Chemical composition, antioxidant activity and ...

South African Journal of Botany 116 (2018) 131–139

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Chemical composition, antioxidant activity and acetylcholinesterase inhibitory of wild Mentha species from northeastern Algeria A. Benabdallah a,d,⁎, M. Boumendjel b, O. Aissi c, C. Rahmoune d, M. Boussaid c, C. Messaoud c a

Department of Agronomy, SAPVESA Laboratory, Nature and Life Sciences Faculty, University Chadli Bendjedid El-Tarf, 36000, Algeria Department of Biochemistry, Biochemistry and Environmental Toxicology Laboratory, University Badji Mokhtar Annaba, 23000, Algeria Department of Biology, Laboratory of Plant Biotechnology, National Institute of Applied Science and Technology (INSAT), BP. 676, 1080 Tunis Cedex, Tunisia d Department of Natural and Life Sciences, Laboratory of Ecotoxicology and Abiotic Stress, University of Constantine 1, 25000 Constantine, Algeria b c

a r t i c l e

i n f o

Article history: Received 18 July 2017 Received in revised form 29 January 2018 Accepted 2 March 2018 Available online xxxx Edited by AM Viljoen Keywords: Mentha species Essential oil Algeria Antioxidant Acetylcholinesterase inhibitory

a b s t r a c t The aim of this work is to evaluate the chemical composition and biological activities of essential oils obtained from aerial parts of six wild Algerian Mentha species (M. aquatica, M. arvensis, M. x piperita, M. pulegium, M. rotundifolia and M. x villosa), collected from the National Park of El-Kala. Chemical composition was analyzed by GC‐MS, the DPPH, β-carotene bleaching and ion chelating assays were carried to assess the antioxidant activity, the Ellman method were used to determine the inhibition of acetylcholinesterase. Essential oil yields and compositions varied among species. The highest yield of oils (1.8%) recorded for M. pulegium. 27 compounds were identified with the predominance of oxygenated monoterpenes such as menthofurane (73.38%), rotundifolone (65.99%), pulegone (59.12%), α menthol (49.89%), menthone (20.84%), neomenthol (20.76%), 1.8-cineole (18.16%). M. aquatica and M. arvensis exhibited the strongest DPPH radical scavenging activity (IC50 = 0.69 ± 0.06 mg/ml and 0.76 ± 0.20 mg/ml, respectively) and the highest capacity to prevent β-carotene bleaching (IC50 = 0.16 ± 0.02 mg/ml and 0.22 ± 0.01 mg/ml, respectively). The uppermost ferrous ion chelating activity was observed for M. aquatica, M. arvensis and M. villosa (1.72 b IC50 b 1.73 mg/ml). Whereas essential oil of M. arvensis was found to be the most efficient (IC50 = 27.5 μg/ml) against acetylcholinesterase. Consequently, essential oils of Mentha species could be exploited for their pharmacological application in order to prevent induced diseases relied to oxidative stress. © 2018 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction The genus Mentha, belonging to Lamiaceae family, includes 61 species belonging to four sections (Pulegium, Tubulosae, Eriodontes, and Mentha) that are spread all over the world, especially in temperate and subtemperate regions (Šarić-Kundalić et al., 2009). Natural interspecific hybridization is observed with high frequency both in cultivation and in wild population of Mentha species (Smolik et al., 2007). Many species of mints have substantial interest due to their good flavor and appreciated oil, which represent one of the most important essential oil crops. They are used in traditional medicinal treatments as herbal remedies, food additives and taste enhancers for their olfactory properties (Dorman et al., 2003). Mentha genus, which common name in Algeria is “Naânaâ”, has large utilization in cooking and folk medicine. Infusion, decoction and hydrolat of the aerial parts of various Mentha species have been used for centuries as tonics, carminative, digestive, stomachic, antispasmodic, ⁎ Corresponding author at: Department of Agronomy, SAPVESA Laboratory, Nature and Life Sciences Faculty, University Chadli Bendjedid El-Tarf, 36000, Algeria. E-mail address: [email protected] (A. Benabdallah).

https://doi.org/10.1016/j.sajb.2018.03.002 0254-6299/© 2018 SAAB. Published by Elsevier B.V. All rights reserved.

and anti-inflammatory agents in Algerian folk medicine (Brahmi et al., 2016a). Recently, studies on the chemical composition, antimicrobial, antioxidant and insecticidal activities of Mentha pulegium, Mentha rotundifolia and Mentha spicata (Brahmi et al., 2016a, 2016b) collected from Bejaia (Northern Algeria), in the semi-humid climate, have been done. Moreover, the methanol extracts of Mentha species evaluated previously showed considerable antioxidant levels correlated to the strong polyphenol content (Benabdallah et al., 2016). Effective results on the acetylcholinesterase inhibitory ability by essential oils of Mentha species have been reported (Mata et al., 2007; de Sousa Barros et al., 2015). Whereas, there is no previous report on the acetylcholinestersae inhibitory of Algerian Mentha species. Mentha species are widely used by native habitants of El-Tarf region, situated in the extreme northeastern of Algeria, as condiment, flavor or herb in culinary preparations but also used for therapeutic properties as carminative, sedative, antispasmodic and well known to treat stomach pain. Despite ongoing research on mints, the presence of six wild Mentha species has not been reported previously, neither in the National Park of El-Kala (NPEK, El-Tarf region) nor in Algeria. Therefore, the interest of this study was to compare the oil composition of six

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A. Benabdallah et al. / South African Journal of Botany 116 (2018) 131–139

Fig. 1. Algerian Mentha species. A: M. arvensis/B: M. pulegium/C: M. x piperita/D: M. rotundifolia/E: M. x villosa/F: M. aquatica.

