agronomy
Article
Sesquiterpenes-Rich Essential Oil from Above
Ground Parts of Pulicaria somalensis Exhibited
Antioxidant Activity and Allelopathic Effect on Weeds
Abdulaziz Assaeed 1 , Abdelsamed Elshamy 2,3 , Abd El-Nasser El Gendy 4 , Basharat Dar 1 ,
Saud Al-Rowaily 1 and Ahmed Abd-ElGawad 1,5, *
1
2
3
4
5
*
Plant Production Department, College of Food & Agriculture Sciences, King Saud University,
P.O. Box 2460 Riyadh 11451, Saudi Arabia; assaeed@ksu.edu.sa (A.A.); baseratali@gmail.com (B.D.);
srowaily@ksu.edu.sa (S.A.-R.)
Department of Natural Compounds Chemistry, National Research Centre, 33 El Bohouth St., Dokki, Giza,
12622, Egypt; elshamynrc@yahoo.com
Faculty of Pharmaceutical Sciences, Tokushima Bunri University, Yamashiro-cho, Tokushima 770-8514, Japan
Medicinal and Aromatic Plants Research Department, National Research Centre, 33 El Bohouth St., Dokki,
Giza 12622, Egypt; aggundy_5@yahoo.com
Department of Botany, Faculty of Science, Mansoura University, Mansoura 35516, Egypt
Correspondence: aibrahim2@ksu.edu.sa or dgawad84@mans.edu.eg;
Tel.: +20-100-343-8980 or +966-562-680-864
Received: 12 February 2020; Accepted: 12 March 2020; Published: 14 March 2020
Abstract: Pulicaria genus (fleabane) is characterized by its fragrant odor due to the presence of essential
oil (EO). According to the literature reviews, the EO of Pulicaria somalensis O.Hoffm. (Shie) is still
unexplored. For the first time, 71 compounds were characterized in EO derived from above-ground
parts of P. somalensis collected from Saudi Arabia. Sesquiterpenes represented the main components
(91.8%), along with minor amounts of mono-, diterpenes, and hydrocarbons. Juniper camphor (24.7%),
α-sinensal (7.7%), 6-epi-shyobunol (6.6%), α-zingiberene (5.8%), α-bisabolol (5.3%), and T-muurolol
(4.7%) were characterized as main constituents. The correlation analysis between different Pulicaria
species showed that P. somalensis has a specific chemical pattern of the EO, thereby no correlation
was observed with other reported Pulicaria species. The EO showed significant allelopathic activity
against the weeds of Dactyloctenium aegyptium (L.) Willd. (crowfoot grass) and Bidens pilosa L. (hairy
beggarticks). The IC50 value on the germination of D. aegyptium was double that of B. pilosa. The
IC50 values on the root growth of B. pilosa and D. aegyptium were 0.6 mg mL−1 each, while the shoot
growths were 1.0 and 0.7 mg mL−1 , respectively. This variation in the activity could be attributed to
the genetic characteristics of the weeds. Moreover, the EO exhibited significant antioxidant effects
compared to ascorbic acid. Further studies are necessary to verify if these biological activities of the
EO could be attributable to its major compounds.
Keywords: Pulicaria somalensis; essential oil; sesquiterpenes; phytotoxicity; antioxidant activity;
juniper camphor
1. Introduction
Since their early presence on Earth, humans have depended largely on plants for food, energy,
and medicine [1]. Nowadays, even with highly scientific and technological developments, aromatic
and medicinal plants are still the main source of food and medicinal products. Most of the scientists
focused on finding and developing new products derived from plants, plant extracts, and constituent
choices for the treatment of different diseases and illnesses [2].
Agronomy 2020, 10, 399; doi:10.3390/agronomy10030399
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Asteraceae or Compositae is a widely distributed family throughout the world and contains around
1600 genera with more than 23,000 plant species [3]. Pulicaria (fleabane) genus (family Asteraceae)
comprises around 75 species widely distributed in Africa, Europe, and Asia [4]. Pulicaria species are
used in the treatment of several diseases such as cancers, fever, hypoglycemia, microbial, inflammation,
and spasmodic diseases [5–7].
The chemical characterization of Pulicaria plants revealed the presence of various secondary
metabolites, such as mono-, sesqui-, and diterpenoids [8–12], flavonoids, and phenolics [5–7]. Several
reports described the chemical characterization of essential oils (EOs) from Pulicaria species such as
Pulicaria dysenterica (L.) Bernh. (common fleabane) [13], Pulicaria gnaphalodes (Vent.) Boiss. (false
fleabane) [14], Pulicaria mauritanica Batt. (fleabane) [15], Pulicaria jaubertii E.Gamal-Eldin. (Araar) [16],
and Pulicaria undulata (L.) C.A. Mey (Gethgath). [17]. All these studies deduced that members of
this genus are rich with terpenoids, especially mono- and sesquiterpenoids. The EOs extracted from
Pulicaria species exhibited numerous biological potentialities, such as antibacterial, antioxidant, and
antifungal activities [15,18]. A previous chemical study of P. somalensis O.Hoffm. (Shie) described that
this plant is rich with diterpenoids as well as flavonoids [19]. The methanolic extract of this plant has
remarkable antioxidant, antifungal, and antibacterial activities [20].
