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Industrial Crops and Products 96 (2017) 120–125

Contents lists available at ScienceDirect

Industrial Crops and Products


journal homepage: www.elsevier.com/locate/indcrop

Phytochemical profiling of volatile components of Lavandula


angustifolia Miller propagated under in vitro conditions
Nese Kirimer a,∗ , Sam Mokhtarzadeh a , Betul Demirci a , Fatih Goger a ,
Khalid Mahmood Khawar b , Fatih Demirci a,c
a
Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University, 26140 Eskisehir, Turkey
b
Tarbiyotek-Agricultural Biotechnology Section, Department of Field Crops, Faculty of Agriculture, Ankara University, 06110 Diskapi, Altindag, Ankara,
Turkey
c
Faculty of Health Sciences, Anadolu University, 26140 Eskisehir, Turkey

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to compare the chemical composition of L. angustifolia volatiles from the field
Received 25 July 2016 crop plant versus in vitro micropropagated plantlets. The rationale of this work was to develop in vitro
Received in revised form culture methods for the fast and independent propagation of medicinal and aromatic plants in particular
17 November 2016
Lavender.
Accepted 28 November 2016
Lavandula angustifolia Miller (Lamiaceae), also known as Lavender, is widely used in herbal medicine,
cosmetic industry, and for culinary purposes. This species is highly valuated for its industrial purposes.
Keywords:
It is a fact that there is a gap in the biotechnological production of industrially valuable crops such as
Lavandula angustifolia
Plant tissue culture
Lavender. As a contemporary approach the plant tissue culture strategy of medicinal and aromatic plants
Volatiles by micropropagation serves as a useful technology to produce sufficient amounts of bioproducts e.g. plant
GC–FID material for multiple purposes.
GC–MS The plant samples were subjected both to hydro- and microdistillation for the isolation of volatiles.
The resulting subsequent volatiles were simultaneously analysed both by GC–FID and GC–MS systems.
The main compounds characterized from the hydrodistillation of micropropagated plantlets were
linalool (22.1%), lavandulyl acetate (15.3%) and linalyl acetate (14.7%). The main compounds identified
through microdistillation of this sample were linalool (14.6%), lavandulyl acetate (12.8%) and linalyl
acetate (4.7%). On the other hand the main compounds of field crop plant from hydro- and microdistilla-
tion were T-cadinol (16.9–9.3%), borneol (8.7–14.0%) and
3-carene (8.7–8.6%), respectively. As a conclusion, the obtained results suggested that volatile compo-
sition of the micropropagated samples resembles to the composition of the officinal Lavender essential
oils, which can be industrially exploited.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction whereas dry leaves are used in perfumery and cosmetic industry.
As the plant contains linalool and linalyl acetate; it is also used for
Lavender or “English Lavender” (Lavandula angustifolia Miller, the production of skin care/skin cleaning lotions, scented bathing
Syn L. vera,) of Lamiaceae is an important crop utilized to obtain soap, and foams (Baytop, 1984; Naik, 1998; Lis-Balchin, 2002 and
both the medicinal and aromatic valuable commercial essential oil. Cavanagh and Wilkinson, 2002).
The plant is found natively in South Europe, Mediterranean coun- Lavender is a perennial evergreen shrub with a lifetime of
tries of Northern Africa, France, Bulgaria, England, America and approximately 10–20 years. L. angustifolia grows up to 50 cm with
Austria. (Gonçalves and Romano, 2013 and Mokhtarzadeh, 2011). linear-lanceolate leaves grey tomentose, becoming greener with
Fresh or dried tips of L. angustifolia flowering branches are used its age. Inflorence stalk is usually unbranched 10–25 cm long with
for medicinal purposes such as the preparation of herbal drugs, a compact spike, with a lower flower cluster distant from the main
spike, blue/mauve, rarely violet pink in colour. Flowering time is
June-July, with a natural variation and a characteristic fragrance
due to its essential oil (Mill, 1982; Lis-Balchin, 2002)
∗ Corresponding author.
E-mail addresses: nkirimer@gmail.com, nkirimer@anadolu.edu.tr (N. Kirimer).

http://dx.doi.org/10.1016/j.indcrop.2016.11.061
0926-6690/© 2016 Elsevier B.V. All rights reserved.
N. Kirimer et al. / Industrial Crops and Products 96 (2017) 120–125 121