Mentha species (Fig. 1) growing wild in the North-East of Algeria (El Tarf), then to evaluate their antioxidant and acetylcholinesterase inhibitory activities. This study constitutes a tool for a better valorization of these wild species as important medicinal herbs to improve their conservation. 2. Materials and methods 2.1. Plant material For each species, aerial parts of twenty plants were harvested at their flowering stage and sampled from the National Park of El-Kala, situated in North-East Algeria (El Tarf region, 36°49′N 8°25′/Rainfall:

910–1200 mm per year). Before analyses, aerial parts were air-dried at room temperature for 2 weeks. 2.2. Essential oil Extraction and analysis For each species, aerial parts were ground then submitted to hydrodistillation for 3 h using a Clevenger-type apparatus; the obtained oils were dried with anhydrous sodium sulphate and then stored at 4 °C until analyses (Belhattab et al., 2014). The essential oil composition was determined by GC–MS analyses following the methods of Messaoud and Boussaid (2011), essential oil components were identified by comparison of their retention indices determined with reference to a homologous series of C9–C24 n-alkanes and with those of authentic


standards. Identification was confirmed by comparison of their mass spectra with those recorded in NIST08 and W8N08 libraries. 2.3. Antioxidant activities To assess the in-vitro antioxidant activity of Mentha species essential oils, three methods were used: the free radical scavenging, the ferrous ion chelating activities and the inhibition of β-carotene bleaching test. 2.3.1. Free radical scavenging activity The DPPH radical-scavenging capacity was measured as described by Sarikurkcu et al. (2012) with slight modifications. In this study, 50 μl of each essential oil was mixed with 950 μl of DPPH methanolic solution (60 μM). The reaction was allowed to stand at room temperature in the dark for 30 min and the absorbance was recorded at 517 nm. The scavenging activity (SA) was estimated using the following equation: SA (%) = 100× (Ac – As / Ac), where Ac is the absorbance of the control reaction (containing all reagents except the test sample) and As is the absorbance of the tested sample. The concentration of extract that could scavenge 50% of the DPPH radicals (IC50) was calculated. Trolox and was used as positive reference. 2.3.2. Ferrous ion chelating activity The ferrous ion chelating ability of essential oils was measured according to Messaoud et al. (2012), with slight modifications. In this study, 500 μl of each essential oil were added to 500 μl of FeSO4 (0.125 mM). After 5 min, the reaction was initiated by adding 500 μl of ferrozine (0.3125 mM), and incubated again for 10 min at room temperature. The absorbance of the solution was measured at 562 nm and the ability of essential oils to chelate ferrous ion was calculated using the following formula: Chelating effect (%) = [(Ac-As/Ac)] × 100; where Ac is the absorbance of the control sample and As is the absorbance of the tested sample. Results were expressed as IC50 (efficient concentration corresponding to 50% ferrous ion chelating). EDTA was used as a positive control. 2.3.3. Inhibition of β-carotene bleaching Inhibition of β-carotene bleaching by mints essential oils was carried out according to Mata et al. (2007). A solution of β-carotene was prepared by dissolving 2 mg of β-carotene in 20 ml of chloroform. 2 ml of this solution was mixed with 20 mg of linoleic acid and 200 mg of Tween 40. After the chloroform was removed at 40 °C under vacuum, 50 ml of oxygenated ultrapure water was added, and then the emulsion was vigorously shaken. Aliquots (750 μl) of this emulsion were transferred into different test tubes containing essential oils (50 μl). As soon as the emulsion was added to each tube, zero time absorbance of the control, containing methanol instead of essential oil, was measured at 470 nm. The test samples were then incubated in a water bath at 50 °C for 120 min, when the absorbance was measured again. The β-carotene bleaching inhibition was calculated using the following equation: Inhibition (%) = [(At − Ct) / (C0 − Ct)] × 100, where At and Ct are the absorbance values measured for the test sample and control, respectively, after incubation for 120 min, and C0 is the absorbance value for the control measured at zero time during the incubation. The results are expressed as IC50 values, the concentration required to cause a 50% β-carotene bleaching inhibition. BHT was used as a positive control. 2.4. Acetylcholinesterase inhibitory activity Inhibition of acetylcholinesterase was determined by Ellman method according to Eldeen et al. (2005), with slight modifications. Lyophilized acetylcholinesterase (AChE, from electric eel, type VI-S) was dissolved in buffer A (50 mM Tris–HCl, pH 8.0) in order to have 500 U/ml of stock solution, and further diluted with buffer B (50 mM Tris–HCl,

