Chemical and morphological characterization of Allium tuncelianum (Amaryllidaceae) and its antioxidant and anticholinesterase potentials

Songul KARAKAYA 1,*, Gulnur EKSI 2, Mehmet KOCA 3, Betul DEMIRCI 4, Haluk Caglar KAYMAK 5, Mehmet Emin KAPLAN 6 & Ozkan AKSAKAL 7

1,6 Department of Pharmacognosy, Faculty of Pharmacy, Ataturk University, Erzurum, Turkey.

2 Department of Pharmaceutical Botany, Faculty of Pharmacy, Ankara University, Ankara, Turkey.

3 Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Ataturk University, Erzurum, Turkey.

4 Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University, Eskisehir, Turkey.

5 Department of Horticulture, Faculty of Agriculture Ataturk University, Erzurum, Turkey.

7 Department of Biology, Faculty of Science, Ataturk University, Erzurum, Turkey.

* Corresponding author:,



4 betuldemirci,






Alzheimer’s disease is the main reason for dementia, which increases with age. Cholinesterase inhibition and antioxidant potentials of extracts and essential oils from bulbs of A. tuncelianum (Kollmann) Özhatay & al., an endemic species to Tunceli (easthern Turkey), were evaluated. The fraction extracted of ethyl acetate had the highest phenolics level, 1,1-diphenyl-2-picrylhydrazyl, and thiobarbituric acid antioxidant capacity. Also, the ethyl acetate fraction presented the highest acetylcholinesterase (15.98 ± 2.76%), and butyrylcholinesterase inhibition (47.33 ± 3.27%). Diallyl disulfide (49.8%), diallyl trisulfide (27.9%) and allyl methyl trisulfide (6.9%) were found to be the major components of essential oil. This paper shows that the ethyl acetate fraction of A. tuncelianum could be a potent source of antioxidant and anticholinesterase components.

Keywords. Allium tuncelianum, anticholinesterase, endemic, essential oil, morphology.



La enfermedad de Alzheimer es la causa principal de la demencia, cuya aparición aumenta según la edad. Se evaluaron la inhibición de la colinesterasa y el potencial antioxidante de los extractos y los aceites esenciales de los bulbos de A. tuncelianum (Kollmann) Özhatay & al., una especie endémica de Tunceli (este de Turquía). La fracción extraida de acetato de etilo presentó los niveles más altos de fenoles, 1,1-difenil-2-picrilhidrazilo y capacidad antioxidante, ácido tiobarbitúrico. Asimismo, la fracción de etil acetato presentó la mayor capacidad de inhibición de acetilcolinesterasa (15.98 ± 2.76%) y butirilcolinesterasa (47.33 ± 3.27%). El disulfuro de dialilo (49.8%), el trisulfuro de dialilo (27.9%) y el trisulfuro de metil alilo (6.9%) fueron los componentes principales del aceite esencial. Este artículo muestra que la fracción de etil acetato de A. tuncelianum podría ser una fuente potencial novedosa de componentes antioxidantes y anticolinesterasa.

Palabras clave. Aceite esencial, Allium tuncelianum, anticolinesterasa, endémico, morfología.


Received: 25‒III‒2019; accepted: 28‒V‒2019; published on-line: 28‒X‒2019; Associate Editors: M.C. Sánchez Mata & R. Morales.

How to cite this article: Karakaya S., Eksi G., Koca M., Demirci B., Kaymak H.C., Kaplan M.E. & Aksakal O. 2019. Chemical and morphological characterization of Allium tuncelianum (Amaryllidaceae) and its antioxidant and anticholinesterase potentials. Anales del Jardín Botánico de Madrid 76 (2): e085.

Title in Spanish: Caracterización química y morfológica de Allium tuncelianum (Amaryllidaceae) y potenciales antioxidantes y anticolinesterasa.

Copyright: © 2019 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (CC BY 4.0).





Alzheimer’s disease (AD) is a neurodegenerative disease characterized by an accumulation of extracellular amyloid-beta peptide (Aβ) and intracellular neurofibrils resulting in a loss of memory. Aβ is the principal constituent of senile plaques that are thought to play a central role in the healing and progression of oligomer and fibril forms of AD. Besides, many studies have shown that oxidative stress and mitochondrial dysfunction might have a substantial role in AD and that they are suppressed or reduced by using antioxidant agents, suggesting a therapeutic intervention for AD patients. It is reported that numerous antioxidant components protect the brain from Aβ neurotoxicity (Sgarbossa & al. 2015). Pharmacological treatments available for AD occur by relaxation of the symptoms rather than targeting the etiological mechanisms (Ng & al. 2015).

