; Guo, H. Antioxidant activity evaluation of dietary flavonoid hyperoside using saccharomyces cerevisiae as a model. Molecules 2019, 24, 788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wang, Y.-S.; Shen, C.-Y.; Jiang, J.-G. Antidepressant active ingredients from herbs and nutraceuticals used in TCM: Pharmacological mechanisms and prospects for drug discovery. Pharmacol. Res. 2019, 150, 104520. [Google Scholar] [CrossRef] [PubMed]
  47. Zhang, N.; Ying, M.-D.; Wu, Y.-P.; Zhou, Z.-H.; Ye, Z.-M.; Li, H.; Lin, D.-S. Hyperoside, a flavonoid compound, inhibits proliferation and stimulates osteogenic differentiation of human osteosarcoma cells. PLoS ONE 2014, 9, e98973. [Google Scholar] [CrossRef] [PubMed]
  48. Pei, K.; Ou, J.; Huang, J.; Ou, S. p-Coumaric acid and its conjugates: Dietary sources, pharmacokinetic properties and biological activities. J. Sci. Food Agric. 2016, 96, 2952–2962. [Google Scholar] [CrossRef]
  49. Salehi, B.; Venditti, A.; Sharifi-Rad, M.; Kręgiel, D.; Sharifi-Rad, J.; Durazzo, A.; Lucarini, M.; Santini, A.; Souto, E.B.; Novellino, E.; et al. The Therapeutic Potential of Apigenin. Int. J. Mol. Sci. 2019, 20, 1305. [Google Scholar] [CrossRef] [Green Version]
  50. Mancuso, C.; Santangelo, R. Ferulic acid: Pharmacological and toxicological aspects. Food Chem. Toxicol. 2014, 65, 185–195. [Google Scholar] [CrossRef]
  51. Zhao, Z.; Moghadasian, M.H. Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: A review. Food Chem. 2008, 109, 691–702. [Google Scholar] [CrossRef]
  52. Neha, K.; Haider, M.R.; Pathak, A.; Yar, M.S. Medicinal prospects of antioxidants: A review. Eur. J. Med. Chem. 2019, 178, 687–704. [Google Scholar] [CrossRef]
  53. Pistollato, F.; Battino, M. Role of plant-based diets in the prevention and regression of metabolic syndrome and neurodegenerative diseases. Trends Food Sci. Technol. 2014, 40, 62–81. [Google Scholar] [CrossRef]
  54. Román, G.C.; Jackson, R.E.; Gadhia, R.; Román, A.N.; Reis, J. Mediterranean diet: The role of long-chain ω-3 fatty acids in fish; polyphenols in fruits, vegetables, cereals, coffee, tea, cacao and wine; probiotics and vitamins in prevention of stroke, age-related cognitive decline, and Alzheimer disease. Rev. Neurol. 2019, 175, 724–741. [Google Scholar] [CrossRef]
  55. Satija, A.; Hu, F.B. Plant-based diets and cardiovascular health. Trends Cardiovasc. Med. 2018, 28, 437–441. [Google Scholar] [CrossRef] [PubMed]
  56. Zengin, G.; Ceylan, R.; Guler, G.O.; Carradori, S.; Uysal, S.; Aktumsek, A. Enzyme inhibitory effect and antioxidant properties of Astragalus lagurus extracts. Curr. Enzym. Inhib. 2016, 12, 177–182. [Google Scholar] [CrossRef]
  57. Kondeva-Burdina, M.; Shkondrov, A.; Simeonova, R.; Vitcheva, V.; Krasteva, I.; Ionkova, I. In vitro/in vivo antioxidant and hepatoprotective potential of defatted extract and flavonoids isolated from Astragalus spruneri Boiss. (Fabaceae). Food Chem. Toxicol. 2018, 111, 631–640. [Google Scholar] [CrossRef] [PubMed]
  58. Chen, R.-Z.; Tan, L.; Jin, C.-G.; Lu, J.; Tian, L.; Chang, Q.-Q.; Wang, K. Extraction, isolation, characterization and antioxidant activity of polysaccharides from Astragalus membranaceus. Ind. Crops Prod. 2015, 77, 434–443. [Google Scholar] [CrossRef]