Lavender grows naturally in the Mediterranean area mostly As an initial study, the rationale of this present work was to
on rocky soils and mild coastal climates. The agricultural prac- develop biotechnological simple and sustainable in vitro culture
tices directly influence the secondary metabolites produced in methods for the fast and independent propagation of potentially
the plants, and thus the quality. Lavender is cultivated mostly in valuable medicinal and aromatic plants.
Europe. The change of volatiles over the year is essential in deter- The aim of the present work was to appraise the composition
mining the appropriate organ type and the period of harvest, which of Lavender essential oil obtained from crops grown in Turkey, and
is another topic for research. Lavadula sp. synthesize and accu- compare its profile with the volatiles obtained from micropropa-
mulate its volatiles in specialized secretory capitate and peltate gation plant tissues as a preliminary study.
oil glands located abundantly on the surface of the calyx and on
the leaves. Weather parameters such as temperature and rainfall
are known to influence essential oil content and composition of
lavender, along with fertilization (Lis-Balchin, 2002; Hassiotis et al.,
2. Materials and methods
2014).
It is a well-known fact that the commercial essential oil obtained
2.1. Plant material
from Lavandula sp. is produced mainly by steam distillation and to a
lesser extent by hydro-diffusion. Hydro- and steam distillation pro-
The flowering herba and seeds of Lavandula angustifolia Miller
cesses can be relatively time consuming, which are performed at
were provided from Prof. Dr. Neset Arslan, from the Section
high temperatures also resulting in degradation of thermally unsta-
Medicinal and Aromatic Plants, Department of Field Crops, Fac-
ble compounds. Consequently, Lavandula volatiles can be extracted
ulty of Agriculture, Ankara University, Ankara, Turkey (for different
by solvent extraction and by modern techniques such as microwave
growth stages, see Fig. 1.). The flowering herba was collected in the
and supercritical extraction methods. Nevertheless, Lavandula sol-
morning hours at 20 ◦ C in June 2013. The seeds were collected after
vent extracts may contain fats, waxes, pigments, artefacts and
the flowering period.
solvent residues along with volatile compounds. Considering the
pros and cons of the extraction methods, new supercritical CO2
extracts are penetrating more and more the markets due to special
natural product requests, which cannot be classified as “essential
oils” by definition (Danh et al., 2013; Lis-Balchin, 2002; Baser and 2.2. Lavandula angustifolia micropropagation
Buchbauer, 2009).
Among others, the quality of Lavandula essential oils are The culture conditions for the surface sterilization for 50 seeds
regulated by ISO standards (The International Organization for of lavender of field cultivated plant material were determined.
Standardization). Also various international standards such as The lavender seeds were surface sterilized with 5% commercial
European Pharmacopoeia (PhEur) contain monographs on various bleach (5% NaOCl) for 5 min followed by 3 × 5 min rinsing with
Lavandula sp. preparations securing pharmaceutical grade quality bi-distilled sterilized water. The seeds were germinated on soil
(Council of Europe, 2014). and MS (Murashige and Skoog, 1962) medium supplemented with
According to previous information and applications it is pos- 30 g/L sucrose 0.65% agar (Sigma type A). The pH of all culture
sible to increase the generation of bioproducts, active ingredients media was adjusted to 5.7 ± 0.1 before autoclaving at 120 ◦ C for
and secondary metabolites such as volatile constituents of plants 20 min. About 35 mL of autoclaved medium was poured into each
using plant tissue culture techniques (Alfermann and Petersen, of the petri dish or culture vessels. All cultures were incubated
1995; Dornenburg and Knorr, 1996; Ravishankar et al., 1999; at 24 ± 1 ◦ C under 16 h light photoperiod provided by cool white,
Ramachandra and Ravishankar, 2002 and Zuzarte et al., 2010). Also fluorescent light (4000 Lux). The cotyledon node explants were
it is known that tissue culture techniques have been applied to taken from 30 to 45 days old seedlings. Cotyledon nodes of ger-
several Lavandula species (Zuzarte et al., 2010 and references cited minating seeds were used as explants that were cultured on MS
herein). Micropropagation of rapid multiplying selected Lavandula medium containing 2 mg/L BAP (6-benzylaminopurine) for eight
sp. genotypes is a modern technique for the modern agricultural weeks. Well-developed micropropagated shoots were rooted on
practices (Echeverrigaray et al., 2005; Machado et al., 2013). Out of MS medium containing the 1.25 mg/L IBA (indole-3-butyric acid).
approximately billion US-Dollars annual world essential oil trade, Thereafter, the rooted plants were transferred to peat moss con-
50 million US-Dollars trade consists of lavender essential oil. Turk- tained in black colored polythene tubes at room temperature. The
ish lavender oil needs are increasing with the passage of time peat moss was previously sterilized at 160 ◦ C for 2 h. Microprop-
and increasing population (Lis-Balchin, 2002; Baser and Buchbauer, agated plants were acclimatized under field conditions as seen in
2009). Figs. 2 and 3 (Mokhtarzadeh, 2011).

