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Fattahi2019 Effects of Cadmium and Lead On Seed Germination, Morphological Traits, and
Fattahi2019 Effects of Cadmium and Lead On Seed Germination, Morphological Traits, and
a
Department of Horticultural Science, Tarbiat Modares University (TMU), P.O. Box 14115-336, Tehran, Iran
b
Department of Food Science and Technology, Tarbiat Modares University (TMU), P.O. Box 14115-336, Tehran, Iran
Keywords: The negative impact of contaminated soil with heavy metals on plant and human health is an important global
Environmental pollution concern. The aim of this study was to explore the influence of cadmium (Cd) and lead (Pb) on seed germination,
Heavy metals morphological traits, and essential oil (EO) composition of sweet basil (Ocimum basilicum L.). Two months prior
Medicinal plant to the experiment, soils pre-treated using Cd (0, 5, 10, 20) and Pb (0, 100, 200, 400) in mg kg soil−1. Seeds were
Stress
sown in the pots containing the contaminated soil under greenhouse conditions at 26 ± 6 °C and 60–70 %RH.
Vegetable crop
The amount and composition of EO were determined using Gas chromatography–mass spectrometry (GC-MS).
The contaminated soil had a negative impact on seed germination, leaf area, and flowering, stem growth and
plant dry mass. The extracted EO yield was varied (P > 0.05) among the applied treatments from 0.28 to 0.39%
(v/w). The GC-MS analysis of the EO identified the presence of 38 compounds. The major identified components
of the EO were included estragole (18.80–50.32%), 2, 6- octadienal (3.2–11.95%), caryophyllene oxide
(0.98–10.69%), caryophyllene (0.42–5.70%), phthalic acid (1.43–47.89%), and geranial (2.60–9.43%). The
canonical correspondence analysis (CCA) showed a positive correlation between the plant height and phthalic
acid contents. In conclusion, sweet basil cultivation in the Cd and Pb contaminated soils could cause undesirable
effects on the seed germination and morphological traits, but might be have a positive influence on the EO yield,
composition and phytoremediation of the soil.
⁎
Corresponding author.
E-mail address: arzani_k@modares.ac.ir (K. Arzani).
https://doi.org/10.1016/j.indcrop.2019.111584
Received 1 February 2019; Received in revised form 16 June 2019; Accepted 17 July 2019
0926-6690/ © 2019 Elsevier B.V. All rights reserved.
B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
2011). Furthermore, Zheljazkov et al. (2006) found that increasing Besides, for uniform distribution of heavy metals, the soil was passed
copper (Cu) concentration (from 20 to 60 & 150 mg L−1) significantly several times through the 2 mm sieve. The moisture content of the soil
reduced plant dry mass, plant height (PH), and oil yield in dill plants as was adjusted at 60–65% field capacity (FC). Then, the soil was in-
compared to the control. They indicated that the concentration of cubated for two months at 24 ± 4 °C. Thereafter, the soil of each
150 mg L−1 was phytotoxic and inhibited dill plant growth. Moreover, treatment was placed into the black plastic pots containing 8–10 kg dry
plant leaf area and dry weight of the aerial parts in peppermint were soil and the seeds were sown in 1 cm depth. A total amount of 15 plants
reduced under Cd and Pb treatments as compared to the control plant per pot were allowed to grow while the remaining plants were re-
(Amirmoradi et al., 2012). As stated by Kranner and Colville (2011), moved. The pots were then kept under the greenhouse conditions at
heavy metals can induce toxicities at different growth stages of the 26 ± 6 °C temperature and 60–70% RH. The pots were irrigated in a
plants starting from germination. According to them, heavy metals such day intervals with purified tap water based on 80% FC. Therefore, the
as Cd, Cu, and arsenic (As) can inhibit seed germination even at the low plants were left to grow under the aforementioned conditions for three
concentrations. Likewise, Peralta et al. (2001) indicated that Lucerne months.
seed germination was very susceptible to the presence of heavy metals
as all the germination indices reduced under heavy metal treatments.