  59. Xu, X.; Li, F.; Zhang, X.; Li, P.; Zhang, X.; Wu, Z.; Li, D. In vitro synergistic antioxidant activity and identification of antioxidant components from Astragalus membranaceus and Paeonia lactiflora. PLoS ONE 2014, 9, e96780. [Google Scholar] [CrossRef] [Green Version]
  60. Alam, M.N.; Bristi, N.J.; Rafiquzzaman, M. Review on in vivo and in vitro methods evaluation of antioxidant activity. Saudi Pharm. J. 2013, 21, 143–152. [Google Scholar] [CrossRef] [Green Version]
  61. Laličić-Petronijević, J.; Komes, D.; Gorjanović, S.; Belščak-Cvitanović, A.; Pezo, L.; Pastor, F.; Ostojić, S.; Popov-Raljić, J.; Sužnjević, D. Content of total phenolics, flavan-3-ols and proanthocyanidins, oxidative stability and antioxidant capacity of chocolate during storage. Food Technol. Biotechnol. 2016, 54, 13–20. [Google Scholar] [CrossRef]
  62. Kalogeropoulos, N.; Yanni, A.E.; Koutrotsios, G.; Aloupi, M. Bioactive microconstituents and antioxidant properties of wild edible mushrooms from the island of Lesvos, Greece. Food Chem.Toxicol. 2013, 55, 378–385. [Google Scholar] [CrossRef]
  63. Wang, T.; Jonsdottir, R.; Ólafsdóttir, G. Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem. 2009, 116, 240–248. [Google Scholar] [CrossRef]
  64. Rauf, A.; Jehan, N. Natural products as a potential enzyme inhibitors from medicinal plants. In Enzyme Inhibitors and Activators; InTech: Rijeka, Croatia, 2017; pp. 165–177. [Google Scholar]
  65. Sun, L.; Warren, F.J.; Gidley, M.J. Natural products for glycaemic control: Polyphenols as inhibitors of alpha-amylase. Trends Food Sci. Technol. 2019, 91, 262–273. [Google Scholar] [CrossRef]
  66. Mukherjee, P.K.; Biswas, R.; Sharma, A.; Banerjee, S.; Biswas, S.; Katiyar, C. Validation of medicinal herbs for anti-tyrosinase potential. J. Herb. Med. 2018, 14, 1–16. [Google Scholar] [CrossRef]
  67. Chang, T.-S. Natural melanogenesis inhibitors acting through the down-regulation of tyrosinase activity. Materials 2012, 5, 1661–1685. [Google Scholar] [CrossRef] [Green Version]
  68. Jhong, C.H.; Riyaphan, J.; Lin, S.H.; Chia, Y.C.; Weng, C.F. Screening alpha-glucosidase and alpha-amylase inhibitors from natural compounds by molecular docking in silico. Biofactors 2015, 41, 242–251. [Google Scholar] [CrossRef] [PubMed]
  69. Saeedi, M.; Eslamifar, M.; Khezri, K. Kojic acid applications in cosmetic and pharmaceutical preparations. Biomed. Pharmacother. 2019, 110, 582–593. [Google Scholar] [CrossRef]
  70. Jung, S.-Y.; Jung, W.-S.; Jung, H.-K.; Lee, G.-H.; Cho, J.-H.; Cho, H.-W.; Choi, I.-Y. The mixture of different parts of Nelumbo nucifera and two bioactive components inhibited tyrosinase activity and melanogenesis. J. Cosmet. Sci. 2014, 65, 377–388. [Google Scholar]
  71. Liao, L.; Chen, J.; Liu, L.; Xiao, A. Screening and binding analysis of flavonoids with alpha-amylase inhibitory activity from lotus leaf. J. Braz. Chem. Soc. 2018, 29, 587–593. [Google Scholar] [CrossRef]
  72. Zheng, Y.; Tian, J.; Yang, W.; Chen, S.; Liu, D.; Fang, H.; Zhang, H.; Ye, X. Inhibition mechanism of ferulic acid against α-amylase and α-glucosidase. Food Chem. 2020, 317, 126346. [Google Scholar] [CrossRef]
  73. Zolghadri, S.; Bahrami, A.; Hassan Khan, M.T.; Munoz-Munoz, J.; Garcia-Molina, F.; Garcia-Canovas, F.; Saboury, A.A. A comprehensive review on tyrosinase inhibitors. J. Enzym. Inhib. Med. Chem. 2019, 34, 279–309. [Google Scholar] [CrossRef] [Green Version]