Fig. 1. L. angustifolia from field conditions in different growth stages.


122 N. Kirimer et al. / Industrial Crops and Products 96 (2017) 120–125

Fig. 2. Micropropagation in cotyledon node explant.


a,b. MS medium with 2.00 mg/L BAP for shoot regeneration on cotyledon node explants of L. angustifolia.
(bar a, b ≈ 1.66 cm).

Fig. 3. The effect of IBA concentrations in rooting for shoots. a,b. MS medium with 1.25 mg/L IBA (bar a, b ≈ 1.5 cm).

2.3. Essential oil extraction ational conditions. Relative percentage amounts of the separated
compounds were calculated from FID chromatograms.
2.3.1. Hydrodistillation
Air-dried flowering herba of field cultivated and micropropa-
gated plants were subjected to hydrodistillation for 3 h using a 2.4.2. Gas chromatography −mass spectrometry analysis
Clevenger-type apparatus, according the PhEur 8.0 with modifica- The GC–MS analyses were carried out using an Agilent 5975
tions (Council of Europe, 2014). GC–MSD system. Innowax FSC column (60 m x 0.25 mm, 0.25 mm
film thickness) was used with helium as carrier gas (0.8 mL/min).
GC oven temperature was kept at 60 ◦ C for 10 min and programmed
2.3.2. Microdistillation
to 220 ◦ C at a rate of 4 ◦ C/min that was kept constant at 220 ◦ C for
The volatiles were obtained after microdistillation of the dried
10 min and followed by elevating the temperature to 240 ◦ C at a
lavender flowers (400–750 mg) using an Eppendorf MicroDistiller
rate of 1 ◦ C/min. Split ratio was adjusted at 40:1. The injector tem-
(Germany) system. Using the distillation program, the sample vial
perature was set at 250 ◦ C. Mass spectra were recorded at 70 eV,
was heated to 108 ◦ C at a rate of 20 ◦ C/min for 90 min followed
where the mass range was m/z 35–450.
by heating at 112 ◦ C at the rate of 20 ◦ C/min for 30 min (for more
detail, see Tabanca et al., 2010). Thereafter, the organic layer in
the collection vial was separated and analysed by gas chromatog- 2.5. Identification of components
raphy (GC) and gas chromatography-mass spectrometry (GC–MS)
simultaneously. Identification of the essential oil components were carried out
by comparison of their relative retention times with those of
2.4. Analysis conditions authentic samples or by comparison of their relative retention
index (RRI) to series of n-alkanes. Computer matching against com-
2.4.1. Gas chromatography analysis mercial (Wiley GC–MS Library, MassFinder 3 Library) (McLafferty
The GC-FID analyses were carried out using an Agilent 6890N and Stauffer, 1989 and Koenig et al., 2004) and in-house “Başer
GC system using FID detector temperature of 300 ◦ C. To obtain Library of Essential Oil Constituents” built up by genuine com-
the same elution order with GC–MS, simultaneous auto-injection pounds and components of known oils. Additionally, MS literature
was done on a duplicate of the same column at the same oper- data (Joulain and Koenig, 1998) was also used for the identification.
N. Kirimer et al. / Industrial Crops and Products 96 (2017) 120–125 123

Table 1
Chemical composition of Lavandula angustifolia volatiles.

