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Industrial Crops and Products 69 (2015) 329–334

Contents lists available at ScienceDirect

Industrial Crops and Products


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

Comparison of essential oil composition and phenolic acid content of


selected Salvia species measured by GC–MS and HPLC methods
Bo Li a , Chenlu Zhang b , Liang Peng a,c , Zongsuo Liang a,d,∗ , Xijun Yan e ,
Yonghong Zhu e , Yan Liu f
a
College of Life Sciences, Northwest A&F University, Yangling 712100, PR China
b
College of Biological Science & Engineering, Shaanxi University of Technology, Hanzhong 723001, PR China
c
College of Pharmacy, Shaanxi University of Chinese Medicine, Xi’an 712046, PR China
d
College of Life Sciences, Zhejiang Sci-Tech University, Hangzhou 310018, PR China
e
Tianjin Tasly Holding Group Co., Ltd., Tianjin 300410, PR China
f
Tianjin Tasly Modern Traditional Chinese Medicine Resources Co., Ltd., Tianjin 300402, PR China

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

Article history: Salvia is an important genus containing nearly 1000 species of the Labiatae family; most species of Salvia
Received 5 September 2014 are traditional herbal medicines and industrial materials with various active components. Salvia is also
Received in revised form 12 February 2015 evidently rich in essential oils and phenolic acids. This study aimed to investigate the chemical compo-
Accepted 21 February 2015
sition of the essential oils and the content of phenolic acids in four Salvia species cultivated in Yangling,
PR China. The essential oils from the fresh leaves and flowers of Salvia miltiorrhiza, Salvia przewalskii,
Keywords:
Salvia officinalis, and Salvia deserta were obtained by simultaneous distillation extraction and evaluated
Salvia miltiorrhiza
by GC–MS; the phenolic acids were analyzed by HPLC. Essential oil derived from S. deserta flowers con-
Salvia przewalskii
Salvia officinalis
tained at most 72 compounds, while 11 compounds were common to all Salvia oils. Aromadendrene
Salvia deserta oxide-(1) (8.3%) and ␤-caryophyllene (11.05%) were the major constituents in essential oils from S. mil-
Essential oils tiorrhiza leaves and flowers, respectively. The limonene content in leaf oil markedly differed from that of
GC–MS flower oil from S. przewalskii; thujone was the predominant component in both the leaf and flower oils
Phenolic acids of S. officinalis. Moreover, ␤-phellandrene (29.74%) was the most abundant compound in the essential
HPLC oil of S. deserta flowers. Composition of essential oils from these Salvia species showed strong tissue and
organ specificity. Furthermore, the contents of ferulic acid, caffeic acid and rosmarinic acid in the aerial
parts of these species were also investigated. The leaves of S. przewalskii and flowers of S. officinalis were
rich in rosmarinic acid, with contents of 64.1 ± 3.9 and 53.4 ± 2.9 mg/g dry weight, respectively. Thus, S.
przewalskii leaves could be considered a good source of rosmarinic acid.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction Salvia miltiorrhiza, commonly called “Danshen”, is a traditional


Chinese medicine that has been used to treat cardiovascular and
The genus Salvia, which includes over 900 morphological cerebrovascular diseases since ancient times (Cheng, 2007). Salvia
species, is one of the largest members of the Labiatae family. It przewalskii, instead of S. miltiorrhiza, is an endemic medicinal plant
is widely distributed from the coastal region of the Mediterranean used in western China. The levels of tanshinone IIA, the main effec-
to Asia (Rajabi et al., 2014). Approximately 84 species of Salvia are tive component in S. przewalskii roots, are significantly higher in
distributed throughout China, mostly in the southwestern regions, this species than in “Danshen” plants (Skala and Wysokinska, 2005).
such as Sichuan, Yunnan, and Tibet (Wu and Raven, 1994). Many Other closely related species, such as Salvia officinalis and Salvia
sages are important aromatic and commercial species; they have deserta, are also used as indigenous herbal medicines and indus-
long been used as folk medicines and contain many active com- trial materials throughout the world (Capek and Hribalova, 2004;
pounds (Rzepa et al., 2009; Walch et al., 2011). The dry root of Tezuka et al., 1998).
The flowers and leaves of different Salvia species are an abun-
dant source of essential oils, which originate from a series of plant
secondary metabolism processes. Essential oils are responsible for
∗ Corresponding author. Tel.: +86 29 87092262; fax: +86 29 87092262. the characteristic aroma and flavor of these plants; thus, they
E-mail address: liangzs@ms.iswc.ac.cn (Z. Liang).

http://dx.doi.org/10.1016/j.indcrop.2015.02.047
0926-6690/© 2015 Elsevier B.V. All rights reserved.
330 B. Li et al. / Industrial Crops and Products 69 (2015) 329–334