  74. Fan, M.; Ding, H.; Zhang, G.; Hu, X.; Gong, D. Relationships of dietary flavonoid structure with its tyrosinase inhibitory activity and affinity. LWT-Food Sci. Technol. 2019, 107, 25–34. [Google Scholar] [CrossRef]
  75. Li, K.; Yao, F.; Xue, Q.; Fan, H.; Yang, L.; Li, X.; Sun, L.; Liu, Y. Inhibitory effects against α-glucosidase and α-amylase of the flavonoids-rich extract from Scutellaria baicalensis shoots and interpretation of structure-activity relationship of its eight flavonoids by a refined assign-score method. Chem. Cent. J. 2018, 12, 82. [Google Scholar] [CrossRef]
  76. Wang, Y.; Hao, M.-M.; Sun, Y.; Wang, L.-F.; Wang, H.; Zhang, Y.-J.; Li, H.-Y.; Zhuang, P.-W.; Yang, Z. Synergistic promotion on tyrosinase inhibition by antioxidants. Molecules 2018, 23, 106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Abedi, F.; Razavi, B.M.; Hosseinzadeh, H. A review on gentisic acid as a plant derived phenolic acid and metabolite of aspirin: Comprehensive pharmacology, toxicology, and some pharmaceutical aspects. Phytother. Res. 2019, 1–13. [Google Scholar] [CrossRef] [PubMed]
  78. Agunloye, O.M.; Oboh, G.; Ademiluyi, A.O.; Ademosun, A.O.; Akindahunsi, A.A.; Oyagbemi, A.A.; Omobowale, T.O.; Ajibade, T.O.; Adedapo, A.A. Cardio-protective and antioxidant properties of caffeic acid and chlorogenic acid: Mechanistic role of angiotensin converting enzyme, cholinesterase and arginase activities in cyclosporine induced hypertensive rats. Biomed. Pharmacother. 2019, 109, 450–458. [Google Scholar] [CrossRef] [PubMed]
  79. Grzesik, M.; Naparło, K.; Bartosz, G.; Sadowska-Bartosz, I. Antioxidant properties of catechins: Comparison with other antioxidants. Food Chem. 2018, 241, 480–492. [Google Scholar] [CrossRef]
  80. Uysal, A.; Zengin, G.; Mollica, A.; Gunes, E.; Locatelli, M.; Yilmaz, T.; Aktumsek, A. Chemical and biological insights on Cotoneaster integerrimus: A new (−)-epicatechin source for food and medicinal applications. Phytomedicine 2016, 23, 979–988. [Google Scholar] [CrossRef]
  81. Maruyama, H.; Kawakami, F.; Lwin, T.-T.; Imai, M.; Shamsa, F. Biochemical characterization of ferulic acid and caffeic acid which effectively inhibit melanin synthesis via different mechanisms in B16 melanoma cells. Biol. Pharm. Bull. 2018, 41, 806–810. [Google Scholar] [CrossRef] [Green Version]
  82. Park, J.Y.; Han, X.; Piao, M.J.; Oh, M.C.; Fernando, P.M.D.J.; Kang, K.A.; Ryu, Y.S.; Jung, U.; Kim, I.G.; Hyun, J.W. Hyperoside induces endogenous antioxidant system to alleviate oxidative stress. J. Cancer Prev. 2016, 21, 41. [Google Scholar] [CrossRef] [Green Version]
  83. Yang, B.; Yang, Q.; Yang, X.; Yan, H.B.; Lu, Q.P. Hyperoside protects human primary melanocytes against H2O2-induced oxidative damage. Mol. Med. Rep. 2016, 13, 4613–4619. [Google Scholar] [CrossRef] [Green Version]
  84. Bystrická, J.; Vollmannová, A.; Margitanová, E. Dynamics of polyphenolics formation in different plant parts and different growth phases of selected buckwheat cultivars. Acta Agric. Slov. 2010, 95, 225. [Google Scholar] [CrossRef]
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Figure 1. Relative antioxidant capacity index of different parts of A. macrocephalus subsp. finitimus.
Figure 1. Relative antioxidant capacity index of different parts of A. macrocephalus subsp. finitimus.