No. RRI Compound HD1 % MD1 % HD2 % MD2 % Identification method

1 1014 Tricyclene 0.2 0.3 – – MS


2 1032 ˛-Pinene 4 5.5 – – tR , MS
3 1035 ˛-Thujene 0.8 1 – – MS
4 1072 ␣-Fenchene 0.1 0.2 – – tR , MS
5 1076 Camphene 3.3 4.5 – 2.1 tR , MS
6 1118 ˇ-Pinene 5 6.3 – 0.4 tR , MS
7 1132 Sabinene 0.9 1.1 – – tR , MS
8 1159 ı-3-Carene 8.7 8.6 – – MS
9 1174 Myrcene 1.3 1.1 0.8 0.6 tR , MS
10 1176 ˛-Phellandrene 0.8 1.3 – – tR , MS
11 1187 o-Cymene 0.2 0.2 – – MS
12 1188 ˛-Terpinene 0.2 0.2 – – tR , MS
13 1203 Limonene 4 3.7 0.4 2.6 tR , MS
14 1213 1,8-Cineole 5.9 5.8 – 3.1 tR , MS
15 1246 (Z)-ˇ-Ocimene 0.1 0.1 3.5 1.1 MS
16 1255 -Terpinene 0.3 0.3 – – tR , MS
17 1265 3-Octanone – – 1.2 0.6 tR , MS
18 1266 (E)-ˇ-Ocimene 0.5 0.5 10.4 3.9 MS
19 1278 m-Cymene 1 1.1 – – MS
20 1280 p-Cymene 2.3 2.5 0.2 1.6 tR , MS
21 1282 Hexyl acetate – – 0.8 0.4 tR , MS
22 1286 Isoterpinolene 0.6 0.5 – – MS
23 1290 Terpinolene 0.3 0.2 – – tR , MS
24 1345 3-Octyl acetate – – 0.3 – tR , MS
25 1429 Perillene 0.1 tr – – MS
26 1450 trans-Linalool oxide (Furanoid) – – – 0.6 MS
27 1452 1-Octen-3-ol 0.2 0.2 – – tR , MS
28 1458 cis-1,2-Limonene epoxide 0.1 0.1 – – MS
29 1474 trans-Sabinene hydrate 0.2 0.2 – – MS
30 1478 cis-Linalool oxide (Furanoid) – – – 0.4 MS
31 1483 1-Octyl acetate – – 1.6 – tR , MS
32 1532 Camphor 1.3 2.3 – 1.5 tR , MS
33 1553 Linalool 0.3 0.3 22.1 14.6 tR , MS
34 1556 cis-Sabinene hydrate 0.1 tr – – MS
35 1565 Linalyl acetate – – 14.7 4.7 tR , MS
36 1583 ˛-Santalene 1.4 1.3 – – MS
37 1588 Bornyl formate 0.6 0.6 – 0.5 MS
38 1591 Bornyl acetate 0.5 0.9 – 0.7 tR , MS
39 1611 Terpinen-4-ol 0.6 0.5 – – tR , MS
40 1612 ˇ-Caryophyllene 2.9 2.4 5.1 1.2 tR , MS
41 1617 Lavandulyl acetate 1 1.3 15.3 12.8 tR , MS
42 1639 Cadina-3,5-diene 0.6 0.4 – – MS
43 1668 (Z)-ˇ-Farnesene – – 1.4 – MS
44 1670 trans-Pinocarveol 0.4 0.6 – – tR , MS
45 1686 Lavandulol 0.4 0.6 1.6 1.5 tR , MS
46 1690 Cryptone 0.5 1 – 3.9 MS
47 1704 -Muurolene 5.9 4 – – MS
48 1706 ˛-Terpineol 0.1 0.2 2.1 1.9 tR , MS
49 1719 Borneol 8.7 14 0.8 7.4 tR , MS
50 1722 Bicyclosesquiphellandrene 0.3 0.4 – – MS
51 1733 Neryl acetate – – 0.8 1 tR , MS
52 1751 Carvone 0.2 0.2 – 0.9 tR , MS
53 1765 Geranyl acetate – – 1.6 1.4 tR , MS
54 1776 -Cadinene – – 1.7 2.3 MS
55 1776 Cumin aldehyde 0.5 0.3 – 1.9 tR , MS
56 1808 Nerol – – 0.4 – tR , MS
57 1845 trans-Carveol 0.1 0.4 – – tR , MS
58 1849 Calamenene 0.4 0.4 – – MS
59 1856 m-Cymen-8-ol 0.3 1.3 – – MS
60 1857 Geraniol – – 1.4 1.7 tR , MS
61 1864 p-Cymen-8-ol 0.2 0.8 – 0.7 tR , MS
62 2001 Isocaryophyllene oxide 0.4 0.4 – – MS
63 2008 Caryophyllene oxide 4.3 3.8 0.5 3.4 tR , MS
64 2071 Humulene epoxide-II 0.1 0.1 – – MS
65 2080 Cubenol 1.3 0.8 0.6 1 MS
66 2113 Cumin alcohol 0.1 0.2 – 0.7 tR , MS
67 2131 Hexahydrofarnesyl acetate – – – 0.5 MS
68 2187 T-Cadinol 16.9 9.3 9.6 11.1 MS
69 2232 ˛-Bisabolol 0.4 tr – – tR , MS
70 2349 Cadina-4,10(15)-dien-3-one 0.8 0.4 – – MS
Monoterpene Hydrocarbons 40.5 45 15.3 15.4
Oxygenated Monoterpenes 15.7 24.8 60.8 54.9
Sesquiterpene Hydrocarbons 11.5 8.9 8.2 3.5
Oxygenated Sesquiterpenes 24.2 14.8 10.7 15.5
Others 0.8 1.2 3.9 5.4
Total 92.7 94.7 98.9 94.7

