Phytochemical Classification and Antioxidant Activity of Some Medicinal Plant Species Growing in

Tabuk Region (KSA)

Abdelrahim A. Elbalola1* and Zahid Noor Abbas1

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1* Biology Department, Faculty of Science, Tabuk University.

2 Biology Department, Faculty of Science, Tabuk University.

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Corresponding author email [email protected]

Abstract

This study aimed at the investigation of phytochemical classification of nine medicinal plant species from

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three different families growing in Tabuk region of Saudi Arabia, evaluation of the antioxidant efficiencies
of the plant extracts, and inspection of possible associations between different phytochemical classes and

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the antioxidant activities of the plant extracts. Phytochemicals in plant extracts were identified using the
gas chromatography-mass spectrometry GC-MS technique. DPPH free radical scavenging assay was used
to measure the antioxidant activity of plants under investigation. Paleontological Statistics (PAST) 4.12
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was employed to carry out statistical analyses crucial to answering the research questions, and to produce
required plots. Plant extracts contained 190 different phytochemicals belonging to 36 compound classes.
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Plant extracts exhibited high antioxidant efficiencies, with Asteraceae species being the most efficient and
close to each other's in chemical composition and antioxidant activities. Organooxygen compound,
coumarin, phenol and unsaturated hydrocarbon contents showed positive associations with antioxidant
activities of plant extracts.
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Key words: phytochemicals, classification, antioxidant, activity, association.

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1. Introduction

The term "medicinal plant" refers to any plant species that contains naturally occurring active ingredients that
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are used to treat illness or relieve pain (Okigbo, 2002). Traditional herbal medicine has been described as the
culmination of knowledge, abilities, and perspectives based on culturally specific beliefs and experiences that
are employed in the maintenance of health and the prevention, diagnosis, improvement, or treatment of
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physical and mental illness (WHO, 2000). Since almost 80% of the world's population relies mostly on
traditional herbal medicine for their primary healthcare, it continues to play a significant part in the healthcare
system. A limitless supply of pharmacologically active substances like phenolic compounds, tannins,
flavonoids and alkaloids can be found in medicinal and aromatic plants from different parts of the world
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(Silvia et al., 2015; Junqueira et al., 2015). A wide range of medicinal plants exhibit excellent antimicrobial
and antioxidant activities (Razak et al., 2015) depending on plant species, variety, extraction and/or processing
methods, and the growing environment (Ayoub et al., 2017). (Bhatt et al., 2013) defined antioxidant as a
substance that even in small amounts, can prevent or delay the oxidation of easily oxidizable materials.

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 Antioxidants forbid oxidation of substrates (Halliwell et al., 1990)], some of which hold free or non-free
radicals and can motivate plasma membrane destruction leading to DNA mutations and lipid peroxidation
among many other consequences. The Tabuk region lies at the extreme Northwestern part of Saudi Arabia.

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Tabuk region is known to have a noticeable plant species diversity. Many wadies (valleys), mountains, sand
dunes and plateaus of the region are favorable sites for plant growth. Furthermore, they support various
medicinal plant species with multiple traditional uses which are in the popular legacies of the region (Elbalola

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et al., 2022). The main bulk of medicinal plant species traditionally utilized in Tabuk region falls within the
Asteraceae family, a well-known family for its multiple traditional herbal medicine values (Chithan et al.,
2012). A considerable number of Asteraceae genera are widely distributed throughout the region, including
Artemisia which comprises more than 400 species. A. monosperma, A. herba-alba, A. Judaica are commonly
used by the local people for treatment and remedy of many illnesses, in addition to many other uses. Genus

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Pulicaria also contributes greatly to the traditional herbal medicine practices in the area, represented by many

