ANALYSIS OF CHEMICAL PROFILES OF DIFFERENT PISTACIA ATLANTICA PARTS AT SULAYMANIYAH AND HALABJA REGION IN IRAQ

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Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 561 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
ANALYSIS OF CHEMICAL PROFILES OF DIFFERENT PISTACIA
ATLANTICA PARTS AT SULAYMANIYAH AND HALABJA
REGION IN IRAQ
AHMAD, Z. M.1* – HAMZAH, H. M.2 – LAZIM, Z. S.1
1Department of Horticulture, College of Agricultural Engineering Sciences, University of
Sulaimani. Sulaymaniyah, Iraq
e-mail: zaynab.lazim@univsul.edu.iq
2Department of Biology, College of Science, University of Sulaimani. Sulaymaniyah, Iraq
e-mail: haider.hamzah@univsul.edu.iq
*Corresponding author
e-mail: zhala.ahmad@univsul.edu.iq
(Received 19th Aug 2022; accepted 11th Nov 2022)
Abstract. The current study estimated the chemical constituents of wild Pistacia atlantica parts. Leaves,
fruits, and rachis in spring and autumn were chosen. In addition, the analysis covered the bark and gum of
the plant. Between April and October 2020, samples were collected from Sulaymaniyah and Halabja
governorates in Kurdistan (Northeastern Iraq). Notably, at various locations, spring leaves contained more
nitrogen, phosphorus, potassium, and carbohydrates than autumn leaves. Moreover, Qaradagh autumn fruits
contained the highest levels of fixed oil (32.08%). GC analysis of autumn fruit oil showed the
concentrations of palmitic acid (11.02-11.69%), stearic acid (2.7-4.2%), oleic acid (44.25-45.39%), linoleic
acid (13.11-15.36%) and linolenic acid (0.36-0.77%). Lastly, Qaradagh spring leaves had the highest total
phenolic content (307.057 mg/g), while Ranya spring leaves had the highest total flavonoid concentration
(101.483 mg/g). HPLC analysis of Ranya spring leaves revealed that the concentrations of quercetin, rutin,
catechin, ferulic acid, and ellagic acid were 168.9 µg/g, 149.7 µg/g 124.5 µg/g, 122.4 µg/g, and 97.4 µg/g,
respectively. Phenolic compounds are abundant in Qaradagh spring leaves. As such, further studies are
needed to investigate the potential therapeutic uses of bioactive compounds isolated from Qaradagh spring
leaves of P. atlantica.
Keywords: plant parts, locations, fixed oil, phenolic composition, flavonoids
Introduction
The Pistacia plant is a member of the Anacardiaceae family. The genus Pistacia
consists of at least 11 species, some of which have edible nuts and are commercially
important (Kafkas and Perl-Treves, 2001). Three Pistacia species are found in the
Kurdistan region of Iraq; P. atlantica and P. khinjuk are wild species. P. vera, on the other
hand, is a cultivated species (Shabaz, 2010). P. atlantica is known as Daraban or Qazwan
in Kurdistan and is one of the most common Pistacia species worldwide (Dyary et al.,
2017). In the Islamic Rebublic of Iran, P. atlantica is called Baneh and is the most
economically important tree species in many rural areas (Saber-Tehrani et al., 2013).
P. atlantica is indigenous to Kurdistan in northern Iraq, southern-east Turkey,
northwestern Iran, Afghanistan, Syria, and Armenia (Shabaz, 2010). Leaves, fruits, and
gum of Pistacia are valuable for their medicinal, cosmetic, and nutritional value;
Pistacia’s gum is used to make natural Kurdish chewing gum (Paraschos et al., 2007).
Parts of Pistacia plant contain phytochemical constituents such as phenolic compounds,
terpenoids, fatty acids, and sterols (Labdelli et al., 2019; Hasheminya and Dehghannya,
2020; Najafiasl et al., 2022).

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 562 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Pistacia atlantica fruits produce a considerable yield of oil. The fruits are widely
consumed as a nutrient by the local population and are used in traditional medicine to
treat a variety of diseases. Also, the oil can be used in food and cosmetics (Saber-Tehrani
et al., 2013). Its oil contains both saturated and unsaturated fatty acids; the ratio of
unsaturated fatty acids to saturated fatty acids indicates that the content of unsaturated
fatty acids is approximately three times higher than that of saturated fatty acids (Labdelli
et al., 2019). Also, the oil is rich in mono-unsaturated fatty acids, particularly oleic acid,
which is inversely related to cholesterol levels (Ahmed et al., 2021).