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Biology 09 00231 g002 550
Figure 2. Relative antioxidant capacity index (dashed line with triangle) and antioxidant activity (solid line with circle) of each different part of A. macrocephalus subsp. finitimus.
Figure 2. Relative antioxidant capacity index (dashed line with triangle) and antioxidant activity (solid line with circle) of each different part of A. macrocephalus subsp. finitimus.
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Biology 09 00231 g003 550
Figure 3. Principle Component Analysis (PCA) and hierarchical clustering analysis. (A): Loading plot. (B): Contribution of biological activities to each dimension of PCA. (C): Samples plot. (D): Hierarchical clustering on the fact.
Figure 3. Principle Component Analysis (PCA) and hierarchical clustering analysis. (A): Loading plot. (B): Contribution of biological activities to each dimension of PCA. (C): Samples plot. (D): Hierarchical clustering on the fact.
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Table
Table 1. Extraction yield, total phenolic and flavonoid contents of the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
Table 1. Extraction yield, total phenolic and flavonoid contents of the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
SamplesYield (%)Total Flavonoids (Mg QE/g Extract) Total Phenolics (Mg GAE/g Extract)
Aerial parts10.5621.06 ± 0.11 c10.01 ± 0.17 b
Flowers6.9529.90 ± 0.95 b6.96 ± 1.08 bc
Leaves3.4639.23 ± 1.64 a37.68 ± 0.74 a
Roots17.836.03 ± 0.05 d5.60 ± 0.06 c
Stems11.787.91 ± 0.37 d8.29 ± 1.13 bc
x Within each column, means sharing the different superscripts (a–d) show comparison between the extracts using Tukey’s test at p < 0.05, GAEs and QEs, gallic acid and quercetin equivalents, respectively.
Table
Table 2. Concentration (µg/g extract) of selected phytochemicals in the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
Table 2. Concentration (µg/g extract) of selected phytochemicals in the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
CompoundsAerial PartsFlowersLeavesRootsStems
Gallic acid2.28 ± 0.03 d8.76 ± 0.18 a2.24 ± 0.01 d4.93 ± 0.12 b3.03 ± 0.04 c
Protocatechuic acid14.37 ± 0.08 c16.80 ± 0.47 b18.90 ± 0.16 a13.51 ± 0.64 c8.06 ± 0.05 d
Chlorogenic acid8.99 ± 0.24 a10.29 ± 4.02 a0.75 ± 0.26 b3.06 ± 0.69 ab1.59 ± 0.19 b
2,5-Dihydroxybenzoic acid9.96 ± 1.74 cnd23.14 ± 0.06 and16.86 ± 1.09 b
4-Hydroxybenzoic acid12.78 ± 0.16 c28.83 ± 0.62 b2.72 ± 0.07 e31.86 ± 0.76 a8.13 ± 0.28 d
(−)-Epicatechinndnd5.60 ± 0.11ndnd
Caffeic acid2.77 ± 0.11 bnd3.94 ± 0.03 andnd
Vanillic acid23.30 ± 0.23 c100.53 ± 8.83 a4.36 ± 0.26 d57.78 ± 4.27 b51.53 ± 3.73 b
Syringic acid6.71 ± 0.03 d20.89 ± 0.71 b2.08 ± 0.06 e33.47 ± 1 a17.27 ± 1.52 c
Vanillin3.42 ± 0.11 cndnd55.68 ± 0.68 a23.62 ± 0.13 b
Verbascoside43.48 ± 0.25 a8.68 ± 0.30 b1.13 ± 0.08 e7.29 ± 0.14 c2.64 ± 0.11 d
Sinapic acid7.41 ± 0.01 b52.66 ± 1.36 a3.41 ± 0.52 cndnd
p-Coumaric acid76.85 ± 0.47 b146.78 ± 1.89 a33.12 ± 0.35 c6.81 ± 0.60 e22.12 ± 0.51 d
Ferulic acid52.79 ± 2.88 b64.20 ± 2.45 a37.61 ± 0.30 c10.53 ± 0.48 d17.40 ± 0.96 d
