Antimicrobial, antioxidant, and phytochemical activities of Rhus coriaria L. and its phenolic compounds and volatile component analyses

Öz, M., Baltacı, C., Fidan, M. S., and Karataş, S. M. (2023). “Antimicrobial, antioxidant, and phytochemical activities of Rhus coriaria L. and its phenolic compounds and volatile component analyses,” BioResources 18(4), 6842-6861.

Abstract

Volatile oil analysis, phenolic constituents, antioxidant capacity, antimicrobial activity, vitamin C, and enzyme activities of the fruits of Rhus coriaria L. were studied. The chemical with the highest percentage was sesquiterpene hydrocarbons with 40.4%. The major compound was detected as caryophyllene (36.9%). The main phenolic constituents of fruit samples were gallic acid, syringic acid, protocatechuic acid, and 4-hydroxybenzoic acid. The highest phenolic constituents of fruits were gallic acid. Ferric (III) ion reducing antioxidant power (FRAP) capacity (14.9 mg FeSO₄ eq./g), free radical scavenging (ABTS) capacity (68.8 mg AA eq./g), ABTS % inhibition rate (98.0%), free radical scavenging (DPPH) (53.1 mg AA eq./g), and DPPH % inhibition (79.6%) amounts were determined in antioxidant capacities of the samples. The bioactive component contents of the samples were total antioxidant amounts (TAC) (32.8 mg GA/g), total flavonoid substance amounts (TFC) (73.8 mg QE eq./g), and total phenolic substance amounts (TPC) (41.4 mg GA eq./g). The results of the antimicrobial activity analysis of R. coriaria fruit samples showed antimicrobial activity against Staphylococcus aureus and Listeria monocytogenes microorganisms. The amount of vitamin C and enzyme inhibitor activity in the fruits of R. coriaria were determined as 35.5 mg/100 g and 0.07 mg/mL, respectively.

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Antimicrobial, Antioxidant, and Phytochemical Activities of Rhus coriaria L. and its Phenolic Compounds and Volatile Component Analyses

Mehmet Öz,^a Cemalettin Baltacı,^b Muhammed Said Fidan,^c,* and Şeyda Merve Karataş ^b

DOI: 10.15376/biores.18.4.6842-6861

Keywords: GC-MS/FID; HPLC-DAD; Chemical and phenolic composition; Antioxidant-antimicrobial-enzyme activities; Rhus coriaria L.

Contact information: a: Gümüşhane University, Department of Forestry, Gümüşhane 29100, Türkiye; b: Gümüşhane University, Department of Food Engineering, Gümüşhane 29100, Türkiye; c: Bursa Technical University, Department of Forest Industry Engineering, Bursa 16310, Türkiye;

*Corresponding author: said.fidan@btu.edu.tr

INTRODUCTION

The bioactive constituents of nutrients offer to promote health and support for the human immune system (Najafi et al. 2016; Tahvilian et al. 2016; Zangeneh et al. 2016; Galanakis 2020; Zannou et al. 2022). Meanwhile, new challenges facing the world in nutrition, demographics, and health have led to the search for viable and sustainable ways to solve them. For example, bioactives-containing food ingredients are of big relevance as promising solutions for nutrition, health, and cosmetics industries (Gürbüz et al. 2019; Baltacı et al. 2022; Ji and Ji 2022; Zannou et al. 2022). A wide variety of biomolecules, such as phenolics, tocopherols, carotenoids, and sterols, are found in plants (Sarikurkcu and Tlili 2022). Since early times, plants have generally played a crucial role in disease treatment and health care (Fereidoonfar et al. 2019). Different plant species have been utilized for the prevention and cure of many diseases, ranging from simple headaches to main illnesses like cognitive and cancer ailments. This could be attributed to the large biodiversity in plants’ bioactive secondary metabolites (Elagbar et al. 2020). From this perspective, R. coriaria has great potential as a public medicine.

Fig. 1. R. coriaria leaves and fruits (Photo: Mehmet Öz, 19.09.2021)

Rhus coriaria is a wild-growing herb of the Anacardiaceae family (Langroodi et al. 2019). It is widely known as sumac (Alsamri et al. 2021). While the genus Rhus contains rougly 250 species (Gök et al. 2020) worldwide, there is only R. coriaria in Türkiye (Davis 1965). It is distributed over Southern Europe, the Middle East, North Africa, Iran, and Afghanistan (Brunke et al. 1993; Kosar et al. 2007). The appearance of the fruits and leaves of R. coriaria is shown in Fig. 1.