P. atlantica leaves are known to be an excellent source of phenolic compounds (Toul
et al., 2017). Over 8000 phenolic compounds have been identified from various plant
parts via different techniques, making them one of the most abundant bioactive molecules
in the plant kingdom (Ramos, 2007). The majority of these compounds have the potential
to be therapeutic agents (Tungmunnithum et al., 2018). Thus, the extraction and
separation of polyphenols such as phenolic acids, flavonoids, lignans and stilbenes are
vital for their potential uses in medicine (Baiano and Del Nobile, 2016). However,
choosing and developing the right separation techniques can be challenging.
Despite the Pistacia tree’s natural occurrence in Iraq’s Kurdistan, there is a paucity of
literature on the chemical constituents of various parts collected from local locations. As
such, the goal of this study was to examine the bioactive components of plant materials
and determine the best location containing plant parts with the highest concentrations of
active compounds.
Materials and methods
Locations of the study
The plant parts were gathered from four locations; Qaradagh, Ranya, Sharbazher in
Sulaymaniyah, and Hawar in Halabja (Fig. 1).
Figure 1. Map of the distribution of collection sites of the studied plant materials

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
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APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Table 1 shows the highest and lowest temperatures, as well as rainfall, in the selected
locations.
Table 1. Daily average of minimum and maximum temperatures and rainfall during January
to October 2020 for the study locations
Month
Qaradagh
Ranya
Sharbazher
Halabja
Air temp. ᵒc
Rain
fall
(mm)
Air temp. ᵒc
Rain
fall
(mm)
Air temp. ᵒc
Rain
fall
(mm)
Air temp. ᵒc
Rain
fall
(mm)
Min
Max
Min
Max
Min
Max
Min
Max
January
2
9
171
0
7
277.4
-2.5
2.4
124
3
11.4
91.4
February
3
12
245.5
2
10
172.8
-5.2
4.1
242
4.7
13.8
67.9
March
9
19
241.3
6
15
171.8
2.5
11.3
270
9.7
20.8
124.5
April
13
21
101
13
20
71.4
6.3
12
94
12.9
25
83.6
May
19
29
16
16
25
29.5
11.6
21
31.5
18.6
35.3
10
June
20
35
0
22
33
0
16.8
30.8
0
23.6
42
0
July
26
42
0
25
41
0
15.9
32.2
0
29
45.9
0
August
24
40
0
24
39
0
17.1
29.7
0
26.4
43.5
0
September
22
37
0
20
37
0
19.8
25.9
0
24.4
42
0
October
16
30
0
17
27
0
13.1
20.1
0
17
34.3
0
* The data were obtained from the meteorological station in Sulaimani
Regarding soil characteristics, Table 2 depicts some physical and chemical
characteristics of the soil taken from the study locations.
Table 2. Physical and chemical characteristics of the soil of locations under study
Characteristics
Qaradagh
Ranya
Sharbazher
Halabja
Ec dS m-1
0.2
0.4
0.5
0.2
pH
6.95
7.12
7.08
7.05
Available N mg kg-1
45
32
31
39
Available P mg kg-1
16.65
16.42
15.52
18.23
Available K mg kg-1
172.63
160.98
140.53
180.23
O.M g kg-1
58
28.3
24.3
48.4
CaCo3 g kg-1
331.2
114.8
103.7
100.0
Sand g kg-1
444
439
262
430
Silt g kg-1
367
316
480
380
Clay g kg-1
189
245
258
190
Texture
Loam
Loam
Loam
Loam
*Soil analysis was carried out in a central laboratory for soil, water and plant analysis in the College of
Agricultural Engineering Sciences / University of Baghdad
Plant materials collection and preparation
Between April and October 2020, spring leaf, spring fruit, spring rachis, bark, gum,
autumn leaf, autumn fruit, and autumn rachis of Pistacia atlantica were collected from
each location (Table 3). The samples were taken randomly with five replications. Figure 2
shows the tree, leaf, fruit, and gum of Pistacia atlantica with a gum collector.
Following collection, samples were prepared for analysis at the University of
Sulaimani’s Research Laboratory. All of the spring leaves, spring fruits, spring rachis,
bark, autumn leaves, autumn fruits, and autumn rachis were air-dried at room temperature
and ground to a fine powder with an electric blender, except the gum. All of the samples
were then stored at 4 °C for future research.

