Industrial Crops & Products xxx (xxxx) xxxxxx

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Industrial Crops & Products

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

Essential oil composition of purple basils, their reverted green varieties

(Ocimum basilicum) and their associated biological activity

Adolna R. Korocha, James E. Simonb, H. Rodolfo Julianib,
a
The City University of New York, Borough of Manhattan Community College, 199 Chambers St., Science Dept., 10007, NY, USA
b
New Use Agriculture and Natural Plant Products Program, Department of Plant Biology, School of Environmental and Biological Sciences (SEBS) Rutgers University, 59
Dudley Road, New Brunswick 08901, NJ, USA

A R T I C L E I N F O A B S T R A C T

Keyword: Essential oils provide the characteristic aroma notes to basil varieties and are partially responsible for basil
Basil biological activities. The search for new aromas and biological activities are important steps to nd new
Oil composition applications for industrial crop and products. The objective of this study was to evaluate the chemical
Bioactivity composition of the essential oils from purple basil varieties and their progeny that reverted to green varieties,
Eugenol
and to compare the composition of these oils with other nonpigmented basil varieties. This work also evaluated
Linalool
selected biological activities of some of these green and basil varieties in search of new biological activities. The
Methyl eugenol
green purple varieties derived from Dark Opal and Osmin Purple varieties exhibited a remarkable similarity,
suggesting that these plants reverted to the same green ancestor. Their aromatic volatile oils and their main
components exhibited a wide range of antioxidant and antimicrobial activities, with several chemotypes (Sweet,
Osmin Purple basils) expressing high antioxidant and antimicrobial activities. Some of the reverted green types,
showed higher levels phenylpropanoids (e.g. higher in eugenol) compared with their parent types (Purple
Rues). These biological activities of the aromatic oils appear to be related to their phenolic constituents and
concentration of the oils (e.g. eugenol, methyleugenol). The results showed that the essential oils of these basils
have a number of additional attributes and applications for the nutraceutical industry in addition to their aroma
and avor impact.

1. Introduction
Purple basils (Ocimum basilicum, Lamiaceae) have been commer-
cialized for both culinary and their ornamental value. The instability of
purple basils, where a percentage of the progeny reverts to a green
ancestor that same season of production, has limited their use as
ornamental plants and also limited their potential applications for other
markets. Phippen and Simon (2000) showed that Purple Rues basil
varieties can have a reversion back to partially green sectoring on its
leaves up to 35%. Basil essential oils are complex mixtures that can
include over a hundred chemical constituents. However, only a few of
these components are found in high relative concentrations, such as
citral, 1,8-cineole, linalool, methyl chavicol, eugenol, methyl eugenol
and methyl cinnamate and it is the blend or ratio of all the constituents
that together provide the basis of the herbs aroma (Simon et al., 1990).
Oils from aromatic plants have been known since antiquity to
possess biological activity, mainly antibacterial, antifungal and anti-
oxidant properties (Koroch et al., 2007).
Previously, it was reported the antioxidant activity in leaves extracts
of some Ocimum spp (Koroch et al., 2010; Juliani and Simon, 2002
Juliani and Simon, 2002).
The objective of this study is to evaluate the chemical composition
of purple basil essential oils and their progeny reverted to green
varieties, and to compare the composition of these oils with other basil
varieties. This work also seeks to evaluate the biological activities of
some of these green and basil varieties in search of new biological
activities. The search for new uses is an important strategy to nd
industrial crop applications for herbs and aromatic plants. This an
expanded study of our previous work (Juliani and Simon, 2002) now
centered on the reversion of purple varieties.
2. Materials and methods
Seeds from purple Ocimum basilicum varieties: Dark Opal (DO),
(Richters Seeds, Goodwood Ontario, Canada), Osmin Purple (OP),
Purple Rues (PR) (Johnnys Selected Seeds) and the corresponding
green reversions varieties: Green Dark Opal (GDO), Green Osmin Purple
(GOP) and Green Purple Rues (GPR) were grown in ats before

Corresponding author.
E-mail addresses: hjuliani@rutgers.edu, rodolfojuliani@yahoo.com.ar (H.R. Juliani).

http://dx.doi.org/10.1016/j.indcrop.2017.04.066
Received 15 February 2017; Received in revised form 17 April 2017; Accepted 19 April 2017
0926-6690/ 2017 Published by Elsevier B.V.