Rhus coriaria has been accepted in herbal medicine as an antiseptic, food flavoring agent, natural antioxidant, and an antimicrobial constituent (Nasar-Abbas and Halkman 2004; Kosar et al. 2007; Gharaei et al. 2013; Langroodi et al. 2019). The many curative impacts of R. coriaria could be attributed to its numerous biological properties, for example antioxidant, antibacterial, anti-inflammatory, antipyretic, hypoglycemic, DNA protective, anti-ischemic, hepatoprotective, vasorelaxant, hypolipidemic activities (Beretta et al. 2009; Chakraborty et al. 2009; Mohammadi et al. 2010; Pourahmad et al. 2010; Peter 2012; Abu-Reidah et al. 2014; Foroughi et al. 2016; Zhaleh et al. 2018; Sakhr and El Khatib 2020). Consumption of sumac fruits is increasing worldwide and is of great economic importance as a natural source of bioactive compounds (Kizil and Turk 2010; Shabbir 2012; Morshedloo et al. 2018).

In folk medicine, R. coriaria is recommended to treat the liver, diarrhea, wound healing, for respiratory system illnesses like catarrh and the common cold, ulcers, diabetes, diuresis, stroke, hypertension, indigestion, anorexia, hemorrhagia, kidney stones, gout, hematemesis, dysentery, urinary system issues, dentistry, rash, edema, bruise, atherosclerosis, smallpox, stomach ache, ophthalmia, hyperglycemias, measles, aconuresis, timulate perspiration, headaches, reduce cholesterol, pox incidence in the eye, eye trachoma, uric acid level, and blood sugar (Tabata et al. 1994; Honda et al. 1996; Mohammadi et al. 2010; Polat et al. 2013; Tuttolomondo et al. 2014; Abu-Reidah et al. 2015; Paksoy et al. 2016; Giovanelli et al. 2017; Farag et al. 2018; Mahdavi et al. 2018; Morshedloo et al. 2018; Fereidoonfar et al. 2019; Elagbar et al. 2020; Gök et al. 2020; Alsamri et al. 2021). It has been used as a conventional medicine for the cure of several diseases including cancer (Farag et al. 2018; Elagbar et al. 2020; Sakhr and El Khatib 2020).

Presently, over 200 phytochemicals have been extracted from R. coriaria, and these contain flavonoids, isoflavonoids, terpenoids, phenolic acids, phenolic constituents conjugated with malic acid derivatives, organic acids, anthocyanins, hydrolysable tannins, and other constituents, for instance coumarin, iridoid, and butein derivatives (Tohma et al. 2019; Alsamri et al. 2021). Former works demonstrated that sumac included essential oil, tannins, anthocyanin, phenolic acids, flavonoids, nitrite, and nitrate contents (Mavlyanov et al. 1997; Özcan and Akbulut 2007; Zannou et al. 2022). Volatile oils can be extracted from several parts as fruits, leaves, flowers, stems, and roots. During the last years, there has been a rising interest in pharmacological studies on volatile oils, and it appears that the volatile oils have been useful for control and inhibition of human and animal bacterial infections (Zhaleh et al. 2018; Radonić et al. 2020). R. coriaria is rich in β-caryophyllene and cembrene with regard to volatile oil constituents, which are potent antibacterial agents (Dahham et al. 2015; Zhaleh et al. 2018).

As far as the authors’ knowledge, in comparison to many other pharmaceutical-industrial plants, there is particularly minimal data about the vitamin C, enzyme inhibition, phenol constituents, and antimicrobial properties of R. coriaria volatile oil collected in Gümüşhane province, northeast of Türkiye. Hence, the goal of the current research is to ensure a comprehensive overview of the pharmacological and phytochemical on R. coriaria fruits.