The effect of contaminated soil with different Cd and Pb levels on 2.2. Germination experiment
the leaf colorophyl pigments and photochemical efficiency of photo
system ІІ (Fv/Fm ratio) of sweet basil was evaluated and reported by The germination of sweet basil seeds was prepared for evaluation
Fattahi et al. (2017). This study was performed to evaluate the impact using Cd and Pb treatments in the different experiment, under the la-
of different Cd and Pb levels on seed germination and some morpho- boratory conditions. The basil seeds were first disinfected with sodium
physiological traits as well as EO composition of the sweet basil. In hypochlorate for 20 min and then were placed on a tissue paper in the
addition, the canonical correlation of the morphological traits and the Petri dishes each containing 20 seeds. The tissue papers were wetted
oil compositions under Cd and Pb treatments were examined. with different Cd (0, 1, 2, 4, 8, & 16 mg L−1) and Pb (0, 5, 10, 20, 40, &
80 mg L−1) solution concentrations (Table 1). Petri dishes were sealed
with cellophane covers to prevent water loss and seed infestations, then
2. Materials and methods placed in a germinator at 24 °C and 64% RH. The germinated seeds
were counted every day, so the minimum radicle length emergance
2.1. Experimental setup (RE) at 2 mm was considered as the germination count. The seeds
germination counts were continued for 20 days. The quantity and
This experiment was conducted under greenhouse conditions at the quality traits for seed germination were evaluated as follows (Fattahi
Department of Horticultural Science, Tarbiat Modares University et al., 2011):
(TMU), Iran. Sweet basil seeds of a local population were purchased Germination start (GS) = T2 – T1 (1), where T1 is the day of seed
from Pakan Seed Co., Isfahan, Iran. The suitable fertile soil with the sowing, and T2 is the day of beginning of first seed germination;
following physical and chemical characteristics was used in the ex- Germination percentage = (n/N)×100 (2), where n denotes to the total
periment. The soil texture was silty loam with 23, 29 and 48% clay, number of germinated seeds and N shows the number of total seeds
sand and silt, respectively. The pH of the soil was 7.6 with 3.28 dS m−1 sowed; Also, the Germination rate (GR) was calculated using the fol-
EC and 0.07%, 0.68%, and 199 mg.kg-1 and 7.5 mg.kg-1 for nitrogen lowing equation as described by Burgert and Burnside (1972):Germi-
(N), carbon (C), potassium (K) and phosphorus (P), respectively. The nation rate (GR) = ∑(number of germinated seeds till n-1)/n (3), where n
concentration of cadmium and lead in the soil was 0.49 and 0.97 mg.kg- is incubation days.
1
respectively.
Note that, two months prior to seed sowing, different concentrations
of Cd (0, 5, 10 and 20 mg kg−1 dry soil) and Pb (0, 100, 200 and 2.3. Determination of morphological traits
400 mg kg−1 dry soil) were uniformly applied into the soil. The related
codes for the applied treatments presented in Table 1. In order to pre- Plants were grown for three months and thereafter various morpho-
pare the contaminated soil for the experiment, nitrate salts of Cd and Pb physiological traits were measured. Morphological traits were recorded
were dissolved in distilled water (DW) and sprayed into the soil. at the flowering stage, including plant height (PH, in cm), the sec-
ondary stems length (SSL, in cm), leaf length (LL, in cm), leaf width
Table 1 (LW, in cm), root and shoot fresh and dry weights (RFW, SFW, RDW, &
The related codes for the applied treatments on sweet SDW, in gr), internodes length (IL, in cm), flowering stem length (FSL,
basil (Ocimum basilicum L.). in cm), collar diameter (CD, in mm), stem diameter (SD, in mm), and
leaf area index (LAI in cm2). The leaf area for each treatment was
Treatments Related Codes
calculated using a digital leaf area meter (Nguy-Robertson et al., 2012).
Cadmium 0 Control
Cadmium 5 Cd5
Cadmium 10 Cd10 2.4. Soil and plant analysis for cadmium and lead
Cadmium 20 Cd20
Lead 0 Control
The pre-contaminated soil for the experiment was analyzed for Cd
Lead 100 Pb100
Lead 200 Pb200 and Pb before treatments applications. Also, at the end of the experi-
Lead 400 Pb400 ment and after destructive plants harvest, the pot soil was re-analyzed
Cadmium 1 Cd1 for the amount of Cd and Pb based on the DTPA (diethylene triamine
Cadmium 2 Cd2
penta-acetic acid) method that described previously by Beckett (1989).
Cadmium 4 Cd4
Cadmium 8 Cd8 Note that, for Cd and Pb measurements in the leaves and roots, plants
Cadmium 16 Cd16 materials were first oven dried at 60 °C for 72 h and then ground
Lead 5 Pb5 powdered. Tissue powder (0.5 g) was digested in 25 ml nitric acid
Lead 10 Pb10 (65%), and Cd and Pb concentrations were determined according to the
Lead 20 Pb20
method described by Sekabira et al. (2011) using atomic absorption
Lead 40 Pb40
Lead 80 Pb80 spectrometry (Flow Injection Analysis System 400AA 100; Perkin-
Elmer, Waltham, MA, USA).
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B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
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B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
Table 2
Means comparisons of morphological traits (Mean values of four replications ± standard error of the mean) of sweet basil (Ocimum basilicum L.) under cadmium (Cd)
and lead (Pb) concentrations (mg. kg−1 soil).