Table 1 with a unique scent was obtained; the oils were stored in sealed
Salvia species collected from different regions of China.
tubes and protected from light with silver paper at 4 ◦ C prior to
Species Subgenus Location Altitude (m) Accession GC–MS analysis.
S. miltiorrhiza Subg. Sclarea Shandong 200 SM001 The remaining Salvia leaves and flowers were dried in an oven at
S. przewalskii Subg. Salvia Tibet 3890 SP008 a constant temperature of 45 ◦ C for 72 h. Subsequently, the samples
S. officinalis Subg. Salvia Sichuan 500 SO015 were comminuted into a powder with a mortar, sieved through a
S. deserta Subg. Sclarea Shaanxi 560 SD012 0.45 mm mesh screen, and then prepared for the phenolic acids
analyses by HPLC.

are extensively applied in the perfume and cosmetic industries,


as aromatherapeutics and food flavorings (Jenks and Kim, 2013). 2.3. Essential oils analyses by GC–MS method
Moreover, many Salvia species are very important in several fields,
from food chemistry to pharmaceutics (Flamini et al., 2007). Sage The essential oils from different Salvia leaves and flowers were
essential oils are complex chemical mixtures of various individual analyzed with a GC/MS–QP2010 Ultra system (Shimadzu, Japan)
components. Because of their low boiling points, they can be recov- equipped with an rxi-5MS capillary column (30 m × 0.25 mm; film
ered from different plant tissues by steam distillation (Giannouli thickness 0.25 ␮m). High purity helium at a flow rate of 1 mL/min
and Kintzios, 2000). The essential oil extracted from S. officinalis was used as the carrier gas. The purge flow rate was at 3.0 mL/min,
is considered to contain a variety of components (Stesevic et al., and the linear velocity was 36.8 cm/sec. The temperature was
2014); other sages also possess extraordinary fragrance, indicating programmed as follows: 80 ◦ C for 5 min, followed by a gradual
the presence of essential oils. Phenolic acids are phenylpropanoids increase to 290 ◦ C at a rate of 4 ◦ C/min and a hold at 290 ◦ C for
compounds derived from phenylalanine and the tyrosine metabolic 30 min as previously described (Liang et al., 2009). One microliter
pathways that are active in many Salvia species (Zhang et al., 2013). of diluted sample (split ratio 1/10) was injected into the GC at 250 ◦ C
Various phenolic acids exhibit notable antioxidant activities and with an autosampler (Shimadzu, Japan). The MS was operating in
free radical scavenging abilities (Chen et al., 1999). Rosmarinic acid, the electron impact mode (70 eV) at an interface temperature of
one of the most abundant phenolic acids, is common in many Salvia 280 ◦ C; the ion source temperature was 230 ◦ C. The chemical com-
species (Kan et al., 2007) and is extensively utilized in the pharma- ponents of essential oils were identified by matching their mass
ceutical and cosmetic industries for its high antioxidant activity spectra to mass spectral libraries (NIST08.L and NIST08s.L) and
(Shekarchi et al., 2012). comparing their retention indices to literature values (Babushok
The differences of the essential oil composition and phenolic and Andriamaharavo, 2012; Djabou et al., 2012; Falco et al., 2013;
acid content between the leaves and flowers of S. miltiorrhiza, S. Hosni et al., 2010; Sellami et al., 2012). The concentration of the
przewalskii, S. officinalis, and S. deserta are not clear. Thus, this study identified compound was computed based on the percentage of
investigated the chemical composition of essential oils from dif- the relative peak area (%).
ferent fresh aerial parts of these four Salvia species and aimed
to illustrate the chemical polymorphism among different species 2.4. Phenolic acids analyses by HPLC method
based on the characteristics of essential oils. Moreover, we also
analyzed the contents of three phenolic acids in the selected The HPLC analysis was performed according to a method
Salvia species to evaluate their potential application as industrial adapted from a previous study (Yang et al., 2009). Samples (0.02 g)
materials. of the dried leaves and flowers of the four Salvia plants were
extracted with 4 ml of 70% methanol for 12 h. The extracts were
2. Materials and methods treated with ultrasound for 45 min and then centrifuged at 9820 × g
for 10 min. The supernatant was passed through a 0.45 ␮m milli-
2.1. Plant material pore filter in preparation for analysis. The phenolic acid content
was analyzed using an HPLC system (Waters, USA) coupled to a
S. miltiorrhiza and three closely related species (S. przewalskii, S. 1252 binary HPLC pump, 2487 dual ␭ absorbance detector and
officinalis, and S. deserta) were collected from different natural habi- 2707 autosampler. A Waters Symmetry C18 (250 × 4.6 mm, 5 ␮m)
tat regions in China (Table 1). Different wild plantlets were gathered reverse-phase silica gel column was used. The data were acquired
and cultivated in the medicinal botanical garden at the College and processed using the Breeze software (Waters, USA). All samples
of Life Sciences, Northwest A&F University, Yangling, PR China in were tested in triplicate.
2012. Research fellow Yansheng Chen certified all plants, and the HPLC grade acetonitrile (Tedia, NJ, USA), analytical grade
voucher specimens were deposited at Northwest A&F University. methanol (Xilong, Shantou, China) and ultrapure H2 O (Shang-
Different Salvia species were cultivated at the same conditions. The hai Ultrapure Technology, China) were applied in present study.
fresh leaves and flowers of these species were collected in June 2014
at the flowering stage of the plants. Table 2
Gradient elution method for the phenolic acids analyses of Salvia species.
2.2. Essential oils extraction and samples drying process No. Time (min) Flow (ml/min) % Aa % Bb