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species such as P. undulata and P. incisa. Apiaceae is another flowering plant family that satisfies food,
flavoring, fragrance, and medical purposes (Sayed Ahmed et al., 2017). Lamiaceae family includes a wide
range of species that have biological and medical values (Utiru et al., 2018). T. vulgaris and L. coronopifolia
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are well- known members of this family. Many investigations of medicinal plants used in Tabuk region to
cure several illnesses were carried out (Al Harbi, 2017; Rajasab, 2011; Fakhry et al., 2016). None of them
quantified or classified the active constituents of medicinal plants or investigated their antioxidant activities.
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This study tries to pioneer such kind of research in the region and fill a part of this research gap, to address
the relationship between bioactive chemical contents and the antioxidant behavior of plant extracts, and to
inspect similarities and distances between plant species from different families in their contents of
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phytochemicals and antioxidant activities. Furthermore, the study tries to establish a baseline for future
wholistic investigations that cover a wider range of medicinal plants in which the region is rich.
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2. Materials and Methods

2.1. Collection, identification, and preparation of plant samples.

Aerial parts of the plant species (Pulicaria undulata L., Pulicaria incisa Lam., Artemisia herba-alba Asso.,
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Artemisia monosperma Delile, Artemisia judaica L. and Achillea fragrantissima Forssk. from Asteraceae
family, Ducrosia flabellifolia Boiss. from Apiaceae family, Thymus vulgaris L. and Lavandula coronopifolia
Poir. from Lamiaceae family), were collected from different natural vegetation sites within the Tabuk region
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during the Spring-Summer interface of the year 2022 when most of the plant species were in the peak stage
of growth. Then samples were placed separately in paper bags and transferred to the laboratory for cleaning
and drying in shade. Identification of plant species was corroborated by making use of the Flora of the
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Kingdom of Saudi Arabia (Chaudhary, 1999) and Plants of the World Online Facilitated by the Royal Botanic
Gardens, Kew. Plant samples were then grounded into fine powders and kept for further analyses.

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 2.2. Phytochemical analysis and classification
We followed the procedure described by Medeiros, (2018) to identify Phytochemicals in plant ethanolic
extracts using gas chromatography- mass spectrometry GC-MS analysis. We classified phytochemicals using

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the Automated Chemical Classification with a comprehensive, computable taxonomy (Djoumbou et al., 2016).

2.3. Determination of Antioxidant and Free Radical Scavenging Activities

The 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical scavenging assay was used to measure the antioxidant

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activity of the plants under investigation (Liyana-Pathirana, and Shahidi, 2005). In this experiment, different
doses of 0.135 mM DPPH (200–1000 g/mL) were mixed with 1 mL of the extract. The mixture was held at
room temperature in the dark for 40 minutes while being gently stirred. A positive control was ascorbic acid.
DPPH scavenging activity (%) = [(Abs control Abs sample)/Abs control] 100, where Abs control is the

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absorbance of DPPH + methanol and Abs sample is the absorbance of DPPH radical. The absorbance of the

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samples and the control solutions were measured at 517 nm and % of DPPH scavenging activity of the extract
was calculated using the following equation: DPPH scavenging activity (%) = [(Abs control − Abs
sample)/Abs control] × 100, where Abs control is the absorbance of DPPH + methanol and Abs sample is the
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absorbance of DPPH radical.

2.4. Statistical Analysis

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All compound classes detected in plant extracts were compiled in a matrix with their percentage compositions
in different plant extracts. Compound abundances estimated from the chromatographic peak area, which
reflects the amount of compound in the extract, was used as a basis for calculating phytochemical class
percentages. Then this matrix was used to produce Bray-Curtis similarity matrix and the classical clustering
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dendrogram of plant species based on their chemical compositions. One-way analysis of similarity between
plant extracts in their free radical scavenging abilities was also carried out to test the significance (p< 0.05) of
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similarity and distance between plant species, and a similarity matrix was obtained. Linear r Pearson's
correlation test was carried out between antioxidant activities of plant extracts and their contents of the major
phytochemical classes (organooxygen compounds OOC, Terpenoids, benzene and substituted derivatives
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BSD, unsaturated hydrocarbons USH, phenols, coumarins and fatty acyls FA, and a correlation plot was
obtained. All statistical analyses were caried out using Paleontological Statistics (PAST) 4.12.