Recent investigations have indicated that numerous medicinal herbs are a significant source of antioxidants. Plants include a large number of free radical scavenging molecules, such as alkaloids, tannins, steroids, rotenoids, carotenoids, dietary glutathione, anthocyanins, saponins, terpenoids, and flavonoids. Consequently, medical herbs become popular as a cheap source to discover novel antioxidants (Chand & al. 2018).

Volatile oils are found to have several pharmacological activities such as hepatoprotective, carminative, antispasmodic, antiviral, and anti-tumor, etc. Nowadays, many volatile oils have been characterized as natural antioxidants and proposed as potential sources for food preservation. Additionally, biologically active natural compounds are of interest to the pharmaceutics industry for the control of human ailments of microbial origin and for the containment of lipid peroxidative damage, which has been implicated in specific pathological diseases such as AD, ischemia-reperfusion injury, cancer, coronary, atherosclerosis, and aging (Mimica & al. 2004).

The representatives of family Amaryllidaceae J.St.-Hil. have been characterized by high phenolics content (Resetár & al. 2017) and some members of this family have been used in the treatment of AD. Galanthamine is an alkaloid of the Amaryllidaceae that is a competitive selective, long-acting, and reversible acetylcholinesterase inhibitor that maintains the beneficial effects even after treatment (López & al. 2002).

Garlic has been produced and eaten worldwide and has attracted attention due to its preservative potentials against various diseases. Previous investigations indicated that garlic has numerous biological and pharmacological effective compounds. It is used for medical aims since ancient times, and its usage for cancer treatment dates back to 3,500 years ago (Özkan & al. 2013).

The genus Allium L. (Amaryllidaceae; cf. APGIII 2009) consists of more than 900 species which naturally grow in the northern hemisphere (Duman & al. 2017; Ekşi & al. 2016). According to phylogenetic analyses, A. tuncelianum (Kollmann) Özhatay, B.Mathew & Şiraneci belongs to the Allium sect. Allium. Fritsch & Friesen (2002) have proposed that the wild progenitor of garlic species should grow in the district from South Central Asia to the Mediterranean, according to their taxonomic investigations. Mathew (1996) proposed that A. tuncelianum might be the wild progenitor of A. sativum L. and both share general characters such as the odor of leaves and bulbs.

Because of its similarity to the widespread garlic, it is locally named as ‘Ovacik garlic’ or ‘Tunceli garlic’ in the district. Allium tuncelianum generally consists of a single cloved white bulb, unlike garlic, which has bulbs with multiple cloves (Kiralan & al. 2013). Even though A. tuncelianum has been considered as a close relative of A. sativum, the precise phylogenetic or genetic relationships are not well known yet.

In this regard, the aim of this paper was to report the cholinesterase inhibitory and antioxidant activity of the methanol, hexane, dichloromethane, ethyl acetate, butanol, and aqueous extracts and essential oils of bulbs of A. tuncelianum. The total phenolic content of extracts and essential oil, as well as the essential oil composition and morphology of A. tuncelianum, were assessed.


Plant specimenTOP

Allium tuncelianum was gathered from Ovacık, Tunceli province (Eastern Turkey). The voucher specimens have been preserved at the Herbarium of Ataturk University, Faculty of Science under the code ATA-9877.


Dried bulbs of A. tuncelianum (50 g) were crushed and macerated with methanol (3 times, 8 h) in a water-bath not exceeding 35°C (3 × 100 ml) by 200 rpm with using of a mechanical mixer. Combined bulbs extracts were filtered and concentrated by rotary evaporator to dryness, then dissolved in methanol: water (1 : 9) and fractionated three times with 150 ml of n-hexane, dichloromethane, ethyl acetate, and n-butanol, respectively.

On the other hand, 50 g of bulbs of A. tuncelianum were crushed and macerated with 200 ml of distilled water for 8 h/3 days at 30 to 35°C. The aqueous extract was filtered, frozen and lyophilized to attain aqueous extracts of bulbs. Amounts of the powdered parts of A. tuncelianum and acquired extracts/fractions are shown in Table 1.