1 0 1 5 95
The essential oils were obtained by hydrodistillation for 3 h 2 10 1 20 80
using a modified simultaneous distillation extraction (SDE) appa- 3 15 1 25 75
ratus according to a previous study (Chaintreau, 2001). First, 45 g 4 20 1 25 75
of fresh Salvia leaves and flowers were soaked in 300 ml of distilled 5 25 1 20 80
6 28 1 30 70
H2 O for 1 h; the resultant mixture was then subjected to hydrodis-
7 36 1 30 70
tillation for 3 h. The distillates were simultaneously extracted with 8 37 1 100 0
ether (Kermel, Tianjin, China) in a volume of 100 ml. The extracts 9 44 1 100 0
were collected, dried over anhydrous sodium sulfate (Kermel, Tian- 10 45 1 5 95
jin, China) and then concentrated with a rotary evaporator under a
A, acetonitrile.
b
reduced pressure. Finally, a small amount of yellowish essential oil B, ultrapure H2 O contained phosphoric acid (0.02%).
B. Li et al. / Industrial Crops and Products 69 (2015) 329–334 331

Table 3
Major chemical components in the essential oils of different Salvia species.

Compounds R. time RIa RIb % Relative peak area

SM-Lc SM-F SP-L SP-F SO-L SO-F SD-L SD-F

␤-Phellandrene 4.10 964 1004 – – – – – – – 29.74


1-Octen-3-ol 4.12 969 962 5.95 6.43 – – – – 4.98 –
␤-Pinene 4.24 943 979 – – 3.36 0.71 2.85 15.15 – 0.68
␤-Myrcene 4.32 958 991 – 0.36 0.71 – 0.49 0.64 – 0.71
o-Cymene 4.99 1042 1025 0.31 0.18 – – 0.39 0.52 – 2.15
Limonene 5.12 1018 1030 – – 20.5 3.65 – – – 0.96
Eucalyptol 5.14 1059 1032 1.38 – – – 14.82 14.91 – 0.73
␥-Terpinene 5.56 998 1060 0.14 trd 0.4 – 0.25 0.78 – 3.02
cis-␤-Terpineol 5.92 1158 1141 – – 1.52 – 0.26 – – 2.62
Diethyl sulfone 6.24 926 926 1.26 0.59 – – – – – –
Linalool 6.50 1082 1099 1.54 2.91 3.93 0.56 1.48 0.12 – tr
␤-Thujone 6.76 1062 1115 – – – – 14.86 6.05 – –
␣-Thujone 7.01 1062 1089 0.49 – – – 6.36 19.63 – 0.2
␤-Terpinol 7.78 1158 1137 – – 1.16 – – 0.34 – –
Camphor 7.83 1121 1143 – 0.11 2.34 0.12 12.7 1.63 – –
Borneol 8.32 1138 1150 0.24 1.56 1.4 0.22 10.17 6.71 – –
4-Terpineol 8.60 1137 1155 2.16 – 1.14 – 0.77 1 – 10.91
␣-Terpineol 8.95 1143 1189 0.91 0.78 4.66 0.77 0.49 0.73 – 0.72
n-Dodecane 9.03 1214 1200 – – – 1.22 0.15 0.14 2.53 0.79
Bornyl acetate 11.70 1277 1285 2.52 5.79 3.44 – 2.86 0.12 – –
␣-Copaene 13.70 1221 1376 0.8 0.26 – – tr – tr 0.84
␤-Bourbonene 14.86 1339 1386 2.70 1.4 – – – – – –
cis-Jasmone 14.94 1338 1371 1.96 0.39 tr – – – – –
␤-Elemene 15.03 1398 1391 0.83 0.67 – – – – – 0.38
n-Tetradecane 15.12 1413 1392 – – – 0.91 0.16 – 1.66 0.52
␤-Caryophyllene 15.95 1494 1419 4.72 11.05 0.3 – 3.38 4.64 0.25 4.6
␣-Humulene 17.00 1579 1460 1.73 3.61 – – 3.59 3.43 – 0.99
Germacrene D 17.28 1515 1556 6.82 3.45 – – tr – – 0.94
␥-Muurolene 17.70 1435 1477 – – tr 0.11 tr – 0.21 0.16
cis-␣-Farnesene 18.53 1458 1508 0.62 2.43 – – – – – –
␦-Cadinene 19.10 1469 1524 1.49 0.67 – 0.28 0.11 tr – 0.33
Caryophyllene oxide 20.97 1570 1581 2.60 7.93 2.78 2.39 1.93 1.87 5.99 4.95
Ledol 21.19 1530 1600 – – – – 5.96 7.92 8.36 6.98
Epiglobulol 21.25 1475 1548 1.05 0.94 – – – – – –
Humulene II epoxide 21.75 1592 1608 3.18 – 0.22 0.11 1.38 0.91 0.94 1.26
␥-Eudesmol 22.40 1626 1617 – 2.68 2.72 1.69 – – – –
␤-Eudesmol 22.97 1593 1641 – 3.53 4.08 – – – – –
␣-Cadinol 23.06 1580 1645 7.31 – – – – – – –
␣-Eudesmol 23.06 1598 1653 – 5.8 3.61 3.12 – – – –
Spathulenol 23.56 1536 1572 0.18 1.97 – – – – – –
Allo-aromadendrene oxide-(2) 23.81 1462 1623 1.78 0.27 – – – – – 0.59
Ledene oxide-(II) 24.00 1293 1293 1.51 0.67 – – – – – –
(2,2,6-Trimethyl-bicyclo[4.1.0] hept-1-yl)-methanol 27.52 1266 1266 – – 1.37 1.41 – – – –
Hexahydrofarnesyl acetone 28.17 1754 1835 – 0.68 – 0.36 – tr 0.45 tr
Aromadendrene oxide-(1) 28.76 1462 1462 8.30 4.3 – – tr – – 2.15
Aromadendrene oxide-(2) 31.62 1462 1443 3.49 2.75 – – – – 0.39 –
n-Heneicosane 32.13 2109 2100 – – – 0.47 – tr 0.56 –
Manool 33.74 2016 1961 0.93 0.76 0.44 2.83 1.23 1.91 1.39 4.83
Total compounds 62 63 68 51 71 69 63 72
Yield % 1.47 1.02 1.61 1.30 1.08 1.52 1.26 0.91