Please cite this article as: Koroch, A.R., Industrial Crops & Products (2017), http://dx.doi.org/10.1016/j.indcrop.2017.04.066
A.R. Koroch et al.
transferring to six inches pot with a sterilized soil mix at the Rutgers
University Research Greenhouse (New Jersey Agricultural
Experimental Station, Rutgers University New Brunswick, NJ). For
comparison purposes other basils were included in this study: O.
basilicum varieties (Sweet Basil, SE, Red Rubin, RR, Cinnamon
Basil,CI; Italian Large Leaf, ILL), O. sanctum (Holly Basil, HO) and O.
x citriodorum (Sweet Dani Lemon Basil, LE) (Juliani and Simon, 2002).
Plants were irrigated daily to soil saturation capacity and grown under
day/night temperatures of 2630 C and 1821 C, respectively. The
above-ground biomass of each individual plant was harvested at full
bloom, placed in a paper bag and dried in a forced-air drier at 38 C for
7 days prior to essential oil extraction and analysis.
The essential oils were extracted from dried leaves in a 1.5 L ask
with distilled water (1:15 v/w) using a clevenger apparatus (Charles
and Simon, 1990). Essential oil content was expressed as mL of oil per
100 g of dry weight. Volatile oils were analyzed by a gas chromato-
graph coupled to a mass spectrometer and ame ionization detector
(Juliani et al., 2008). The ABTS radical cation assay was used to
evaluate the free radical scavenging eect of the oils and their main
components (Re et al., 1999). Stock solution of the oils and standards
(eugenol, methyl eugenol, methyl chavicol, methyl-E-cinnamate, 1,8
cineole, linalool, citral) were diluted in ethanol. All assays were carried
out at least three times and in duplicate. This method is based on
reduction of the ABTS radical cation (2,2-azino-bis (3-ethylbenzthiazo-
line 6 sulfonic acid) measured by absorbance at 734 nm. Results
are expressed as percentage of Trolox equivalent antioxidant capacity/
mL EO (TEAC, mol Trolox/mL EO). For the ferric reducing power
(FRAP) method, the oils and standards were diluted in a Tween 80
(10%) water solution and then vortexed for 3 min at full speed. The
FRAP assay was used to assess the ascorbic acid equivalent antioxidant
activity (AEAC, mol Trolox/mL EO) (Benzie and Strain, 1996). For
antimicrobial tests, the essential oils from selected Ocimum varieties
and pure oil components (methyl eugenol, eugenol, methyl chavicol,
methyl cinnamate, linalool and 2-allylphenol) were dissolved into 300
microliters (l) of DMSO (Dimethylsulfoxide). Growth of microorgan-
isms (Escherichia coli, Staphylococcus aureus and Saccharomyces
cerevisiae) and the antimicrobial screenings were performed as de-
scribed by Poulev et al. (2003). A dendrogram was constructed using
the unweighted pair- group method with arithmetical average (UP-
GMA). The data were transformed with the stand procedure from
NTSYS-pc (Rohlf, 1990; Juliani et al., 2008). The experimental design
was fully randomized. Data were analyzed statistically by analysis of
variance (ANOVA) followed by the LSD test (5%).
3. Results and discussion
The chemical composition of the dierent types of basils showed a
remarkable diversity (Juliani and Simon, 2002) (Table 1). The compar-
ison of the oil prole of the purple and their green counterparts showed
some similarities (Table 1). The purple rues (PR-GPR) pair belonged
to a methylchavicol chemotype, with GPR showing higher amounts of
phenylpropanoids, methylchavicol 50.3% and much higher levels of
eugenol (8%) as compared with the PR, 46.4% and 0.5% for methy-
chavicol and eugenol, respectively.
The Dark Opal pair (DO-GDO) belonged to a linalool-eugenol
chemotype showing a similar prole with linalool (54.3 and 57.2%
for DO and DGO respectively), eugenol (6.9 and 7.3%), 1,8 cineole (8.7
and 9.4%) exhibiting similar amounts (Table 1). The Osmin Purple pair
(OP, GOP) also a linalool-eugenol type showed the highest amounts of
linalool for the GOP (59%), and lower amounts of eugenol (7.0%),
while the OP showed lower levels of linalool (51.1%) and the highest
amounts of eugenol (14.7%) among the purple basils (Table 1).
A cluster analysis conducted with these pairs and our previous data
(Juliani and Simon, 2002) (Fig. 1), showed the presence of three
clusters, that separated the three species of Ocimum, Lemon basil (LE)
(a hybrid, O. x citriodorum) and Holy basil (O. tenifolium). All the
Industrial Crops & Products xxx (xxxx) xxxxxx
varieties of O. basilicum were grouped and separated in two groups,