EXPERIMENTAL

Plant Material

In this research, R. coriaria fruit samples were gathered in Torul-Köstere Village (40°36ꞌ20ꞌꞌN, 39°19ꞌ17ꞌꞌE, Altitude: 1040 m) located within the borders of Gümüşhane Province, Türkiye. The leaves and fruits of the plant samples are shown in Fig. 1. The fruit (500 g) samples from R. coriaria were gathered. The taxonomic diagnosis of plant sample was identified by Assoc. Prof. Mutlu GÜLTEPE (Department of Forestry, Dereli Vocational School, Giresun University, Giresun, Türkiye). The plant sample was listed in the Herbarium of Department of Biology (located in Karadeniz Technical University, Faculty of Science), with the identification number of KTUB Gültepe 719.

Extraction and GC-MS/FID Analysis

The volatile oil obtained by hydrodistillation method (at 100 °C) in the modified Clevenger system, which is cooled inside and outside, was dissolved in hexane, passed through a 0.45-micron filter, and placed in amber colored vials and placed in the autosampler. Components were determined by gas chromatography-flame ionization detection (GC-MS/FID; MS Agilent 5975C, GC-FID Agilent-7890A model, Agilent Technologies Inc, Santa Clara, CA, USA). After the volatile constituents were separated on the gas chromatography column, the mass spectra of each of them were taken individually in the mass spectrophotometer and their structures were elucidated by comparing the mass spectra of each component with the reference constituents of the Willey and NIST libraries. To confirm the detected constituents, the Kovats indices of the constituents were compared with the literature data. The measurement of the volatile oil was made with the GC-FID instrument. For GC, the split ratio was adjusted as 1:5 by injecting 1 µL of volatile oil in hexane into the same column. The GC-MS/FID analyses were performed on Agilent-7890 model device and an HP-5 model apolar capillary column (30 m x 0.32 mm, film thickness 0.25 µm) was used for analysis. The injector, ion source and quadrupole rod temperatures were 250, 230, and 150 °C, respectively. Injections were applied in split (25:1) mode using helium (>99.999%), as the carrier gas with a flow rate of 1 mL/min. Then, 1 µL of essential oil solution in hexane (GC class) was injected and initially the GC oven temperature program kept at 60 °C for 2 min, increased to 240 °C with a rise of 3 °C/min, and spectra were obtained. Mass spectra were acquired at a scan speed of 2 spectra per second after a solvent delay of 3.8 min, and the mass scan range was set at m/z 45 to 450. The FID detector temperature was maintained at 250 °C with a hydrogen flow of 35 mL/min and air flow of 350 mL/min.

Extraction with Methanol

The extraction process was performed using an ultrasonic bath (3 L 320 W Bandelin Ultrasonic Bath). After the fruit parts were ground, 10 g were taken, 50 mL of 80% aq. MeOH was added, and then ultrasound-assisted extraction process was applied at 60 min and 40 °C. At the end of 60 min, it was filtered 2 times through Whatman 1 filter and centrifuged at 4000 rpm for 10 min and plant extracts were obtained. At the end of centrifugation, the upper part was taken into a beaker and the extracts were obtained by completely evaporating the methanol at 40 °C (Dranca and Oroian 2016).

Determination of Phenolic Constituents

All specimens were ultrasonically bathed for 20 min and filtered through a syringe filter (0.45 µm) before analysis. Chromatographic analysis of methanol extracts of fruit samples was performed using an Agilent 1260 Infinity high performance liquid chromatography-diode array detector HPLC-DAD system (Agilent Technologies, Waldbronn, Germany) device. Due to its speed, simplicity and convenience, HPLC-DAD is the most widely used among various chromatographic techniques (Irakli et al. 2012). Pyrzynska and Biesaga (2009) stated that routine detection in HPLC and CE typically relies on measuring UV absorption, usually using diode array detection (DAD), and that the DAD detector can simultaneously detect chromatograms of different wavelengths. For the analysis, the following were used as standards: gallic acid, sesamol, paracoumaric acid, benzoic acid, protocatechuic acid, catechin, syringic acid, vanillin, syringaldehyde, rutin, protocatechuic aldehyde, vanillic acid, rutin, 4-hydroxybenzoic acid, ferulic acid, coumarin, epicatechin, rosmarinic acid, t-cinnamic acid, quercetin, kaempferol, caffeic acid, and chyricin. The analysis method of the phenolic compounds of the samples was studied by modifying the gradient flow of the mobile phase with some changes (Paje et al. 2022). Chromatographic isolation of individual constituents was performed using a Hypersil HPLC Column (250 x 4.6 mm², 5 µm). Mobile phase solvent A was used as mixture 0.5% acetic acid in water (0.5: 95.5, v/v) and acetonitrile (solvent B). The gradient elution was started with 95% of solvent A and reduced to 75% after 20 min. Solvent A was reduced to 50% at 45 min and to 10% at 55 min. It was then increased to 65% at 65 min and continued for up to 70 min. The flow ratio was 1.0 mL/min and the injection capacity was 10 µL. The wavelength used in the DAD detector were 240, 250, 254, 280 and 324 nm.