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 564 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Table 3. Number of samples, plant parts, and collection date at the different locations under
study
No. of samples
(trees)
Plant parts
Collection date
5
Spring leaf, bark
April
spring fruit, spring rachis
May
Gum
July- August
Autumn leaf
September
Autumn fruit, autumn rachis
October
*Five trees for each location and eight parts for each tree
Figure 2. P. atlantica with different parts (A) Tree. (B) Leaf. (C) Fruit. (D) Handmade clay cup
with collected gum (resin)
Total nitrogen, phosphorus, and potassium %
After digesting half of each sample (0.5 g) with concentrated sulfuric acid and 30%
hydrogen peroxide, total nitrogen in leaves was measured using a microkjeldahl apparatus
(Labconco, Kansas). Phosphorus was determined using a colorimetric method by a
spectrophotometer (Thermo Electron, UK) at 410 nm, and potassium was measured using
a flame photometer (Janeway PFP 7, UK). The percentage of elements was calculated
using dry weight (Estefan et al., 2013).

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 565 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Carbohydrate %
Carbohydrate was measured colorimetrically (Joslyn, 1970). Briefly, 0.2 g of dry
samples were put into the test tubes separately, then 8 ml of HClO₄ (1N) was added. The
mixture was placed in a water bath at 60 °C for 60 minutes. Thereafter, the samples were
centrifuged at 3000 rpm for 15 minutes. All three mentioned steps are repeated three
times. The supernatants collected the volume completed to 100 ml by adding distilled
water. Then, 1 ml of the diluted solution was taken, and 1 ml of 5% phenol and 5 ml of
H₂SO₄ (97%) were added. Finally, total carbohydrates were determined using a
spectrophotometer (Thermo Electron, UK) at 490 nm. Measurement of total
carbohydrates in leaves was performed using the following equation:
  
  (Eq.1)
Extraction and analysis the constituents of fixed oil
Fixed oil was measured by Soxhlet (Simax, Czechia) method (Ferreira-Dias et al.,
2003). 50 g dried-ground powder was placed in a Soxhlet thimble and extracted with
250 ml n-hexane solvent for 2 hours in Soxhlet extraction system. The remaining solvent
was evaporated by a rotary evaporator (BUCHI, Germany). After drying, the dried
extracts were weighed and the oil content calculated as follows:
  󰇛󰇜
󰇛󰇜  (Eq.2)
The fixed oil compounds were analyzed using gas chromatography (Shimadzu, Japan),
where the ionized flame detector (FID) and SE-30 capillary column (30 m length,
0.25 mm inner diameter) were used. Injection area, detector and separator column
temperature were 280 °C, 310 °C and 120–290 °C (10 °C/min), respectively. The gas
flow rate was 100 Kpa (Zhang et al., 2015).
Measurement of total phenolic and flavonoid contents
Samples were prepared using the Tabart et al. (2007) and Michiels et al. (2012)
methods. Briefly, 1 g of samples were placed in 15 ml tubes. The tubes were then filled
with 10 ml of 80% methanol. The samples were shaken in a water bath for 3 hours at
38 °C before being centrifuged at 5000 rpm for 15 minutes at 4 °C. The upper layer was
removed and transferred to a new, clean, labeled 15 ml tube, which was then stored in a
refrigerator at 4 °C until use.
Total phenolic content was determined in the methanolic extract with a standard
Folin-Ciocalteu reagent described by Rodrigues et al. (2019) with some modifications.
100 μl of each methanolic extract is mixed with 4 ml of 10% Folin-Cioculate reagent
(Thomasbaker, India), and allowed to react for 5 minutes at room temperature. After that,
2 ml of 20% saturated Na2CO3 solution was added then left for 60 minutes in the dark at
38 °C. Regarding blanks, same previous steps were repeated except 100 μl of water was
used instead for the samples. The measurement was done at 765 nm using a
spectrophotometer (Thermo Electron, UK) to calculate the phenolic content using the
calibration curve made with gallic acid (0.1, 0.2, 0.3, 0.4, 0.5, 0.6, 0.7, 0.8, 0.9 and
1 mg/ml) and expressed as milligrams of gallic acid equivalent (GAE) per gram dry
weight.

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
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APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Total flavonoid content was determined by the aluminum chloride (AlCl3) colorimetric
method (Hassan et al., 2020) with minor modifications. In brief, 0.5 ml of each sample
extract was mixed with 1.5 ml with 80% methanol, 0.1 ml of 10% (w/v) AlCl3 solution,
0.1 ml of 1M potassium acetate, and 2.8 ml of distilled water. Then the mixture was
incubated at room temperature for 45 minutes. 0.5 ml of water was mixed with the same
amount of chemicals in the previous step as a blank. The absorbance of the reaction
mixture was determined at 415 nm using a spectrophotometer (Thermo Electron, UK).