according to their main components and 1,8-cineole content. The basils,
Sweet basil (SE) and Cinnamon basil (CI) were low in 1,8-cineole
content in contrast to all others which were higher (59%). This latest
group could then be further sub-grouped based on the high methyl
chavicol and low linalool content (Italian Large Leaf (ILL), Purple
Rues (PR) and Green Purple Rues (GPR); absence of methyl
chavicol and high linalool Red Rubin (RR)); or low linalool and eugenol
content absent in the former groups: Dark Opal (DO), Green Dark
Opal (GDO), Osmin Purple (OP) and Green Osmin Purple (GOP) (Fig. 1,
Table 1). In a similar study, Carovi-Stanko et al. (2011) used cluster
analysis (dendrogram), discriminated Ocimum species and O. basiculum
varieties in two main clusters rich in methylchavicol and linalool.
Interesting to note was that DO and GDO were grouped in dierent
subclusters, suggesting that GDO reverted to a green ancestor similar to
the OP/GOP type. PR and GPR were grouped in the same cluster as the
ILL basils, suggesting a similar origin (Fig. 1). The total essential oil
accumulation was signicantly higher in GOP and GDO than in their
purple counterparts (Table 2).
These chemical variations and the presence of phenylpropanoids
have important eect on their biological activities. The highest radical
scavenging activity was associated with the linalool-eugenol chemo-
types, with the highest activity observed in those with highest content
of eugenol, OP essential oils (Tables 1 and 2). Those varieties that
belong to the linalool-methyl chavicol (PR and GPR) exhibited the
lowest activity (5059 mol/mL EO, TEAC). The reducing ability of
oils, measured as AEAC showed a similar trend to TEAC, with SE (Sweet
Basil) and OP essential oils exhibiting the highest activity (2281 and
1263 mol/mL EO respectively). The DO, GDO, and GOP basils showed
signicantly lower activity (from 269 to 469 mol/mL EO respectively).
Comparatively, PR and GPR exhibited the lowest antioxidant activity
(31 to127 mol/mL EO). The antioxidant activity of the essential oils of
basil was similar using both in vitro chemical models. As the ability of
the antioxidants to scavenge free radicals (ABTS) and the ability to
reduce iron (FRAP) is closely related (R2 = 0.68), these results provide
additional conrmation of the dierential response based on the major
chemical constituents in the essential oils. The antioxidant activity of
the major oil constituents showed that eugenol exhibited the highest
antioxidant activity in both models (Table 2). Furthermore, there was a
close relationship between antioxidant activity in both assays and the
amount of eugenol in the dierent essential oils (TEAC R2 = 0.75;
AEAC R2 = 0.75). Essential oils rich in 1,8-cineole, linalool showed a
very low antioxidant activity. These results illustrate the importance of
the hydroxyl group in the aromatic ring to confer the antioxidant
activity to a molecule like eugenol, in contrast methyl-E-cinnamate
(CI), which lacks this group showed a very low antioxidant activity
(Table 2). In the case of methyl eugenol (HO oil), where the hydroxyl
group is blocked by methylation, the antioxidant activity decreased
considerably. Methyl eugenol antioxidant activity in both assays was
higher than that of methyl chavicol, suggesting that an additional
methoxy group increases the antioxidant activity in methyl eugenol.
The higher antioxidant activity of eugenol compared with Trolox could
be associated with the presence of the methoxy group in the eugenol
molecule. Volatile constituents, lacking a phenolic ring such as linalool,
citral (neral and geranial) and 1,8-cineol or having the hydroxyl group
blocked by methylation (methyl chavicol), exhibited the lowest anti-
oxidant activity (Table 2).
From a nutraceutical perspective, eugenol is an interesting compo-
nent of essential oils due to its high antioxidant and antibacterial
activities. The challenge in its incorporation in botanical products is
due to the strong taste and odor impact that a small concentration of
eugenol can impart to nal products. The highest antioxidant activity
(1105 TEAC-2281 AEAC) within this range of chemotypes was asso-
ciated with the linalool-eugenol chemotype. The essential oils from
selected basils showed dierent antimicrobial activities. All the oils
tested inhibited 100% of the growth of yeast. SE oil exhibited the
2
A.R. Koroch et al. Industrial Crops & Products xxx (xxxx) xxxxxx