Table 1. Amounts of the powdered parts of A. tuncelianum (Kollmann) Özhatay & al. and acquired extracts/fractions.
Extracts/Fractions (g) Aerial part
MeOH 14.21
Hexane 2.08
CH2Cl2 5.11
EtOAc 1.03
BuOH 3.23
Methanolic residue 2.96
Lyophilised aqueous extract 15.44

Isolation of the essential oil, GC-FID and GC/MS analysesTOP

The essential oil isolation, GC-FID, and GC/MS assays were done in accordance with Karakaya & al. (2016). The crushed part, the percentage of essential oil, and the color of the essential oil are displayed in Table 2.

Table 2. The crushed part, essential oil % yield A. tuncelianum (Kollmann) Özhatay & al. and color of essential oil (w/v, %).
Part Crushed Yield Colour Collection
bulbs 220 g 0.0046 White 2018

Determination of total phenolic contentTOP

The total phenolic content of the samples was done in accordance with Karakaya & al. (2018). The procedure was repeated three times for each sample.

Antioxidant activityTOP

The quantitative 1,1-diphenyl-2-picrylhydrazyl (DPPH) of the samples was done in Karakaya & al. (2018). The IC50 values of samples were established by linear regression analysis in triplicate.

Anti-lipid peroxidation activityTOP

The anti-lipid peroxidation activity of the samples was done according to Karakaya & al. (2018). The IC50 values were established through linear regression assay.

Evaluation of AChE and BuChE inhibition activitiesTOP

The evaluation of AChE and BuChE inhibition followed Karakaya & al. (2018). The procedure was repeated three times for each plate. All data were denoted as mean ± SE of three independent tests.

Statistical analysisTOP

Overall indications are denoted as mean ± SE and statistically analyzed through ANOVA one-way analysis followed by way of complementary analysis of Bonferroni (P < 0.05), planned to determine statistical significance.


General morphologyTOP

Allium tuncelianum (Kollmann) Özhatay, B.Mathew & Şiraneci, Kew Bull. 50 (4): 723 (Özhatay & Mathew 1995). A. macrochetum subsp. tuncelianum Kollmann, Notes Roy. Bot. Gard. Edinburgh 41: 262 (Kollmann & al. 1983), bason. Tipo: [Turkey] Tunceli, Munzur Da., Aksu Dere above Ovacik, 1800 m a.s.l., 21 Jul. 1957, Davis 31498 leg. (holo-: E!; iso-: K!). Figs. 1 and 2.

Fig. 1.  Allium tuncelianum (Kollmann) Özhatay, B.Mathew & Şiraneci: a, b, plant during the anthesis; c, plant during the pre-anthesis [AEF 24116; illustrated by Gülnur Ekşi].


Fig. 2.  Allium tuncelianum (Kollmann) Özhatay, B.Mathew & Şiraneci: a, e, f, h, anthesis; b, bulb; c, d, early stages of the anthesis; g, bulbs at a local market. [Photos: a, b, d-f, h, Gülnur Ekşi; c, g, Mehmet Koyuncu].


Bulb 1.5–5.5 cm in diameter, ovoid; outer tunics thick, membranous, brownish to dirty yellowish-white; inner tunics thin, membranous, white; bulblets 1–2. Scape 50–150 cm. Leaves 4–8, 1–2.5 cm wide, flat, canaliculate, glabrous, shorter than scape. Spathe 10–20 cm, 1-valved, deciduous. Umbel 2–8 cm in diameter, spherical, dense (100–200 flowers), bracteolate. Perigone 2.5–3.5 mm, campanulate, pale pinkish to white, smooth. Stamens longer than perigone. Capsule 3–4 mm. Chromosome number (2n) 16.

Distribution and habitat.—East Anatolia; rocky areas, calcareous soils; 1000–2200 m a.s.l.

Phenology.—Flowering time from June to August.

Experimental sectionTOP

The methanol extracts of bulbs of A. tuncelianum were fragmented using solvents with different polarities (C6H14, CH2Cl2, C4H8O2, and C4H10O). Also, the lyophilised aqueous extract of bulbs was obtained. The extracts, fractions and essential oil were assessed for antioxidant and cholinesterase inhibitory activities. Also, the morphological study of A. tuncelianum was also evaluated.