The results of the total flavonoid content were calculated based on a standard curve
prepared using quercetin at different concentrations (0.05, 0.1, 0.15, 0.2, 0.25, 0.3, 0.35,
0.4, 0.45, and 0.5 mg/ ml) and expressed as milligrams of quercetin per gram dry weight.
Extraction and isolation of phenolic compounds for HPLC analysis
Phenolic compounds were extracted from the homogenized plant sample (3 g) using
ethanol/water (70/30) ratio. Extraction process was accomplished using an Ultrasonic
Bath (Smith-Kline, USA) at room temperature for 60 sec. After filtration, the solvent was
removed by the rotary evaporator (BUCHI, Germany) under vacuum, and dried at 40 °C
to the constant mass. Dry extracts were stored in glass bottles at 4 °C to prevent oxidative
damage until analysis. Reversed phase HPLC analysis was used to perform quantification
of individual phenolic compounds, using a HPLC (SYKAMN, Germany)
chromatographic system equipped with a UV detector, chemstation software, binary
pump, online vacuum degasser, autosampler and Zorbax Eclipse Plus-C18-ODS column
(4.6 x 250 mm). The gradient elution method, with eluent A (methanol) and eluent B (1%
formic acid in water) was performed, as follows: 40 % B (0-4 min); 50 % B (4-10 min).
The column temperature was 30 ºC and flow-rate of 0.7 ml/min. The injected volume of
samples and standards was 100 μl and was done automatically using an autosampler. The
spectra were acquired in the 280 nm (Radovanović et al., 2015).
Statistical analysis
A statistical software package, XLSTAT (Version 2016.02.28451), was used to
perform statistical analysis. Two way Completely Randomized Design (locations and
plant parts) with five replicates (five trees) was conducted. The means were compared to
determine critical values using the Duncan’s Multiple Range Test at P ≤ 0.05.
Results
Nitrogen, phosphorus, potassium, and carbohydrates content of P. atlantica leaves
Table 4 shows the percentage of nitrogen, phosphorus, potassium, and carbohydrates
in spring and autumn leaves of P. atlantica at different locations. The highest value
(6.70%) of nitrogen content appeared in spring leaves collected from Qaradagh with
significant differences compared to other treatments. Whereas, the lowest value was in
autumn leaves (1.94%) collected from Ranya, which was not significantly different from
spring leaves collected from the same location (2.30%).
The highest percentage of phosphorus occurred in the spring leaves collected from
Halabja (2.03%) and the lowest value was in the autumn leaves (0.57%) collected from
Ranya, which did not differ significantly with autumn leaves collected from Qaradagh
(0.62%). Regarding the potassium percentage, it was noticed that the spring leaves
collected from Halabja gave the highest value (2.25%), which did not significantly differ

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 567 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
from autumn leaves collected from the same place (2.14%); the lowest percentage
occurred in the spring leaves collected from Ranya (0.48%).
Carbohydrate results showed the highest percentage (30.83%) was found in the spring
leaves collected from Qaradagh. No significant difference was between the Ranya leaves
collected from the same season (30.14%) and the lowest percentage was in the autumn
leaves (20.31%) that were collected from Sharbazher.
Table 4. Nitrogen, phosphorus, potassium, and carbohydrates (%) in spring and autumn
leaves
Nitrogen
Phosphorus
Potassium
Carbohydrate
Locations
Spring
leaves
Autumn
leaves
Spring
leaves
Autumn
leaves
Spring
leaves
Autumn
leaves
Spring
leaves
Autumn
leaves
Qaradagh
6.70 a
2.67 de
0.99 b
0.62 de
2.03 b
1.68 d
30.83 a
22.67 e
Ranya
2.30 ef
1.94 f
0.96 b
0.57 e
0.48 f
1.84 c
30.14 ab
23.57 de
Sharbazher
4.90 b
2.56 de
0.96 b
0.73 c
0.92 e
1.76 cd
29.26 bc
20.31 f
Halabja
3.70 c
2.74 d
2.03 a
0.68 cd
2.25 a
2.14 ab
28.89 c
24.21 d
* Different letters have significant difference between them according to Duncan test at p< 0.05
Total fixed oil and GC analysis for its constituents
Fixed oil content and GC analysis results in autumn fruit and bark of P. atlantica at
different locations are illustrated in Table 5. Significant differences were found in the
autumn fruit collected from various locations, while slight insignificant differences
appeared among the barks collected from different locations. Significant differences were
observed between the highest levels of total fixed oil found in autumn fruit collected from
Qaradagh (32.08%) and the lowest level found in the bark collected from Halabja
(3.10%).
