Iron-urea nano-complex improves bioactive compounds in essential oils of Ocimum basilicum L.

Scientia Horticulturae 265 (2020) 109222

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Iron-urea nano-complex improves bioactive compounds in essential oils of Ocimum basilicum L.

T

Vahid Tavallalia,*, Vahid Rowshanb, Hossein Gholamic, Shadi Hojatia a

Department of Agriculture, Payame Noor University (PNU), P.O. Box: 19395-3697 Tehran, Iran Department of Natural Resources, Fars Agricultural and Natural Resources Research and Education Center, AREEO, Shiraz, Iran c Department of Horticultural Sciences, Faculty of Agriculture, Shiraz University, Shiraz, 7144165186, Iran b

A R T I C LE I N FO

A B S T R A C T

Keywords: Nitrogen Iron Nanoparticle Sweet basil Antioxidant activity Antimicrobial potential

This study was conducted to evaluate the influences of [Fe-urea] nano-complex on phytochemical compounds, antioxidant activity and antimicrobial potential of the essential oil of sweet basil (Ocimum basilicum L.). Three different levels (0, 0.1 and 0.2 %) of Fe-EDDHA, urea, and Fe-urea nano-complex were sprayed at 1) four leaved stage and 2) previous the flowering inception of sweet basil seedlings. The highest amount of the major compounds in the essential oil, epi-α-cadinol (27.09 ± 2.5 %) and trans-α-bergamotene (14.93 ± 1.77 %), were achieved by the application of 0.2 % n[Fe-urea]. Application of 0.2 % n[Fe-urea] in comparison with control treatment decreased the n-Decane quantity significantly (by 99.1 %). Amongst the flavonoids and phenolic compounds, rosmarinic acid was the prevailing compounds in basil’s essential oils. The highest amount of rosmarinic acid (5.81 ± 0.18 mg g−1) was found in 0.2 % [Fe-urea] nano-complex treatment. The highest antioxidant activity (21.98 ± 1.3 mg AAE g−1) was found in n[Fe-urea] treated plants. Also, The lowest minimal inhibitory concentration (MIC) for Bacillus subtilis, Staphylococcus aureus, Escherichia coli, Salmonella typhimurium, Aspergillus niger, and Candida albicans were 0.042 ± 0.008, 0.016 ± 0.003, 0.238 ± 0.024, 0.166 ± 0.025, 0.101 ± 0.021 and 0.129 ± 0.011 mg mL-1 of essential oil derived from treated basils with 0.2 % n[Fe-urea] foliar spraying, respectively. The results revealed that nanoparticles can provide new prospects in medicinal plant production and the improvement of pharmaceutical properties of medicinal plants.

1. Introduction Major part of the Iran’s soils has been calcareous, with crop product in soils due to high pH, deficiency of micronutrients and lack of sufficient organic material has always been faced with some difficulties. Alkaline pH and high concentration of calcium ion have caused some of the nutrients that can be absorbed by pH to be insoluble and unusable for the plant (Jafari et al., 2012). Despite increasing soil pH, the large amount of bicarbonate ion produced in calcareous soils, reduces the ability to absorb of micronutrients by the plant, especially iron (Hejazi and Kafashi Sedghi, 2000). Iron is one of the essential and immobile elements. This element in the partitioning the elements necessary for the growth and development of plants, based on biochemical function involves in a group which plays an important role in the reactions of electron transfer (ET). It is one of the most important elements in oxidation-reduction (redox) reactions of plants (Taiz and Zeiger, 2010). Iron is very important in enzymatic system and plants respiration so that is the part of catalytic group of lots of redox enzymes such as

⁎

catalase and peroxidase (Sun et al., 2007). Also, the iron plays a role in forming cytochrome, nonheme iron proteins and azote stability (Evans and Sorger, 1966). Nitrogen as one of the main structural elements in many important molecules including proteins, nucleic acids, some of hormones and chlorophyll play a significant role in plant nutrition (Nijjar, 1990). Efficient use of nitrogen fertilizers to improving productivity is an important goal in all agricultural systems (Dong et al., 2002). Urea is a white crystalline solid containing 46 % of nitrogen which is used as one of the common and available sources for foliar application (Shamsudin et al., 2012). Among nitrogenous compounds, urea is the most common form of nitrogen for spraying due to rapid absorption, inexpensive price and high solubility (Bondada et al., 2001). It has been revealed that the cuticular membrane is 10–20 times more permeable to urea than other nitrogen sources, including nitrate and ammonium (Yamada et al., 1965). Therefore, the leaves are able to absorb urea during the foliar application. Foliar application is considered as a quick way to add water-soluble

Corresponding author. E-mail address: [email protected] (V. Tavallali).

https://doi.org/10.1016/j.scienta.2020.109222 Received 17 October 2019; Received in revised form 20 January 2020; Accepted 22 January 2020 0304-4238/ © 2020 Elsevier B.V. All rights reserved.