R Characteristics* Unit Control Cd5 Cd10 Cd20 Pb100 Pb200 Pb400 CV (%)
1 PH cm 27.07 ± 0.49 ab 25.98 ± 0.14b 27.20 ± 0.35ab 28.41 ± 1.38ab 26.18 ± 0.99ab 28.75 ± 1.05a 26.27 ± 1.12ab 6.21
2 SSL cm 2.14 ± 0.52c 3.84 ± 0.79bc 5.00 ± 0.55ab 4.18 ± 0.22ab 4.48 ± 0.78ab 4.27 ± 0.65ab 5.79 ± 1.83a 30.82
3 IL cm 5.93 ± 0.44ab 3.82 ± 0.18b 4.21 ± 0.41ab 5.59 ± 0.47ab 7.90 ± 3.38a 5.24 ± 0.63ab 6.24 ± 0.48 ab 32.46
4 FSL cm 4.98 ± 0.18b 9.60 ± 0.33a 8.73 ± 0.22a 8.93 ± 1.28a 8.65 + 0.13 a 8.33 ± 0.81a 7.92 ± 1.54a 22.00
5 LL cm 2.35 ± 0.02ab 1.73 ± 0.01c 1.84 ± 0.06c 2.50 ± 0.15ab 2.01 ± 0.13bc 2.43 ± 0.22ab 2.55 ± 0.31a 15.66
6 LW cm 1.30 ± 0.02a 0.88 ± 0.01b 0.95 ± 0.04b 1.29 ± 0.09a 1.00 ± 0.07a 1.26 ± 0.12a 1.30 ± 0.12a 14.59
7 CD mm 1.21 ± 0.05c 1.37 ± 0.04bc 1.58 ± 0.19abc 1.97 ± 0.07a 1.77 ± 0.19ab 1.79 ± 0.15a 1.89 ± 0.16a 16.18
8 SD mm 0.91 ± 0.02c 1.09 ± 0.01c 1.38 ± 0.22ab 1.54 ± 0.07a 1.47 ± 0.22ab 1.42 ± 0.12ab 1.61 ± 0.14a 19.11
9 SDW gr 15.2 ± 0.95a 9.50 ± 1.31bc 7.90 ± 0.29c 10.77 ± 0.52b 8.92 ± 0.39bc 10.35 ± 0.90bc 9.07 ± 1.31bc 18.34
10 LAI cm2 211.25 ± 1.31a 198.00 ± 3.62b 191.25 ± 1.93b 190.25 ± 3.52b 203.75 ± 4.15b 202.50 ± 3.52b 201 ± 2.19b 10.37
*
PH = plant height; SSL = secondary stems length; IL = internode length; FSL = flowering stem length; LL = leaf length; LW = leaf width; CD = collar diameter;
SD = stem diameter; SDW = shoot dry weight; LAI = leaf area index.
Cd and Pb in EO chemical compounds in peppermint reduced leaf area 3.4. The percentage of EO
and dry weight of the aerial parts in Cd and Pb treatments in com-
parison with control (Amirmoradi et al., 2012). The EOs isolated among the samples in this experiment was yellow
in color and showed over the range of 0.28-0.39% (v/w). In addition,
the amount of EO was varied among the different treatments
3.3. Soil and plant analysis for cadmium and lead (P > 0.01). The highest and lowest amount of EO was belonged to the
Cd20 (0.39%) and control samples (0.28%), respectively. An increase in
Results showed that by increasing Cd and Pb concentrations in the Cd and Pb concentration enhanced the EO yield. The average EO per-
soil, the higher content of these metals was observed in the leaf and root centage for different treatments shown in Fig. 3. Padalia et al. (2017)
samples (Fig. 2a, 2b). In addition, Cd and Pb content in the leaf were reported 0.53% EO yield that obtained from the basil at flowering stage.
higher than in the root samples. Also, lead concentration in plant tissues The report from the other experiment indicated that, the effect of 80%
was higher than Cd concentration (Fig. 2). It has been reported that the FC water stress in comparison with the 100% FC resulted to the increase
world allowable standard levels of Cd and Pb in basil leaves are 0.1 and in the basil EO content, while the 60% FC treatment reduced EO yield
0.3 mg.kg−1 plant dry weight, respectively (Sharma and Prasad, 2010). extract (Sirousmehr et al., 2014).