Only the main components were reported. – : not detected.


a
Retention indices on rxi-5 column.
b
Retention indices relative to literature values.
c
SM-L and SM-F, S. miltiorrhiza leaves and flowers; SP-L and SP-F, S. przewalskii leaves and flowers; SO-L and SO-F, S. officinalis leaves and flowers; SD-L and SD-F, S. deserta
leaves and flowers.
d
tr, trace (<0.1%).

The gradient elution method was performed with acetonitrile and multiple variables to two or three new ones while retaining most
ultrapure H2 O that contained HPLC-grade phosphoric acid (0.02%) the information of samples (Flamini et al., 2014).
(Table 2). Three phenolic acids were simultaneously detected at A cluster analysis based on the chemical composition of all
288 nm. Each phenolic acid was identified by comparing its reten- essential oils was implemented using the NTSYS software version
tion time with that of a standard substance; the phenolic acid 2.10 e with the unweighted pair group method with arithmetic
content was quantified based on a standard curve generated in our mean (UPGMA) clustering algorithm.
lab.

3. Results and discussion


2.5. Data analyses
3.1. Yield of essential oil
A principal component analysis (PCA) of the common com-
pounds in the essential oils was performed with the SPSS The yield of essential oil strong varied for different leaves and
software version 16.0. This approach is commonly used to reduce flowers of these four Salvia species. The yield of leaf oil ranged from
332 B. Li et al. / Industrial Crops and Products 69 (2015) 329–334

1.08 to 1.61% (v/w), while that of flower oil fluctuated between 0.91 Table 4
Component matrixa .
and 1.52%. The yield of oil was highest in the leaves of S. przewalskii
and flowers of S. officinalis. All essential oils were yellowish and Component
fragrant.
PC1 PC2 PC3 PC4
Essential oils extracted from aromatic plants have a wide range
␤-Myrcene .473 −.573 .494 .276
of medicinal and industrial applications, such as antiseptic, preser-
␥-Terpinene .943 .007 .267 .180
vatives, and antiphlogistic uses (Samejo et al., 2013). The plant Linalool −.550 −.499 .272 .565
essential oil composition depends on diverse factors, such as the 4-Terpineol .918 .075 .129 .276
harvest periods and stages of plant development (Verma et al., ␣-Terpineol −.171 −.848 .210 .266
2014). Moreover, the yield of essential oil strongly increased at dif- ␤-Caryophyllene −.064 .471 .317 .698
␦-Cadinene −.111 .417 −.510 .681
ferent plant harvest times, particularly at the vegetative phase after Caryophyllene oxide −.175 .612 .639 .218
a long period of drought stress (Jug-Dujaković et al., 2012). In the Humulene II epoxide .257 .166 −.832 .389
present study, all Salvia species were cultivated under the same Hexahydrofarnesyl acetone −.474 .660 .540 −.156
environmental conditions, including precipitation, temperature, Manool .872 .263 .144 −.244
Eigenvalue 3.386 2.604 2.224 1.807
solar radiation, and soil condition; consequently, the influences
% of variance 30.78 23.677 20.218 16.43
of the environmental and technical parameters were considered
a
negligible, and the differences in the essential oil yield and com- Four components were extracted; extraction method, principal component
analysis (PCA).
position could mainly be attributed to the genotypes of different
Salvia species.