3. Results
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3.1. Phytochemical classification

The GC-MS system revealed a total of 190 phytochemicals belonging to 36 compound classes in the extracts
of all plants under study (Table 1 & supplementary material). Terpenoids, organooxygen compounds,
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unsaturated hydrocarbons, benzene and substituted derivatives and fatty acyls were the most abundant and the
most frequent phytochemical classes. Terpenoids contributed by 28.15%, 43.40%, 27.78%, 15.53%, 65.92%
and 91.33 to A. fragrantissima, A. herba-alba, A. judaica, D. flabellifolia. P. undulata and T. vulgaris extracts
respectively, while A. monosperma and L. coronopifolia extracts were free from terpenoids. T. vulgaris/P.

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 undulata was the most similar pair of species in chemical composition (Table 2). Asteraceae pairs of species
A. herba-alba/A. fragrantissima, A. judaica/A. fragrantissima, A. judaica/A. herba-alba and P. undulata/A.
herba-alba exhibited relatively high closeness in their chemical composition. D. flabellifolia was the most

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distant species from others (Figure 1).

Table 1 Percetage composition and Distribution of phytochemical classes in plant extracts

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Plant species
Phytochemical classes A. f A. h-a A. j A. m D. f L. f P. i P. u T. v

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Dihydrofurans 1.58% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Lactones 1.11% 5.64% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%

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USH 14.79% 12.06% 1.09% 4.80% 0.00% 0.00% 52.12% 0.00% 0.00%
ONC 0.56% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Terpenoids 28.15% 43.4% 27.78% 0.00% 15.53% 0.00% 6.76% 65.92% 91.33%
Tetrahydrofurans 6.23% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Polycyclic hydrocarbons 1.28% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Fatty acyls 0.76% 4.24% 0.00% 0.00% 1.27% 51.72% 2.25% 3.1% 2.53%
Organic oxides
Terpene lactones
3.41%
0.68%
0.00%
0.00%
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0.00%
0.00%
0.00%
0.00%
0.00%
1.21%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
0.00%
Phenanthrenes 1.21% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Benzofurans 12.90% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
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BSD 6.27% 0.98% 2.88% 11.27% 73.20% 1.13% 1.45% 11.47% 3.87%
Steroids and derivatives 0.63% 0.00% 0.00% 0.00% 1.17% 1.27% 0.00% 1.39% 0.00%
OOC 20.42% 20.52% 29.50% 48.14% 0.00% 26.77% 4.46% 13.18% 0.00%
OMC 0.00% 4.03% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Organobromides 0.00% 1.88% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Anthracenes 0.00% 7.24% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
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Azolines 0.00% 0.00% 2.15% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Pyridines and derivatives 0.00% 0.00% 2.18% 0.00% 5.04% 0.00% 0.00% 0.00% 0.00%
Organic oxides 0.00% 0.00% 1.08% 0.00% 0.00% 0.00% 1.26% 0.00% 0.00%
Phenols 0.00% 0.00% 24.85% 0.00% 0.00% 6.47% 0.00% 0.00% 0.00%
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Flavonoids 0.00% 0.00% 5.06% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00%
Hopanoids 0.00% 0.00% 3.44% 2.62% 0.00% 0.00% 0.00% 0.00% 2.27%
Coumarins 0.00% 0.00% 0.00% 33.17% 0.00% 0.00% 0.00% 0.00% 0.00%
Oxepanes 0.00% 0.00% 0.00% 0.00% 1.05% 0.00% 0.00% 0.00% 0.00%
Saturated hydrocarbon 0.00% 0.00% 0.00% 0.00% 1.53% 0.00% 0.00% 0.00% 0.00%
Pyrans 0.00% 0.00% 0.00% 0.00% 0.00% 2.50% 0.00% 0.00% 0.00%
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Carboxylic acids 0.00% 0.00% 0.00% 0.00% 0.00% 9.51% 0.68% 0.00% 0.00%
Glycerolipids 0.00% 0.00% 0.00% 0.00% 0.00% 0.63% 0.00% 0.00% 0.00%
Allyl-1,3-dipolar OC 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 1.08% 0.00% 0.00%
Epoxides 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 1.58% 0.00% 0.00%
Pyrroloazepines 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 2.33% 0.00% 0.00%
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Diazinanes 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 26.02% 0.00% 0.00%
Phenol ethers 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 0.00% 4.94% 0.00%
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Figure 1 Bray-Curtis paired group(UPGMA) classical clustering dendrogram between plant species based on
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chemical composition.
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Table 2 Bray-Curtis similarity matrix between plant species in their contents of phytochemical classes.
A. f A. h-a A. j A. m D. f L. f P. i P. u T. v
A. f 1
A. h-a 0.6348 1
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A. j 0.5217 0.5037 1
A. m 0.3149 0.2630 0.36088 1
D. f 0.2319 0.1778 0.2058 0.1127 1
L. f 0.2294 0.2574 0.34368 0.279 0.0357 1
P. i 0.2822 0.2651 0.1484 0.1071 0.0948 0.0852 1
P. u 0.4899 0.6066 0.43837 0.2445 0.2944 0.1868 0.14920 1
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T. v 0.3278 0.4691 0.3292 0.0614 0.2067 0.0366 0.10460 0.7232 1