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fertilizers to the plant leaves (Solanki et al., 2015). Foliar application is very efficient when the root of the plant is incapable to absorb sufficient quantities of mineral elements from the soil (Fageria, 2009). Foliar application of mineral elements is very useful not only for the arrival of the plant to the higher performance, but also to improve the nutrient deficiencies and to improve the macro- and microelements in the plant (El-Sheikh et al., 2007). The foliar application is used as a method to provide complementary amounts of macro- and microelements, plant growth regulation (PGR), and other important materials. Given to the type of plant species, type and concentration of minerals applied, application time and plant growth phase, the plants’ response to the foliar application is positive, negative or neutral (Fageria, 2009). The usability of nanotechnology in different fields of agricultural sciences and natural resources is much more extensive than other sciences. Nanotechnology is a science of change, manipulation, and placing particles in Nano-sizes in order to build human used tools. As we approach the nano scales, the ratio of the surface to the volume of materials increases; in this case, the number of molecules existed in the surface increases compared to the inner particles; this factor causes: a) Those on the surface are more active, b) The ability of bonding increases in these molecules and c) In the case of the catalytic property existence, this property would increase. Higher plants interact strongly with their surrounding environment, so they are expected to be influenced by nanoparticles (Castiglione et al., 2011). On the nano scale, most atoms are on the surface of the substance that do not have the conditions and limitations of inner atoms. The development of nanotools and nano-materials can provide new applications in plant biotechnology (Scrinis and Lyons, 2007). Nano agricultural chemicals enclosed should have all the necessary features, including effective concentration (solubility, stability and high efficiency), controlled diffusion time in response to the specific stimuli, increased targeted activities and less toxicity associated with easy-use (Green and Beestman, 2007; Moraru et al., 2003; Tsuji, 2001). This study was an attempt to obtain new data on the efficiency and superiority of[Fe-urea] nanocomplex on phytochemical compounds, antioxidant activity and antimicrobial potential of the essential oil of sweet basil.

Fig. 1. The TEM image of Fe-urea nano-complex.

thinning and previous the flowering inception of plants, they were divided in 7 groups; control (deionized water), plants sprayed with 0.1 or 0.2 % Fe-EDDHA, plants sprayed with 0.1 or 0.2 % Fe-urea nano complex and plants sprayed with 0.1 or 0.2 % urea. The fertilizers were obtained from a knowledge-based organization named “Zist Nano Fanavaran Atiyeh Pajooh” located at the Fars Science and Technology Park (Shiraz, Iran). The size of Fe-urea nano particles were determined by the transmission electron micrographs (TEM) (100 kV Philips, EM208) (Fig. 1). Using Tensor II FTIR spectrometer, the FTIR spectra were obtained (Fig. 2). Basils were collected at full bloom stage, and afterward were dried in the shade for 5 days.

2. Materials and methods

2.2. Extraction of EOs

2.1. Plant material

The Essential oils were obtained from dry aerial parts of sweet basil by hydrodistillation for 3 h using a clevenger type device (British pharmacopoeia, 1988). The extracted EOs were then dried over anhydrous sodium sulphate (Na2SO4) and were preserved at 3−5 °C until analysis.

To study the effects of Fe-EDDHA, urea and Fe-urea nano complex foliar application on growth parameters, phytochemical compounds, antioxidant activity and antimicrobial potential of the essential oil of sweet basil (Ocimum basilicum L.), a factorial experiment was set up in a randomized complete design (RCD) in a greenhouse located at the 29º 31´ N; 52º 31´ E in Shiraz, Iran. Plants were grown under natural light in the greenhouse (approximately 800–1000 μmol m−2 s−1 PAR-photosynthetically active radiation) with a 12 h photoperiod and temperature between 23−26 °C. The soil samples were air-dried. Then, they were passed through a 2-mm sieve and mixed uniformly. Physical and chemical characteristics of the soil were measured by standard methods (Table 1). 50 mg P and N kg−1 soil as KH2PO4, NH4NO3 were applied to the soil, while 5 mg Mn, Zn and Cu kg−1 soil as MnSO4.H2O, ZnSO4.7H2O and CuSO4.5H2O were applied, respectively. Seeds of sweet basil were collected from an herbal garden of Bazrco Company in Tehran, Iran. They were potted in 7 L plastic pots filled with soil. Pots were irrigated twice a week using deionized water. After

2.3. Analysis of the EOs The analyses of essential oil volatile components were determined by gas chromatography (GC) and gas chromatography-mass spectrometry (GC–MS). The gas chromatography analysis was used with Agilent GC series 7890A, G3440A and Flame Ionization Detector (FID). Analytical GC was carried out in a autosampler (Agilent, series 7683B) and HP-5 fused silica capillary column (30 m ×0.32 mm i.d.; film thickness 0.25 μm, 5 % phenylmethylpolysiloxane). To volatile extracts analyses by the gas chromatography–mass spectrometry device (Model 5975 C), and equipped with a HP-5MS fused silica capillary column (30 m × 0.25 mm i.d.; film thickness 0.25 μm) joint with 5975-C mass

Table 1 Physiochemical properties of the soil in the experimental site. soil texture

pH

ECe

CEC

Organic matter

N

K

P

Zn

Fe

sandy loam

7.1

dS m−1 1.3

Cmc kg−1 11

g kg−1 8.8

(%) 0.08

mg kg−1 61

12

1.5

1.01

2

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number of control and absorption number of samples: [(A540blank ˗ A540sample)/A540blank]. 2.5.3. TBARS scavenging assay Determination of TBARS scavenging activities of the essential oils were performed by using the MDA test (Kavoosi and Rowshan, 2013). The reaction mixture (200 μL) contained 100 μL of the essential oils (00.5 mg mL−1 in DMSO) and 100 μL of the MDA (0.1 mM in acetic acid pH = 4). Then the samples were incubated at a temperature of 36 °C for 120 min. After adding one volume of thiobarbituric acid (0.3 mM in acetic acid pH = 4), the solutions were incubated at 90 °C for 60 min. Eventually, samples’ absorptions were read at a wavelength of 532 nm. The percentage of TBARS scavenging was then calculated by using the following formula: [(A532blank ˗ A532sample/A532blank].