Table 1
Chemical composition of purple basils and other selected Ocimum spp. varieties.

RIa Component ILLb PR GPR RR DO GDO OP GOP SE CI HO LE

938 pinene 0.1d 0.2 0.2 0.1 0.2 0.5 0.2 0.2 0c 0.1 0.2
953 camphene 0.0 0.0 0.0 0.1 0.2 0.0 0.1 0.0 0.0 0.2
977 sabinene 0.1 0.3 0.4 0.2 0.3 0.4 0.3 0.3 0.0 0.1 0.1
981 pinene 0.2 0.7 0.5 0.5 0.6 1.0 0.7 0.6 0.1 0.3 0.2
991 myrcene 0.3 1.0 0.8 0.7 0.9 1.3 0.9 0.8 0.1 0.3 0.0
1032 limonene 0.1 0.4 0.5 0.2 0.6 0.7 0.5 0.5 0.1 0.2 0.1 0.0
1036 1,8-cineole 5.2 7.2 8.2 8.2 8.7 9.4 9.4 8.7 0.9 3.7 0.0
1051 (E) ocimene 0.4 0.0 0.0 0.5 0.0 0.2 0.0 2.2 0.5 0.0
1070 cis linalool oxide 0.2 0.1 0.2 0.2 0.2 0.2 0.1 0.2 0.1 0.1
1091 terpineol 0.1 0.7 0.7 0.4 1.2 0.8 1.4 1.0 0.1 0.1 0.0 0.1
1108 linalool 24.6 24.9 19.0 59.4 54.3 57.2 51.1 59.0 54.6 19.8 0.2
1119 fenchol 0.1 0.1 0.4 0.3 0.3 0.2
1150 camphor 0.3 0.0 0.0 1.3 1.8 0.8 1.0 0.7 0.3 0.0
1170 borneol 0.2 0.2 0.2 0.2 0.3 0.3 0.2 0.2 0.3 0.2 1.1
1192 terpineol 0.8 0.7 0.9 1.0 1.0 1.1 1.1 1.0 0.3 0.5 0.0 0.1
1208 methyl chavicol 59.5 46.4 50.3 0.0 0.0 0.0 8.4 4.5
1223 fenchyl acetate 0.2 0.6 0.7 0.8 0.4
1229 nerol 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.4
1249 neral 29.2
1256 geraniol 0.2 0.1 0.1 0.1 1.0 1.2 1.3 1.4 0.1 0.1 1.3
1272 geranial 0.0 0.0 0.0 0.0 38.5
1288 bornylacetate 0.2 0.1 0.1 0.0 0.3 0.5 0.3 0.3 0.1 0.1 0.0
1363 eugenol 0.6 0.5 8.0 6.9 7.3 14.7 7.0 19.2 4.1 1.4 0.2
1366 nerylacetate 0.3
1380 copaene 0.0 0.1 0.2 0.2 0.2 0.1 0.1 0.2 0.1 0.1 1.3 0.1
1384 geranyl acetate 0.0 0.0 0.0 0.1 0.4 0.3 0.3 0.3
1394 cubebene 0.2 0.6 0.4 1.2 1.0 1.1 0.5 1.1 0.6 0.6 0.0
1395 E methyl cinnamate 45.9
1398 elemene 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.2 0.8 0.3
1406 methyl eugenol 0.3 0.2 0.2 0.2 2.7 0.2 3.6 0.5 1.3 0.1 74.7
1424 (E) caryophyllene 0.0 0.5 0.7 0.1 1.2 0.9 0.7 0.9 0.1 0.1 11.6 3.0
1443 (E) bergamontene 0.1 5.8 7.2 9.4 0.7 0.0 0.3 0.6 0.2 0.5 0.1 0.7
1451 humulene 0.0 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.2 0.1 0.7 0.8
1459 (Trans) - farnesene 0.2 0.3 0.2 0.4 1.1 0.0 0.8 0.8 0.4 0.6 0.0
1486 germacrene D 0.7 1.1 1.5 2.1 2.5 2.3 2.1 2.2 2.3 2.2 3.7 3.5
1491 selinene 1.5
1494 selinene 1.4
1497 bicyclogermacrene 0.3 0.1 0.1 1.1 1.2 0.9 0.9 1.0 1.3 1.4 0.1
1509 (trans) guaiene 0.2 0.8 0.9 1.9 1.9 1.8 1.1 1.7 0.6 1.4 0.4 0.2
1526 cadinene 0.1 0.4 0.4 0.7 0.3 0.2 0.2 0.2 0.3 0.1 0.3 0.2
1581 caryophyllene oxide 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.2
1619 1,10 di epi cubenol 0.2 0.3 0.4 0.4 0.4 0.3 0.3 0.3 0.7 0.4 0.0
1646 epi cadinol 1.6 1.7 2.1 2.8 3.1 2.2 1.8 2.2 4.6 2.8 0.2
1655 eudesmol 0.0 0.1 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.1
1659 cadinol 0.1 0.1 0.2 0.3 0.2 0.2 0.1 0.2 0.2 0.2 0.1 0.1