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 3.2. Antioxidant activities

Table 3 showed that the investigated plant species' extracts were highly efficient in antioxidant activities. A.
monosperma exhibited the highest antioxidant activity for two extract concentrations (100 and 500 µg/ml), A.

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herba-alba had the highest activity at 300 µg/ml, A. judaica at 200 µg/ml and P. incisa at 400 µg/ml. Generally
there was an increase in free radical scavenging abilities of plant extracts with the increase in concentration.
The pairs of taxa P. incisa/A. fragrantissima, A. monosperma/ T. vulgaris, A. monosperma/A. herba-alba, A.

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judaica/ A. fragrantissima, A. judaica/ A. herba-alba and A. judaica/L. coronopifolia showed similar
antoxidant activities according to Bray-Curtis analysis of similarity showed in table 4. Moreover, D.
flabellifolia exhibited significant (p< 0.05) dissimilarity in antioxidant activity with six of the plant species.
Pearson's linear correlation test between the extract contents of the major phytochemical classes and

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antioxidant activities was shown in figure (2). Antioxidant activity was found to be significantly (p< 0.05)
positively correlated to OOC content, positively correlated to phenol, coumarins and USH contents.

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Terpenoids and BSD had negative correlation coefficients to antioxidant activities of plant extracts.

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Table 3 DPPH free radical scavenging capacity of the plant extracts at different concentrations.

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r
% Inhibition (Mean ± SE)
Conc.(µg/ml) P. u D. f T. v A. f P. i A. m A. h-a L. c A. j

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100 21.4084±0.7210 15.5070±0.1905 18.9639±0.5229 36.4343±0.1167 34.6080±0.016 43.6598±0.1255 36.5713±0.1442 31.7866±0.0259 35.9000±0.6077
200 51.8296±0.2367 23.2781±0.1788 54.4824±0.2592 58.2821±0.0243 56.7284±0.067 55.1128±0.0618 53.9975±0.4411 58.7190±0.0090 61.4270±0.0687

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300 77.5500±0.0582 28.1520±0.1813 70.4045±0.1518 74.8945±0.2613 71.1903±0.204 76.6538±0.1685 79.3341±0.2451 76.8986±0.0450 76.3251±0.0642
400 81.0160±0.1458 47.9559±0.2183 79.5928±0.3300 84.8778±0.0430 86.3190±0.005 84.9899±0.0368 85.9520±0.1952 81.7866±0.0259 84.0704±0.3714

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500 90.9680±0.0116 40.3878±0.1727 88.5705±0.2831 88.8557±0.0167 90.8872±0.049 92.5695±0.0935 91.0768±0.2513 88.7185±0.0090 89.1778±0.2129

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n o
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Figure 2 linear r Pearson's correlation (p < 0.05 boxed) plot between antioxidant activity of plant extracts
and their contents of the main phytochemiv classes. OOC = organooxygen compounds, USH = unsaturated
hydrocarbons, BSD = benzene and substituted derivatives, FA = fatty acyls, T = terpenoids.