Fig. 2. The FTIR spectra of urea and Fe-urea nano-complex.

2.5.4. H2O2 scavenging assay The percentage of H2O2 scavenging was measured based on Kavoosi and Rowshan (2013) at the wavelength of 230 nm. The reaction mixture (200 μL) contained 100 μL of the essential oils (0–0.5 mg mL−1 in DMSO) and 100 μL of the H2O2 (100 mM in 200 mM phosphate buffer pH = 7.4). In the next step, the samples were incubated at a temperature of 36 °C for 75 min. The percentage of H2O2 scavenging was then calculated using the formula: [(A230blank ˗ A230sample)/A230blank].

spectrometer was carried. Helium was selected as carrier gas with the ionization voltage of 70 eV. The Retention Indices (RIs) of essential oil volatile components were determined based on Retention Times (RT) for n-alkanes (C8-C25) under temperature-programmed and the same chromatographic conditions (Adams, 2007). 2.4. Identification of phenolics and flavonoids of the extracts

2.5.5. Antifungal and antibacterial assay Minimum inhibitory concentration (MIC) of essential oils was characterized by using the microdilution procedure suggested by Clinical and Laboratory Standards Institute (CLSI, 2012) by means of a spectrophotometer at the wavelength of 640 nm. For this purpose, by two foodborne fungi [Aspergillus niger PTCC 5010 (ATCC 9142) and Candida albicans PTCC 5027 ATCC 10231], two foodborne Gram-negative bacteria [and Salmonella typhimurium PTCC 1609 and Escherichia coli PTCC 1330 (ATCC 8739)] and two foodborne Gram-positive bacteria [Staphylococcus aureus PTCC 1112 (ATCC 6538) and Bacillus subtilis PTCC 1023 (ATCC 6633)] were used. Fungi and bacteria were collected from the Persian Type Culture Collection (PTCC), Tehran, Iran. Suspended fungi and bacteria strains in Luria–Bertani (LB) media were tuned to 0.6 McFarland standards at 640 nm (108 CFU/ml). Then, densities were diluted to 105 (CFU/ml) with Luria–Bertani. In the next step, to 500 μL essential oils, 500 μL of suspensions of fungi and bacteria was added. The samples were shaken with incubating at 36 °C for 24 h. Positive control included in Ketoconazole, Gentamicin and Ampicillin for fungi, Gram-negative and Gram-positive bacteria, respectively. Also, a medium without fungi and bacteria and a medium without essential oils but with bacteria as sterile and growth control were considered, respectively. Measuring the minimum inhibitory concentration (MIC) was calculated by using the following formula: [(A640blank - A640sample/A640blank]×100

The standards for all phenolic compounds (rosmarinic acid, gallic acid, carvacrol, cinnamic acid and ferulic acid) and flavonoids (catechin, kaempferol, luteolin, rutin, and quercetin) were used based on the Sigma-Aldrich brand. To measure the amounts of phenolics compounds and flavonoids by the HPLC device (Agilent 1200 series) was used. The UV detector was set at a wavelength of 280 and 320 nm with an oven temperature of 30 °C. 20 μL of the dissolved extract was injected into Zorbax eclipse (XDB) C18 column (4.6 × 5 μm i.d.; ×150 mm film thickness). Methanol: formic acid 1 % was selected as mobile phase with the flow rate of 1 ml min−1. Accordingly, gradient elution program was selected from (10:90); next it was planned to reach (25:75) during 10 min; shifting to (60:40) in 20 min. In the next step, the ratio was selected on (70:30) which was kept isocratic for 40 min. 2.5. Antioxidant activity of the EOs 2.5.1. ROS scavenging assay Determination of antioxidant activity was performed by using free radical 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging potential according to Burits et al. (2001). Therefore 30 μL of 0–0.5 mg mL−1 essential oils in DMSO was mixed with 230 μL of 120 mmol L−1 DPPH in methanol at room temperature for 30 min. Samples’ absorptions was measured at 515 nm wavelength with EL × 808 absorbance microplate reader, BioTek Instruments, Inc., USA. Concentration that can neutralize free radicals by 50 % (IC50 is a parameter for comparing the antioxidant activity of the essential oils) was calculated and reported by the nonlinear regression plots using MATLAB (MathWorks®, USA). Measuring the percentage of ROS scavenging was calculated by using the following formula and the use of ascorbic acid as standard (purchased from the brand MERCK, Germany). [(A515sample‒A515blank)∕A515control]× 100

2.5.6. Statistical analysis Data are presented as mean values ± standard deviation (S.D.) from at eight replications. Data were analyzed by using Duncan’s multiple range test (P < 0.05) by SPSS, version 20 for Windows. 3. Results and discussion 3.1. FTIR spectra analysis

2.5.2. NO scavenging assay The method proposed by Kavoosi and Rowshan (2013) was used for measuring NO scavenging activities of the essential oils by means of a spectrophotometer (Shimadzu 1601, Japan) at wavelength of 540 nm. Briefly, to 100 μL of the essential oils (0–0.5 mg mL−1 in DMSO), 250 μL of sodium nitrite (0.02 mg mL−1 in 100 mM sodium citrate) was added, then the samples was kept for 120 min at 36 °C. In the next step, to this mixture, 600 μL of Griess reagent was added. The percentage of RNS scavenging was calculated as the difference between absorption