Determination of Antioxidant Activity

The antioxidant activities of the attained methanol extract of R. coriaria fruits were found according to ferric (III) ion reducing antioxidant power (FRAP) capacity, free radical scavenging (ABTS and DPPH) activities. In addition, some bioactive component amounts were detected by total antioxidant amounts (TAC), total flavonoid substance amounts (TFC), and total phenolic substance amounts (TPC) studies. The FRAP analysis of methanol extracts was determined using the Ahmed et al. (2015) method using FRAP solution. A total of 500 µL of distilled water was utilized as blank. A total of 250 µL of the standards were taken and the same procedures were performed. The FRAP amounts in samples using the correct equation of the calibration graph obtained with the FeSO₄ solution, the total iron reducing capacity was determined as mg FeSO₄ equivalent/g (Ahmed et al. 2015). The ABTS activity analysis (Ahmed et al. 2015) was made using ABTS solution according to the method. A total of 150 µL of methanol was utilized as blank. Then, 150 µL of standards (ascorbic acid) were taken and the same procedures were performed. The acquired solution was then read at a spectrophotometer absorbance at 734 nm. The ABTS cation removal activity amounts in the samples were calculated following Ahmed et al. (2015), Eq. 1. Results are given as mg AA eq./g, mg Trolox eq./g, and % free radical removal.

Inhibition(%)=(Control Absorbance–Example Absorbance/Control Absorbance)x100 (1)

The DPPH activity of the methanol extracts obtained from the fruit was determined using 2,2-diphenyl-1-picrylhydrazil according to the Sanchez-Moreno method (Sağdıç et al. 2011). The method was applied by mixing the methanol extract and DPPH solutions with specific concentrations by vortexing and keeping them at room temperature and in the dark for 30 min. At the end of the period, the absorbance of the specimens at 517 nm was read, and the amount of DPPH remaining in the reaction medium was calculated according to Eq. 2. Results are given as mg AA eq./g, mg Trolox eq./g, and % free radical removal.

Inhibition(%)=(Control Absorbance-Example Absorbance/Control Absorbance)x100 (2)

The analysis of TAC content in methanol extract of fruit was performed using molybdate reagent according to the Kasangana method. A total of 250 µL of pure water was utilized instead of the sample as a blank. The absorbance of the resulting reaction mixtures was measured in a 695 nm spectrophotometer. A total of 500 µL of the standards were taken and the same procedures were performed. The amount of TAC in methanol extract samples was given as mg GA eq./g using the correct equation of the calibration graph obtained with the solution of ascorbic acid (Kasangana et al. 2015). The TFC content in methanol extracts of fruit was detected following the Kasangana method. The absorbance of the resulting mixture was read in a spectrophotometer at 506 nm. A total of 500 µL of pure water was utilized as blank. Then, 500 µL of the standards were taken and the same procedures were performed. The amount of TFC in the samples was determined as mg QE eq/g using the correct equation of the calibration graph obtained with Catechin or Quercetin (ethanol was dissolved) solution (Kasangana et al. 2015). Analysis of the TPC amount, one of the bioactive components of methanol extracts, was carried out according to the Kasangana method using Folin-Ciocalteu reagent (Kasangana et al. 2015). After the prepared mixture was whirlpooled, it was incubated in the dark at room temperature for 120 min. At the end of the incubation period, the absorbance of the mixture at 760 nm was read. The amount of 3.7 mL water, 500 µL methanol + 100 µL Folin-Ciocalteu reagent + 600 µL 10% Na₂CO₃ mixture was used as a blank. The amounts of phenolic substances in the samples were expressed as mg GA eq/g using the correct equation of the calibration graph obtained with the gallic acid solution.