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P. u
P.u. D.f. T.v A.f P.i A.m
r
Table 4 Bray-Curtis similarity matrix (p. values uncorrected significance) - one-way analysis of similarity (ANOSIM) for comparison between pairs of taxa in antioxidant activity.

r
A.h L.c

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D. f 0.0584
T. v 0.9314 0.0711

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A. f 0.9046 0.0264 0.9843
P. i 0.9502 0.0325 0.8752 1
A. m
A. h
L. c
A. j
0.9348
0.9532
1
0.9332
0.0161
0.0245

t
0.0325
0.0335
1
0.9681
1
0.9931 p 0.9217
0.9542
0.9346
1
0.9925
0.9349
0.96
0.9816
1
0.945
0.9199
0.9926
1 1

n o
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 4. Discussion

The wide variety of phytochemical classes in the plant extracts proved that strong, healthy plant biosynthetic
machinery had been developed, ensuring the beneficial use of the unique plant components by a variety of

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consumers. It also demonstrated that plants' high phytochemical diversity, which contributes to the variability
needed to increase the likelihood of producing a small number of biologically active compounds when
ecological conditions call for an increase in plant defense, allows them to resist herbivory, pests, pathogenicity,

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invasion, and allelopathy (Berenbaum et al, 1996). Due to their significant phytochemical diversity, the plants
under study have complicated biochemical pathways and are more likely to create one or more active
compounds at any given time if their absolute diversity of secondary metabolites is higher (Wetzel et al. 2020;
Jones and Firn (1991). Concentration of extract had an influence on plant antioxidant activity, which increased

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with the increase in extract concentration. Superiority of A. monosperma in antioxidant activity over other
species at two extract concentrations is possibly interpreted by the presence of high organooxygen compounds

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and coumarins in its extract. The most abundant OCC in A. monosperma extract was Pinacol which is a tertiary
alcohol with a hydroxyl group – OH attached to a saturated carbon atom. Aswathanarayanappa et al. (2013)
synthesised a few tertiary alcohols and tested them for their antioxidant properties to determine how
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functionalization at the carbonyl carbon and substitution at the biphenyl ring affected these properties. They
found that the antioxidant property was improved by adding a hydroxyl group to the carbonyl carbon. Bicas
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et al., (2011) also hydroxylated the terpene hydroxy carbon (Limonene) to a tertiary alcohol (alpha- terpeniol)
and found that its antioxidant activity was improved. The coumarin Xanthotoxol found in A. monosperma
extract in this investigation was isolated by Liu et al., (2000) from Chinese herbs and tested for antioxidant
activity, it exhibited potent antioxidative activity. Pharmacological activities of Xanthotoxol with many other
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coumarins were also reviewed by Mottaghipisheh et al, (2020). Organooxygen compounds, along with
terpenoids and phenols made the highest phytochemical contents in A. judaica extract which showed the best
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antioxidant efficacy at 200 µg/ml. The Compound Paeonol found in A. judaica extract boosted cell viability
in the presence of neurotoxicity, increased uptake in the presence of H2O2, and recovered ALS model cell
lines by lowering mitochondrial oxidative stress brought on by glutamate (Latif et al., 2022). When the
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hepatocellular carcinoma (HCC) rat model was used, paeonol also dramatically boosted serum WBC, TP,
ALB, AIG, TNF- alpha and IFN and liver antioxidant enzyme activities. It also considerably decreased the
serum AST, ALT, ALP, GGT, AFU, and liver MDA levels. (Bendong et al., 2012). Mairaj et al., (2022) also
found that Paeonol from Paeona suffruticosa has a meliorating effect on arsenite-induced oxidative stress,
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suggesting that it enhances the activity of antioxidants and prevents oxidative stress damage by transforming
ROS to a neutral and non-toxic end product. The OOC Xanthoxylin which dominated A. judaica extract was
identified by Mustafa et al., (2018) and Ngidi et al., (2021) in the essential oil of P. undulata and in the
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endophytic Pseudomonas aeruginosa from Anredera cordifolia leaves with powerful antioxidant properties.
A. judaica extract also contained Phenol, 4-methoxy-2,3,6- trimethyl-, it was extracted from leaves and stems
of some herbs by Al-Juhaimi et al., (2011) and showed high free radical scavenging activity. The phenol and
pyrogallol derivative 5- tert- Butylpyrogallol antioxidant potential was examined, the Racimat induction time