HD1: Hydrodistillation of field cultivar, HD2: Hydrodistillation of micropropagated plants, MD1: Microdistillation of field cultivar, MD2: Microdistillation of micropropagated
plants, RRI: Relative retention indices calculated against n-alkanes, %: Calculated from FID data, tr: Trace (<0.1%). Identification method: tR , identification based on the retention
times (tR ) of genuine compounds on the HP Innowax column; MS: Identified on the basis of computer matching of the mass spectra with those of the Wiley and MassFinder
libraries and comparison with current literature data.
124 N. Kirimer et al. / Industrial Crops and Products 96 (2017) 120–125

Fig. 4. Comparative terpene composition of hydrodistilation (HD1, HD2) and microdistilation (MD1, MD2).

The identified compounds were listed in Table 1. See Fig. 4 for the However, L. angustifolia samples showed qualitative differences in
distribution of the main components. the composition of their volatiles. These results are highlighted and
illustrated in Fig. 4, comparatively.
3. Results This report is the first investigation and comparison of L.
angustifolia field cultivated and biotechnologically micropropa-
The yield of the flowering herba and micropropagated plants gated sample and the phytochemical profiling of their volatiles by
showed 0.7% and 2.6% essential oil, which was calculated on a hyrdro- and microdistillation methods, respectively. To the best of
dry weight base, respectively, suggesting further feasibility stud- our knowledge this is the first report on the comparative production
ies. The GC-FID analysis showing the relative percentages (%) of and distillation methods of lavender grown in Turkey.
the separated compounds as calculated from FID chromatograms
are listed in Table 1. GC and GC–MS analyses of the hydrodis- 4. Discussion
tilled and microdistilled essential oil of micropropagated plants
were identified as 25 and 35 compounds representing 98.9% According to previous work on L. angustifolia from Xinjiang,
and 94.7% of the obtained essential oils, respectively. The main China, 17 compounds were identified in the hydrodistilled oil
compounds obtained by hydrodistillation were linalool (22.1%), with linalool (44.5%), geraniol (11%), lavandulyl acetate (10.8%),
lavandulyl acetate (15.3%), linalyl acetate (14.7%), (E)-␤-ocimene 3,7-dimethyl-2,6-octadien-1-ol (10.4%), and isoterpineol (6.8%)
(10.4%), T-cadinol (9.6%), ␤-caryophyllene (5.1%), (Z)-␤-ocimene as the main components (Cong et al., 2008). Three major con-
(3.5%), ␣-terpineol (2.1%), and ␥-cadinene (1.7%). Microdistil- stituents of the leaf oil of the cultivated lavender from Iran were
lation results showed presence of 35 compounds. The main identified as 1,8-cineole (65.4%), borneol (11.5%) and camphor
compounds obtained characterized from the microdistillation were (9.5%) (Hajhashemi et al., 2003). Whereas, linalool (35.3%), linalyl
linalool (14.6%), lavandulyl acetate (12.8%), T-cadinol (11.1%), bor- acetate (13.4%) and lavandulyl acetate (10.9%) were main com-
neol (7.4%), linalyl acetate (4.7%), (E)-␤-ocimene (3.9%), cryptone ponents of lavender from Iran (Fakhari et al., 2005). The Brazil
(3.9%), caryophyllene oxide (3.4%), and 1,8-cineole (3.1%). When lavender oil main components were reported as borneol (22.4%),
the relative percentage amounts of compounds were compared, epi-␣-muurolol (13.4%), ␣-prococene I (13%) and 1,8-cineole by
hydrodistillation showed the maximum percentage of linalool Mantovani et al., 2013. Verma et al. (2010) observed linalyl acetate