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pH 8.0, containing 0.1% bovine serum albumin) to get 0.28 U/ml. Tested essential oils were dissolved in methanol (5% in buffer B). Essential oils (20 μl) was mixed with 25 μl of AChE (0.28 U/ml) and incubated for 15 min at 37 °C. Subsequently, 100 μl of 0.15 mM ATCI in water, 500 μl of 0.3 mM DTNB in Buffer C (50 mM Tris–HCl, pH 8.0, containing 0.1 M NaCl, 0.02 M Mg Cl2-6H2O) and 355 μl of Buffer B were added then incubated for 30 min at 37 °C. The absorbance was measured at 405 nm. Percentage of inhibition of AChE enzyme was determined by comparison of reaction rates of samples relative to blank sample (5% methanol or buffer B) using the formula 100×(Bs − Ts) / Bs, where Bs is the activity of enzyme without test sample, and Ts is the activity of enzyme with test sample. Results were also expressed as IC50. 2.5. Statistical analysis All tests were performed in triplicate and results were expressed as mean ± standard error. For each analysis, the results were compared by analysis of variance (ANOVA) followed by Duncan's multiple range test using SAS v.9.1.3 program. The UPGMA Cluster Analysis, based on essential oil composition, was applied to examine the inter-relationships between species. Correlations between essential oil compounds or and biological activities were determined with PROC CORR procedure using SAS program. 3. Results 3.1. Essential oil yields The yield of each essential oil varied among Mentha species (Fig. 2). M. pulegium showed the highest yields with 1.8%, followed by M. rotundifolia with 1.65% and M. arvensis with 1.2%, while the lowest values were recorded for M. piperita, M. aquatica and M x villosa with 1.0%, 0.92% and 0.8%, respectively. 3.2. Chemical variation of Mentha species essential oil composition The identified compounds and their percentages were listed in Table 1. Qualitative and quantitative variations were recorded for the essential oil components between the studied species. The identified compounds in essential oils varied from 11 to 27, with percentages ranged from 90.13% to 98.64%. Mentha species from El-Tarf region were rich in the oxygenated monoterpenes menthofuran, rotundifolone (piperitenone oxide), pulegone, menthol, menthone, neomenthol, β-caryophyllene and 1.8-cineol (eucalyptol). Essential oil of M. aquatica presents 14 compounds representing 98.64% of the total oil composition which is characterized by menthofurane (73.38%), followed by 1.8-cineole (10.26%) and βcaryophyllene (4.57%) as major components. As minor ones, we found Δ-cadinol (1.98%), γ-muurolene (1.95%), α-limonene (1.72%) and α-terpineol (1.37%). In M. arvensis, we record 27 constituents representing 95.65% of the total oil composition with menthofurane (29.69%), 1.8-cineole (18.16%) and β-caryophyllene (12.55%) as main components while Δ-cadinol (7.5%), γ-muurolene (5.48%), borneol (3.64%), β-fenchol (3.01%) and pulegone (2.72%) were in lower amounts. M. x piperita presents 11 compounds with 97.6% of the total essential oil composition characterized by menthol (49.89%) and menthone (20.84%) whereas isomenthone (7.25%), 1.8-cineole (6.73%) and ciscarane (4.99%) where the minor constituents (Table 1). In essential oils extracted from M. pulegium, 19 compounds were identified, corresponding to 95.62% of the total oil. Pulegone (59.12%) and neomenthol (20.76%) stood out, followed by menthone (6.59%) while isomenthone (2.13%) and trans-isopulegone (1.55%) were recorded in lower amounts (Table 1). Essential oils of M. rotundifolia present 22 constituents (91.87% of the total oil). The rotundifolone (65.99%) was the main component, whereas

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Fig. 2. Essential oil yields of the analyzed Mentha species.

Table 1 Chemical composition of Algerian Mentha species essential oils.

Compounds

M. aquatica

M. arvensis

M. x piperita

M. pulegium

M. rotundifolia

M. x villosa

Monoterpene hydrocarbons α-Pinene β-Pinene α-Limonene Camphene Cis-carane Δ4(8)menthene Oxygenated monoterpenes 1.8-Cineole Piperitone oxide Cis-jasmone Trans-isopulegone β-Fenchol p-Menth-1-en-8-ol Bornyl acetate Borneol Isopulegol α-Terpineol Piperitone Piperitenone Rotundifolone Menthofurane Pulegone Al canphor Menthol Neomenthol Isomenthone p-Menthone Sesquiterpene hydrocarbons Bicyclogermacrene α-Copaene Δ-Cadinene α-Caryophyllene α-Gurjunene β-Caryophyllene β-Bourbonene γ-Murolene Aromadendrene β–Farnesene β-Elemene Germacrene D Oxygenated Sesquiterpenes Spathulenol Caryophyllene epoxide Δ-cadinol 1.6-Germacradien-5-ol Total identified (%)

3.14 0.2 0.86 1.72 – 0.36 – 86.04 10.26 – – – – – 0.58 – – 1.37 – – – 73.38 0.45 – – – – – 7.48 – – – 0.67 0.29 4.57 – 1.95 – – – – 1.98 – – 1.98 – 98.64