The ultrasound assisted reaction of Fe(NO3)3 and urea in 1:3 mol ratio lead to synthesis of iron-urea nano-complex. Same as pure urea ligand, the chelate FTIR spectra display an absorption template in the region of 4000−400 cm−1. The CO] spectrum has transferred from 1755 to 1682 cm−1. The CNe frequency has transferred from 1448 to 1285 cm−1. The NHe frequency has transferred from 3278 to 3305 cm−1. Compared to free urea, the NeH deformation band in nanocomplex moved toward lower frequency about 1555 cm−1. According 3

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nitrogen plays an important role in developing the new cells containing essential oil, channels, glands, and glandular trichomes. The researchers reported that the application of nitrogen increases the secretory glandular of essential oil in peppermint leaves (Marotti et al., 1994). The reason for the increase of the essential oil glands is production and the consumption of simple carbohydrates and consequently development of the leaf surface. Therefore, nitrogen increases vegetative growth, the development of the leaves and consequently producing essential oil (Brown, 2003). Essential oils contain the terpeneid compounds that their constructor units such as isopentenyl pyrophosphate and dimethylallyl pyrophosphate have an urgent need for ATP and NADPH, and with regard to the subject that the nitrogen and iron are essential for the formation of recent compounds, and ultimately have improved essential oil yields. The positive effect of foliar application of nano iron chelate on the essential oil yields of cress (Salarpour et al., 2013), peppermint (Zehtab-Salmasi et al., 2008) and chamomile (Nasiri et al., 2010) has been reported. Given to the effect of iron on plant growth, one of the reasons for the increase of photosynthetic activity is the role of this element in structure of the chloroplast, which leads to the production of more essential oil glands in leaves (Evans, 2009). It seems that micronutrients increase the essential oil yields through their effect on dry matter and not the turgor pressure (Ziaeyan and Malakouti, 1998).

Table 2 Essential oil yields and variables of vegetative growth of sweet basil after the treatments of iron and nitrogen sources. Treatments

Fe-EDDHA 0.1 Fe-EDDHA 0.2 n[Fe-urea] 0.1 n[Fe-urea] 0.2 Urea 0.1 % Urea 0.2 % Control

% % % %

Essential oil yields (g 100 g−1)

Plant height (mm)

−1

Plant weight (g plant )

0.47 ± 0.011e 0.51 ± 0.013 cd 0.52 ± 0.013 cd 0.56 ± 0.014a 0.49 ± 0.011cde 0.53 ± 0.012bc 0.33 ± 0.006f

310 ± 2d 313 ± 2 cd 317 ± 2b 322 ± 3a 311 ± 2d 315 ± 3bc 214 ± 2e

266 ± 3f 279 ± 3e 292 ± 3c 311 ± 4a 285 ± 3d 306 ± 5b 170 ± 2 g

Data are mean ± standard deviation of eight replications. † Means followed by the same letter within a column are not significantly different according to Duncan’s multiple range test at P < 0.05.

to these shifting frequencies, it is concluded that the urea has coordinated with iron through nitrogen atom of NeH group and oxygen atom of C]O group. 3.2. Essential oil yields and variables of vegetative growth Results showed that the application of iron and urea sources significantly increased the essential oil yields and variables of vegetative growth compared to the control treatment (p < 0.05) (Table 2). The application of 0.2 % Fe-urea nano complex caused the highest amount of plant weight (311 ± 4 g plant−1) which was 82.94 % more than the control treatment. According to our results, the application of this treatment can increase the plant height of sweet basil by 50.46 %, compared to the control treatment (Table 2). The effect of nitrogen on raising the vegetative growth is caused by a change in the balance of plant hormones in vegetative parts. The consumption of nitrogen by decreasing the ratio of abscisic acid to gibberellin leads to an increase in plant’s vegetative growth (Marschner, 2012). Nitrogen is involved in synthesis of critical compounds such as amino acids, proteins and nucleic acids, and is an important component of chlorophyll and rubisco molecules. Nitrogen caused to produce carbohydrates and thus increased performance by increasing carbon-uptake level and developing aerial parts (Salardini, 2003; Tso, 2005). Iron role in the nitrogen fixation and the activity of some enzymes such as catalase, peroxidase and cytochrome oxidase have been well studied (Sun et al., 2007). Given to the role of iron in the biosynthesis of hormones, nitrogen uptake and photosynthesis (Hänsch and Mendel, 2009), increasing the vegetative growth and biomass production are expected. In general, there is a close relationship between the content of nitrogen and iron in leaves and the photosynthetic capacity (Taiz and Zeiger, 2010). There has been observed the effect of foliar application of iron fertilizers in increasing vegetative growth of basil (El-Gendy et al., 2001), anis (Pirzad et al., 2013), corn (Whitty, 1998) and coriander (Said-Al Ahl and Omer, 2009) due to the role of iron in the biosynthesis of chlorophyll and the concentration of indole acetic acid (IAA). Also, there was a direct correlation between nitrogen consumption and increase in biomass production in basil (Yassen et al., 2003; Biesiada and Kuś, 2010; Arabaci and Bayram, 2004), moldavian dragonhead (Safikhani, 2007), oregan (Barreyro and Ringuele, 2005) and lemon balm (Abbaszadeh et al., 2009), which is in consistent with the results of this research. Our results showed that the application of foliar spraying of 0.2 % Fe-urea nano complex resulted in higher essential oil yields (0.56 ± 0.01 g 100g−1) in sweet basil (Table 2). In previous studies, the positive effect of nitrogen has been reported on improving the essential oil yields in Ocimum basilicum (Kndeel et al., 2002), Anethum graveolens (Bist et al., 2000), Nigella sativa (El-Sayed et al., 2000) and Artemissia annua L. (Özgüven et al., 2008). The increase in essential oil yields due to the nitrogen consumption can be attributed to the fact that the