a
RI: retention indexes on a polar column (HP5-MS, methyl silicone).
b
IIL (Italian Large Leaf), SE (Sweet Basil), CI (Cinnamon basil), HO (Holy Basil), DO (Dark Opal), GDO (Green Dark Opal), OP (Osmin Purple), GOP (Green Osmin Purple), PR (Purple
Rues), GPR (Green Purple Rues), RR (Red Rubin), LE (Sweet Dani Lemon Basil).
c
0.0: traces components (less than 0.04%), blank space: not detected.
d
Relative percentage, individual component in relation to total oil.

strongest activity against E. coli and S. aureus (65% and 100%,
respectively). OP and CI (Cinnamon basil) showed higher antimicrobial
activity against S. aureus (40% and 70%, respectively), lower percen-
tages of inhibition were observed for E. coli (15% for OP and 10% CI).
HO showed strongest antimicrobial activity against E. coli (50%) (data
not shown). The basil essential oils are more active against Gram (+)
than Gram () bacteria, and our results agree with previous reports
(Burt, 2004).
To infer which constituents were responsible of these antimicrobial
activities, dierent standard pure chemical constituents (at 3.2%) that
are found as the major oil constituents were then tested against the
microorganisms under identical conditions. All the pure standard
highest concentrations showed the same or greater activity than the
same constituents found naturally in the essential oil. The strongest
antimicrobial activity of SE can be attributed to eugenol (19% of oil)
and linalool (54%) content and a synergistic eect should be consid-
ered. Eugenol at 3.2% completely inhibited the growth of E. coli and S.
aureus. The antimicrobial activity of HO can be attributed to its main
component methyl eugenol (75%) both showing similar bioactivities
(Table 1). Methyleugenol showed lower inihibition for E. coli (70%) and
S. aureus (20%).
The lower activity of OP oil could be associated to its high linalool
(50%), and CI to the methyl-E-cinamate and linalool content (Table 1).
Linalool showed no activity for E. coli and S. aureus. methyl-E-cinamate
showed higher activities for both bacteria E. coli (70%) and S. aureus
(20%) (data not shown).
Basil essential oils with methylchavicol as the main component were
also reported to have low antimicrobial activity (Bozin et al., 2006).
The results clearly showed a positive correlation between the main
constituents in the essential oil and the relative percentage composition
in the oil with their antimicrobial activity. The functional groups of the
components of the oils play an important role, components with
phenolic structures such as eugenol showed the highest antimicrobial
activity when compared with the methylated components (such as
methyl eugenol).
The importance of the free hydroxyl group of the phenolic structure