5.4 0.83 2.19 1.75 0.23 0.4 – 59.05 18.16 – 0.36 – 3.01 – – 3.64 – 0.44 – – 0.86 29.69 2.72 – – – – 0.17 22.55 0.42 – 0.6 2.06 0.54 12.55 0.22 5.48 0.19 – 0.49 – 8.65 0.19 0.72 7.5 0.24 95.65

12.06 2.09 1.59 2.97 – 4.99 0.42 85.54 6.73 – – – – – – – 0.41 – – – – – 0.42 – 49.89 – 7.25 20.84 – – – – – – – – – – – – – – – – – – 97.6

2.01 – 0.44 0.91 – 0.66 – 92.03 0.23 – – 1.55 – – – – 0.3 0.57 0.44 – 0.19 – 59.12 0.15 – 20.76 2.13 6.59 0.75 – – – 0.34 – 0.21 – – – – – 0.2 0.83 – 0.19 0.64 – 95.62

0.57 – – 0.57 – – – 71.3 0.14 – 1.1 – – 0.68 – 0.29 – 0.13 – 1.37 65.99 0.26 1.34 – – – – – 17.24 0.47 0.9 1.16 – 0.26 2.51 0.21 6.19 – 5.12 0.42 – 2.76 0.91 0.3 1.55 – 91.87

0.27 – – 0.27 – – – 70.1 – 2.5 2.72 – – 2.08 – 2.63 – 2.13 – 2.09 52.17 – 3.78 – – – – – 16.79 – 0.82 1.93 – – 5.14 – 3.14 1.03 3.45 0.39 0.89 2.97 1.01 1.96 – – 90.13

Entries in bold represent major compounds with amounts superior to 5%.


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Fig. 3. Cluster analysis based on the essential oil composition of Mentha species.

γ-muurolene (6.19%), β-farnesene (5.12%), and β- caryophyllene (2.51%) turned out in lower amounts. M. villosa oils present 19 compounds (90.13%), with rotundifolone (52.17%) as major constituent, while β-caryophyllene (5.14%), pulegone (3.78%), β-farnesene (3.45%) and γ-muurole (3.14%) were minor ones. In our study, the cluster analysis constructed from the chemical data of the six Mentha species is represented in Fig. 3. The analyzed species were found to be clustered into two major groups, with M. rotundifolia, M. villosa, M. piperita, M. arvensis and M. aquatica being grouped on the first group and M. pulegium comprised the second one. These clustering are strongly associated with the taxonomy of the genus Mentha. In fact, the five first species represented the section Mentha whereas the single position of M. pulegium in the second brunch is representative of the section Pulegium. This result indicates a high amount of sharing of chemical compounds among the studied species. The first cluster, which constitutes the section Mentha is subdivided into three distinct subgroups. The first one includes M. rotundifolia with M. villosa, at a higher hierarchical level, which is related to the presence of rotundifolone as main compound. On the other hand, M.x villosa is a hybrid issued from the hybridization of the two basic species M. rotundifolia (M. suaveolens) and M. spicata. The second subgroup was formed by M. piperita, while M. arvensis and M. aquatica were closely related to each other in the third subcluster.

from 0.69 to 4.75 mg/ml, which is lower than IC50 values of the trolox (3.77 ± 0.12 μg/ml). M. aquatica (0.69 ± 0.06 mg/ml) and M. arvensis (0.76 ± 0.20 mg/ml) exhibited the strongest free radical DPPH scavenging activity, followed by M. pulegium (0.97 ± 0.01 mg/ml). The IC50 of M. rotundifolia and M. villosa was 1.5 ± 0.05 and 1.86 ± 0.06 mg/ml, respectively. While M x piperita was the weakest with IC50 of 4.75 ± 0.14 mg/ml. Mentha species revealed a noticeable capacity to prevent β-carotene bleaching with an IC50 ranged from 0.16 to 0.62 mg/ml (Table 2). However these values are very weak regarding the standard BHT (29 ± 0.11 μg/ml). M. aquatica (0.16 ± 0.02 mg/ml) and M. arvensis (0.22 ± 0.01 mg/ml) also showed the highest ability to inhibit βcarotene bleaching, followed by M. rotundifolia (0.54 ± 0.03 mg/ml). M. pulegium and M. villosa showed the same IC50 value (0.62 ± 0.02 mg/ml), whereas M. x piperita was the less effective (1.25 ± 0.01 mg/ml). All essential oils showed a significant ability to chelate ferrous ion with IC50 value ranging from 1.72 ± 0.35 to 4.03 ± 0.02 mg/ml, which is inferior to the standard EDTA with 6.5 ± 0.2 μg/ml (Table 2). The uppermost ferrous ion chelating activity was observed for M. arvensis, M. villosa and M. aquatica (1.72 b IC50 b 1.73 mg/ml). M. x piperita (2.39 ± 0.07 mg/ml) and M. pulegium (2.64 ± 0.28 mg/ml) exhibited acceptable levels, while M. rotundifolia gave the lowest rate (4.03 ± 0.02 mg/ml).