3.3. Chemical components of essential oil Thirty-eight essential oil compounds were identified in the control treatment of the sweet basil’s essential oil (Table 3). The result shows that the main essential oil components of sweet basil in the control treatment were characterized by a high content of epi-α-cadinol (16.67 %), followed by n-Decane (13.39 %), linalool (10.45 %), and bornyl acetate (9.34 %) (Table 3). Foliar application of iron and urea sources considerably has changed chemical components of essential oil. After application of urea (0.2 and 0.1 %), n[Fe-urea] (0.2 and 0.1 %) and FeEDDHA (0.2 and 0.1 %), thirty-nine, fifty-nine, twenty, fifty-eight, fiftynine and fifty-nine compounds were identified in the essential oil, respectively. The major sesquiterpenes in essential oil after foliar spraying were epi-α-cadinol and trans-α-bergamotene. Interestingly, the lowest number of sesquiterpenes in essential oil realized in 0.2 % Fe-urea nano-complexes treatment. Furthermore, the highest amount of epi-αcadinol (27.09 ± 2.5 %) and trans-α-bergamotene (14.93 ± 1.77 %) in the essential oil of basil was achieved by the application of 0.2 % n[Feurea]. Terpenoids have antimicrobial, antioxidant and antitumor activity, and effect on cardiovascular and central nervous systems (QuintansJúnior et al., 2010). Also, terpenoids are widely used as drugs, fragrances, flavors, and colors (Misawa, 2011). Terpenoids play an important role in the redox reactions (lateral chains of ubiquinone and plastoquinone), structure of the membrane (sterols and hopanoids), carotenoid and chlorophyll lateral chains and the plant hormone (Phillipson, 2007). The amount of the essential oil of basil varies from 0.5 to 1.5 percent depending on the climatic conditions of the growth area (Omidbaigi, 2014). Based on available references, the essential oils chemotypes of Persian basil is full of methyl chavicol, linalool, epi-αcadinol and trans-α-bergamotene (Sajjadi, 2006; Tavallali et al., 2018). In addition to basil, epi-α-cadinol is an alcoholic compound that has been found in essential oil of Cinnamomum osmophloem. It has an antiinflammatory effect (Tung et al., 2008). It is also found in the essential oil of Taiwania cryptomerioides, which has anti-mite effect against Dermatophagoides pteronyssinus and Dermatophagoides farina haghes (Chang et al., 2001). In a research by Rustaiyan et al. (2006), α-cadinol was identified as the dominant component of essential oil of Ballota aucheri. Our results showed that the application of 0.2 % n[Fe-urea] in comparison with control treatment decreased the n-Decane quantity significantly (99.1 %) from 13.399 ± 1.92 % to 0.12 ± 0.01 %. nDecane is an alkane hydrocarbon with the chemical formula C10H22 4

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Table 3 Effect of iron and nitrogen sources on concentrations of chemical compounds (%) identified in essential oil of sweet basil. No.

