This article was downloaded by: [Heriot-Watt University]

On: 07 March 2015, At: 09:51

Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered
office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Natural Product Research: Formerly

Natural Product Letters
Publication details, including instructions for authors and
subscription information:
http://www.tandfonline.com/loi/gnpl20

Chemotypes of essential oil of unripe

Click for updates
galls of Pistacia atlantica Desf. from
Algeria
a a b
Ibrahim Sifi , Nadhir Gourine , Emile M. Gaydou & Mohamed
a
Yousfi
a
Laboratoire des Sciences Fondamentales à l'Université Amar
TÉLIDJI de Laghouat, Route de Ghardaïa BP37G (03000),
Laghouat, Algérie
b
Laboratoire de Recherche en Systèmes Chimiques Complexes,
Faculté des Sciences et Technique de Saint-Jérôme, Université
Paul Cézanne, Marseille, France
Published online: 24 Feb 2015.

To cite this article: Ibrahim Sifi, Nadhir Gourine, Emile M. Gaydou & Mohamed Yousfi (2015):
Chemotypes of essential oil of unripe galls of Pistacia atlantica Desf. from Algeria, Natural Product
Research: Formerly Natural Product Letters, DOI: 10.1080/14786419.2015.1012164

To link to this article: http://dx.doi.org/10.1080/14786419.2015.1012164

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the
“Content”) contained in the publications on our platform. However, Taylor & Francis,
our agents, and our licensors make no representations or warranties whatsoever as to
the accuracy, completeness, or suitability for any purpose of the Content. Any opinions
and views expressed in this publication are the opinions and views of the authors,
and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content
should not be relied upon and should be independently verified with primary sources
of information. Taylor and Francis shall not be liable for any losses, actions, claims,
proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or
howsoever caused arising directly or indirectly in connection with, in relation to or arising
out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any
substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,
systematic supply, or distribution in any form to anyone is expressly forbidden. Terms &
 Conditions of access and use can be found at http://www.tandfonline.com/page/terms-
and-conditions
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015
 Natural Product Research, 2015
http://dx.doi.org/10.1080/14786419.2015.1012164

SHORT COMMUNICATION
Chemotypes of essential oil of unripe galls of Pistacia atlantica Desf. from
Algeria
Ibrahim Sifia, Nadhir Gourinea*, Emile M. Gaydoub and Mohamed Yousfia
a
Laboratoire des Sciences Fondamentales à l’Université Amar TÉLIDJI de Laghouat, Route de Ghardaı̈a
BP37G (03000), Laghouat, Algérie; bLaboratoire de Recherche en Systèmes Chimiques Complexes,
Faculté des Sciences et Technique de Saint-Jérôme, Université Paul Cézanne, Marseille, France
(Received 20 October 2014; final version received 19 January 2015)
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015

The essential oils (EOs) of unripe galls (from male and female plants) of a total number
of 52 samples of Pistacia atlantica collected from different regions in Algeria were
analysed by GC/MS and GC. The yields of the extraction of the EO by hydrodistillation
vary from low to high values (0.08– 1.89% v/w). The results of both methods of
principal component analysis and hierarchical ascendant classification revealed the
presence of two different chemotypes: a-pinene chemotype and a-pinene/sabinene/
terpinen-4-ol chemotype.
Keywords: Pistacia atlantica; unripe galls; essential oil; chemotypes

1. Introduction
The genus Pistacia (Anacardiaceae) is widely distributed in the Mediterranean area. Pistacia
atlantica Desf. is a tree located in north Africa, which can reach 25 m in height and grows in arid
and semi-arid areas (Barrero et al. 2005). In Algeria, the galls of P. atlantica are used as an
embalming agent by rural inhabitants. They are also known in Arabic as ‘Afse’ and are edible
and sold in markets.
Only few studies on the chemical composition of the essential oils (EOs) of the galls parts of
P. atlantica were reported (Mecherara-Idjeri et al. 2008; Gourine et al. 2011; Bozorgi et al.
2013; Rowshan et al. 2013). Considering the fact that the smell, the colour and the yields of the
EOs of the unripe galls found in our investigation are quite different from those of mature galls,
the aim of this work is to study the chemical composition of these EOs at a large scale (different
regions, male and female trees) and to investigate the possible occurrence of different
chemotypes within these EOs.