Determination of Antimicrobial Activity

Microorganisms utilized in the research were attained from the laboratories of Gümüşhane University, Department of Food Engineering. The antimicrobial analyses of the methanol extracts were detected by disk-diffusion method against 13 microorganisms, including 10 bacteria and 3 yeast-molds (Matuschek et al. 2014). Antimicrobial activity was realized in two phases: preparation of bacteria and yeasts and preparation of examples. Bacteria were used in Nutrient Broth medium after 24 h of first activation at 36 °C and after 18 h of second activation at 36 °C. A total of 1% of the microorganisms to be used in the study were added to the prepared sterile solid media and they were poured into petri dishes and allowed to solidify. Then, 5 mm diameter wells were opened on the solidified media. The incubation process was conducted by adding the solutions of the methanol extract prepared with hexane to the opened wells. Petri dishes including bacteria were incubated for 24 h at 36 °C, and petri dishes including yeast and mold were incubated for 48 h at 27 °C. After the determined period, the outcomes were found by measuring the transparent areas around the discs.

Determination of Enzyme Inhibitory Activities

The α-glucosidase inhibitory activity of the samples was studied by modifying it (Yu et al. 2012). In the study, first, 650 μL of phosphate buffer (pH: 6.8 and 0.1 M) was added to the test tubes. Then, 20 μL of sample and 30 μL of α-glucosidase enzyme (Saccharomyces cerevisiae, lyophilized powder ≥ 10 units/mg protein) prepared in phosphate buffer were added. After the mixture was incubated at 37 °C for 10 min, 75 μL of substrate (4-nitrophenyl-α-D-glucopyranoside) was added. The mixture was kept at 37 °C for 20 min; then 650 μL of 1 M Na₂CO₃ was added to all tubes and the reaction was stopped. Absorbance ratios were measured at 405 nm in an ultraviolet/visible (UV/VIS) spectrophotometer (UV 1800, Shimadzu, Kyoto, Japan). Different concentrations of acarbose (positive control) were studied as the standard inhibitor. The study was performed in three parallel and reagent-sample blanks. The IC₅₀ values of acarbose and samples (sample concentration that halves the enzyme activity present in the environment) were calculated.

Determination of the Analysis of Vitamin C

Vitamin C analyses of the specimens were made using the HPLC-UV device with UV 1000 detector according to HPLC-UV detector method (Thermo Finnigan, San Jose, CA, USA). Analytical column RP C18 (250 x 4,6 mm, 5 µm), mobile phase: methanol: water (5:95, v/v) pH= 3 (H₃PO₄), flow 1 mL/min, injection volume 20 µL, with detection by UV at 254 nm. For the calibration curve, standard solutions of 10, 30, 60, 90, and 120 mg/L concentrations were prepared from L-ascorbic acid. Then, 10 g of R. coriaria fruits were taken and divided into pieces in a shredder. A total of 70 mL, a sufficient amount of metaphosphoric acid (15% m/m), was added to the smashed fruits and mixed in the homogenizer. The homogenized samples were completed to 100 mL and filtered through filter paper. After the filtrates were passed through a 0.45-micron filter, they were taken into vials and given to the HPLC device. The amount of analyzed vitamin C in the sample was calculated using the calibration graph method (y = 9498.7 x – 4236) (Öz et al. 2018).

RESULTS AND DISCUSSION

The GC-MS/FID analysis and chromatogram results of volatile oils attained from R. coriaria fruits are shown in Table 1 and Fig. 2. As a result of the analysis of essential oils by GC-MS/FID processes, the structure of a total of 74 constituents in R. coriaria fruits was found, but the structure of 4 constituents could not be defined. Caryophyllene (36.9%), thunbergene (12.95%), and (E,E)-2,4-decadienal (5.99%) were observed to be the highest constituents in volatile oils isolated from fruits. It is seen that the most common major compound in fruit samples is caryophyllene.