Compound

Class

RI

Fe-EDDHA 0.1%

Fe-EDDHA 0.2%

n[Fe-urea] 0.1%

n[Fe-urea] 0.2%

Urea 0.1%

Urea0.2%

Control

1 2 3 4 5

α-Pinene Sabinene β-Pinene Myrcene n-Decane

MH MH MH MH OT

933 973 977 991 1000

0.153 ± 0.01b 0.527 ± 0.04b 0.669 ± 0.04b 1.161 ± 0.12b 1.513 ± 0.14d

0.578 ± 0.05a 0.966 ± 0.07a 1.577 ± 0.10a 2.451 ± 0.17a 1.275 ± 0.10e

0.037 ± 0.004c 0.109 ± 0.02c 0.194 ± 0.02c 0.578 ± 0.04c 0.388 ± 0.03f

ND ND ND ND 0.121 ± 0.01 g

0.620 ± 0.05a 0.957 ± 0.07a 1.600 ± 0.14a 2.449 ± 0.22a 2.560 ± 0.17c

ND ND ND ND 4.072 ± 0.46b

6

α-Phellandrene

MH

1006

0.021 ± 0.002b

0.052 ± 0.004a

ND

0.064 ± 0.004a

ND

7

α-Terpinene

MH

1017

0.026 ± 0.004c

0.045 ± 0.004b

ND

0.058 ± 0.006a

ND

ND

8

p-Cymene

MH

1024

0.637 ± 0.05a

ND

0.023 ± 0.002b

ND

ND

9 10 11 12

Limonene 1,8-Cineole (Z)-β-Ocimene Benzene acetaldehyde

MH OM MH OM

1028 1031 1036 1044

6.657 ± 0.71a 3.116 ± 0.12e 0.059 ± 0.005b 0.019 ± 0.002a

0.008 ± 0.0006c 3.092 ± 0.34b 4.343 ± 0.15d 0.079 ± 0.05b 0.023 ± 0.002a

ND 5.449 ± 0.31c ND ND

1.161 ± 0.15d 5.235 ± 0.25c 0.106 ± 0.01a 0.023 ± 0.002a

ND 5.955 ± 0.30b ND ND

2.188 ± 0.13c 7.349 ± 0.69a ND ND

13 14 15 16 17

(E)-β-Ocimene γ-Terpinene cis-Sabinene hydrate Terpinolene Linalool

MH MH OM MH OM

1046 1058 1066 1089 1099

1.005 ± 0.16b 0.061 ± 0.004c 0.222 ± 0. 02a 0.224 ± 0.03b 9.921 ± 1.25a

1.776 ± 0.18a 0.098 ± 0.008b 0.077 ± 0.005c 0.417 ± 0.05a 5.377 ± 0.51c

0.003 ± 0.0005c 0.005 ± 0.0005d 0.001 ± 0.0003c 0.251 ± 0.02e 3.321 ± 0.15e 0.012 ± 0.002c 0.003 ± 0.0006b 0.549 ± 0.04b 0.023 ± 0.001d 0.139 ± 0.02b 0.121 ± 0.02c 7.980 ± 0.67b

ND ND ND ND 13.399 ± 1.92a ND

ND ND ND ND 5.254 ± 0.55c

1.888 ± 0.15a 0.127 ± 0.02a 0.091 ± 0.007c 0.388 ± 0.03a 7.784 ± 0.70b

ND ND ND ND 7.895 ± 0.70b

18

1-Octen-3-yl acetate

OTacetate

1112

0.095 ± 0.007a

0.045 ± 0.005c

ND

Camphor δ-Terpineol Terpinen-4-ol α-Terpineol

OM OM OM OM

1145 1167 1177 1189

0.069 ± 0.005b 0.057 ± 0.004c 0.043 ± 0.003a 0.464 ± 0.03 cd

0.052 ± 0.005b 0.093 ± 0.006b 0.024 ± 0.002b 0.723 ± 0.05c

ND ND ND 1.758 ± 0.18a

0.065 ± 0.006bc 0.010 ± 0.003c 0.086 ± 0.006b 0.043 ± 0.005a 0.600 ± 0.04 cd

ND

19 20 21 22

0.081 ± 0.007ab 0.147 ± 0.02a 0.147 ± 0.02a 0.056 ± 0.004a 1.060 ± 0.22b

0.374 ± 0.04c ND ND ND 10.450 ± 1.28a ND

23 24

n-Dodecane Octanol acetate

OT OTacetate

1200 1212

0.342 ± 0.03c 0.840 ± 0.06bc

0.326 ± 0.04c 0.968 ± 0.06ab

0.373 ± 0.04c 0.558 ± 0.04c

0.342 ± 0.05c 1.134 ± 0.11a

1.521 ± 0.11a 1.029 ± 0.09ab

1.589 ± 0.10a 0.217 ± 0.02d

25 26

Trans-Carveol Linalyl acetate

MH OMacetate

1222 1256

0.124 ± 0.02c 0.047 ± 0.004a

0.205 ± 0.03b 0.019 ± 0.004c

0.201 ± 0.02b ND

Bornyl acetate δ-Elemene α-Terpinyl acetate

OMacetate SH OMacetate

1286 1337 1350

3.395 ± 0.21c 0.217 ± 0.02b 0.202 ± 0.02ab

0.020 ± 0.004d 0.040 ± 0.005ab 3.331 ± 0.17c 0.265 ± 0.02b 0.153 ± 0.01bc

ND ND

27 28 29

0.134 ± 0.02c 0.027 ± 0.003bc 3.917 ± 0.19c 0.419 ± 0.04a 0.214 ± 0.02a

3.674 ± 0.22c ND ND

5.106 ± 0.44b 0.239 ± 0.03b 0.121 ± 0.01 cd

2.398 ± 0.15d 0.230 ± 0.03b 0.148 ± 0.01c

30 31

Eugenol α-Copaene

OM SH

1358 1375

5.411 ± 0.53d 0.146 ± 0.02a

6.854 ± 0.63c 0.103 ± 0.01b

6.700 ± 0.62c ND

β-Cubebene β-Elemene Methyl eugenol

SH SH OM

1390 1392 1406

0.131 ± 0.02b 5.806 ± 0.49bc 0.365 ± 0.03d

0.157 ± 0.02a 6.168 ± 0.56b 0.416 ± 0.05d

0.147 ± 0.01ab 5.178 ± 0.49c 0.991 ± 0.07b

0.079 ± 0.006c 4.543 ± 0.34d 0.330 ± 0.02d

35 36 37

Cis-α-Bergamotene (E)-Caryophyllene β-Gurjunene

SH SH SH

1415 1419 1429

0.076 ± 0.005b 0.337 ± 0.03b 0.023 ± 0.004c

0.070 ± 0.005b 0.649 ± 0.05a 0.057 ± 0.004a

ND 0.185 ± 0.01c ND

trans-α-Bergamotene

SH

1436

9.327 ± 1.13 cd

10.027 ± 1.20c

10.476 ± 1.21c

7.978 ± 0.77d

39 40 41 42 43

α-Guaiene (Z)-β-Farnesene α-Humulene (E)-β-Farnesene allo-Aromadendrene

SH SH SH SH SH

1439 1443 1453 1458 1463

0.596 ± 0.04 cd 0.162 ± 0.01b 1.630 ± 0.08c 0.398 ± 0.02c 0.988 ± 0.07b

0.979 ± 0.08a 0.159 ± 0.01b 2.920 ± 0.13a 0.331 ± 0.03d 0.929 ± 0.06b

0.821 ± 0.06b 0.219 ± 0.02a 1.747 ± 0.10b 0.453 ± 0.03b 1.398 ± 0.09a

0.065 ± 0.005b 0.357 ± 0.02b 0.032 ± 0.003bc 10.081 ± 1.16 cd 0.547 ± 0.05 cd 0.152 ± 0.01b 1.808 ± 0.09b 0.320 ± 0.02d 0.630 ± 0.04d