*Corresponding author. Email: n.gourine@mail.lagh-univ.dz, gourine.nadir@gmail.com

q 2015 Taylor & Francis

 2 I. Sifi et al.

2. Results and discussion

Freshly collected unripe galls were characterised by white colour tending to a little brownish
one. The EOs of the unripe galls were obtained at different yield values (exhibiting low and high
values) ranging from 0.08 up to 1.98% (v/w). Although the lowest yields are pretty similar for
both ripe and unripe galls EOs, there is a major difference regarding the upper yields. Indeed, in
mature galls the upper yield range of variation did not exceed 0.15% (Supplementary Tables 1S
and 2S). The EOs of unripe galls were obtained as transparent (colourless) and with a light good
smell. Unlike unripe galls, the EOs of mature galls are characterised by yellow to dark brownish
colours, and their smells are very strong and very characteristic.
The composition of EOs of a total number of 52 samples (male and female trees from different
regions) of unripe galls of P. atlantica was analysed by GC and GC – MS. Quantitative and
qualitative differences were found between the studied EO samples. Twenty-seven compounds of
the EOs were identified. The contents of the monoterpenes in the EO samples were in the range of
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015

22.9 –97.7% with a clear dominance of monoterpenes hydrocarbons (19.3 – 95.1%). The main
components of the EOs identified were not evenly distributed in all samples. In fact some major
components in some samples were minor components in other samples: sabinene (tr –28.0%),
myrcene (0.5 – 20.4%), p-cymene (0.4 – 11.4%), terpinen-4-ol (0.2 – 20.9%) a-pinene
(12.5 – 81.5%) and b-pinene (2.3 –18.0%).
This variability of the content of the main compounds supposes the existence of different
chemotypes within the same plant. Taking into account this last consideration, this study
involves the use of multivariate statistical analysis (principal component analysis [PCA] and
hierarchical ascendant classification [HAC]) which aims to determine the possible occurrence of
different chemotypes in the EO of unripe galls of P. atlantica.
The results of PCA (Figure 1 , Supplementary Figure 1S) show the appearance of two
distinguished clusters ‘clouds’ of EO samples. Similar to the PCA method, the result of HAC
revealed the same results ‘clusters I and II’ (Figure 2). The distance measuring the dissimilarity
was very important between the two identified clusters, which means that the two chemotypes
could be easily distinguished. Group (I) is referred to the first chemotype a-pinene, while group
(II) is referred to the second chemotype sabinene/terpinen-4-ol. Moreover, the result of both
PCA and HAC showed that the identified chemotypes were not related to the region of
collection, or to the type of the tree (male and female).
Chemotype I (a-pinene chemotype) is characterised by the highest percentage of a-pinene
which had reached a maximum value of 81.5% and with range of composition values of
(mean ^ SD) 55.2 ^ 15.7% (see Supplementary Table 1S and Figure 2S). On the other hand,
the percentages of both sabinene and terpinen-4-ol for this chemotype were low and they were
less than 1.9% and 3.8%, respectively. In contrast to the first chemotype, the second chemotype
(a-pinene/sabinene/terpinen-4-ol chemotype) is characterised by the highest content of both
sabinene and terpinen-4-ol compounds, and relatively lower content of a-pinene. In fact, the
content range of sabinene varies between 8.1% and 28.0%, and that for terpinen-4-ol is in the
range of 8.7 –20.9%, but for a-pinene the variation interval was 14.2 –32.8%. For this
chemotype, the content range of a-pinene is less important than previously recorded in the
first chemotype; still, the percentage of a-pinene was very important (mean value ¼ 23.2%).
So, a-pinene is considered the main compound for both chemotypes, and sabinene and terpinen-
4-ol were considered the main compounds in the second chemotype only. It is important to
notice that the content of some compounds varies from low to high percentages; this is the case
of b-pinene 2.3 – 18.0% and myrcene 0.5– 20.4%. As a general consideration, it was observed
that despite using the main compounds in the differentiation between the two chemotypes, all the
remaining components have practically no effect on chemotype differentiations. After the
examination of the repartition of the two separated chemoptypes using PCA and HAC, it was
 Natural Product Research 3

Samples after rotation Varimax (axes F1 et F2 : 52,76 %)

4

3 A02F

Chemotype II
2 A05F
(α-Pinene/Sabinene/Terpinen-4-ol)
A03F
-- axis F2 (18.84 %) -->

LK1M A19F
A21F
1
LT1M A03M A14F
A12M LT2F A15F
A13F A08F
A04M A23F
A10F A02M A01M A07F A18F A08M
A04F LT1F A26F A12F
0 A17F A09M
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015

A22F A25F A09F LT??

A06M A20F
A07M L1M
A16F A24F
A13M A10M
A11M LK1F
LK2F A01F
–1 L1F A27F
LK2M A11F
LK3F

LK3M LK4F

–2

Chemotype I
–3
A05M
(α-Pinene)

–4
–2 –1.5 –1 –0.5 0 0.5 1 1.5 2
-- axis F1 (33.92 %) -->
A: Region of Aïn-Oussera, L: Region of Laghouat, K: Location of Kheneg, T: Location of Tihlghemt,
M: male tree, F: female tree.