3.3. Antioxidant activity 3.4. Acetylcholinesterase inhibitory ability All mint essential oils exhibited significant antioxidant activity as determined by the three methods (Table 2.), but still lower than standards used. For the free radical DPPH scavenging, the IC50 was ranged Table 2 Antioxidant activities and acetylcholinesterase inhibitory of Mentha species essential oils. DPPH

M. aquatica M. arvensis M. x piperita M. pulegium M. rotundifolia M. villosa

β-Carotene bleaching

Chelating ability

Acetylcholinesterase inhibitory

(IC50, mg/ml) (IC50, mg/ml)

(IC50, mg/ml) (IC50, μg/ml)

0.69e ± 0.06 0.76e ± 0.20 4.75a ± 0.14 0.97d ± 0.01 1.50c ± 0.05

0.16d ± 0.02 0.22d ± 0.01 1.25a ± 0.01 0.625b ± 0.02 0.54c ± 0.03

1.73c ± 0.17 1.72c ± 0.35 2.39b ± 0.07 2.64b ± 0.28 4.03a ± 0.02

32.58e ± 0.22 27.50f ± 0.29 63.92c ± 2.07 108.75b ± 0.83 52.5d ± 1.44

1.86b ± 0.06

0.62b ± 0.02

1.72c ± 0.35

137.5a ± 1.44

Values are given as mean ± SD (n = 3).Values in each column followed by different letters are significantly different. (p ˂ 0.05). IC50 values for the Trolox: 3.77 ± 0.12 μg/ml (DPPH scavenging activity). IC50 values for the BHT: 29 ± 0.11 μg/ml (β-carotene bleaching inhibition). IC50 values for the EDTA: 6.5 ± 0.2 μg/ml (Chelating ability). IC50 value for the Donepezil: 18 ± 0.1 μg/ml (acetylcholinesterase inhibitory).

All tested essential oils possessed the ability to inhibit AChE (Table 2). However, significant differences in AChE inhibitory properties were established between the studied species, and IC50 values varied from 27.5 to 137.5 μg/ml, which is still lower than the standard used donepezil (18 ± 0.1 μg/ml). The most potent mint was M. arvensis (27.5 μg/ml) followed by M. aquatica (32.58 ± 0.22 μg/ml), M. rotundifolia (52.5 μg/ml) and M. piperita (63.916 μg/ml) demonstrated moderate inhibitory activity. Thus, lowest IC50 values were recorded for M. pulegium (108.5 μg/ml) and M. villosa (137.5 μg/ml). 4. Discussion Since interest has increased in naturally bioactive compounds that can preserve human health from oxidative stress damage, and inhibit enzymes involved in several diseases (Harkat-Madouri et al., 2015), our work aimed to investigate, for the first time, six wild Algerian Mentha species through essential oil chemical composition analyses, antioxidant and acetylcholinesterase inhibitory assays. Regarding essential oil yields, M. pulegium showed greater yield comparing to