Autumn fruit oil contained more saturated fatty acids (palmitic and stearic acids) and
unsaturated fatty acids (oleic, linolic, and linolenic acids) than bark at various locations.
The highest value of palmitic acid (11.69%), stearic acid (4.20%), oleic acid (45.39%),
linolic acid (15.36%), and linolenic acid (0.77%) content appeared in autumn fruit oil
collected from Ranya. While the lowest value of palmitic acid (2.55%), stearic acid
(0.66%), oleic acid (5.89%), linolic acid (3.69%), and linolenic acid (0.14%) content was
found in bark oil collected from Halabja.
Table 5. The concentration of total fixed oil, saturated and unsaturated fatty acids (%) in
autumn fruits and bark oil
Locations
Total fixed oil
Palmitic acid
Stearic acid
Oleic acid
Linolic acid
Linolenic acid
Autumn
fruits
Bark
Autumn
fruits
Bark
Autumn
fruits
Bark
Autumn
fruits
Bark
Autumn
fruits
Bark
Autumn
fruits
Bark
Qaradagh
32.08 a
3.62 e
11.48 a
2.97 b
3.60 b
0.85 ef
45.02 ab
6.22 c
14.22 b
4.88 e
0.61 b
0.29 c
Ranya
31.16 b
3.48 e
11.69 a
3.05 b
4.20 a
0.91 e
45.39 a
6.39 c
15.36 a
5.00 e
0.77 a
0.20 c
Sharbazher
26.16 c
3.31 e
11.28 a
2.68 b
3.10 c
0.74 ef
44.79 ab
6.00 c
13.69 c
3.98 f
0.58 b
0.36 d
Halabja
18.04 d
3.10 e
11.02 a
2.55 b
2.70 d
0.66 f
44.25 b
5.89 c
13.11 d
3.69 f
0.36 c
0.14 d
* Absence of this compound in other parts of the plant. *Different letters have significant difference
between them according to Duncan test at p< 0.05

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 568 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Total phenolic content of P. atlantica parts (mg/g)
Table 6 shows the value of total phenolic content in all parts of P. atlantica. Spring
and autumn leaves are richer in total phenolic content than other parts at all locations. On
the other hand, at all locations, the gum contained a low amount of total phenol, with no
significant differences observed between gum collected from different locations. There
were significant differences between the maximum concentration in the Qaradagh spring
leaves (307.057 mg/g) and the minimum concentration of the gum in the Sharbazher
collection (1.409 mg/g).
Table 6. The concentration of total phenolic content (mg/g) in different parts
Locations
Spring
leaves
Autumn
leaves
Spring
fruits
Autumn
fruits
Spring
rachis
Autumn
rachis
Bark
Gum
Qaradagh
307.057 a
299.673 e
297.457 f
99.999 u
243.995 n
294.504 h
120.675 t
1.426x
Ranya
304.546 c
295.981 g
287.267 j
100.295 u
185.658 q
261.865 l
134.706 r
1.415x
Sharbazher
305.876 b
303.956 c
295.981 g
93.796 w
240.302 o
274.271 k
128.651 s
1.409x
Halabja
302.331 d
301.593 d
209.436 p
97.784 v
250.493 m
293.322 i
135.444 r
1.442x
* Different letters have significant difference between them according to Duncan test at p< 0.05
Total flavonoid content of P. atlantica parts (mg/g)
Table 7 shows the concentration of total flavonoid content in eight parts of P. atlantica.
Spring leaves at all locations contain a higher amount of total flavonoid than other parts
and the significant differences were observed among locations. Bark and gum contain a
low amount of total flavonoid and no significant value was observed between bark and
gum collected from different locations. However, significant differences were observed
between the highest concentration value in the spring leaves of Ranya (101.483 mg/g)
and lowest concentration in the bark collected from Halabja (0.399 mg/g).