To the best of our knowledge, there are no reports concerning P. somalensis EO. Thereby, in the
present study, we aimed to (1) determine the chemical composition of the EO from the above-ground
parts of P. omalensis, (2) assess the allelopathic activity of the EO against two weeds, Dactyloctenium
aegyptium (crowfoot grass, Poaceae) and Bidens pilosa (hairy beggarticks, Asteraceae), and (3) evaluate
the antioxidant properties of the EO.
2. Materials and methods
2.1. Plant Materials
We collected the above-ground parts of P. somalensis from three populations at Alwashla, Riyadh
region, Saudi Arabia (24◦ 25’36.1” N 46◦ 39’07.3” E). Within each population, we collected samples
from five individuals and mixed them as one composite sample. At the laboratory, we cleaned the
samples from dust, dried them in a shaded place at room temperature, and ground them into powder
using a grinder (IKA®MF 10 Basic Microfine Grinder Drive, Breisgau, Germany). We identified the
plant according to Chaudhary [21] and deposited a voucher specimen (RIY-15647) in the National
Herbarium and Genebank, Riyadh, Saudi Arabia.
2.2. Extraction of EO
Hydro-distillation of the prepared plant materials from above-ground parts of P. somalensis (400 g)
was achieved using a Clevenger-type apparatus for three hours. The dark yellow oil (0.5% w/w) was
separated and then dried with anhydrous NaSO4 . EOs from all the three samples of P. somalensis
populations were extracted in the same way and stored at 4 ◦ C until further gas chromatography-mass
spectrometry (GC-MS) analysis was performed.
2.3. GC-MS Analysis and Identification of Components of EO
The chemical composition of the extracted EO samples was analyzed separately by GC-MS
according to our published protocol [22].
2.4. Allelopathic Activity of the EO
To assess the allelopathic activity of the extracted EO from the above-ground parts of P. somalensis,
we targeted two weeds from different families: D. aegyptium (Poaceae) and B. pilosa (Asteraceae). The
seeds of D. aegyptium were collected from newly reclaimed fields near New Mansoura City, northern
Nile delta, Egypt (31◦ 29′ 57.3” N 31◦ 21′ 59.3” E), while the seeds of B. pilosa were collected from the
gardens of Mansoura University campus, Mansoura, Egypt (31◦ 02′ 38.1” N 31◦ 21′ 01.7” E). We selected
Agronomy 2020, 10, 399
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seeds of both weeds with homogenous size and color. We surface sterilized the seeds with sodium
hypochlorite (0.3%), rinsed them with water (distilled and sterilized), and then dried them over a
sterilized Whatman® cellulose filter paper (Sigma-Aldrich, Taufkirchen, Germany) [23].
We prepared different concentrations (0.2, 0.4, 0.6, 0.8, and 1.0 mg mL−1 ) of the extracted EO
using 1% Tween® 80 (Sigma–Aldrich, Darmstadt, Germany). For bioassay, we placed 20 seeds of
each weed in sterilized Petri plates (Ø: 9 cm) lined with sterilized Whatman No. 1 filter paper and
immediately added 4 mL of each concentration. The plates were sealed with Parafilm® and incubated
at 27 ± 2 ◦ C in a growth chamber with a light cycle of 8 h dark and 16 h light. Tween (1%) was used
as a negative control. After seven days for B. pilosa and ten days for D. aegyptium, we counted the
number of germinated seeds and measured the length of the seedling root and shoot for both weeds.
The inhibition of seed germination, root growth, and shoot growth was calculated according to the
following equation:
Inhibition (%) = 100 ×
(Length/Number of control − Length/Number of treatment)
Length/Number of control
(1)
The bioassay experiment was repeated three times with three replications (three plates), and the
IC50 (the concentration of EO required for 50% inhibition)was calculated graphically as the amount of
the EO necessary for 50% inhibition.
2.5. Antioxidant Activity of the EO
The antioxidant activity of the extracted EO from P. somalensis was performed based on
2,2-Diphenyl-1-picrylhydrazyl (DPPH) and 2,2′ -azino-bis(3-ethylbenzothiazoline-6-sulphonic acid
(ABTS) free radical scavenging activity.