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precedent studies from different localities, such as from Iran (0.65%) (Kamkar et al., 2010), Portugal (0.7%) (Mata et al., 2007) and Turkey (0.3–1.2%) (Baser et al., 2012) but lower than yield from Morroco pennyroyal (2.7%) (Ait-Ouazzou et al., 2012). M. rotundifolia, harvested from our region, yielded 1.65% which is higher than oils from Tunisia which gave 1.26% (Riahi et al., 2013) and Morroco 1.17% (Kasrati et al., 2015), but inferior to yields recorded from other locations, in Algeria 1.8% (Brada et al., 2007) and Morroco 4.33% (Benayad et al., 2012). The yield of M. arvensis oils from El-Tarf is about 1.2% (Fig. 2). Near rates were obtained for Indian samples, with percentage of 0.6–1% (Singh et al., 2005). Whereas, Sharma et al. (2009), who worked on the same species, from different regions of India, reported lower yields of 0.31–0.38%. In the case of M. piperita, we recorded a yield of 1%, comparable to values from Morroco 1.02% (Derwich et al., 2010), Pakistan 1.2% (Hussain et al., 2010) and Iran with 1.38% (Moghaddam et al., 2013). Result of M. aquatica essential oil yield was 0.92%, which is similar to that recorded for Brazilian 0.93% (Agostini et al., 2009) and Serbian watermint 0.94% (Jerkovic and Mastelic, 2001). Dhifi et al. (2011) reported a higher rate (1.2%) for Tunisian species, while lower yield of 0.69% was obtained from Yugoslavia (Mimica-Dukic et al., 2003). Samples of M. villosa gave 0.8% (Fig. 2), comparable to yield observed from Czech Republic, which yielded 0.83% (Nedorostova et al., 2009). Hence Brazilian samples exhibited lower yields of 0.1% and 0.5%, according to Lima et al. (2014) and Sousa et al. (2009), respectively. Considering the chemical composition of the six Mentha species, our results are in accordance with that reported for Indian M. aquatica where menthofurane was the main compounds with 40% (Bhat et al., 2002). Whereas, for Tunisian and Brazilian populations, menthone (27.69%- 77.76%) and pulegone (39.36%, 14.39%) were found to be the major compounds, respectively (Dhifi et al., 2011; Agostini et al., 2009). Concerning M. arvensis, a related percentage of 1, 8-cineole (10.04%) was noticed by de Sousa Barros et al. (2015), for Brazilian corn mint. The same author mentioned the high content of linalool (34.57%). Gracindo et al. (2006), from the same country, reported that linalool was the main compound with 78.5%. On the other hand, Sharma et al. (2009), who analyzed corn mint oils from three localities of North India, reported L-menthone, menthol, isomenthone, 1, 8-cineole, piperitone oxide, carvone, limonene, transdihydrocarvone, and germacrene-D, with great percentages. For M. piperita, the findings on menthol and menthone as main constituents of oil were in agreement with previous reports. According to Moghaddam et al. (2013) and Hussain et al. (2010), menthone was recorded in noticeable amounts in oil from Iran (30.63%) and Pakistan (28.13%). Menthol was even found as major compound in essential oil of Iran (25.16%), whereas it was detected in a lower amount from Pakistanian peppermint (4.83%). However, the Brazilian species showed a total different composition with d-carvone (58.79%) and limonene (28.29%) as main constituents (de Sousa Barros et al., 2015). Furthermore, the Colombian peppermint oils, were highly rich in pulegone (44.54%) and iso-menthone (26.15%) (Roldan et al., 2010). Regarding M. pulegium, the pulegone was also the most abundant compounds in M. pulegium of different countries, with high percentages. For Moroccan pennyroyal, pulegone were ranged from 33.65% to 69.8% (Cherrat et al., 2014; Ait-Ouazzou et al., 2012), for Egyptian 43.5% (El-Ghorab, 2006). In addition, M. pulegium from southeastern Algeria showed similar proportions of pulegone (46.31%) and menthone (6.2%) as major components (Ouakouak et al., 2015). Nevertheless, the highest contents of pulegone ranged from 85 to 95% were recorded for Indian pennyroyal (Bhat et al., 2002). For M. rotundifolia, our results are in agreement to samples collected from Argentina and Brasil where rotundifolone was recorded as main compound with high percentages of 63.3% and 79%, respectively (Gende et al., 2014; Gracindo et al., 2006). Riahi et al. (2013), who studied the Tunisian species noticed that there is a difference in chemical

compositions between the locality of Beja situated in north western Tunisia, where β-caryophyllene (26.67%) was the main component while those harvested from north eastern of Tunisia (Bizerte) had pulegone (32.09%) chemotype. This is in accordance with Morrocan samples where pulegone was the major constituent with 85.5% (El Arch et al., 2003). About M. villosa, related contents have been reported by Sousa et al. (2009), where M. x villosa leaves essential oil revealed rotundifolone in high concentration (79.03%), while β-caryophyllene (2.82%) and γmuurolene (2.18%) were turned out to have lower amounts. Lima et al. (2014) have also recorded, for Brazilian species, rotundifolone (70.96%) as main component, whereas limonene (8.75%), germacrene D (3.81%), myrcene (3.10%), trans-caryophyllene (1.46%) and other constituents in a low quantity. Moreover, Teles et al. (2013), who conducted his analysis in three different municipalities of Brazil, also noted the great content of rotundifolone (69–72%) and γ-muurolene (1.50–2.60%) as minor compounds. However chemical analysis results of oils from thee populations of M x villosa in the USA demonstrated carvone (44.2–68.1%), dihydrocarvyl acetate (18.0%) and cis-dihydrocarvone (14.1%) as major constituents (Lawrence, 1978). Variation in chemical composition is strongly related to environmental factors, such as climate, soil type (Brada et al., 2007), agronomic conditions and genotype content (Burt, 2004). The drying method, oil extraction technique (Singh et al., 2012) and harvesting season (Giray et al., 2008) also influenced the composition of essential oils. In fact, the oil content depends upon both biotic (Bhat et al., 2002) and abiotic factors affecting plant growth (Boukhebti et al., 2011). The distribution of oil compounds could be very interesting to assess the chemotaxonomy among species (Messaoud and Boussaid, 2011). In our study, the cluster analysis constructed from the chemical data of the six Mentha species is represented in Fig. 3. The analyzed species were found to be clustered into two major groups, with M. rotundifolia, M. villosa, M. piperita, M. arvensis and M. aquatica being grouped on the first group and M. pulegium comprised the second one. These clustering are strongly associated with the taxonomy of the genus Mentha. In fact, the five first species represented the section Mentha whereas the single position of M. pulegium in the second brunch is representative of the section Pulegium. This result indicates a high amount of sharing of chemical compounds among the studied species. The first cluster, which constitutes the section Mentha is subdivided into three distinct subgroups. The first one includes M. rotundifolia with M. villosa, at a higher hierarchical level, which is related to the presence of rotundifolone as main compound. On the other hand, M.x villosa is a hybrid issued from the hybridization of the two basic species M. rotundifolia (M. suaveolens) and M. spicata. The second subgroup was formed by M. piperita, while M. arvensis and M. aquatica were closely related to each other in the third subcluster. According to our results (Table 1), M. x piperita, which constitutes the second subgroup (Fig. 3), is the only species rich in menthol (49.89%) and menthone (20.84%), so very different chemically from the other species. Moreover, M. x piperita is created from the hybridization of M. spicata with M. aquatiqua. The third subcluster comprises M. arvensis and M. aquatica, these two species were rich in menthofurane and have great morphological resemblance. Studies have attempted to describe the genetic relationships in genus Mentha using cytological, morphological (Šarić-Kundalić et al., 2009), and genetic characteristics (Wang et al., 2013; Attiya et al., 2012). Consequently, essential oil composition alone was not fully reliable to differentiate species and hybrids of the genus Mentha L. and did not equivocally reflect the true evolutionary and phylogenetic relationships among mints. Many researchers evaluated the antioxidant activities of Mentha species only by DPPH radical scavenging (Derwich et al., 2011; Ouakouak et al., 2015), or in combination to β-carotene-linoleic acid methods (Mata et al., 2007; Kamkar et al., 2010; Cherrat et al., 2014; de Sousa Barros et al., 2015). The antioxidant abilities of essential oils