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 (IP) result of the pyrogallol derivative was higher than the biodiesel and was above the accelerated oxidative
test American Society for Testing and Materials (ASTM) D6751 standard (Sutanto et al., 2019). At 300 µg/ml,
A. herba-alba extract was the best antioxidant agent coupled with high terpenoid and organooxygen compound

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contents. Marrubium vulgare essential oil was regarded a good antioxidant agent because it contained the
monoterpenoid 3- Thujanone (Rached et al., 2022), which was detected in this study in A. herba-alba extract.
Thujone also is a monoterpenoid found in the same plant species. It was isolated from leaves of Elaeagnus

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indica and Memecylon edule and it exhibited high antioxidant efficiency (Srinivasan et al., 2020). P. incisa
extract was dominated by unsaturated hydrocarbons and exhibited the highest antioxidant activity at 400
µg/ml. One USH identified in its extract was 1,3-Cyclopentadiene, 5,5-dimethyl-1-ethyl- , which was
obtained invitro in A. herba-alba essential oil by Bouzidi et al., (2016). This essential oil was found to have
interesting antioxidant activity. Another USH in P. incisa extract is 3-Eicosene, (E)-, previously identified by

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Anthony et al., (2013) in the volatile constituent from the leaf oil of Thaumatococcus danielli, which displayed

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significant antioxidant activity against DPPH and Nitric oxide radicals. In contrast, D. flabellifolia showed
the lowest antioxidant activity at all concentrations, and it was dissimilar to other species, given that its extract
contained the highest benzene and substituted derivatives and high terpenoid contents. Significant (p< 0.05)
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positive correlation between OOC content of plant extracts and their antioxidant activities indicated that OOC
are responsible for this activity. In addition, coumarins, USH and phenols were positively related to
antioxidant activity of plant extracts based on their positive associations with antioxidant activities of plant
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extracts. Negative relationship between terpenoids and BSD contents and antioxidant activity does not
necessarily mean that these phytochemical classes decrease antioxidant activity of plant extracts, but this
relationship needs to be further studied to be clearly addressed and interpreted.
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5. Conclusion

The studied plant species were highly diverse in phytochemicals, demonstrating the development of robust
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and healthy plant biosynthetic pathways. Organooxygen compounds, terpenoids, unsaturated hydrocarbons,
benzene and substituted derivatives and fatty acyls were the most abundant and frequent compound classes in
plant extracts. Asteraceae species were relatively close to each other's in both chemical composition and
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antioxidant activities of their extracts, while D. flabellifolia extract (Apiaceae) was the least efficient and was
distant from other species. A. monosperma followed by A. judaica, A. herba-alba and P. incisa (Asteraceae)
were more efficient in antioxidant activity. Organooxygen compound content of plant extracts had significant
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(p< 0.05) positive correlation with antioxidant activity of plant extracts. Coumarins, phenols, and unsaturated
hydrocarbons contents also were positively correlated to antioxidant activity. The study of correlation between
phytochemical constituents and antioxidant activity has drawn attention to certain phytochemical classes to
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be subject for further investigations.

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