3.2. Essential oils composition

The detailed compositions of the leaf and flower oils iden-


tified by GC–MS displayed remarkable chemical polymorphism
among the four Salvia species (Table 3). A minimum of 51 com-
pounds were identified in the essential oil of S. przewalskii flowers;
however, S. deserta flower oil contained a maximum of 72 com-
pounds. Eleven compounds were shared among the essential oils
of all investigated Salvia species. The major shared components
were ␤-caryophyllene (0.25–11.05%), 4-terpineol (0.77–10.91%),
caryophyllene oxide (1.87–7.93%), manool (0.44–4.83%) and
linalool (0.12–3.93%) (Table 3).
The essential oil of S. miltiorrhiza leaves primarily consisted of
aromadendrene oxide-(1) (8.3%), followed by ␣-cadinol (7.31%) and Fig. 1. PCA analysis with 11 common components of essential oils from different
germacrene D (6.82%); ␤-caryophyllene (11.05%), caryophyllene aerial parts of four Salvia species.
1–2, S. miltiorrhiza leaves and flowers; 3–4, S. przewalskii leaves and flowers; 5–6,
oxide (7.93%), and 1-octen-3-ol (6.43%) were most abundant in the S. officinalis leaves and flowers; 7–8, S. deserta leaves and flowers. PC1, the first
essential oil of S. miltiorrhiza flowers (Table 3). In the present study, principal component; PC2, the second principal component.
caryophyllene and its oxide were found in the essential oils of all
Salvia species, which was in accordance with previous work that
reported it as an effective anti-inflammatory, antioxidant and anti- were confirmed to be the principal components in the essential
microbial (Liang et al., 2009). Moreover, the germacrene D from oil of S. deserta flowers (Table 3).
essential oils can be used as a larvicidal crop protector (Teles et al.,
2013). Limonene (20.5%) was the most abundant compound in S. 3.3. Relationship among Salvia species based on the essential oil
przewalskii leaf oil; ␣-terpineol (4.66%) and ␤-eudesmol (4.08%) composition
were also abundant in this sage oil. However, the essential oil of S.
przewalskii flowers contained markedly less limonene (3.65%) than A principal component analysis (PCA) of 11 common com-
the leaf oil (Table 3). pounds in the essential oils of these Salvia species revealed that four
Seventy-one compounds were identified in the oil of S. offic- principal components with eigenvalues than 1 explained 91.1% of
inalis leaves, and among these compounds ␤-thujone (14.86%), the total variance (Table 4). The first principal component, which
eucalyptol (14.82%) and camphor (12.7%) were most prominent. mostly contributed by ␥-terpinene, 4-terpineol and manool posi-
However, the content of ␣-thujone (19.63%) was highest in the tively, explained 30.78% of the total variance; PC1 clearly separated
essential oil of S. officinalis flowers; ␤-pinene (15.15%) and euca- Salvia species rich in ␥-terpinene from the sage plants that contain
lyptol (14.91%) were also significant components of S. officinalis high amounts of linalool. The second principal component posi-
flower oil (Table 3). This result indicated that thujone, which is tively correlated with caryophyllene oxide and hexahydrofarnesyl
a natural substance found in several plants and commonly used acetone, but it negatively related to the content of ␣-terpineol; this
as ingredient in foods and beverages (Farhat et al., 2009), was component explained 23.68% of the total variance (Table 4). PC2
the major constituent in S. officinalis oil. Thujone and other active could easily distinguish the leaves and flowers of the sage species
compounds in the essential oil of S. officinalis, such as camphor, rich in caryophyllene oxide and ␣-terpineol, respectively.
were demonstrated to exert a potentially synergistic anticancer PCA analysis based on these shared constituents also showed
effect (Russo et al., 2013). We also analyzed the chemical char- that the chemical profiles of essential oils derived from the aerial
acteristics of essential oils from S. deserta cultivated in Yangling, parts of S. miltiorrhiza, S. przewalskii flowers and the leaves of S.
PR China, and this species was mainly distributed in the Xinjiang deserta were similar (Fig. 1). However, the leaves of S. przewal-
Autonomous Regions of China (Tezuka et al., 1998). Ledol (8.36%), skii and S. officinalis revealed a consistent chemotype based on the
caryophyllene oxide (5.99%) and 1-octen-3-ol (4.98%) were the pri- composition of essential oils. The chemical composition of Salvia
mary constituents in the leaf oil derived from this sage species; essential oils depends on the tissue specificity and the genetic
␤-phellandrene (29.74%), 4-terpineol (10.91%) and ledol (6.98%) diversity of the plants, which strongly influence and regulate the
B. Li et al. / Industrial Crops and Products 69 (2015) 329–334 333