Figure 1. Two dimensional plot on axes F1 and F2 of the EO samples of P. atlantica from Algeria using PCA.

noted that the studied samples are almost evenly divided between the two chemotypes identified:
a-pinene chemotype represents 59.6% of the total tested individuals and a-pinene/sabinene/
terpinen-4-ol chemotype represents a value of 40.4%, which is practically very close to the first
chemotype.
The chemical compositions of the EOs of unripe galls of P. atlantica were compared to those
of mature galls. It was noted that the percentage values of the main compounds in the EOs of
mature galls were very close to those of the a-pinene chemotype, with the exception of the
contents of terpinen-4-ol which were relatively very high and similar to ‘a-pinene/sabinene/
terpinen-4-ol chemotype’ (Tables 1S and 2S).
Comparison between the compositions of P. atlantica galls EOs from Algeria with those
reported in the literature (Mecherara-Idjeri et al. 2008; Gourine et al. 2011) reveals the existence
of both significant similarities and differences for the main component percentages. In fact, this
study confirms the presence of a-pinene and a-pinene/b-pinene chemotypes found in the
previous reports (Mecherara-Idjeri et al. 2008; Gourine et al. 2011), but the new chemotype (a-
pinene/sabinene/terpinen-4-ol) found in our investigation was not yet reported; this could be due
to the fact that previous reports were not involved in large scale investigations. Finally, we also
remind that in our recent report (Gourine et al. 2011), we have identified a new chemotype which
 4 I. Sifi et al.

294

Dendrogram
245

196
Dissimilarity

147
(I) (II)

98
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015

49

0
A02F
A04M
A03M
A04F
A03F
LK1M
A02M
LT1F
A12M
A05F
A21F
LT1M
A13M
A22F
A25F
A16F
A13F
A10F
A11M
A06M
LK3M
A05M
A07M
A24F
A01F
A11F
LK4F
LK3F
LK2F
LK2M
L1F
A09M
A08M
A23F
LK1F
A27F
A26F
A20F
A10M
A09F
A12F
A08F
A17F
A15F
A07F
A18F
A19F
A14F
A01M
LT2F
LT
L1M
A: Region of Aïn-Oussera, L: Region of Laghouat, K: Location of Kheneg, T: Location of Tihlghemt,
M: male tree, F: female tree.

Figure 2. Dendrogram obtained from the cluster analysis of 52 EO samples of P. atlantica from different
regions in Algeria. Samples are clustered using Ward’s technique with an Euclidean distance measure.

was characterised by the presence of a unique major compound (d-3-carene: 75.3%); and since
this chemotype was very rare, it did not appear in the studied samples of this study.

3. Conclusion
The multivariate statistical analysis (PCA and HAC methods) used in this investigation that
involved the study of a large number of EO samples of unriipe galls of P. atlantica collected from
different regions has revealed the existence of a second chemotype (a-pinene/sabinene/terpinen-
4-ol), not yet reported previously. This new chemotype is characterised by higher contents of
sabinene and terpinen-4-ol. On the other hand, it was found that the yields of the EOs of unripe
galls (up to 1.89% v/w) are effectively more important (i.e. more interesting) than those reported
for ripe galls. On the contrary for the reported characteristics of ripe galls, the EOs of unripe galls
were transparent (colourless) and had a light good smell. In the same context, let us remind that
these characteristics are those two sought for food additives (natural antioxidants and
conservators) and also for antibacterial treatment as a medicine. Finally, the appearance of
different chemotypes should have certainly some effect on the biological activities of these EOs;
hence, future studies involving the determination of their activities should take into consideration
those two chemotypes.

Supplementary material
Experimental details relating to this article are available online.

References
Barrero A, Herrador M, Arteaga J, Akssira M, Mellouki F, Belgarrabe A, Blázquez M. 2005. Chemical composition of
the essential oils of Pistacia atlantica Desf. J Essent Oil Res. 17:52–54. doi:10.1080/10412905.2005.9698828.
 Natural Product Research 5

Bozorgi M, Memariani Z, Mobli M, Salehi Surmaghi MH, Shams-Ardekani MR, Rahimi R. 2013. Five Pistacia species
(P. vera, P. atlantica, P. terebinthus, P. khinjuk, and P. lentiscus): a review of their traditional uses,
phytochemistry, and pharmacology. Sci World J. 2013:1–33. doi:10.1155/2013/219815.
Gourine N, Sifi I, Gaydou EM, Yousfi M. 2011. Chemical composition of the essential oil of unripe galls of Pistacia
atlantica Desf. from Algeria. Nat Prod J. 1:125– 127.
Mecherara-Idjeri S, Hassani A, Castola V, Casanova J. 2008. Composition of leaf, fruit and gall essential oils of Algerian
Pistacia atlantica Desf. J Essent Oil Res. 20:215–219. doi:10.1080/10412905.2008.9699995.
Rowshan V, Bahmanzadegan A, Tarakemeh A. 2013. Volatile compounds of pistacia atlantica Desf. galls and leaves by
Combi-PAL system technique. Tech J Eng Appl Sci. 3:796–798.
Downloaded by [Heriot-Watt University] at 09:51 07 March 2015