The GC-MS/FID analyses of the volatile oils determined 57 compounds in total. (E)-caryophyllene (50.3%), n-nonanal (23.3%), cembrene (21.7%), α-pinene (19.7%), and (2E,4E)-decadienal (16.5%) were determined as the major compounds of the volatile oils (Morshedloo et al. 2018). The results demonstrated that β-caryophyllene (34.3%) was the most frequently found constituent in R. coriaria (Zhaleh et al. 2018). β-caryophyllene (30.7%) was the main compound of Iranian sumac volatile oils (Gharaei et al. 2013). (E)-Caryophyllene, one of the main components of the species examined in this study, has been described as the main component of sumac essential oil in previous studies in Southeastern region of Türkiye (Bahar and Altug 2009), in Türkiye (Brunke et al. 1993), in Italy (Giovanelli et al. 2017), and in northern Iran (Gharaei et al. 2013). Alike, α-pinene is often explained as the major component of sumac volatile oils (Brunke et al. 1993). Fidyt et al. (2016) reported that β-caryophyllene and β-caryophyllene oxide have the ability to increase the efficacy of classical anticancer drugs such as paclitaxel or doxorubicin, as well as their direct anti-cancer activities. Sain et al. (2014) reported that beta caryophyllene and caryophyllene oxide, which they isolated, can act as potent anti-inflammatory agents. These compounds, which were identified as the main components within the scope of the present study, can potentially be used for the stated benefits.

The main components obtained in this study were similar to the main components found in previous studies. However, it was determined that there were differences in the percentages of these components. Different amounts and main components of R. coriaria were formerly shown for the volatile oil compound and dissimilar chemical profiles have been reported from dissimilar geographical and environmental conditions of the World (Brunke et al. 1993; Akbulut et al. 2009; Bahar and Altug 2009; Peter 2012; Giovanelli et al. 2017; Morshedloo et al. 2018).

Table 1. The Volatile Oil Constituents of Fruits in R. coriaria

RT: Retention time, RI^a: Retention indices computed against, RI^b: Literature retention indices supported on NIST, WILLEY, and Adams 2007.

Fig. 2. GC-MS/FID chromatograms of the volatile oils from fruit of R. coriaria

In Table 2, 74 constituents, whose structures were clarified regarding the outcomes of the analysis on the fruits of the R. coriaria plant, were classified as 10 groups. These groups and numbers of constituent were determined as alcohols 6, aldehydes 20, ketones 3, hydrocarbons 10, monoterpenes 8, monoterpenoids 8, sesquiterpenes 6, sesquiterpenoids 9, diterpenes 3, and others 1. As a result of the analysis of the fruits of the R. coriaria, the highest common chemical classes were determined as sesquiterpenes with 40.42% and aldehydes with 23.68%.

Among the monoterpenoids, α-pinene (19.7%) was the most plentiful constituent in the studied species. In contrast, sesquiterpenoids consisted primarily of caryophyllene oxide, α-humulene, and (E)-caryophyllene. Diterpenes and aliphatic constituents, including fatty acids and aldehydes, were the other major chemical classes of volatile oil constituents (Morshedloo et al. 2018).

Table 2. Chemical Classification of Constituents Determined in Fruits Volatile Oil of R. coriaria

The analysis and chromatogram results of phenolic constituents of R. coriaria fruits by HPLC-DAD methods are shown in Table 3 and Fig. 3.

Table 3. Phenolic Constituents in Fruits of R. coriaria

*0.1 mg/kg: LoQ (limit of quantitation) value

The main phenolic constituents of fruit samples were gallic acid (3708.60 mg/kg), syringic acid (465.71 mg/kg), protocatechuic acid (327.23 mg/kg), and 4-hydroxybenzoic acid (362.72 mg/kg). The highest phenolic constituents of fruits are gallic acid. A naturally occurring gallic acid is highly antioxidant and may play a protective role in healthy individuals by inhibiting apoptosis (Zahrani et al. 2007).

Phenolic constituents are among the rich sources of natural antioxidants (Akbulut et al. 2009). Gallic acid was determined as the major phenolic compound in both the authors’ study and previous study (Kosar et al. 2007). The authors’ results confirmed the data explained in the former works that noticed the same findings (Kosar et al. 2007; Fereidoonfar et al. 2019).