A. Benabdallah et al. / South African Journal of Botany 116 (2018) 131–139 Table 3 Correlation coefficients (R) between major oil compounds and antioxidant and antiacetylcholinesterase activities.

Rotundifolone Menthofurane Pulegone Menthol 1,8-Cineole β-Caryophyllene Neomenthol γ-Muurolene

DPPH

β-Carotene bleaching

Chelating ability

Acetylcholinesterase inhibitory

−0.147 −0.423 −0.236 0.963⁎⁎ −0.107 −0.464 −0.220 −0.505

0.006 −0.693 0.062 0.854⁎ −0.417 −0.673 0.075 −0.531

0.540 −0.488 0.128 0.010 −0.542 −0.490 0.145 0.283

0.339 −0.618 0.458 −0.073 −0.749⁎ −0.399 0.428 −0.361

⁎ Significant at p b 0.05. ⁎⁎ Significant at p b 0.01.

could be associated with their chemical content, especially to their major compounds (Derwich et al., 2011). In our results, the antioxidant activity may be attributed to the high content of oxygenated monoterpenes in all species, mainly menthofuran, 1,8-cineole, rotundifolone, menthol and pulegone. This is in agreement to Mimica-Dukic et al. (2003) and Yadegarinia et al. (2006), who reported that oxygenated monoterpenes were the most effective on radical scavenging compounds. Whereas, Ruberto and Baratta (2000) noted that monoterpene hydrocarbons had the strongest antioxidant ability. In our study, the antioxidant variation observed among species reflects their essential oil composition differences. The constituent contributing most to the variation of antioxidant activities between samples was Menthol (Table 3). However, the absence of significant correlation between amounts of other compounds and antioxidant activities does not exclude their antioxidant potentialities, since their biological activities have been widely proven. So, in many cases, the antioxidant activity may be attributed to minor components of essential oils rather than major ones (Mukazayire et al., 2011). Furthermore, both minor and major constituents could act on synergism to create chemical mixture, which contributes to a better antioxidant activity of essential oils (Wang et al., 2008). The antioxidant activity of essential oils may be associated with multiple systems, as they possess chemical mixture with diverse functional groups, polarity and chemical behavior (Boumendjel and Boutebba, 2003, Rodrigo and Bosco, 2006; Tepe et al., 2006). Reports of antioxidant activities evaluated by multiple tests are not, necessarily, in agreement (Candan et al., 2003; Trouilla et al., 2003; Sachetti et al., 2005; Tepe et al., 2005). Relating to acetylcholinesterase inhibitory effect of essential oil obtained from Algerian wild mints, our results agree to Miyazawa et al. (1998), who studied inhibition of acetylcholinesterase activity by essential oils of Mentha species from Japan, observed an important acetylcholinesterase inhibitory of oxygenated monoterpenes such as menthofuran, rotundifolone, menthol and pulegone, which are the main components of our mint essential oils. On the other hand, Öztürk (2012) and Savelev et al. (2003), who worked on other Lamiaceae species (Satureja thymbra and Salvia lavandulaefolia), noted anticholinesterase properties of other terpenes, as well as α-pinene, 1,8-cineole, camphor, linalool … etc. However, de Sousa Barros et al. (2015), who analyzed Brazilian mint oils for AChE inhibitory, did not record any activity for menthol and pulegone, known as strong inhibitors. Mata et al. (2007) also reported a moderate AChE inhibitory activity for oxygenated monoterpenes of Portuguese Mentha samples. The acetylcholinesterase inhibitory effect of the essential oils could be explained by their richness in monoterpenes that found to act as competitive or uncompetitive inhibitors due to their hydrophobicity and their ability to interact with the hydrophobic site of this enzyme (Aazza et al., 2011). The observed variation of acetylcholinesterase inhibitory between species could be attributed to their composition differences mainly to 1, 8-cineole (Table 3).