Luteolin 7-glucoside17.63 ± 0.89 ab28.59 ± 9.16 a13.45 ± 0.17 ab6.20 ± 0.75 b11.35 ± 0.16 b
Hesperidin7.69 ± 0.04 ab8.44 ± 1.45 a7.05 ± 0.03 ab4.99 ± 0.06 b9.14 ± 0.75 a
Hyperoside401.68 ± 6.72 b90.45 ± 1.39 d1828.94 ± 21 a2.90 ± 0.46 e321.43 ± 7.64 c
Rosmarinic acid2.10 ± 0.11 c26.95 ± 3.30 a1.25 ± 0.02 c10.46 ± 0.65 b5.43 ± 0.27 bc
Apigenin 7-glucoside23.68 ± 0.08 c63.56 ± 1.94 a16.85 ± 0.19 d44.54 ± 0.35 b20.24 ± 0.04 cd
Pinoresinolndndnd6.40 ± 0.37 a6.80 ± 0.23 a
Eriodictyol0.44 ± 0.05 c2.58 ± 0.36 b0.30 ± 0.01 c6.97 ± 0.12 a0.73 ± 0.01 c
Quercetin6.47 ± 0.02 b11.11 ± 0.04 a3.27 ± 0.06 d4.58 ± 0.13 c4.74 ± 0.12 c
Luteolin32.06 ± 0.45 cd81.94 ± 0.28 b32.58 ± 1.07 c108.11 ± 1.20 a28.77 ± 0.73 d
Kaempferol1.58 ± 0.25ndndndnd
Apigenin29.07 ± 0.50 c52.33 ± 1.34 b23 ±0.12 c181.90 ± 6.23 a42.81 ± 0.52 b
x Within each row, means sharing the different superscripts (a–d) show comparison between the samples using Tukey’s test at p < 0.05. nd, not detected.
Table
Table 3. Antioxidant activities of standards and the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
Table 3. Antioxidant activities of standards and the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
AssaysAerial PartsFlowersLeavesRootsStemsTroloxEDTA
Effective concentration (EC50: mg/mL)
Phosphomolybdenum2.52 ± 0.23 c2.67 ± 0.08c1.81 ± 0.12 b2.77 ± 0.03 c2.77 ± 0.15 c1.14 ± 0.02 a-
DPPH radical9.30 ± 0.20 c14.20 ± 0.12e2.65 ± 0.05 b10.54 ± 0.52 d8.73 ± 0.22 c0.26 ± 0.02 a-
ABTS radical cation1.66 ± 0.01 b3.35 ± 0.01d1.45 ± 0.04 b3.88 ± 0.11 e1.93 ± 0.07 c0.25 ± 0.02 a-
CUPRAC reducing power2.37 ± 0.06 c3.62 ± 0.16d1.06 ± 0.02 b5.28 ± 0.39 e2.90 ± 0.12 cd0.32 ± 0.03 a-
FRAP reducing power1.75 ± 0.02 c2.46 ± 0.05d0.73 ± 0.01 b2.83 ± 0.12 e1.93 ± 0.08 c0.12 ± 0.02a-
Ferrous ion chelating1.08 ± 0.01 b1.03 ± 0.01b1.65 ± 0.05 c1.07 ± 0.01 b1.05 ± 0.03 b-0.036 ± 0.004 a
Antioxidant activity
Phosphomolybdenum (mmol TEs/g extract)1.85 ± 0.17 b1.73 ± 0.05b2.56 ± 0.17 a1.67 ± 0.02 b1.67 ± 0.09 b--
DPPH radical (mg TEs/g extract)24.97 ± 0.61 bc15.42 ± 0.15d94.66 ± 1.97 a21.75 ± 1.21 c26.80 ± 0.76 b--
ABTS radical cation (mg TEs/g extract)161.59 ± 0.86 b78.94 ± 0.01d185.65 ± 5.03 a67.98 ± 2.01 d138.54 ± 4.74 c--
CUPRAC reducing power (mg TEs/g extract)126.91 ± 3.50 b78.76 ± 3.96d297.74 ± 4.90 a50.23 ± 4.64 e101.35 ± 4.66 c--
FRAP reducing power (mg TEs/g extract)59.81 ± 0.67 b42.59 ± 0.89c142.69 ± 2.15 a37.05 ± 1.63 c54.37 ± 2.15 b--
Ferrous ion chelating (mg EDTAEs/g extract)66.81 ± 0.36 a70.11 ± 0.51a43.41 ± 1.39 b67.45 ± 0.18 a68.59 ± 2.00 a--
x Within each row, means sharing the different superscripts show comparison between the samples using Tukey’s test at p < 0.05. EC50 (mg/mL), effective concentration at which the absorbance was 0.5 for reducing power and phosphomolybdenum assays and at which 50% of the DPPH and ABTS radicals were scavenged and the ferrous ion-ferrozine complex were inhibited. EDTA, ethylenediaminetetraacetic acid (disodium salt). “-”, not determined. TEs and EDTAEs, trolox and ethylenediaminetetraacetic acid (disodium salt) equivalents, respectively.