2.5.1. DPPH Radical Scavenging Activity
The EO capability to react with the free DPPH radical (Sigma-Aldrich, Darmstadt, Germany) and
reduce its color was determined according to the method of Miguel [24]. In brief, we prepared different
concentrations (10, 20, 40, 60, 80, 100 µg mL−1 ) of the EO in methanol (70%). A reaction mixture of
2 mL of each concentration and 2 mL of DPPH (0.3 mM) was prepared in screwcap test tubes, shaken
well, and incubated in dark conditions at 25 ◦ C for 15 min. Negative control was performed using
2 mL of 1% Tween instead of the EO. We measured by a spectrophotometer (Milton Roy Spectronic
21D UV-Visible Spectrophotometer, California, USA) at 512 nm. In addition, positive control with
ascorbic acid (as a standard antioxidant) was prepared in a range of 1–25 mg mL−1 and treated as
previously mentioned for the EO treatments. We calculated the scavenging activity according to the
following equation:
Scavenging activity (%) = 100 ×
Absorbancecontrol − Absorbancesample
Absorbancecontrol
(2)
Also, the IC50 was calculated as the concentration of the EO required for 50% scavenging of
the DPPH.
2.5.2. ABTS-Free Radical Scavenging Activity
To confirm the antioxidant activity of the extracted EO, we determined the scavenging of the
ABTS radical (Sigma-Aldrich, Darmstadt, Germany) according to the method of Re et al. [25]. The free
radical was prepared using 7 mM of ABTS and 2.45 mM of K2 S2 O8 . The mixture (1/1, v/v) was kept at
room temperature (25 ± 2 ◦ C) in dark conditions. We then diluted the radical by MeOH until it reached
the absorbance of 0.700 ± 0.02 at 734 nm. A reaction mixture of 2 mL of each concentration of the EO
and 2 mL of the freshly prepared ABTS was prepared, mixed well, and incubated at room temperature
(25 ◦ C) for 6 min. We then measured the absorbance at 734 nm using a spectrophotometer (Milton
Agronomy 2020, 10, 399
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Roy Spectronic 21D UV-Visible Spectrophotometer, California, USA). Ascorbic acid was also used as a
positive control. We calculated the scavenging activity and the IC50 as mentioned in DPPH method.
2.6. Treatment of Data
We repeated the experiments of allelopathic and antioxidant activity three times with three
replications for each. We subjected the data of antioxidant experiments, as a percentage of scavenging
activity in triplicates, to a one-way analysis of variance (ANOVA) test followed by Duncan’s test, where
the significant differences among the various tested concentrations were assessed at p ≤ 0.05 using
CoStat software program, version 6.311 (CoHort Software, Monterey, CA, USA). However, the data
of allelopathic activity, as a percentage of inhibition in triplates, were subjected to two-way ANOVA
at p ≤ 0.05 using the CoStat program, version 6.311 (CoHort Software, Monterey, CA, USA), which
afforded the concentration of the EO and the types of weed as two factors.
Based on the EO composition, the correlation between the present studied plant (P. somalensis) and
other reported Pulicaria species, including P. dysenteric [13,26], P. glutinosa (Boiss.) Jaub. & Spach [27],
P. gnaphalodes [14,28], P. incisa (Lam.) DC. (wild tea) [29,30], P. jaubertii [16], P. mauritanica (Ifenzi
oudaden) [31,32], P. odora (L.) Rchb. (Mediterranean fleabane) [18], P. sicula (L.) Moris (fleabane) [33],
P. stephanocarpa Balf.f. (derbeb) [17], P. undulata [34–37], and P. vulgaris Gaertn. (false fleabane) [38–40],
was assessed by agglomerative hierarchical cluster (AHC) as well as principal component analysis
(PCA). We constructed a data matrix from the percentage of various classes of the EO (mono-, di-,
sesquiterpenes, and others) in different Pulicaria species (12 species representing 21 samples) and
then subjected them to PCA. However, we performed the AHC based on a data matrix of a total of
44 major identified chemical compounds, with concentration >5%, from the EO of 12 Pulicaria species.
We performed the AHC based on the similarity using Pearson’s coefficient of correlation and with
the agglomeration method of unweighted pair-group average. The AHC and the PCA analyses were
performed using XLSTAT statistical computer software package, version 14 (Addinsoft, New York, USA).
3. Results and Discussion
3.1. Chemical Composition of the EO
The EO with a dark yellow color from the above-ground parts of P. somalensis, collected from
Saudi Arabia, was extracted by the hydrodistillation method and yielded 0.5% (v/w) oil. The EO was
analyzed via GC-MS. The chromatogram, including the main components, is indexed in Figure 1. All
the identified constituents of EO comprising 71 compounds are listed in Table 1, representing 100%
of the total mass. Mono-, di-, and sesquiterpenes as well as hydrocarbons and aromatic phenolic
compounds were characterized as components of the EO.