In the present research, Cd and Pb concentrations in the leaf and root
tissues of basil plants were higher than the standard. So, it is not sug- 3.5. EO composition
gesting for fresh consumption, those basil plants that grown under
heavy metals polluted soils. The higher concentrations of Cd and Pb in The identified chemical components of sweet basil are provided in
the leaf sample tissues that recorded from this experiment will suggest Table 3. In the studied samples about 38 of these components re-
possible using basil plant for the purpose of phytoremediation of con- presented about 90.14–97.74 % of the oil (Table 3). A sample GC-MS
taminated soils. It has been shown in the other experiment that some of chromatogram of sweet basil and mass spectra of some components are
medicinal plants can be used for phytoremediation of contaminated shown in Fig. 4. Oxygenated monoterpene and sesquiterpene hydro-
soils (Zheljazkov, et al. 2006). The high uptake rates of arsenic by carbons formed the major part of the studied EO yield. Ladwani and
different basil species (O. basilicum, O. tenuiflorum and O. gratissimum) Salman (2018) reported the similar results regarding oxygenated
showed high arsenic concentration in the leaves and roots, suggested monoterpene (60.76%) and sesquiterpene hydrocarbons. In another
that basil plantation might be a suitable plant for arsenic remediation study, monoterpene containing compounds were found as the pre
(Siddiqui et al., 2013). dominant components of basil EO (more than 70%). In addition, Telci
et al. (2006) evaluated the variation of basil oil chemical composition
Fig. 2. Cadmium (Cd) and lead (Pb) concentrations in soil, leaf and root tissues of basil plants in Cd treatments (A) and Pb treatments (B) after destructive plants
harvest. Mean values of four replications ± standard error of the mean.
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B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
Table 3
Essential oil components percentage of sweet basil (Ocimum basilicum L.) grown under cadmium (Cd) and lead (Pb) concentrations (mg. kg−1 soil).
R Compounds Empirical Formula RI Control Cd5 Cd10 Cd20 Pb100 Pb200 Pb400
1 α- Thujene C10H16 845 0.84 0.61 0.52 0.23 0.93 0.71 0.52
2 α-Pinene C10H12O 928 2.46 0.51 0.41 0.25 0.61 0.53 0.39
3 1- Octan-3-ol C8H16O 963 0.84 0.27 0.14 0.12 0.14 0.22 0.32
4 6-Methyl-5- hepten C8H14O 995 0.49 0.35 0.21 t 0.22 0.12 t
5 β-myrcene C10H16 981 t 0.58 t t 1.21 t t
6 β-pinene C10H16 984 0.54 0.2 t 0.10 1.32 0.25 0.20
7 L-Limonene C10H16 1028 t 0.2 0.12 t 1.14 0.13 t
8 1,8- Cineole C10H18O 1032 0.22 0.1 t 0.12 1.13 t 0.15
9 Octanal C8H16O 1005 0.19 0.12 0.10 0.10 1.70 0.11 t
10 Octanol C8H18O 1010 0.10 0.21 0.25 0.33 0.40 0.58 0.36
11 Linalool C10H18O 1099 0.18 0.42 0.25 0.38 0.20 0.32 0.38
12 Fenchone C10H16O 1093 t – t t 2.12 0.38 t
13 Heptadienal C7H10O 1124 t – 0.1 t 2.18 0.21 0.15
14 Estragole C10H12O 1213 23.69 24.87 41.99 18.80 27.76 28.78 50.32
15 2,6- Octadienal C8H12O 1232 6.93 11.95 11.20 4.06 4.26 14.76 3.2
16 Nerol C10H18O 1234 2.48 2.27 2.19 1.68 2.59 2.42 2.20
17 Fenchole C10H18O 1242 t 0.10 0.15 0.18 0.15 – –
18 Cyclohexanedim ethanol C8H16O2 1254 0.22 0.25 – – t t –
19 Geraniol C10H18O 1252 2.32 4.52 3.21 2.53 2.13 0.91 1.93
20 Geranial C10H16O 1274 9.43 8.95 6.92 2.60 6.24 8.54 6.31
21 Neryl acetate C12H20O2 1366 0.22 1.89 0.62 0.85 0.45 0.25 0.44
22 Geranyl acetat C12H20O2 1368 0.39 0.97 0.46 0.61 0.61 0.55 0.48
23 α-Copaene C15H24 1369 0.54 0.91 t t t 0.62 t
24 Methyl eugenol C11H14O2 1442 2.47 2.37 3.29 0.45 0.94 1.50 1.79
25 Caryophyllene C15H24 1451 5.70 3.98 4.67 1.21 1.79 3.20 0.42
26 β- Farnesene C12H20O2 1459 – 0.68 0.67 0.21 0.24 0.92 1.32
27 β- Selinene C15H24 1491 2.28 0.94 1.16 0.23 1.42 0.83 0.33
28 Germacrene D C15H24 1495 0.66 t 1.06 t 1.45 0.42 t
29 β- Bisabolene C15H24 1498 0.96 0.48 2.40 t – 0.88 0.49
30 γ-Cadinene C15H24 1514 t 0.16 0.21 0.25 1.31 0.33 1.44
31 Cis-α-Bisabolene C15H24 1544 2.58 2.15 1.85 1.33 0.32 1.81 0.45
32 Caryophyllene oxide C15H24O 1584 7.39 10.69 7.41 0.99 1.21 0.98 9.28
33 Farnesole C15H26O 1592 t 0.21 0.41 1.67 1.21 0.42 0.65
34 Neophytadiene C20H38 1605 0.52 0.65 1.2 3.13 1.75 1.85 1.92
35 Humulene epoxide II C15H24O 1610 2.66 1.26 t 0.32 t 0.21 2.27
36 Oxabicyclo dodeca C15H24O 1625 0.21 2.41 1.30 1.12 0.56 1.77 2.15
37 2-Pentadecanone C15H30O 1642 0.17 0.22 0.14 0.12 0.12 t t
38 Phthalic acid C8H6O4 1680 20.06 8.32 1.43 47.89 20.33 14.57 0.42
Monoterpene hydrocarbons – – 1.38 1.59 0.52 0.45 4.6 0.71 0.52