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Consequently, it is difficult to attribute the AChE inhibitory property to one constituent present in high amounts of essential oils, but it is better to take account of both major and minor compounds which could react in a synergistic or antagonistic way. 5. Conclusions This study reports, for the first time, qualitative and quantitative analysis of six wild Algerian Mentha species, which are M. aquatica, M. arvensis, M. x piperita, M. pulegium, M. rotundifolia and M. x villosa. Yield, chemical composition, antioxidant activity and acetylcholinesterase inhibitory varied among species. The high proportion of oxygenated monoterpenes menthofuran, rotundifolone, pulegone, menthol, menthone, neomenthol, βcaryophyllene and 1.8-cineol was observed. A noticeable antioxidant activity was recorded, especially for M. aquatica, whereas M. arvensis was the most efficient toward acetylcholinesterase inhibitory. According to our evaluation, Algerian wild Mentha species could be investigated as promising antioxidant sources and neuroprotective agents through their chemical variability and functional properties. Further studies of cytotoxicity and in-vivo tests of these potential mint essential oils are required in order to be exploited in food and pharmaceutical industries. To provide relevant information regarding the conservation of these medicinal plants, the analysis of the genetic variation within and among populations of Mentha species based jointly on several traits such as morphological, chemical and molecular markers is necessary. Conflict of interest statement The authors declare that there are no conflicts of interests. References Aazza, S., Lyoussi, B., Miguel, M.G., 2011. Antioxidant and antiacetylcholinesterase activities of some commercial essential oils and their major compound. Molecules 16: 7672–7690. https://doi.org/10.3390/molecules16097672. Agostini, F., Atti Dos Santos, A.C., Rossato, M., Pansera, M.R., Dos Santos, P.L., Atti Serafini, L., Molon, R., Moyna, P., 2009. Essential oil yield and composition of Lamiaceae species growing in southern Brazil. Brazilian Archives of Biology and Technology 52: 473–478. https://doi.org/10.1590/S1516-89132009000200026. Ait-Ouazzou, A., Loran, S., Arakrak, A., Laglaoui, A., Rota, C., Herrera, A., Pagan, R., Conchello, P., 2012. Evaluation of the chemical composition and antimicrobial activity of Mentha pulegium, Juniperus phoenicea, and Cyperus longus essential oils from Morocco. Food Research International 45:313–319. https://doi.org/10.1016/j. foodres.2011.09.004. Attiya, J., Bin, G., Bilal, H.A., Zabta, K.S., Tariq, M., 2012. Phylogenetics of selected Mentha species on the basis of rps8, rps11 and rps14 chloroplast genes. Journal of Medicinal Plants Research 6:30–36. https://doi.org/10.5897/JMPR11.658. Baser, K.H.C., Kurkcuoglu, M., Demirci, B., Ozek, T., Tarımcılar, G., 2012. Essential oils of Mentha species from Marmara region of Turkey. Journal of Essential Oil Research 24:265–272. https://doi.org/10.1080/10412905.2012.676775. Belhattab, R., Amor, L., Barroso, J.G., Pedro, L.G., Figueiredo, C.A., 2014. Essential oil from Artemisia herba-alba Asso grown wild in Algeria: variability assessment and comparison with an updated literature survey. Arabian Journal of Chemistry 7:243–251. https://doi.org/10.1016/j.arabjc.2012.04.042. Benabdallah, A., Rahmoune, C., Boumendjel, M., Aissi, O., Messaoud, C., 2016. Total phenolic content and antioxidant activity of six wild Mentha species (Lamiaceae) from northeast of Algeria. Asian Pacific Journal of Tropical Biomedicine 6:760–766. https://doi.org/10.1016/j.apjtb.2016.06.016. Benayad, N., Ebrahim, W., Hakiki, A., Mahjouba Mosaddak, M., 2012. Chemical characterization and insecticidal evaluation of the essential oil of Mentha suaveolens L. and Mentha pulegium L. growing in Morocco. Scientific Study & Research 13, 027–032. Bhat, S., Maheshwari, P., Kumar, S., Kumar, A., 2002. Mentha species: in vitro regeneration and genetic transformation. Molecular Biology Today 3, 11–23. Boukhebti, H., Chaker, A.N., Belhadj, H., Sahli, F., Ramdhani, M., Laouer, H., Harzallah, D., 2011. Chemical composition and antibacterial activity of Mentha pulegium L. and Mentha spicata L. essential oils. Der Pharmacia Lettre 3, 267–275. Boumendjel, M., Boutebba, A., 2003. Heat treatment effect on the physico-chemical and nutritional content of double concentrate tomato paste. Acta Horticulturae 429–432. Brada, M., Bezzina, M., Marlier, M., Carlier, A., Lognay, G., 2007. Variabilité de la composition chimique des huiles essentielles de Mentha rotundifolia du Nord de l'Algérie. Biotechnology, Agronomy, Society 11, 3–7. Brahmi, F., Adjouad, A., Marongiu, B., Porcedda, S., Piras, A., Falconieri, D., Yalaoui-Guellal, D., Elsebai, M.-F., Madani, K., Chibane, M., 2016a. Chemical composition and in vitro antimicrobial, insecticidal and antioxidant activities of the essential oils of Mentha

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