Sesquiterpenes represented the main characterized class (91.8%) of compounds, including both
oxygenated (72.4%) and non-oxygenated (19.3%) sesquiterpenes. Oxygenated monoterpenes were one
of the identified compounds with a concentration of 3.7% from overall identified monoterpenes (4.8%) in
addition to minor monoterpenes hydrocarbons (1.0%). Diterpenoids were the usual minor compounds
in EOs derived from aromatic and medicinal plants [22]. Herein, diterpenes are characterized as minor
constituents with a concentration of 2.5%, including the concentration of 1.8% of oxygenated and
0.7% of non-oxygenated diterpenes. A concentration of 2.0% from overall mass represented the other
compounds, including oxygenated and non-oxygenated hydrocarbons (0.8% and 0.2%) as well as
0.94% of volatile aromatic compounds.
In our findings, sesquiterpenes were the backbone of the characterized compounds in the
EO. From 36 identified oxygenated sesquiterpenes, juniper camphor (24.7%), α-sinensal (7.6%),
6-epi-shyobunol (6.6%), α-bisabolol (5.3%), and T-muurolol (4.7%) represented the main components,
while isoaromadendrene epoxide was a minor one with a concentration of 0.1%. By comparing our
results with the literature survey of EOs of other Pulicaria species, it was clear that the chemical
Agronomy 2020, 10, 399
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composition EO of P. somalensis is comparable to some other Pulicaria species, with a preponderance of
sesquiterpenes such as P. dysenterica [13] and P. gnaphalodes [14].
Figure 1. GC-MS chromatogram of the essential oil from the above-ground parts of Pulicaria somalensis
(Shie). Peaks of the major compounds are numbered 1–6.
The sesquiterpene hydrocarbons characterized as a remarkable identified class with a concentration of
19.3%. α-Zingiberene (5.8%), α-cadinene (3.8%), and valencene (3.7%) were characterized
as the principal
α
components, while as αtrans-caryophyllene represented the minor one with a concentration of 0.1%.
Additionally, numerous reports describe that Pulicaria species have monoterpenes as main
constituents, such as P. undulata [17], P. mauritanica [15], P. jaubertii [16], and P. odora [18]. Our findings
exhibit that the monoterpenes are minor components involving oxygenated (3.7%) and non-oxygenated
(1.0%) ones. Trans-chrysanthenyl acetate (1.3%) was found as a main compound of the oxygenated
monoterpenes, while 1,8-cineole (0.2%) was the minor one. γ-Terpinene and p-cymene were the two
α
α
identified oxygenated monoterpenes
with concentrations
of 0.1% and 0.9%, respectively.
In most of the cases, the EOs derived from the aromatic and the medicinal plants were poor
resources of diterpenoids with some exceptions, such as Lactuca serriola L. (prickly lettuce), where the
diterpene isocembrol was determined in high concentration (17.4%) [22]. This fact was achieved in
our study by minor diterpene constituents. Only two diterpenoid components were identified, which
includes the oxygenated one, geranyl linalool (1.8%) and the non-oxygenated one, geranyl-α-terpinene
(0.7%). The previous studies of EOs of Pulicaria species deduced that these plants almost do not have
γ
diterpene components [16,18]. For example, the EO of P. mauritanica was described to have only one
diterpenoid with a concentration of 0.2 of the total mass [15], while the EOs of P. dysenterica [13],
P. gnaphalodes [14], P. undulata [17], and P. jaubertii [16] had no diterpenes.
Other components with low concentrations characterized in our study included hydrocarbons
and volatile aromatic compounds. With minor concentration, the hydrocarbons comprised only two
oxygenated compounds, γ-palmitolactone (0.8%) and n-octadecanal (0.1%), and two non-oxygenated,
tific
n-heneicosane (0.1%) and n-pentacosane (0.1%). Additionally, our results completely agree with
previous studies of other Pulicaria species that indicate the minor hydrocarbons constituents [13–17].
Volatile aromatic and phenolic terpenoid compounds are very common in the EOs of Pulicaria species,
especially cymene derivatives and isomers such as p-cymene, m-cymene, and p-cymen-8-ol [15,16,18]. In
the same line, the EO of P. somalensis contained only one aromatic compound, p-cymene, with a low
concentration (1.0%).
α
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Table 1. Chemical constituents and concentration of the essential oil from the above-ground parts of
Pulicaria somalensis (Shie).