Oxygenate monoterpene – – 40.60 42.74 55.24 26.87 44.72 42.26 61.8
Sesquiterpene hydrocarbons – – 12.72 12.51 12.65 1.81 4.50 8.09 2.71
Oxygenate Sesquiterpene – – 3.43 10.90 8.63 4.22 3.10 3.38 14.35
Diterpede hydrocarbons 0.52 0.65 1.20 3.13 1.75 1.85 1.92
Others – – 39.09 26.38 17.80 55.38 31.47 32.79 8.98
Total (%) – – 97.74 94.77 96.04 91.86 90.14 90.08 90.28
Eo quantity % (v/w) – – 0.28 0.34 0.34 0.39 0.30 0.32 0.38
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B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
Fig. 4. Gas chromatography–mass spectrometry (GC-MS) peaks and mass spectra spectrum of some essential oil (EO) major components of sweet basil (Ocimum
basilicum L.).
6
B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
(Yadav et al., 2013). The safe range of 40–87% chavicol (estragole) in Table 4
basil oil has been reported by Clarke (2008). Basil plants containing Canonical coefficients, Eigen-values and variance for three canonical corre-
22–88% estragole can be effectively used for aromatherapy (Clarke, spondence analysis (CCA) sets between phytochemicals with morphological
2008). In addition, estragole reported that has anti insect activity, and traits of sweet basil (Ocimum basilicum L.).
can be used as a natural insecticide (Ling Chang et al., 2009). Traits CCA sets of Morphological factors
In present research, all other EO compounds are listed in Table 3. In
addition, the obtained data showed that the raise in the Cd con- 1 2 3
centration in the soil was led to the increase of the compounds such as Essential oil compounds
linalool, octanol, nerol, neryl acetate, γ-cadinene, caryophyllene oxide, Estragole 1.61 −0.56 −1.09
farnesol, and neophytadiene. Besides, it decreased compounds likeα- Nerol 0.84 1.57 −1.48
thujene, α-pinene, 1, 8- cineole, octanal, geranial, methyl eugenol, β- 2,6- Octadienal 0.21 3.80 −2.36
Geraniol 0.38 1.73 4.24
Selinene, cis-α-bisabolene, humulene epoxide II, and phthalic acid
Geranial −0.34 0.86 2.50
(Table 3). Furthermore, increasing Pb concentration enhanced the Methyl eugenol 0.41 2.91 1.15
compounds such as octanol, linalool, nerol, neryl acetate, car- Caryophyllene −1.13 4.92 1.13
yophyllene oxide, neophytadiene, and oxabicyclododeca while de- Cis-α-Bisabolene −1.40 4.25 0.57
Caryophyllene oxide 3.66 2.54 1.14
creasing other compounds like α-pinene, 1- Octan-3-ol, 6-methyl-5-
Phthalic acid −3.00 0.13 −1.75
hepten, β-pinene, 1,8- cineole, octanal, geranial, geranyl acetat, methyl Control 0.20 0.01 0.04
eugenol, caryophyllene, β- selinene, germacrene D, β- bisabolene, cis-α- Cd5 0.12 0.17 0.08
bisabolene, and phthalic acid compared the control treatment (Table 3). Cd10 0.26 0.10 0.01
Prasad et al. (2011) examined the influence of heavy elements on basil Cd20 −0.46 −0.12 −0.17
Pb100 −0.04 −0.14 0.01
oil found that treatment of Cr (chromium), Cd, Pb, and Ni (nickel) in-
Pb200 −0.01 0.07 −0.03
creased methyl chavicol whereas decreasing the amount of linalole in Pb400 0.32 −0.11 0.03
sweet basil. The Cr treatment in Ocimum tenuiflorum L. increased the Morphological factor
biosynthesis of the eugenol (Amirmoradi et al., 2012(. However, Plant Height −0.53 −0.01 −0.75
Sub Stems Length 0.59 −0.27 −0.10
Siddiqui et al. (2013) found no specific process on arsenic treatment in
Internodes’ Length −0.23 −0.84 −0.11
Ocimum tenuiflorum L., Ocimum basilicm L., and Ocimum gratissimum L. Flowering Stem Length 0.68 0.04 −1.46
Leaf Length −0.06 −0.58 −1.12
Leaf Width −0.19 −0.47 −0.97
3.6. Principal component analysis (PCA)
Collar Diameter 0.51 −0.84 −2.12
Stem Diameter 0.71 −0.96 −2.23
The PC1 and PC2 scatter plots were applied to monitor the phyto- Dry Weight Shoot −1.01 0.03 1.43
chemical distance (Fig. 5). The scatter plots showed the phytochemical Leaf Area Index −0.07 −0.31 0.25
distances among the samples within the plot, influenced by their re- Eigen-value 0.031 0.009 4.750
Variance (%) 76.3 23.7 0.001
lationships, the studied populations were divided into three groups. The
EO of the control, Pb100, and Cd20 formed an individual treatment
separated from other samples and characterized by higher phthalic acid
presented a positive amount of nerol (0.84) while showing a negative
(38). In treatment, Cd5 and Pb200 formed other isolated groups with
amount of phthalic acid (-3.00) (Table 4). In other words, the basil
higher 2, 6- octadienal (15). The rest of the EO compounds formed in
plant with higher SSL and FSL had high nerol versus low phthalic acid
another group (Fig. 5).