essential oil biosynthesis under identical growth conditions (Gil


et al., 2007; Lattoo et al., 2006). Furthermore, the essential oil com-
position of several Salvia species was similar, which was mostly
due to the close phylogenetic relationship among the Salvia genus
(Li et al., 2010). This result indicated the feasibility of applying the
characteristics of essential oils as the chemotaxonomic markers for
Salvia species classification.
A cluster analysis of all compounds in the sage oils by UPGMA
showed a distinct result from that of the PCA assay outlined above.
The essential oils derived from aerial parts of S. miltiorrhiza and S.
prezwalskill formed one group with coefficients of 0.83 and 0.72,
respectively, indicating the consistency of the chemical character-
istics of these Salvia oils (Fig. 2). The essential oil compositions of Fig. 2. Cluster analysis by UPGMA based on the composition of essential oils from
the aerial parts of S. officinalis and S. deserta flowers were similar. different aerial parts of four Salvia species.
However, the chemical profile of S. deserta leaf oil was unlike those SM-L and SM-F, S. miltiorrhiza leaves and flowers; SP-L and SP-F, S. przewalskii leaves
of the other sage oils, which was probably attributed to the tissue and flowers; SO-L and SO-F, S. officinalis leaves and flowers; SD-L and SD-F, S. deserta
leaves and flowers.
specificity and different chemotype of Salvia species.

3.4. Phenolic acids analyses ranged from 1.9 ± 0.1 to 2.5 ± 0.2 mg/g dry weight (DW), whereas it
ranged from 0.2 ± 0.1 to 1.3 ± 0.1 mg/g DW in leaves. The ferulic acid
The phenolic acids extracted from various Salvia species have content was highest in S. przewalskii flowers and S. deserta leaves
shown remarkable pharmacological activities and promise as compared to the respective aerial parts of other sages (Fig. 3a). Our
industrial materials purposes (Generalic et al., 2012; Orhan et al., results confirmed that caffeic acid was abundant in the flowers
2012). Three phenolic acids derived from different aerial parts of of Salvia plants and ranged between 2.6 ± 0.1 and 3.0 ± 0.2 mg/g
each selected Salvia species were detected by HPLC. The ferulic DW; however, the leaves of S. przewalskii and S. miltiorrhiza con-
acid content was remarkably higher in flowers than in leaves and tained the highest (1.9 ± 0.1 mg/g DW) and lowest (0.4 ± 0.04 mg/g

Fig. 3. Phenolic acid content in the leaves and flowers of selected Salvia species.
SM, S. miltiorrhiza; SP, S. przewalskii; SO, S. officinalis; SD, S. deserta. (a) Ferulic acid content of selected Salvia species. (b) Caffeic acid content of selected Salvia species. (c)
Rosmarinic acid content of selected Salvia species. Content of each phenolic acid from leaves and flowers of S. miltiorrhiza was a control in the present study. DW, dry weight;
* P < 0.05, ** P < 0.01.
334 B. Li et al. / Industrial Crops and Products 69 (2015) 329–334