No
Rt [a]
Compound
KI [b]
KI [c]
Conc. % [d]
Identification [e]
1
2
3
4
5
6
7
8
9
7.05
11.11
11.99
12.42
12.73
13.44
15.22
15.59
15.73
Oxygenated Monoterpenes
1,8-Cineole
trans-Pinocarveol
cis-Verbenol
endo-Borneol
4-Terpineol
α Terpineol
Pulegone
Carvone
trans-Chrysanthenyl acetate
1031
1183
1142
1139
1177
1189
1237
1242
1235
1047
1180
1144
1140
1179
1188
1239
1243
1234
3.7
0.2 ± 0.01
0.3 ± 0.01
0.9 ± 0.02
0.2 ± 0.01
0.2 ± 0.01
0.1 ± 0.01
0.2 ± 0.01
0.3 ± 0.01
1.3 ± 0.03
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
10
11
7.92
29.06
Monoterpenes Hydrocarbons
γ-Terpinene
p-Cymene
1062
1025
1060
1025
1.0
0.1 ± 0.01
0.9 ± 0.02
MS, KI
MS, KI
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
24.31
25.18
25.54
25.99
26.80
26.98
27.70
27.96
28.26
28.78
28.94
29.65
29.86
30.25
30.35
30.95
31.09
31.27
31.53
31.67
31.87
32.03
32.38
32.51
32.9
33.07
33.33
33.55
1693
1558
1580
1433
1578
1629
1588
1590
1535
1511
1678
1689
1612
1631
1827
1630
1627
1642
1640
1638
1683
1608
1691
1619
1579
1638
1517
1551
1694
1557
1583
1433
1580
1631
1586
1592
1535
1512
1677
1691
1612
1632
1826
1633
1625
1643
1641
1638
1682
1609
1691
1618
1581
1639
1516
1551
72.4
0.3 ± 0.01
0.7 ± 0.02
0.5 ± 0.02
0.7 ± 0.01
0.9 ± 0.02
0.2 ± 0.01
0.7 ± 0.02
0.1 ± 0.01
0.3 ± 0.01
1.3 ± 0.04
1.2 ± 0.02
1.7 ± 0.03
1.7 ± 0.03
0.4 ± 0.02
0.2 ± 0.01
0.7 ± 0.03
0.5 ± 0.02
0.3 ± 0.01
1.0 ± 0.04
0.9 ± 0.02
5.3 ± 0.05
4.7 ± 0.07
24.7 ± 0.06
0.1 ± 0.01
0.1 ± 0.01
0.2 ± 0.01
6.6 ± 0.05
1.8 ± 0.02
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
1714
1715
0.8 ± 0.01
MS, KI
1633
1625
1693
1752
1753
1814
1845
1669
1634
1628
1693
1751
1753
1815
1842
1668
1.6 ± 0.03
0.4 ± 0.01
2.4 ± 0.04
7.6 ± 0.06
1.4 ± 0.03
0.5 ± 0.01
0.3 ± 0.01
0.1 ± 0.01
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
1351
1376
1427
1428
1477
1441
1352
1377
1427
1428
1475
1442
19.3
0.2 ± 0.01
0.2 ± 0.01
0.1 ± 0.01
0.1 ± 0.01
0.1 ± 0.01
0.1 ± 0.01
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
40
34.2
41
42
43
44
45
46
47
48
34.61
35.86
36.07
36.89
37.31
37.49
38.42
40.89
49
50
51
52
53
54
19.25
20.47
21.74
22.28
23.53
23.94
Oxygenated Sesquiterpenes
Germacrone
Dihydro-β-agarofuran
Cubedol
Davana ether 1
Spathulanol
α-Acorenol
Calarene epoxide
Veridiflorol
Nerolidol
Germacrene D-4-ol
cis-alpha-Santalol
8-Cedren-13-ol
Rosifoliol
Agaruspirol
Khusinol acetate
γ-Eudesmol
Fonenol
Cubenol
T-Cadinol
Hinesol
α-Bisabolol
T-Muurolol
Juniper camphor
Humulane-1,6-dien-3-ol
Isoaromadendrene epoxide
Nerolidol-epoxyacetate
6-epi-shyobunol
Diepicedrene-1-oxide
6-Isopropenyl-4,8a-dimethyl-1,2,3,5,6,7,8,
8a-octahydro-naphthalen-2-ol
cis-α-Copaene-8-ol
Aromadendrene oxide-(1)
Z-α-trans-Bergamotol
α-Sinensal
cis-Lanceol
cis-Z-α-Bisabolene epoxide
Hexahydrofarnesyl acetone
E-cis,epi-β-Santalol
Sesquiterpenes Hydrocarbons
α-Cubebene
α-Copaene
Calarene
trans-Caryophyllene
γ-Muurolene
Alloaromadendrene
Agronomy 2020, 10, 399
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Table 1. Cont.