contents. In the second canonical sets, treatments with low IL, SD, and
CD had higher caryophyllene and cis-α-bisabolene contents. The third
3.7. The CCA among morphological and EO traits canonical is demonstrated in Table 4. The scatter plots of CC1 and CC2
were employed to determine more associations between the morpho-
The CCA was employed to explore the influence of morphological logical and phytochemical traits. As it is illustrated in Fig. 6, a positive
characters on the phytochemical composition. The first studied cano- correlation was found between PH of the morphological trait and
nical sets of EO to morphological traits (more than 76%) indicated that phthalic acid contents. Estragole positively correlated with plants
the treatments with positive and notable values of SSL and FSL
Fig. 5. Classification of seven treatments applied on sweet basil (Ocimum basilicum L.) based on the essential oil (EO) chemical composition with biplot of first two
components.
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B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
Fig. 6. Canonical correspondence analysis biplot in the percentage of the major essential oil (EO) components with the morphological traits of sweet basil (Ocimum
basilicum L.).
containing higher SSL. In addition, methyl eugenol, 2, 6- octadienal, Burgert, K., Burnside, O., 1972. Optimum temperature for germination and seedling de-
geraniol, and nerol had a negative correlation with the IL (Fig. 6). velopment of black nightshade. Res. Rep. North Cent. Weed Control Conf 56.
Chaiyarat, R., Suebsima, R., Putwattana, N., Kruatrachue, M., Pokethitiyook, P., 2011.
Effects of soil amendments on growth and metal uptake by Ocimum gratissimum
4. Conclusion grown in Cd/Zn-contaminated soil. Water Air Soil Pollut. Focus. 214, 383–392.
Chalchat, J.-C., Özcan, M.M., 2008. Comparative essential oil composition of flowers,
leavesand stems of basil (Ocimum basilicum L.) used as herb. Food Chem. 110,
The growth of sweet basil was significantly affected by the con- 501–503.
taminated soil with Cd and Pb. In addition, sweet basil cultivation in Clarke, S., 2008. Composition of Essential Oils and Other Materials. Churchill
the contaminated soils and in the fields that are irrigated with waste Livingstone, pp. 123–229.
Davies, N., 1990. Gas chromatographic retention indices of monoterpenes and sesqui-
water can cause undesirable effects on the seed germination and also terpenes on methyl silicon and Carbowax 20M phases. J. Chromatogr. A 503, 1–24.
plant morpho- physiological traits. In such situation, plants producing Deng, B., Yang, K., Zhang, Y., Li, Z., 2016. Can heavy metal pollution defend seed ger-
with higher SSL and early flowering which are not suitable for fresh mination against heat stress? Effect of heavy metals (Cu2+, Cd2+ and Hg2+) on
maize seed germination under high temperature. Environmental Polution 216,
consumption. However, Basil cultivation in contaminated soils by
46–52.
heavy metals could have a positive influence on phyto- remediation. Fattahi, M., Nazeri, V., Sefidkon, F., Zamani, Z., Palazon, J., 2011. The effect of pre-
The amount of EO yield produced under the stresses of heavy metals, sowing treatments and light on seed germination of Dracocephalum kotschyi Boiss:
and the EO components that have a high correlation with the amount of an endangered medicinal plant in Iran. Hort. Environ. Biotechnol. 52 (6), 559–566.
Fattahi, B., Nazeri, V., Kalantari, S., Bonfill, M., Fattahi, M., 2016. Essential oil variation
Cd and Pb contaminations. in wild-growing populations of Salvia reuterana Boiss. Collected from Iran: using
GC–MS and multivariate analysis. Ind. Crops Prod. 81, 180–190.