DW) amounts of caffeic acid, respectively, compared to other sage Generalic, I., Skroza, D., Surjak, J., Mozina, S.S., Ljubenkov, I., Katalinic, A., Simat, V.,
leaves (Fig. 3b). Rosmarinic acid, the main bioactive constituent Katalinic, V., 2012. Seasonal variations of phenolic compounds and biological
properties in sage (Salvia officinalis L.). Chem. Biodivers. 9, 441–457.
in Salvia species, was most abundant in S. przewalskii leaves at Giannouli, A.L., Kintzios, S.E., 2000. Essential oils of salvia spr: examples of
64.1 ± 3.9 mg/g DW and in S. officinalis flowers at 53.4 ± 2.9 mg/g intraspecific and seasonal variation. In: Kintzios, S.E. (Ed.), The Genus Salvia.
DW (Fig. 3c). The wide distribution of selected phenolic acids in Overseas Publishers Association, The Netherlands, pp. 69–79.
Gil, A., Van Baren, C.M., Lira, P.M.D.L., Bandoni, A.L., 2007. Identification of the
three closely related Salvia species was confirmed to be highly con- genotype from the content and composition of the essential oil of lemon
sistent with those in S. miltiorrhiza, which is an effective traditional verbena (Aloysia citriodora Palau). J. Agric. Food Chem. 55, 8664–8669.
Chinese medicine in China (Cheng, 2007). Moreover, the contents Hosni, K., Zahed, N., Chrif, R., Abid, I., Medfei, W., Kallel, M., Ben Brahim, N., Sebei,
L., 2010. Composition of peel essential oils from four selected Tunisian Citrus
of phenolic acids in both the leaves and flowers of S. przewalskii
species: evidence for the genotypic influence. Food Chem. 123, 1098–1104.
were higher than that of S. miltiorrhiza. This result indicated that Jenks, A.A., Kim, S.C., 2013. Medicinal plant complexes of Salvia subgenus
the leaves of S. przewalskii can be exploited as an excellent source Calosphace: an ethnobotanical study of new world sages. J. Ethnopharmacol.
146, 214–224.
of phenolic acid, especially rosmarinic acid.
Jug-Dujaković, M., Ristić, M., Pljevljakušić, D., Dajić-Stevanović, Z., Liber, Z.,
Hančević, K., Radić, T., Šatović, Z., 2012. High diversity of indigenous
4. Conclusions populations of Dalmatian sage (Salvia officinalis L.) in essential-oil composition.
Chem. Biodivers. 9, 2309–2323.
Kan, Y., Gokbulut, A., Kartal, M., Konuklugil, B., Yilmaz, G., 2007. Development and
The GC–MS method was used to analyze the essential oils in this validation of a LC method for the analysis of phenolic acids in Turkish Salvia
study; the chemical composition of essential oils from four Salvia species. Chromatographia 66, S147–S152.
species was notably different. The polymorphism of the chem- Lattoo, S.K., Dhar, R.S., Dhar, A.K., Sharma, P.R., Agarwal, S.G., 2006. Dynamics of
essential oil biosynthesis in relation to inflorescence and glandular ontogeny
ical composition of oils derived from the leaves and flowers of in Salvia sclarea. Flavour Frag. J. 21, 817–821.
these Salvia species indicated that this composition was tissue- and Li, M.H., Peng, Y., Xiao, P.G., 2010. Distribution of tanshinones in the genus Salvia
organ-specific, which may be due to the genetic background diver- (family Lamiaceae) from China and its systematic significance. J. Syst. Evol. 48,
118–122.
sity of these Salvia species. The phenolic acid content of closely Liang, Q., Liang, Z.S., Wang, J.R., Xu, W.H., 2009. Essential oil composition of Salvia
related Salvia species was similar to that of S. miltiorrhiza, which miltiorrhiza flower. Food Chem. 113, 592–594.
revealed a common biosynthetic pathway for phenolic acids in Orhan, I.E., Senol, F.S., Ozturk, N., Akaydin, G., Sener, B., 2012. Profiling of in vitro
neurobiological effects and phenolic acids of selected endemic Salvia species.
the selected Salvia. Furthermore, S. przewalskii is a rich source of Food Chem. 132, 1360–1367.
rosmarinic acid. Rajabi, Z., Ebrahimi, M., Farajpour, M., Mirza, M., Ramshini, H., 2014. Compositions
and yield variation of essential oils among and within nine Salvia species from
various areas of Iran. Ind. Crops Prod. 61, 233–239.
Acknowledgements Russo, A., Formisano, D., Rigano, F., Senatore, S., Delfine, V., Rosselli, M., 2013.
Chemical composition and anticancer activity of essential oils of
The authors are grateful to research fellow Yansheng Chen at Mediterranean sage (Salvia officinalis L.) grown in different environmental
conditions. Food Chem. Toxicol. 55, 42–47.
Northwest A&F University, Yangling, PR China for the plant identi- Rzepa, J., Wojtal, L., Staszek, D., Grygierczyk, G., Labe, K., Hajnos, M., Kowalska, T.,
fication. This work was supported by the National Natural Science Waksmundzka-Hajnos, M., 2009. Fingerprint of selected Salvia species by