No
Rt [a]
Compound
KI [b]
KI [c]
Conc. % [d]
Identification [e]
55
56
57
58
59
60
61
62
63
64
65
24.49
24.64
25.31
25.63
26.40
26.56
27.43
30.73
31.41
32.61
35.48
delta-Cadinene
α-Amorphene
epi-Bicyclosesquiphellandrene
α-Muurolene
α-Cadinene
cis-Calamenene
α-Calacorene
Di-epi-à-cedrene-(I)
Valencene
α-Guaiene
α-Zingiberene
1524
1506
1482
1499
1538
1521
1548
1427
1491
1439
1495
1523
1504
1482
1498
1539
1521
1549
1428
1492
1440
1494
1.0 ± 0.01
0.7 ± 0.01
0.2 ± 0.01
0.8 ± 0.02
3.8 ± 0.05
0.3 ± 0.01
0.7 ± 0.01
2.1 ± 0.03
3.7 ± 0.06
0.1 ± 0.01
5.8 ± 0.06
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
MS, KI
66
44.3
Oxygenated Diterpenes
Geranyl linalool
2444
2443
1.8
1.8 ± 0.03
MS, KI
36.34
Diterpenes Hydrocarbons
Geranyl-α-terpinene
2142
0.7
0.7 ± 0.02
MS, KI
68
69
47.14
56.24
Oxygenated Hydrocarbons
γ-Palmitolactone
n-Octadecanal
2120
1357
2119
1357
0.8
0.8 ± 0.02
0.1 ± 0.01
MS, KI
MS, KI
70
71
46.6
57.85
Non-oxygenated Hydrocarbons
n-Heneicosane
n-Pentacosane
2300
2500
2301
2503
0.2
0.1 ± 0.02
0.1 ± 0.01
MS, KI
MS, KI
67
2142
[a] Rt: Retention time; [b] KI: Kovats retention index on DB-5 column with reference to n-alkanes; [c] experimental
Kovats retention index; [d] values are average ± SD, and [e] the identification of essential oil (EO) components was
performed based on the mass spectral data of compounds (MS) and Kovats indices (RI) with those of Wiley spectral
library collection and NIST (National Institute of Standards and Technology) library database.
3.2. Correlation Between P. somalensis and other Pulicaria Species
The application of PCA on the concentration of various classes of the EO from different Pulicaria
species revealed that P. somalensis, P. stephanocarpa, and P. vulgaris from Italy, P. vulgaris from Tunisia,
P. dysenterica from Greece, P. gnaphalodes from Mashhad, Iran, and P. glutinosa were correlated with
each other due to the similarity in the content of sesquiterpenes (Figure 2a). However, P. dysenterica
from Iran was not correlated with other Pulicaria species, as it was characterized by the presence of
diterpene. On the other hand, P. undulata from Egypt, P. undulata from Sudan, P. vulgaris from Iran,
P. odora, P. mauritanica from Morocco, and P. mauritanica from Algeria, and P. jaubertii were correlated
with each other, since these species have monoterpenes as the major class.
The application of AHC on the data of the major compounds (>5%) of the EO from different
Pulicaria species showed that the P. somalensis was separated from other Pulicaria species (Figure 2b).
These results reflected the characteristic pattern of the chemical composition of P. somalensis. Similarly,
P. odora, P. vulgaris from Iran, P. vulgaris from Italy, P. gnaphalodes from Mashhad, Iran, P. dysenterica
from Iran, P. vulgaris from Tunisia, P. glutinosa, and P. incisa from Algeria were also separated alone.
However, P. undulata from Sudan and Egypt were grouped together into one group, while
P. undulata from Algeria, P. jaubertii, P. incisa from Egypt, P. mauritanica from Morocco, and P. mauritanica
from Algeria were grouped together. P. sicula, P. dysenterica from Greece, and P. stephanocarpa
were separated together, while P. gnaphalodes from Tehran, Iran and P. vulgaris from Iran were
grouped together.
The obtained data from AHC showed that the same species varied in the chemical composition
according to their geographical region. Abd El-Gawad et al. [41] reported that the chemical composition
of the EO varied among different plant ecotypes due to variation in climate, soil, environmental variables,
and the genetic pool. Our previous work on Xanthium strumarium L. (cocklebur), Symphyotrichum
squamatum (Spreng.) Nesom (bushy starwort), and Launaea (Morrar) species indicated that a variation
of the chemical composition of the EO was found to be strongly correlated with variation in the
habitats [42,43].
Agronomy 2020, 10, 399
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The overall correlation analysis showed that P. somalensis has a specific chemical pattern of the
EO, where it could be related to the genetic characteristics. These data of the EO chemical−1composition
could be helpful for the chemotaxonomy of Pulicaria genus.
2
a
Sesquiterpenes
P. vulgaris, Italy
1
F2 (37.27 %)
P. dysenterica, Greece
P. gnaphalodes, Mashhad, Iran
P. glutinosa
P. vulgaris, Tunisia
P. somalensis
P. stephanocarpa
1.5
P. sicula
P. undulata, Iran
P. dysenterica, Iran
P. gnaphalodes, Tehran, Iran
0.5
P. undulata, Algeria
P. incisa, Algeria
0
-0.5
Diterpenes
P. undulata, Sudan
P. vulgaris, Iran
P. odora
Monoterpenes
P. undulata, Egypt
P. mauritanica, Morocco
P. jaubertii P. mauritanica, Algeria
Others
-1
-1.5
-1
-0.5
0
0.5
1
1.5
2
2.5
3
F1 (55.19 %)
-0.09
b
Similarity
0.11
0.31
0.51
0.71
P. incisa, Algeria
P. undulata, Egypt
P. undulata, Sudan
P. undulata, Algeria
P. jaubertii
P. incisa, Egypt
P. mauritanica, Morocco
P. mauritanica, Algeria
P. glutinosa
P. vulgaris, Italy
P. sicula
P. dysenterica, Greece
P. stephanocarpa
P. gnaphalodes, Tehran, Iran
P. undulata, Iran
P. somalensis
P. odora
P. vulgaris, Iran
P. gnaphalodes, Mashhad, Iran
P. dysenterica, Iran
P. vulgaris, Tunisia
0.91
Figure 2. (a) Principal component analysis (PCA) based on the chemical classes of the essential oil, and
(b) agglomerative hierarchical clustering (AHC) based on the major chemical compounds of the EO of
Pulicaria somalensis (Shie) and other reported Pulicaria species.