0.112 ± 0.01a 0.345 ± 0.04b ND

38

0.107 ± 0.01a 0.436 ± 0.03b 0.046 ± 0.003ab 12.604 ± 1.45b

ND 6.850 ± 0.61a 0.466 ± 0.04 cd ND ND ND

7.693 ± 0.72b 0.064 ± 0.007bc 0.092 ± 0.006c 4.911 ± 0.32 0.919 ± 0.07bc

9.382 ± 1.20a 0.094 ± 0.008b

32 33 34

9.499 ± 1.22a 0.065 ± 0.005bc 0.099 ± 0.008c 5.497 ± 0.42c 2.105 ± 0.11a

9.345 ± 1.14a 0.138 ± 0.01c 0.089 ± 0.006d 4.966 ± 0.37d 0.047 ± 0.003c

0.628 ± 0.06c 0.220 ± 0.02a 1.700 ± 0.10bc 0.511 ± 0.04a 0.773 ± 0.06c

44 45

Germacrene D Bicyclogermacrene

SH SH

1481 1496

4.284 ± 0.36de 2.193 ± 0.12 cd

6.107 ± 0.42c 3.552 ± 0.16a

7.540 ± 0.51b 2.768 ± 0.14b

0.509 ± 0.04d 0.081 ± 0.006c 1.404 ± 0.08d 0.225 ± 0.01e 0.693 ± 0.05 cd 3.971 ± 0.25e 1.849 ± 0.08d

46 47 48 49

trans-β-Guaiene α-Bulnesene γ-Cadinene β-Sesquiphellandrene

SH SH SH SH

1499 1506 1514 1521

0.226 ± 0.02a 1.653 ± 0.09 cd 4.087 ± 0.27c 0.930 ± 0.07b

0.217 ± 0.02ab 2.141 ± 0.10a 4.952 ± 0.28a 0.710 ± 0.06d

50 51 52 53 54

δ-Cadinene α-Cadinene (E)-Nerolidol Germacrene D-4-ol Spathulenol

SH SH OS OS OS

1524 1537 1564 1575 1577

0.279 ± 0.02f 0.074 ± 0.005b 0.504 ± 0.04c 0.041 ± 0.003c 0.040 ± 0.003

0.541 ± 0.04bc 0.079 ± 0.006b 0.806 ± 0.07a 0.129 ± 0.01a 0.059 ± 0.005bc

14.937 ± 1.77a ND ND 2.581 ± 0.14 ND ND

ND ND ND 0.349 ± 0.04d

4.367 ± 0.34d 2.305 ± 0.11c

0.256 ± 0.03a 1.850 ± 0.09bc 4.396 ± 0.24b 0.584 ± 0.04e

8.583 ± 0.62a 3.055 ± 0.15ab ND ND 4.801 ± 0.27a ND

0.145 ± 0.01c 1.320 ± 0.08e 4.030 ± 0.22c 0.837 ± 0.07bc

5.618 ± 0.38c 2.204 ± 0.10 cd 0.164 ± 0.02c 1.525 ± 0.09d 4.909 ± 0.29a 1.066 ± 0.08a

0.572 ± 0.04b 0.104 ± 0.01a 0.584 ± 0.04b ND 0.062 ± 0.005b

0.474 ± 0.03d ND ND ND ND

0.516 ± 0.06 cd 0.049 ± 0.005c 0.500 ± 0.05c 0.075 ± 0.006b 0.062 ± 0.005b

0.863 ± 0.07a 0.077 ± 0.007b 0.337 ± 0.04d 0.121 ± 0.01a 0.115 ± 0.02a

ND ND ND 0.479 ± 0.04 cd 0.772 ± 0.05b 0.951 ± 0.06ab 0.256 ± 0.02a ND

0.182 ± 0.02bc 1.185 ± 0.07f 3.221 ± 0.19d 0.808 ± 0.07 cd 0.391 ± 0.03e 0.050 ± 0.004c 0.286 ± 0.02e ND ND

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Table 3 (continued) No.

Compound

Class

RI

Fe-EDDHA 0.1%

Fe-EDDHA 0.2%

n[Fe-urea] 0.1%

n[Fe-urea] 0.2%

Urea 0.1%

Urea0.2%

Control

55 56

1,10-di-epi-Cubenol epi-α-Cadinol

OS OS

1615 1641

1.764 ± 0.12e 18.509 ± 2.11d

2.034 ± 0.12d 19.349 ± 2.15d

2.420 ± 0.14c 24.898 ± 2.26b

2.135 ± 0.13d 18.925 ± 2.12d

3.047 ± 0.16b 22.912 ± 2.17c

2.109 ± 0.11d 16.679 ± 1.95e

57 β-Eudesmol OS 58 α-Cadinol OS 59 β-Bisabolol OS Monoterpene Hydrocarbons Oxygenated Monoterpenes Sesquiterpenes Hydrocarbons Oxygenated Sesquiterpenes Others Total

1650 1654 1686

0.957 ± 0.06d 0.820 ± 0.06c 0.187 ± 0.02c 11.324 29.936 33.114 22.822 2.776 99.972