Table 7. The concentration of total flavonoids content (mg/g) in different parts
Locations
Spring
leaves
Autumn
leaves
Spring
fruits
Autumn
fruits
Spring
rachis
Autumn
rachis
Bark
Gum
Qaradagh
82.970 c
75.624 e
60.528 j
2.715 p
51.713 k
70.739 h
0.687 q
0.548 q
Ranya
101.483 a
63.136 i
49.619 l
2.494 p
40.510 n
45.285 m
0.433 q
0.426 q
Sharbazher
93.953 b
73.053 g
63.063 i
2.118 p
50.978 k
45.138 m
0.441 q
0.478 q
Halabja
81.979 d
74.596 f
26.552 o
2.521 p
51.603 k
60.087 j
0.399 q
0.609 q
* Different letters have significant difference between them according to Duncan test at p< 0.0
HPLC analysis for phenolic compounds
The results of quantitative analysis of each identified phenolic compound by HPLC in
P. atlantica parts are shown in Table 8. Spring leaves from all sites contain high amount
of quercetin and have significant differences observed in comparison with other plant
parts. The significant differences were observed between the highest levels of quercetin
in Ranya spring leaves (168.9 µg/g) and the lowest level in Sharbazher spring rachis
(61.4 µg/g). While quercetin in the Qaradagh spring leaves and Halabja autumn leaves

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 569 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
(160.7 µg/g and 158.9 µg/g, respectively) show a significant difference observed in other
plant parts.
Table 8. HPLC analysis for phenolic compounds of P. atlantica (µg/g)
Phenolics
compounds
Locations
Spring
leaves
Autumn
leaves
Spring
fruits
Autumn
fruits
Spring
rachis
Autumn
rachis
Bark
Gum
Quercetin
Qaradagh
160.7 b
138.9 f
101.4 j
71.5 p
68.7 qr
115.4 h
nd*
nd
Ranya
168.9 a
144.2 e
106.9 i
77.5 n
70.4 pq
122.8 g
nd
nd
Sharbazher
146.9 d
123.9 g
80.4 m
74.5 o
61.4 s
85.5 l
nd
nd
Halabja
155.8 c
158.9 b
92.4 k
80.4 m
66.9 r
114.5 h
nd
nd
Rutin
Qaradagh
140.8 b
119.8 f
98.8 h
52.8 q
60.8 o
88.7 k
22.8 s
29.1 r
Ranya
149.7 a
122.5 e
102.6 g
55.6 p
66.4 n
95.8 i
11.4 u
28.4 r
Sharbazher
124.5 e
98.7 h
88.5 k
51.5 q
51.2 q
75.6 m
18.4 t
22.5 s
Halabja
133.8 d
136.9 c
92.5 j
60.5 o
58.9 o
81.2 l
20.5 st
30.5 r
Cinnamic acid
Qaradagh
105.9 e
124.7 c
80.7 l
68.1 op
57.9 r
92.5 h
22.4 u
17.4 wx
Ranya
120.6 d
133.5 b
84.9 k
73.9 m
60.8 q
104.8 e
12.8 y
15.8 x
Sharbazher
88.5 j
94.5 g
66.8 p
62.5 q
50.1 t
80.1 l
18.9 vw
12.8 y
Halabja
98.7 f
142.6 a
71.4 n
68.9 o
55.2 s
90.6 i
20.5 v
18.7 vw
Catechin
Qaradagh
120.9 b
nd
90.1 f
nd
78.7 h
nd
nd
nd
Ranya
124.5 a
nd
98.7 e
nd
78.7 h
nd
nd
nd
Sharbazher
112.5 d
nd
74.8 i
nd
66.2 j
nd
nd
nd
Halabja
115.8 c
nd
84.5 g
nd
74.8 i
nd
nd
nd
Ferulic acid
Qaradagh
120.8 b
nd
78.9 f
nd
53.5 j
nd
18.9 q
26.8 n
Ranya
122.4 a
nd
88.9 e
nd
55.4 i
nd
6.4 t
24.8 o
Sharbazher
112.8 d
nd
66.5 h
nd
41.8 l
nd
13.6 s
22.5 p
Halabja
118.9 c
nd
74.5 g
nd
50.1 k
nd
15.8 r
28.9 m
Ellagic acid
Qaradagh
91.4 b
62.8 i
60.1 j
42.7 q
38.7 s
66.2 g
25.8 v
nd
Ranya
97.4 a
70.5 e
68.9 f
52.6 m
40.8 r
64.7 h
18.9 y
nd
Sharbazher
64.5 h
66.9 g
44.5 p
41.5 r
32.5 u
50.9 n
20.1 x
nd
Halabja
88.9 c
74.1 d
54.9 l
45.8 o
35.6 t
57.8 k
22.4 w
nd
Tannic acid
Qaradagh
nd
81.3 cd
nd
65.8 g
nd
80.4 de
28.9 j
21.7 l
Ranya
nd
88.5 b
nd
79.8 e
nd
82.4 c
14.7 o
20.4 m
Sharbazher
nd
79.4 e
nd
62.5 h
nd
51.7 i
22 l
18.9 n
Halabja
nd
97.4 a
nd
74.5 f
nd
64.7 g
25.8 k
22.4 l
Kaempferol
Qaradagh
nd
81.4 f
nd
53.8 k
nd
86.9 d
nd
28.7 m
Ranya
nd
91.4 b
nd
60.4 i
nd
84.6 e
nd
27.9 m
Sharbazher
nd
88.9 c
nd
52.9 k
nd
63.5 h
nd
25.9 n
Halabja
nd
98.7 a
nd
56.9 j
nd
71.5 g
nd
30.9 l
Stilbene
Qaradagh
nd
43.9 c
nd