Agronomy 2020, 10, 399
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3.3. Allelopathic Activity of the EO
The extracted EO from P. somalensis above-ground parts exhibited a significant allelopathic
inhibitory activity on the germination and the seedling growth of the tested weeds (B. pilosa and
D. aegyptium) in a dose-dependent manner (Figure 3). At a concentration of 1 mg mL−1 of the
EO, germination, root growth, and shoot growth of B. pilosa were inhibited by 61.4%, 73.6%, and
55.4%, respectively.
100
Germination inhibition %
respect to control
a)
B. pilosa
D. aegyptium
a
80
ab
ab
60
40
bc
c
b
c
d
20
Root inhibition %
respect to control
b)
P value (0.05)
Conc. (C) < 0.0001 ***
Weed (W) < 0.0001 ***
C × W = 0.4518 ns
d
0
100
a
B. pilosa
D. aegyptium
80
a
b
a
b
60
e
b
c
40
d
P value (0.05)
Conc. (C) < 0.0001 ***
Weed (W) = 0.0883 ns
C × W = 0.0218 *
d
20
e
0
0.2
c)
100
0.4
0.6
0.8
1
B. pilosa
D. aegyptium
Shoot inhibition %
respect to control
80
a
b
60
c
a
d
40
bc
20
0
e
c
d
0.2
0.4
b
P value (0.05)
Conc. (C) < 0.0001 ***
Weed (W) = 0.0003 ***
C × W < 0.0001 ***
0.6
0.8
Concentration (mg
1
mL-1)
Figure 3. Allelopathic effect of the essential oil from the above-ground parts of Pulicaria somalensis (Shie)
on (a) seed germination, (b) root growth, and (c) shoot growth of Dactyloctenium aegyptium (crowfoot
grass) and Bidens pilosa (hairy beggarticks). Within each line, different letters indicate statistically
significant differences at p ≤ 0.05. ns: non-significant.
≤ 0.05. ns: non
Agronomy 2020, 10, 399
10 of 14
On the other hand, germination, root, and shoot growth of D. aegyptium were inhibited by 75.0%,
72.1%, and 66.2%, respectively. A highly significant difference in seed germination and shoot growth
was observed between the two test weeds (p < 0.0001), while no significant difference (p < 0.0883) was
observed based on the root growth (Figure 3). Usually, the root is more affected, as it is the first sprout
organ and because it has direct contact with allelochemicals, as described in many studies [23,43–46].
According to the IC50 , the EO showed a more inhibitory effect against D. aegyptium (Figure 4).
The IC50 value on the germination of D. aegyptium was doubled compared to B. pilosa. The IC50 values
on the root growth of B. pilosa and D. aegyptium were comparable (0.6 mg mL−1
−1 , each), while the IC50
−1
values on the shoot growth were 1.0 and 0.7 mg mL
−1 , respectively (Figure 4). Overall, the EO of
P. somalensis showed more inhibitory activity against D. aegyptium than B. pilosa. This variation in the
activity could be attributed to the genetic characteristics of the weeds [47].
1000
B. pilosa
D. aegyptium
IC50 (mg mL-1)
800
600
400
200
0
Germination
Root
Shoot
Figure 4. IC50 values of the essential oil extracts from the above-ground parts of Pulicaria somalensis
(Shie) on germination, root, and shoot growth inhibition of Dactyloctenium aegyptium (crowfoot grass)
and Bidens pilosa (hairy beggarticks).
The inhibitory activity of P. somalensis EO could be attributed to the high content of oxygenated
terpenoid compounds, particularly sesquiterpenes (Table 1). Major compounds such as juniper
camphor, α-sinensal, 6-epi-shyobunol, α-zingiberene, α-bisabolol, and T-muurolol could act either
individually
and the growth of the B. pilosa weed. The
α or synergistically as inhibitors
α for the germination
α
oxygenated terpenoids usually have a significant role in biological activity compared to non-oxygenated
compounds due to the reactivity of oxygen [41]. The EOs from S. squamatum and L. serriola have been
reported to inhibit the germination and the seedling growth of the B. pilosa Abd-ElGawadm et al. [22]
and Abd-ElGawad, et al. [42] due to the presence of sesquiterpenes as major components.