Fig. 3. Chromatogram of phenolic compounds from R. coriaria

Antioxidant activity analysis results of methanol extracts obtained from R. coriaria fruits are presented in Table 4. In the current work, the content of FRAP in methanol extract of fruit was determined as 14.9 mg FeSO₄ eq./g. The ABTS amounts of the samples were determined as 68.8 mg AA eq./g and 100.4 mg Trolox eq./g in fruit methanol extracts. The ABTS % inhibition rate was 98.0 in methanol extract of fruit. While the amount of DPPH was determined by 53.1 mg AA eq./g and 64.1 mg Trolox eq./g in methanol extract of R. coriaria fruit, the % inhibition rate of DPPH in the same samples was 79.6% (Table 4). It is seen that the FRAP, ABTS, and DPPH values in methanol extract of fruit samples studied have similar results with the literature.

In this study, the amount TAC, which is one of the bioactive component contents of the samples, was observed as 32.8 mg GA eq./g in methanol extract of fruit. The TFC content in methanol extract of fruit was 73.8 QE eq./g. The TPC content in methanol extract of fruit was determined as 41.4 mg GA eq./g.

The rates of TPC were determined in ranges of 44.5 to 125.0 mg GA eq./g and 36.3 to 114.5 mg GA eq./g for UA eq./g and HA eq./g, respectively. The TFC ranged from 4.95 to 13.9 mg EC eq./g for UA eq. and from 4.08 to 17.6 mg EC eq./g for HA eq./g (Zannou et al. 2022). In addition, the average TPC in sumac was 498 mg GA eq./g DW (Unver et al. 2009). Further, the average TPC in sumac fruits was determined as 152 mg GA eq./g DW (Raodah et al. 2014). While phenolic amount varied, ascorbic acid ranged from 10.0 to 45.0 mg per g, from 77.5 to 389.3 mg GA eq./g (Fereidoonfar et al. 2019). Anthocyanin fraction contained pelargonidin, petunidin, peonidin, cyanidin, and delphinidin glucosides and coumarates, while gallic acid was the major phenolic acid in the extracts. Phenolic quantity ranged from 77.5 to 389.3 mg GA eq./g DW. The determined phenol value of sumac was 172 mg GA eq./g DW (Kosar et al. 2007).

If the antioxidant activity results obtained from the authors’ plant samples are evaluated, it is seen that they are compatible with the literature. This situation shows parallelism with antimicrobial activities. There are some studies on the antioxidant activity of sumac. Both fruits and leaves have been reported for their antioxidant activities. It was determined that the tannin fractions of these samples had a powerful antioxidant capacity (Zalacain et al. 2000, 2002; Kosar et al. 2007). Phytochemicals and especially phenolic compounds are expressed as secondary metabolites and are known to have strong antioxidant effects. In recent work, it is stated that the consumption of plant materials with antioxidant activity may reduce the risk of various illnesses (Cory et al. 2018). R. coriaria may be useful in the correction or cure of various pathological disorders, for instance overweight and obesity (Jamous et al. 2018; Alsamri et al. 2021), myopathies (Najjar et al. 2017), and skin injuries (Nozza et al. 2020).

Table 4. Antioxidant Activity Contents and Bioactive Compounds of Methanol Extracts Attained from Fruits of R. coriaria

*: Means (The average of three parallel studies), ** ±: Standard deviation

At the end of the study, the results of methanol extract examples showing antimicrobial activity are given in Table 5. It was determined that the fruit of R. coriaria formed zones of 5.10 mm and 8.02 mm in diameter against Listeria monocytogenes and Staphylococcus aureus, respectively. Thus, it was shown that the methanol extracts of R. coriaria fruit showed antimicrobial activity. In the meantime, it was determined that the fruit of R. coriaria has antimicrobial effects against Listeria monocytogenes and Staphylococcus aureus.

Sumac ethanolic extract demonstrated a strong antimicrobial effect against the investigated bacteria. Salmonella enteric, Staphylococcus aureus, Escherichia coli, and Bacillus cereus isolates were the most to the least sensitive bacteria shown toward the ethanolic extract, respectively. E. coli showed the most resistance toward ethanolic extract among the examined standard strains (Mahdavi et al. 2018). There was a similarity in both the authors’ study and a previous study (Mahdavi et al. 2018). In both studies, it was determined that they showed antimicrobial effect against Staphylococcus aureus bacteria.