26.9 i
nd
36.9 e
nd
nd
Ranya
nd
50.9 b
nd
31.5 g
nd
41.9 d
nd
nd
Sharbazher
nd
42.6 d
nd
24.8 j
nd
25.9 i
nd
nd
Halabja
nd
55.2 a
nd
29.8 h
nd
33.6 f
nd
nd
Gallic acid
Qaradagh
nd
nd
nd
nd
nd
nd
nd
9.7 b
Ranya
nd
nd
nd
nd
nd
nd
nd
9.2 c
Sharbazher
nd
nd
nd
nd
nd
nd
nd
8.5 d
Halabja
nd
nd
nd
nd
nd
nd
nd
10.5 a
Apigenin
Qaradagh
nd
nd
nd
nd
nd
nd
10.2 a
nd
Ranya
nd
nd
nd
nd
nd
nd
6.2 d
nd
Sharbazher
nd
nd
nd
nd
nd
nd
7.8 c
nd
Halabja
nd
nd
nd
nd
nd
nd
8.9 b
nd
* Not detected. * Different letters have significant difference between them according to Duncan test at p< 0.05

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 570 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Rutin results showed that the highest value (149.7 µg/g) was found in spring leaves
collected from Ranya, and the lowest value (11.4 µg/g) was obtained from the bark of
the same location.
Autumn leaves from all sites except Sharbazher contain high amounts of cinnamic
acid and have significant differences observed in comparison with other plant parts in
other locations. The highest value (142.6 µg/g) of cinnamic acid content appeared in
autumn leaves collected from Halabja with significant differences compared to other
treatments. Whereas, the lowest concentration was present in bark collected from
Ranya (12.8 µg/g) and gum collected from Sharbazher (12.8 µg/g).
The significant differences were observed between spring leaves collected from all
locations and have high amounts of catechin in comparison with other plant parts. The
highest value (124.5 µg/g) was recorded in spring leaves collected from Ranya
followed by Qaradagh (120.9 µg/g) while the lowest value (66.2 µg/g) was recorded
in spring rachis collected from Sharbazher.
The highest value (122.4 µg/g) of ferulic acid content was recorded for Ranya spring
leaves while the lowest (6.4 µg/g) was for the bark of the same location.
Ranya spring leaves were significantly superior in ellagic acid content (97.4 µg/g)
compared to (18.9 µg/g) in the Ranya bark.
The highest value (97.4 µg/g) of tannic acid appeared in autumn leaves collected
from Halabja with significant differences compared to other plant parts. Whereas, the
lowest value was in bark (14.7 µg/g) collected from Ranya.
Kaempferol results indicate that there were significant differences in the kaempferol
concentration in the autumn parts and gum that collected from different locations. The
highest value (98.7 µg/g) was found in autumn leaves from Halabja, followed by Ranya
and Sharbazher (91.4 µg/g and 88.9 µg/g, respectively), and the lowest value was found
in Sharbazher gum (25.9 µg/g).
Significant differences were observed between the highest level of stilbene in the
autumn leaves at Halabja (55.2 µg/g) and the lowest concentration present in autumn
fruits at Sharbazher (24.8 µg/g).
Regarding the gallic acid concentration in gum, the highest concentration of gallic
acid was found in gum collected from Halabja (10.5 µg/g) with significant differences
from Qaradagh and Ranya gum (9.7 µg/g and 9.2 µg/g, respectively), and the lowest
concentration was found in Sharbazher gum (8.5 µg/g) with significant differences
from other locations gum.
Apigenin results indicate that there were significant differences in the apigenin
content of the bark collected from different locations. The highest value (10.2 µg/g)
was found in bark from Qaradagh, followed by Halabja and Sharbazher (8.9 µg/g and
7.8 µg/g, respectively), and the lowest in Ranya (6.2 µg/g).