Foundation of China (Grant No.81373908) and Key Science and HS–GC–MS analysis of their volatile fraction. J. Chromatogr. Sci. 47, 575–580.
Samejo, M.Q., Memon, S., Bhanger, M.I., Khan, K.M., 2013. Essential oil constituents
Technology Project of Shaanxi Province, China (Grant No. 2012
in fruit and stem of Calligonum polygonoides. Ind. Crops Prod. 45, 293–295.
KTCL 02–07). Sellami, I.H., Rebey, I.B., Sriti, J., Rahali, F.Z., Limam, F., Marzouk, B., 2012. Drying
sage (Salvia officinalis L.) plants and its effects on content, chemical
composition, and radical scavenging activity of the essential oil. Food
References
Bioprocess. Technol. 5, 2978–2989.
Shekarchi, M., Hajimehdipoor, H., Saeidnia, S., Gohari, A.R., Hamedani, M.P., 2012.
Babushok, V.I., Andriamaharavo, N.R., 2012. Use of large retention index database Comparative study of rosmarinic acid content in some plants of Labiatae
for filtering of GC–MS false positive identifications of compounds. family. Pharmacogn. Mag. 8, 37–41.
Chromatographia 75, 685–692. Skala, E., Wysokinska, H., 2005. Tanshinone production in roots of
Capek, P., Hribalova, W., 2004. Water-soluble polysaccharides from Salvia officinalis micropropagated Salvia przewalskii Maxim. Z. Naturforsch. C 60, 583–586.
L: possessing immunomodulatory activity. Phytochemistry 65, 1983–1992. Stesevic, D., Ristic, M., Nikolic, V., Nedovic, M., Cakovic, D., Satovic, Z., 2014.
Chaintreau, A., 2001. Simultaneous distillation-extraction: from birth to Chemotype diversity of indigenous Dalmatian sage (Salvia officinalis L.)
maturity-review. Flavour Frag. J. 16, 136–148. populations in Montenegro. Chem. Biodivers. 11, 101–114.
Chen, H., Chen, F., Zhang, Y.L., Song, J.Y., 1999. Production of lithospermic acid B Teles, S., Pereira, J.A., Santos, C.H.B., Menezes, R.V., Malheiro, R., Lucchese, A.M.,
and rosmarinic acid in hairy root cultures of Salvia miltiorrhiza. J. Ind. Silva, F., 2013. Effect of geographical origin on the essential oil content and
Microbiol. Biotechnol. 22, 133–138. composition of fresh and dried Mentha × villosa Hudson leaves. Ind. Crops Prod.
Cheng, T.O., 2007. Cardiovascular effects of Danshen. Int. J. Cardiol. 121, 9–22. 46, 1–7.
Djabou, N., Muselli, A., Allali, H., Dib Mel, A., Tabti, B., Varesi, L., Costa, J., 2012. Tezuka, Y., Kasimu, R., Li, J.X., Basnet, P., Tanaka, K., Namba, T., Kadota, S., 1998.
Chemical and genetic diversity of two Mediterranean subspecies of Teucrium Constituents of roots of Salvia deserta Schang (Xinjiang–Danshen). Chem.
polium L. Phytochemistry 83, 51–62. Pharm. Bull. 46, 107–112.
Falco, E.D., Roscigno, G., Iodice, C., Senatore, F., 2013. Phytomorphological and Verma, R.S., Padalia, R.C., Chauhan, A., 2014. Chemical composition variability of
essential-oil characterization in situ and ex situ of wild biotypes of oregano essential oil during ontogenesis of Daucus carota L. subsp. sativus (Hoffm.)
collected in the Campania region (Southern Italy). Chem. Biodivers. 10, Arcang. Ind. Crops Prod. 52, 809–814.
2078–2090. Walch, S.G., Kuballa, T., Stuhlinger, W., Lachenmeier, D.W., 2011. Determination of
Farhat, M.B., Jordán, M.J., Chaouech-Hamada, R., Landoulsi, A., Sotomayor, J.A., the biologically active flavour substances thujone and camphor in foods and
2009. Variations in essential oil, phenolic compounds, and antioxidant activity medicines containing sage (Salvia officinalis L.). Chem. Cent. J. 5, 44.
of Tunisian cultivated Salvia officinalis L. J. Agric. Food Chem. 57, 10349–10356. Wu, Z.Y., Raven, P.H., 1994. Flora of China. Science Press, Beijing, China.
Flamini, G., Cioni, P.L., Morelli, I., Bader, A., 2007. Essential oils of the aerial parts of Yang, D.F., Yang, S.S., Zhang, Y.J., Liu, Y.H., Meng, X.H., Liang, Z.S., 2009. Metabolic
three Salvia species from Jordan: Salvia lanigera, S. spinosa and S. syriaca. Food profiles of three related Salvia species. Fitoterapia 80, 274–278.
Chem. 100, 732–735. Zhang, S.C., Ma, P.D., Yang, D.F., Li, W.J., Liang, Z.S., Liu, Y., Liu, H., 2013. Cloning and
Flamini, G., Cosimi, E., Cioni, P.L., Molfetta, I., Braca, A., 2014. Essential-oil characterization of a putative R2R3 MYB transcriptional repressor of the
composition of Daucus carota ssp. major (pastinocello carrot) and nine rosmarinic acid biosynthetic pathway from Salvia miltiorrhiza. PLoS One 8,
different commercial varieties of Daucus carota ssp. sativus fruits. Chem. e73259, http://dx.doi.org/10.1371/journal.pone.
Biodivers. 11, 1022–1033.

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