Declaration of Competing Interest Fattahi, B., Arzani, K., Souri, M.K., Barzegar, M., 2017. Effect of cadmium and lead stress
on the chlorophyll fluorescence and chlorophyll pigments in Ocimum basilicum L. First
International Horticultural Science Conference of Iran (IrHC2017) 225 Abstracts
There are no conflicts of interest. Book, P-98 (189).
Filip, S., Pavlić, B., Vidović, S., Vladić, J., Zeković, Z., 2017. Optimization of microwave-
assisted extraction of polyphenolic compounds from Ocimum basilicum by response
Acknowledgments surface methodology. Food Anal. Methods 10, 2270–2280.
Jayasinghe, C., Gotoh, N., Aoki, T., Wada, S., 2003. Phenolics composition and anti-
We would like to thank Tarbiat Modares University (TMU) for fi- oxidant activity of sweetbasil (Ocimum basilicum L.). J. Agric. Food Chem. 51,
4442–4449.
nancial support. This work was supported under PhD Student Grant Juliani, H., Simon, J.E., Ramboatiana, M.R., Behra, O., Garvey, A., Raskin, I., 2002.
Program by TMU. In addition, greenhouse and laboratory facilities Malagasy aromatic plants: essential oils, antioxidant and antimicrobial activities.
provided by Pomology Lab., Department of Horticultural Science at XXVI International Horticultural Congress: The Future for Appl Res Med Aromat
Plants. 629, 77–81.
TMU are acknowledged.
Kranner, I., Colville, L., 2011. Metals and seeds: biochemical and molecular implications
and their significance for seed germination. Environ. Exp. Bot. 72, 93–105.
References Ladwani, A.M., Salman, M., 2018. Chemical composition of Ocimumbasilicum L. essential
oil from different regions in the kingdom of Saudi Arabia by using gas chromato-
graphy mass spectrometer. J. Med. Plant Res. 6, 14–19.
Adams, R.P., 2007. Identification of Essential Oil Components by Gas Lermen, C., Morelli, F., Gazim, Z.C., da Silva, A.P., Gonçalves, J.E., Dragunski, D.C.,
Chromatography–mass Spectrometry. Allured Publishing Corporation, Coral Stream, Alberton, O., 2015. Essential oil content and chemical composition of Cymbopogon
IL, USA. citratus inoculated with arbuscular mycorrhizal fungi under different levels of lead.
Al Abbasy, D.W., Pathare, N., Al-Sabahi, J.N., Khan, S.A., 2015. Chemical composition Ind. Crops Prod. 76, 734–738.
and antibacterial activity of essential oil isolated from Omani basil (Ocimum basilicum Li, W., Zhang, Y., Wang, M.D., Shi, Y., 2005. Biodesulfurization of dibenzothiophene and
Linn.). J. Trop. Med. 5, 645–649. other organic sulfur compounds by a newly isolated Microbacterium strain ZD-M2.
Amirmoradi, S., Moghaddam, P.R., Koocheki, A., Danesh, S., Fotovat, A., 2012. Effect of FEMS Microbiol. Lett. 247, 45–50.
cadmium and lead on quantitative and essential oil traits of peppermint (Mentha Ling Chang, C., Kyu Cho, I., Li, Q.X., 2009. Insecticidal activity of basil oil, trans-anethole,
piperita L.). Not Sci Biol. 4, 101–109. estragole, and linalool to adult fruit flies of Ceratitis capitata, Bactrocera dorsalis, and
Apelbaum, A., Yang, S.F., 1981. Biosynthesis of stress ethylene induced by water deficit. Bactrocera cucurbitae. J. Econ. Entomol. 102, 203–209.
Plant Physiol. 68, 594–596. Lone, M.I., He, Z.-L., Stoffella, P.J., Yang, X.-E., 2008. Phytoremediation of heavy metal
Azzaz, N., Elsherbiny, E., El-Khateeb, A., 2018. Chemical composition and fungicidal polluted soils and water: progresses and perspectives. J. Zhejiang Univ. Sci. B 9,
effects of Ocimum basilicum essential oil on Bipolaris and Cochliobolus species. 210–220.
JKUAT. 6, 11–18. Majer, B.J., Tscherko, D., Paschke, A., Wennrich, R., Kundi, M., Kandeler, E., Knasmüller,
Beckett, P.H.T., 1989. The use of extractants in studies on trace metals in soils, sewage S., 2002. Effects of heavy metal contamination of soils on micronucleus induction in
sludges, and sludge-treated soils. Adv. Soil Sci. 9, 143–176. Tradescantia and on microbial enzyme activities: a comparative investigation. Mutat.