Table 5. Antimicrobial Activity of Crude Extract of R. coriaria Fruits

*Expressed as inhibition zone in mm, ** Penicillin G (10 mg) was used as the standard for bacteria, yeast, and molds

In the study, the results of the enzyme inhibitor activity in R. coriaria fruits are shown in Table 6. The enzyme inhibitor activity in R. coriaria fruits was 0.07 mg/mL.

Fruit extract α-glucosidase inhibition (IC₅₀) was 56.48 µg/ML (Gök et al. 2020). There was a similarity between the authors’ study and a previous study. Moreover, the authors’ study was slightly higher than their work (Gök et al. 2020).

Yu et al. (2012) stated in their study that the lower the IC₅₀ value of the sample, the more effective it is in enzyme inhibition. The lower the IC₅₀ value of the studied sample, the more effective it is in enzyme inhibition. Inhibitory activities on pancreatic lipase, α-amylase, and α-glucosidase were investigated with 80% extracts made from the fruits and leaves of the plant. Against all three enzymes analyzed, the detected IC₅₀ ratios of the fruit extracts were higher than the leaf extracts. Their research has also demonstrated that R. coriaria fruit and leaf extracts have antidiabetic potentials in vitro (Gök et al. 2020).

Table 6. Amount of Enzyme Inhibitory Activities in Fruits of R. coriaria

*: For positive control, **: The average of three parallel studies, ***±: Standard deviation

The amounts of vitamin C in the examined fruit samples of R. coriaria are given in Table 7. The amount of vitamin C in the fruits of R. coriaria was determined as 35.54 mg/100 g.

Table 7. Amount Vitamin C in Fruits of R. coriaria

*: The average of three parallel studies, SD: Standard deviation

CONCLUSIONS

In the gas chromatography – mass spectrometry with flame ionization detection (GC-MS/FID) analysis of the obtained volatile oils, 74 constituents were detected as the number of compounds in the fruits. The chemical groups with the most constituents in the volatile oils of the fruits of the R. coriaria were aldehydes. Sesquiterpene hydrocarbons were determined with 40.4% in the fruits of the chemical groups with the maximum percentage of constituents in the essential oils of plant parts. The main component found in the essential oils of plant parts was caryophyllene (36.9%) in its fruits.
The main phenolic constituents of fruit samples were protocatechuic acid, syringic acid gallic acid, and 4-hydroxybenzoic acid. The highest phenolic constituents of fruits were gallic acid.
The ABTS amounts of the samples were 68.8 mg AA eq./g and 100.4 mg Trolox eq./g in fruit methanol extracts. ABTS % inhibition rate was 98.0 in methanol extract of fruit. While the amount of DPPH was 53.1 mg AA eq./g and 64.1 mg Trolox eq./g in methanol extract of R. coriaria fruit, the % inhibition rate of DPPH in the same samples was 79.6%. The antioxidant capacity in the methanol extracts of plant parts was 14.9 mg FeSO₄ eq./g in FRAP capacity, 68.8 mg AA eq. and 100.4 mg Trolox eq./g in free radical scavenging (ABTS) capacity, 98.0% in ABTS % inhibition rate, 53.1 mg AA eq./g and 64.14 mg Trolox eq./g in free radical scavenging (DPPH), and 79.6% in DPPH % inhibition rate. Among the bioactive components of the samples, TAC amounts (32.8 mg GA/g), TFC amounts (73.8 mg QE eq./g), and TPC amounts (41.4 mg GA eq./g) were determined.
Concerning the results of the antimicrobial activity analysis of R. coriaria fruit samples, they showed antimicrobial activity against Staphylococcus aureus and Listeria monocytogenes microorganisms. Enzyme inhibitor activity in R. coriaria fruits was 0.069 mg/mL.
It is known that the lower the value of the studied sample, the more effective it is in enzyme inhibition. The amount of vitamin C in the fruits of R. coriaria was 35.5 mg/100 g.

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Article submitted: May 10, 2023; Peer review completed: June 18, 2023; Revised version received: July 16, 2023; Accepted: July 25, 2023; Published: August 7, 2023.

DOI: 10.15376/biores.18.4.6842-6861