The essential oils, extracts, and fractions of bulbs were estimated with regard to antioxidant capacity effect. The data of samples with regard to total phenolics content are displayed in Table 3. The fraction extracted of ethyl acetate (EtOAc) had the highest level of total phenolic (666.45 mg GAE g−1 DW) however the hexane fraction got the lowest phenolic content levels (67.78 mg GAE g−1 DW). DPPH analysis data were presented in Table 4 and the EtOAc fraction got the highest antioxidant activity (17.21 ± 4.33 μg/ml) and the hexane fraction had the lowest phenolic content (128.45 ± 3.56 μg/ml). The findings of the analysis of thiobarbituric acid (TBA) were exhibited in Table 5 as IC50 (μg/ml). The EtOAc fraction and lyophilized aqueous extract had the highest antioxidant potential (IC50 = 54.67 and 65.15 μg/ml, respectively) in TBA analysis.

Table 3. Total phenolic contents of the extracts, fractions and essential oil from A. tuncelianum (Kollmann) Özhatay & al. [The data present the mean ± SD of three independent experiments (p < 0.05)].
Tested samples Total phenolic contents (mg/g) ± SD
MeOH 377.25 ± 4.78
Hexane 67.78 ± 1.56
CH2Cl2 434.61 ± 4.12
EtOAc 666.45 ± 3.21
BuOH 124.05 ± 2.44
Methanolic residue 338.14 ± 5.34
Lyophilised aqueous extract 567.20 ± 3.07
Essential oil 209.01 ± 2.13
Table 4. DPPH radical scavenging activity of the the extracts, fractions and essential oil from A. tuncelianum (Kollmann) Özhatay & al. (μg/ml) [The data present the mean ± SD of three independent experiments (p < 0.05)].
Tested samples IC50 values (μg/ml) ± SD
MeOH 87.35 ± 3.42
Hexane 105.41 ± 3.34
CH2Cl2 31.43 ± 2.56
EtOAc 17.21 ± 4.33
BuOH 93.22 ± 1.66
Methanolic residue 128.45 ± 3.56
Lyophilised aqueous extract 52.57 ± 2.68
Essential oil 55.09 ± 3.22
Chlorogenic acid 2.41 ± 0.58
Propyl gallate 0.005 ± 0.21
Rutin 3.05 ± 0.89
Table 5. Antioxidant activities of the the the extracts, fractions and essential oil from A. tuncelianum (Kollmann) Özhatay & al. in TBA test [The data present the mean ± SD of four independent experiments (p < 0.05)].
Tested samples IC50 values (μg/ml) ± SD
MeOH 451.61 ± 2.98
Hexane >500
CH2Cl2 76.67 ± 3.77
EtOAc 54.67 ± 4.24
BuOH 166.29 ± 2.77
Methanolic residue >500
Lyophilised aqueous extract 65.15 ± 1.79
Essential oil 89.25 ± 2.78
Chlorogenic acid 12.98 ± 4.89
Propyl gallate 3.44 ± 2.05
Rutin 9.65 ±3.09

Cholinesterase inhibitory activity of samples was revealed via colorimetric Ellman’s method (Ellman & al. 1961), some changes were done following the mentioned method and donepezil was used as a standard (Yerdelen & Tosun 2015). In vitro cholinesterase inhibitory activity of samples at 100 μg/ml is displayed in Table 6. The EtOAc and essential oil indicated remarkable inhibition against BuChE (47.33 ± 3.27 and 28.65 ± 2.58%, respectively) at 100 μg/ml. Also, EtOAc and CH2Cl2 fractions displayed inhibition against AChE (15.98 ± 2.76 and 14.12 ± 2.76%, respectively) at 100 μg/ml. On the other side, the methanolic residue fraction had no activity against both enzymes. Moreover, MeOH, lyophilized aqueous extracts and hexane, BuOH fractions had no activity against AChE. EtOAc fraction has been characterized by substantially higher total phenolic content than other samples.