3
A.R. Koroch et al. Industrial Crops & Products xxx (xxxx) xxxxxx

Fig. 1. Essential oil clustering of basil cultivars Italian Large Leaf, Sweet, Cinnamon, Holy, Dark Opal, Green Dark Opal, Osmin Purple, Green Osmin Purple, Purple Rues, Green Purple
Rues, Red Rubin and Sweet Dani Lemon basils. The distances based on similarity (or dissimilarity) in their chemical prole (Table 1) are illustrated as a Similarity Index which serves as
the criteria for grouping or separating basil essential oils (Juliani et al., 2008).

Table 2
Essential oil content and antioxidant activity of selected Ocimum spp. basil oils .

Oil content Antioxidant activity

mL EO/100 g DW a
Sb mol Trolox/mL EO FRAPc mol AA/mL EO

Dark Opal (DO) 1.1 0.05 ad 751.2 434.07 11.6 cd

24.1 abc
Green Dark Opal (GDO) 1.5 0.02 b 769.2 19.1 abc 459.23 8.8 c
Osmin Purple (OP) 0.9 0.01 a 996.7 137.1 ab 1262.9 8.0 b
Green Osmin Purple (GOP) 1.7 0.5 b 678.9 38.4 bc 408.63 15.5 de
Purple Rues (PR) 1.1 0.1 a 50.1 10.2 hi 30.633 0.6 k
Green Purple Rues (GPR) 1.0 0.01 a 52.0 1.7 c 29.3 0.9 f
Eugenol 1.5 1.3
Methyl eugenol 0.314 0.28
Methyl chavicol 0.15 0.02
E-methyl cinnamate/linalool 0.001 0.001
1,8 cineole/Z and E citral 0.001 0.001

a
Essential oils (EO) on a dry weight basis.
b
ABTS radical cation (2,2-azino-bis (3-ethylbenzthiazoline 6 sulfonic acid).
c
Ferric Reducing Power (FRAP).
d
Mean standard error. Mean followed by the same letter in the same column do not dier statistically at p < 0.05 according to LSD test.

can be demonstrated with higher activity of eugenol in relation to
methyl eugenol. It was previously demonstrated that the activity of the
oils is related to the respective oil composition, the structural cong-
uration of the constituent components of the oils and their functional
groups (Bassol and Juliani, 2012; Seow et al., 2014).
4. Conclusions
The chemical diversity of dierent varieties was characterized by
the dendrogram analysis, being separated according their botanical
identity. A remarkable observation was the fact that GDO and GOP
were grouped in the same subcluster, thus suggesting that GDO reverted
to the same green ancestor. Those essential oils showing a high
antioxidant activity also exhibited higher antimicrobial activity, sug-
gesting a relationship with the bioactivities of their main components.
A relationship between the antioxidant and antimicrobial activity was
also observed. Regarding the non- phenolic compounds, methyl-E-
cinnamate (benzenic group) showed higher activity than linalool
(acyclic alcohol). The results show that the essential oils of basil have
a number of additional attributes and applications for the nutraceutical
industry in addition to their aroma and avor impact.
Acknowledgements
We thank the New Jersey Agricultural Experiment Station, the
Rutgers School of Environmental and Biological Resources, the Rutgers
New Use Agriculture and Natural Plant Products program (aesop.rut-
gers.edu/ newuseag), the New Jersey Farm Bureau for their support
of this research project, and support by NIFA HATCH project reports
(NJAES 12131 and 1005685), We also thank the New Jersey culinary
herb growers such as the Dalponte Family Mr. Mint Farm and the Gra
Brothers.
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