Discussion
Analysis of chemical profiles of different parts of Pistacia atlantica at different
locations in Kurdistan is reported for the first time. Concerning the spring and autumn
leaves, it was discovered that nitrogen, phosphorus, potassium and carbohydrate levels
were highest in the spring leaves. The environmental factors such as light, temperature,
rainfall and soil fertility have significant effects on the efficiency of photosynthesis
and chemical constituents (Muhammad et al., 2021). The leaves were fully expanded
with more efficient photosynthesis during spring, so the production of carbohydrate

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 571 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
was higher. These findings corroborate those of Hassan (2016), who discovered that
Qaradagh spring leaves contained the highest levels of carbohydrates. In addition, the
average summer temperature was high, and the plant’s respiration rate was increased.
Autumn saw a gradual decrease in the concentrations of nitrogen, phosphorus,
potassium, and carbohydrate, according to Crous et al. (2022). Also, in addition, the
chemical constituents in autumn leaves decreased. The reason for this could be age, as
photosynthetic capacity and efficiency decline with age (Bauerle et al., 2020).
It is noticed that the Qaradagh location gave the highest value for fixed oil in autumn
fruit due to perhaps the difference of environmental conditions between the locations
under study. Moreover, the Qaradagh soil contains a high proportion of organic matter
which was considered to have a significant impact on the physicochemical properties
of the soil. The main consequence was an improvement in the uptake of micro and
macroelements (Khoshnaw and Esmail, 2020). Leskovar and Othman (2018)
discovered that increasing the amount of organic matter increases porosity, which
decreases soil-specific density and allows microorganisms to penetrate more easily into
the soil environment to use organic compounds, providing plants with better access to
nutrients.
GC analysis of autumn fruit oil showed the concentrations of unsaturated fatty acids
(oleic, linoleic, and linolenic acids) were approximately four times higher than that of
saturated fatty acids (palmitic and stearic acids). These results were similar with other
researchers’ data (Saber-Tehrani et al., 2013; Dorehgirae and Pourabdollah, 2015).
Hashemi et al. (2017) also found high levels of phenolic and flavonoid compounds
in various locations in the leaves. Furthermore, the spring leaves in Qaradagh provided
the highest value for the phenolic compound. The accumulation of secondary
metabolites is strongly dependent on environmental factors such as light, temperature
and soil fertility (Yang et al., 2018). Low temperature promotes the synthesis of
phenolic compounds, whereas high temperature breaks the chemical bonds that exist
between phenolic molecules because these bonds are temperature sensitive (Jan et al.,
2021). When compared to other locations, Qaradagh soil contained the highest
percentage of nitrogen; this is also thought to be a significant cause of high nitrogen
contents in Qaradagh leaves harvested in the spring. The high nitrogen content
increases phenylalanine synthesis as a precursor of phenolic compounds, resulting in a
high phenol rate (Ibrahim et al., 2011). As a result, a positive relationship exists
between the highest percentage of nitrogen and phenolic compounds. Moreover,
Leskovar and Othman (2018) concluded that increasing organic matter in the soil
increases plant biomass, which contributes to increased phenolic and antioxidant
compound production.
Spring leaves collected from Ranya had the highest flavonoid content. Lowering
temperatures, according to Wang et al. (2015), stimulate the enzymatic activity of some
key enzymes involved in flavonoid biosynthesis, such as phenylalanine ammonia-
lyase, which preside over the first step of general phenylpropanoid biosynthesis. This
could explain why Ranya spring leaves had the highest total flavonoid content.
HPLC was used to identify eleven phenolic compounds from various parts,
including quercetin, rutin, cinnamic acid, catechin, ferulic acid, ellagic acid, tannic
acid, kaempferol, stilbene, gallic acid, and apigenin. These findings agreed with those
of Karim (2014) and Hatamnia et al. (2014).

Ahmad et al.: Analysis of chemical profiles of different Pistacia atlantica parts at Sulaymaniyah and Halabja Region in Iraq
- 572 -
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 21(1):561-574.
http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2101_561574
© 2023, ALÖKI Kft., Budapest, Hungary
Conclusion
P. atlantica’s various parts (leaves, fruits, and gum) are valuable for their medicinal,
cosmetic, and nutritional value. The findings of this study confirm that the chemical
profile of P. atlantica is affected by plant parts, and location, with autumn fruit in
Qaradagh having higher fixed oil. Autumn fruit oil contained approximately four times
more unsaturated fatty acids than saturated fatty acids. The Qaradagh spring leaves of
P. atlantica were also found to be high in phenolic compounds. As a result, more
research is needed to investigate the biological activity of phenolic compounds isolated
from P. atlantica Qaradagh spring leaves.
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DOI: http://dx.doi.org/10.15666/aeer/2101_561574
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