Table
Table 4. Correlations among phenolic compounds and assays x.
Table 4. Correlations among phenolic compounds and assays x.
Assays and CompoundsPhosphomolybdenumDPPHABTSCUPRACFRAPFerrous Ion ChelatingTyrosinaseα-Amylase
DPPH0.974 y
ABTS0.7170.712
CUPRAC0.980 y0.968 y0.828
FRAP0.985 y0.987 y0.7890.995 y
Ferrous ion chelating−0.983 y−0.995 y−0.678−0.960 y−0.980 y
Tyrosinase0.5490.7230.5120.6060.655−0.671
α-Amylase0.4970.5250.5280.4770.491−0.5520.439
Total flavonoid0.7920.6570.4710.7540.725−0.6820.0090.012
Total phenolic0.992 y0.992 y0.7270.985 y0.995 y−0.991 y0.6420.478
Hyperoside0.982 y0.987 y0.7940.995 y0.999 y−0.979 y0.6620.494
x Data show the Pearson Correlation Coefficients between the parameters. y Significant at p < 0.01.
Table
Table 5. Enzyme inhibition activities of standards and the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
Table 5. Enzyme inhibition activities of standards and the methanol extracts from different parts of A. macrocephalus subsp. finitimus x.
AssaysAerial PartsFlowersLeavesRootsStemsKojic AcidAcarbose
Inhibition concentration (IC50: mg/mL)
Tyrosinase inhibition1.33 ± 0.10 cd1.41 ± 0.05 d1.02 ± 0.02 b1.18 ± 0.01 bc1.07 ± 0.03 b0.36 ± 0.04 a-
α-Amylase inhibition3.40 ± 0.02 b4.94 ± 0.15 d3.36 ± 0.18 b3.50 ± 0.03 b4.12 ± 0.22 c-1.24 ± 0.06 a
Enzyme inhibitory activities
Tyrosinase inhibition (mg KAEs/g extracts)270 ± 20 cd255 ± 8 d352 ± 7 a304 ± 3 bc336 ± 9 ab--
α-Amylase inhibition (mg ACEs/g extracts)357 ± 2 a245 ± 8 c362 ± 20 a347 ± 3 a294 ± 16 b--
x Within each row, means sharing the different superscripts show comparison between the samples using Tukey’s test at p < 0.05. IC50 (mg/mL), inhibition concentration at which 50% of the α-amylase and tyrosinase activities were inhibited. “-” not determined. ACEs and KAEs, acarbose and kojic acid equivalents, respectively.

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Sarikurkcu, C.; Zengin, G. Polyphenol Profile and Biological Activity Comparisons of Different Parts of Astragalus macrocephalus subsp. finitimus from Turkey. Biology 2020, 9, 231. https://doi.org/10.3390/biology9080231

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Sarikurkcu C, Zengin G. Polyphenol Profile and Biological Activity Comparisons of Different Parts of Astragalus macrocephalus subsp. finitimus from Turkey. Biology. 2020; 9(8):231. https://doi.org/10.3390/biology9080231

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Sarikurkcu, Cengiz, and Gokhan Zengin. 2020. "Polyphenol Profile and Biological Activity Comparisons of Different Parts of Astragalus macrocephalus subsp. finitimus from Turkey" Biology 9, no. 8: 231. https://doi.org/10.3390/biology9080231

APA Style

Sarikurkcu, C., & Zengin, G. (2020). Polyphenol Profile and Biological Activity Comparisons of Different Parts of Astragalus macrocephalus subsp. finitimus from Turkey. Biology, 9(8), 231. https://doi.org/10.3390/biology9080231

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