Juniper camphor has been reported as the main compound (15.5%) of antibacterial, antioxidant,
and phytotoxic active EO from Syzygium samarangense Merr. & Berry (rose apple) Lawal, et al. [48].
Additionally, the EO from Artemisia argyi Levl et Vant (mugwort) has been reported to possess antifungal
activity due to the high content of juniper camphor [49].
3.4. Antioxidant Activity of the EO
The antioxidant capacity of the EO from the above-ground parts of P. somalensis was tested by
the ability to scavenge the DPPH and the ABTS. The results revealed that the scavenging activity was
significantly increased by the increase of EO concentration (Table 2). The EO attained IC50 values of
81.2 mg mL−1 and 64.4 mg mL−1 based on DPPH and ABTS assays, compared to ascorbic acid with
IC50 values of 21.7 mg mL −1 and 18.4 mg mL −1 , respectively. These data showed that the EO of
−1
−1
−1
−1
Agronomy 2020, 10, 399
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P. somalensis has meaningful antioxidant activity. This antioxidant activity could be ascribed to the major
constituents of the EO, such as juniper camphor, α-sinensal, and 6-epi-shyobunol. These oxygenated
sesquiterpenes might act individually or synergistically as antioxidants. The antioxidant role of the
oxygenated compounds might be attributed to the free electrons due to the high oxygenation [42,43].
Although juniper camphor has been reported to have antifungal [49] and antibacterial activity and
cytotoxicity [50], its antioxidant activity has still not been studied. Therefore, we recommend further
studies to determine the biological activity, particularly the antioxidant activity, of the pure form of
major compounds, especially juniper camphor.
Table 2.
Percentage of scavenging activity of 2,2-Diphenyl-1-picrylhydrazyl (DPPH) and
2,2′ -azino-bis(3-ethylbenzothiazoline-6-sulphonic acid (ABTS) as well as the IC50 values of the essential
oil (EO) from Pulicaria somalensis (Shie) compared with ascorbic acid.
Treatment
Concentration
(µg mL−1 )
Pulicaria
somalensis
(EO)
100
80
60
40
20
10
Ascorbic acid
DPPH
Scavenging
(%) *
59.1 ± 2.78A
50.5 ± 0.73B
37.6 ± 0.35C
33.4 ± 0.96D
28.6 ± 0.80E
24.5 ± 1.20F
ABTS
IC50
(µg mL−1 )
Scavenging
(%)
IC50
(µg mL−1 )
81.2
64.0 ± 1.54A
54.3 ± 0.60B
51.7 ± 1.51C
38.7 ± 0.32D
33.3 ± 2.22E
28.1 ± 0.77F
64.4
21.7
18.4
* values are average (n = 3) ± standard error, IC50 : the concentration of the sample that required to reduce the DPPH or
ABTS absorbance by 50%. Different superscript letters within the column mean values significant variation at p < 0.05.
4. Conclusions
For the first time, the present study showed that the EO from P. somalensis has 71 compounds.
Juniper camphor, α-sinensal, 6-epi-shyobunol, α-zingiberene, α-bisabolol, and T-muurolol were found
as main constituents. The correlation analysis revealed that it has a specific EO chemical pattern via
the absence of the correlation with other Pulicaria ecospecies. Biologically, EO showed significant
allelopathic activity on the weeds (B. pilosa and D. aegyptium). Therefore, this EO could be integrated
into the methods of the management of these weeds as an eco-friendly way, but after further study
on the assessment of its activity, durability, and safety as bioherbicide at the field scale. Moreover,
the EO reflected meaningful antioxidant activity compared to ascorbic acid. Because the biological
activities of the pure form of the identified major compounds are still undetermined, a further study is
recommended for the characterization of the pure major compounds, particularly juniper camphor.
Author Contributions: Conceptualization, A.A., A.E. and A.A.-E.; Formal analysis, A.E., A.E.-N.E.G., B.D. and
A.A.-E.; Investigation, A.A., A.E., B.D., S.A.-R. and A.A.-E.; Resources, A.A., A.E., A.E.-N.E.G. and A.A.-E.;
Software, A.A.-E.; Writing – original draft, A.E. and A.A.-E.; Writing – review & editing, A.A., A.E., A.E.-N.E.G.,
B.D., S.A.-R. and A.A.-E. All authors have read and agree to the published version of the manuscript.
Funding: This research was funded by Deanship of Scientific Research at King Saud University, through
research group number RG-1441-302 and the APC was funded also by Deanship of Scientific Research at King
Saud University.
Acknowledgments: The authors extend their appreciation to the Deanship of Scientific Research at King Saud
University for supporting this work through the research group No (RG-1441-302) and National Research Centre,
Egypt (Project No. 120-10-118).
Conflicts of Interest: The authors declare no conflict of interest.
Agronomy 2020, 10, 399
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