with 22.1%, whereas the linalool percentage using the microdis- (47.6%), linalool (28.1%), lavandulyl acetate (4.3%) and ␣-terpineol
tillation method was 14.6% only. Next higher percentage was (3.8%) of lavender cultivated in India. In the lavender essential
determined for lavandulyl acetate with 15.3%, which was 12.8% oil from Trieste-Italy, linalyl acetate (43.1%), linalool (32.7%), and
using the microdistillation method. Same trend was evident in caryophyllene (4.9%) were reported as main compounds (Evandri
the third major compound, namely linalyl acetate (14.7%), which et al., 2005). In another lavender example from Italy, linalool
was reduced to 4.7% using the microdistillation process. Moreover, (35.9–36.5%) and linalyl acetate (21.7–14.4%) were reported as
decrease in the percentage of compounds was not parallel except main compounds (Da Porto et al., 2009).
for linalool and lavandulyl acetate. Zuzarte et al. (2010) suggested that in vitro cultures are helpful
On the other hand, GC and GC–MS analyses of the hydrodistilled in assuring the quality of the essential oils, and such protocols can
and microdistilled samples of field cultivated plant a total number be applied to the propagation of selected chemotypes for further
of 57 compounds were identified representing 92.7% and 94.7% of industrial purposes. There were some recent reports on the chem-
the volatiles, respectively. The main compounds of cultivated field ical composition and quality of micropropagated lavenders from
plant from hydrodistillation and microdistillation samples were various groups. Main volatile components of the micropropagated
identified as T-cadinol (16.9 and 9.3%), borneol (8.7 and 14%), ␦-3- lavender plants from Italy were identified as caryophyllene (19.3%)
carene (8.7 and 8.6%), ␤-pinene (5.0 and 6.3%), 1,8-cineole (5.9 and and 1,8-cineole (11.9%) as reported recently by Pistelli et al. (2013).
5.8%) and ␥-muurolene (5.9 and 4%), respectively. Both distillation The results of this present study are in accordance with the
methods on the field plant resulted in comparable compositions. recent work of Machado et al. (2013), who reported that microprop-
N. Kirimer et al. / Industrial Crops and Products 96 (2017) 120–125 125

agated lavender (L. angustifolia) contained 4% essential oil during Dornenburg, H., Knorr, D., 1996. Production of the phenolic flavour compounds
first and around 5% during second harvest from Southern Brazil. The with cultured cells and tissue of Vanilla planifolia species. Food Biotechnol. 10,
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and 37.3%) and linalyl acetate (10.1 and 12.2%), respectively. dentata from axillary buds of field-grown adult plants. Biol. Plant. 49, 439–442.
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The antimutagenic activity of Lavandula angustifolia (lavender) essential oil in
study were relatively low in linalool content, as it would be the bacterial reverse mutation assay. Food Chem. Toxicol. 43, 1381–1387.
expected in higher percentages in regard to the pharmaceutical Fakhari, A.R., Salehi, P., Heydari, R., Ebrahimi, S.N., Haddad, P.R., 2005.
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analysis of the essential oil components of Lavandula angustifolia Mill. J.
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Chromatogr. A 1098, 14–18.
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Environmental and developmental factors affect essential oil production and
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