Table 6. In vitro AChE and BuChE inhibitory activities of samples from A. tuncelianum (Kollmann) Özhatay & al. at 100 μg/ml. [Superscript: a, standard error mean; b, no activity; c, not detected because of turbidity in the wells of microplates. The data present the mean ± SD of three independent experiments (p < 0.05)
Samples Enyzmes Percentile of inhibition ± S.E.Ma against AChE and BuChE
MeOH AChE -b
BuChE 9.68 ± 1.67
Hexane AChE NDc
BuChE 2.56 ± 2.55
CH2Cl2 AChE 14.12 ± 2.76
BuChE 23.56 ± 2.65
EtOAc AChE 15.98 ± 2.76
BuChE 47.33 ± 3.27
BuOH AChE -b
BuChE 3.98 ± 2.56
Methanolic residue AChE -b
BuChE -b
Lyophilised aqueous extract AChE NDc
BuChE 13.58 ± 1.93
Essential oils AChE 7.59 ± 2.90
BuChE 28.65 ± 2.58
Donepezil AChE 82.45 ± 2.64
BuChE 90.33 ± 4.16

The percentage yield of essential oil of A. tuncelianum and color of essential oil are presented in Table 2. The color of the essential oil was white. A total of five compounds making up 88.9% of the oil were defined in the bulbs of A. tuncelianum. Diallyl disulfide, diallyl trisulfide and allyl methyl trisulfide were the major components, amounting to 49.8%, 27.9 and 6.9%, respectively. Many of the defined compounds were sulphur compounds. The compositions of essential oil are presented in Table 7.

Table 7. The essential oil composition of A. tuncelianum (Kollmann) Özhatay & al. RRI Relative retention indices calculated against n-alkanes. % calculated from FID data.
RRI Compound %
1292 Allyl methyl disulfide 1.9
1438 Allyl propenyl disulfide 2.4
1492 Diallyl disulfide 49.8
1607 Allyl methyl trisulfide 6.9
1811 Diallyl trisulfide 27.9
  Total 88.9


Previously, it was observed that MeOH extract of the bulb of A. tuncelianum showed high antioxidant activities with the DPPH method (51.1 ± 5.5%) and greater content of total phenols (Yumrutaş & al. 2009). Moreover, another study about the antioxidant activity of A. tuncelianum showed that aqueous and EtOH extracts (Ağbaş & al. 2013) and MeOH extract (şehitoğlu & al. 2018) of bulbs got a significant effect. Other research also found a substantial correlation between antioxidant capacity and total phenolic content (Sytar & al. 2015; Granato & al. 2018) as well.

Previous investigations indicated that the major constituents of essential oils of A. tuncelianum bulbs were diallyl tri- sulfides (30.90%) and diallyl disulfide (28.30%) (Takim & al. 2016); diallyl disulfide (in green and red garlic was 67.33% and 72.52%, respectively) (Kiralan & al. 2013).

Nowadays it is known that diallyl disulfide derivatives are chemical agents that modulate various facets of AD (Manral & al. 2015). Also, previous studies showed that some Allium species such as A. sativum and A. tuberosum Rottler ex Spreng. had significant effects on AD (Chauhan 2003; Kim & al. 2007; Ray & al. 2011).

AD is a neurodegenerative disease induced by oxidative stress with a further cholinergic lack in the brain. Particularly, AD is characterised by a reduction in the sum of acetylcholine delivered from cholinergic synapses. A therapy methodology has been stimulated to enhance or maintain the proportion of acetylcholine through inhibiting acetylcholinesterase (Dickson 1997). Essential oils are a miscellaneous family of low molecular weight organic compounds with circumstantial biological activity. Compounds that act as cholinesterase inhibitors still are the only pharmacological therapeutics for AD. Many in vitro examinations showed that some components, in essential oils, may have cholinesterase inhibitory activity (Karakaya & al. 2019).

This paper showed that the EtOAc fraction of A. tuncelianum has cholinesterase inhibitory and antioxidant effects. The uses of antioxidants may be beneficial for AD healing (Gibson & Huang 2005). To the literature surveys, this is the initial exploration of cholinesterase inhibitory activity of extracts, fractions and essential oil from A. tuncelianum.

Especially, EtOAc fraction of A. tuncelianum bulbs displayed a substantial cholinesterase inhibitory and antioxidant potentials. The studied essential oils, extracts and fractions exhibited radical scavenging capacity (RSC), which were detected to be in correlation to the content of phenolic compounds. The essential oil has been characterized by the presence of diallyl disulfide which was determined to have inhibition towards both cholinesterase inhibitory activities. This paper displays that the EtOAc fraction of A. tuncelianum could be a novel potency source of native antioxidant and anticholinesterase components.



This paper was supported by the Research Fund of Ataturk University (FHD-2019–7227).



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