8
B. Fattahi, et al. Industrial Crops & Products 138 (2019) 111584
Res. Genet. Toxicol. Environ. Mutagen. 515, 111–124. Sharma, S., Prasad, F., 2010. Accumulation of lead and cadmium in soil and vegetable
Munzuroglu, O., Geckil, H., 2002. Effects of metals on seed germination, root elongation, crops along major highways in Agra (india). J. Chem. 7 (4), 1174–1183.
and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Bull. Siddique, K., Loss, S., Thomson, B., Saxena, N., 2003. Cool season grain legumes in
Environ. Contam. Toxicol. 43, 203–213. dryland Mediterranean environments of Western Australia: significance of early
Munzuroğlu, Ö., ZENGİN, F.K., Yahyagil, Z., 2008. The abscisic acid levels of wheat flowering. Manage Agri Drought. 151–161.
(Triticum aestivum L. Cv. Çakmak 79) seeds that were germinated under heavy metal Siddiqui, F., Krishna, S.K., Tandon, P., Srivastava, S., 2013. Arsenic accumulation
(Hg++, Cd++, Cu++) stress. J. Fac. Pharm. Gazi. 21, 1–7. inOcimum spp. and its effect on growth and oil constituents. Acta Physiol. Plant. 35,
Nguy-Robertson, A., Gitelson, A., Peng, Y., Viña, A., Arkebauer, T., Rundquist, D., 2012. 1071–1079.
Green leaf area index estimation in maize and soybean: combining vegetation indices Sirousmehr, A., Arbabi, J., Asgharipour, M.R., 2014. Effect of drought stress levels an-
to achieve maximal sensitivity. Agron. J. 104 (5), 1336–1347. dorganic manures on yield, essential oil content and some morphological char-
Padalia, R., Verma, R., Upadhyay, R., Chauhan, A., Singh, V., 2017. Productivity and acteristics of sweet basil (Ocimum basilicum). Biol. 8, 880–885.
essential oil quality assessment of promising accessions of Ocimum basilicum L. From Tanrıkulu, G.İ., Ertürk, Ö., Yavuz, C., Can, Z., Çakır, H.E., 2018. Chemical compositions,
north India. Ind. Crops Prod. 97, 79–86. antioxidant and antimicrobial activities of the essential oil and extracts of Lamiaceae
Peralta, J., Gardea-Torresdey, J., Tiemann, K., Gomez, E., Arteaga, S., Rascon, E., Parsons, family (Ocimum basilicum and Thymbra spicata) from Turkey. IJSM. 4, 340–348.
J., 2001. Uptake and effects of five heavy metals on seed germination and plant Telci, I., Bayram, E., Yılmaz, G., Avcı, B., 2006. Variability in essential oil composition of
growth in alfalfa (Medicago sativa L.). Bull. Environ. Contam. Toxicol. 66, 727–734. Turkish basils (Ocimum basilicum L.). Biochem. Syst. Ecol. 34, 489–497.
Prasad, A., Kumar, S., Khaliq, A., Pandey, A., 2011. Heavy metals and arbuscular my- Varasteh, F., Arzani, K., Barzegar, M., Zamani, Z., 2012. Changes in anthocyanins in arils
corrhizal (AM) fungi can alter the yield and chemical composition of volatile oil of of chitosancoated pomegranate (Punica granatum L. Cv. Rabbab-e-Neyriz) fruit during
sweet basil (Ocimum basilicum L.). Biol Fert Soil. 47, 853. cold storage. Food Chem. 130, 267–272.
Rodrigues, L.B., Martins, A.O., Cesário, F.R., Castro, F.F., de Albuquerque, T.R., Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: A review of
Fernandes, M.N., Silva, B.A., Júnior, L., Costa, J., Coutinho, H., 2016. Anti-in- sources, chemistry, risks and best available strategies for remediation. International
flammatory and antiedematogenic activity of the Ocimum basilicum essential oil and Scholarly Research Network, ISRN Ecology 2011, 20. https://doi.org/10.5402/2011/
its main compound estragole: in vivo mouse models. Chem-Biol Interact. 257, 14–25. 402647. Article ID 402647.
Sekabira, K., Origa, H.O., Basamba, T.A., Mutumba, G., Kakudidi, E., 2011. Application of Yadav, N.P., Meher, J.G., Pandey, N., Luqman, S., Yadav, K.S., Chanda, D., 2013.
algae in biomonitoring and phytoextraction of heavy metals contamination in urban Enrichment, development, and assessment of Indian basil oil based antiseptic cream
stream water. Int. J. Environ. Sci. 8 (1), 115–128. formulation utilizing hydrophilic-lipophilic balance approach. Biomed Res. Int.
Shahid, M., Dumat, C., Khalid, S., Schreck, E., Xiong, T., Niazi, N.K., 2017. Foliar heavy 2013, 1–9.
metal uptake, toxicityand detoxification in plants: a comparison of foliar and root Zheljazkov, V.D., Craker, L.E., Xing, B., 2006. Effects of Cd, Pb, and Cu on growth and
metal uptake. J. Hazard. Mater. 325, 36–58. essential oil contents in dill, peppermint, and basil. Environ. Exp. Bot. 58, 9–16.