1.164 ± 0.08c 0.992 ± 0.07c 0.220 ± 0.02c 11.273 20.387 40.922 24.753 2.664 100

1.325 ± 0.09ab 1.209 ± 0.09b 0.512 ± 0.04a 1.903 23.129 42.594 31.01 1.364 100

3.904 ± 0.21a 27.091 ± 2.50a 1.413 ± 0.10a 1.413 ± 0.09a ND ND 23.301 41.281 33.821 1.597 100

1.291 ± 0.09b 1.236 ± 0.08b 0.265 ± 0.03c 9.646 27.73 32.867 24.489 5.175 99.907

1.468 ± 0.11a 1.588 ± 0.10a 0.376 ± 0.02b 0.201 27.118 36.84 29.964 5.878 100

1.011 ± 0.08d 1.198 ± 0.07b 0.228 ± 0.01c 2.818 33.008 27.539 21.511 15.122 100

RI: Retention Index.; ND: Not Detected.; MH: Monoterpene Hydrocarbons.; OM: Oxygenated Monoterpenes.; SH: Sesquiterpenes Hydrocarbons., OS: Oxygenated Sesquiterpenes.; OT: Others. Data are mean ± standard deviation of eight replications. † Means followed by the same letter within a row are not significantly different according to Duncan’s multiple range test at P < 0.05.

compounds are also responsible for the antibacterial properties of the extracts and essential oils (Zhang et al., 2009). Previous studies have shown that application of micronutrient nano-fertilizers led to an increase in flavonoid and phenolic contents of plants (Tavallali et al., 2017; Mahmoud and Taha, 2018). Our results showed that the application of iron and urea sources causes an increase in the contents of carvacrol in extract (Table 4). Previous studies have shown that this compound has various medicinal properties. It is antioxidant (Jaberian et al., 2013), antiviral (Chaieb et al., 2007), insecticidal (Pete et al., 2012), anti-inflammatory (Damasceno et al., 2014), antifungal (Suntres et al., 2015), cardioprotective (Friedman, 2013), antidiabetics (Bayramoglu et al., 2014) and antibiotic (Varel, 2002).

that is known as an environmental polluter. However, its toxicological properties have not been thoroughly investigated (HSDB, 2002). Previously, the positive effect of nitrogen on chemical composition and yield of essential oil of thyme has been reported (Omidbaigi et al., 2000). Previous studies have shown that iron effectively led to an increase in secondary metabolites, especially the terpenes (Pourebrahimi et al., 2014). It has been reported that foliar application of iron lead to an increase in essential oil yields of basil (Said-Al Ahl and Mahmoud, 2010). 3.4. Phenolic and flavonoid compounds In this study, five flavonoids (catechin, kaempferol, luteolin, rutin, and quercetin) and five phenolic compounds (rosmarinic acid, gallic acid, carvacrol, cinnamic acid and ferulic acid) were detected in the extract of treated basils (Table 4). Interestingly, carvacrol, kaempferol, luteolin, rutin and ferulic acid were not identified in control treatment. When various Fe-EDDHA, Fe-urea nano complexes and urea were applied, the content of both flavonoids and phenolic compounds rose considerably in basil’s extract compared to the control treatment. In between the flavonoids and phenolic compounds, rosmarinic acid was the prevailing compounds in basil’s extracts. The highest amount of rosmarinic acid (5.81 ± 0.18 mg g−1) was found in 0.2 % Fe-urea nano complex treatment followed by 0.1 % Fe-urea nano complex treatment which increased the rosmarinic acid to 5.62 ± 0.22 mg g−1, provided the lowest amount (2.43 ± 0.12 mg g−1) obtained in untreated plants. Iron deficiency in some plants causes a decrease in the phenolic content (Pestana et al., 2010). However, there is a little information about the role of iron in the production of secondary metabolites (Yeritsyan and Economakis, 2001). The use of iron nanoparticles in plants seems to be more efficient than conventional fertilizers. Perhaps one of the reasons for the rise of phenolic compounds in the effect of iron and nitrogen is the rise of the production of the photosynthesis substances and additional carbon allocation to the shikimic acid pathway (Nguyen et al., 2010). An investigation of the local varieties of the basil in Iran showed that the plant has a very diverse phenolic compound, among which rosmarinic acid is the dominant hydroxycinnamic acid ester (Javanmardi et al., 2002). Rosmarinic acid is an ester of caffeic acid and 3, 4-dihydroxyphenyllactic acid. It is commonly found in species of the Boraginaceae and the subfamily Nepetoideae of the Lamiaceae (Wang et al., 2004). A variety of biological activities have been explained for rosmarinic acid such as anti-inflammatory, antiviral, antibacterial and antioxidant effects (Swarup et al., 2007). Redox properties of phenols play an important role in the absorption and neutralization of free radicals (Javanmardi et al., 2002). Phenolic

3.5. Antioxidant activity Antioxidant activities of the sweet basil’s essential oils from various iron and urea treatments were evaluated applying DPPH, MDA, H2O2, and sodium nitrite scavenging effects, shown for ROS, TBARS, H2O2, and RNS scavenging activities, respectively. The IC50 values for RNS, ROS, TBARS and H2O2 scavenging activities of essential oils in comparison with control treatment were decreased when iron and urea sources were applied. The lowest IC50 values for ROS, TBARS, H2O2, and RNS scavenging activities were found in essential oils of basil plants which were treated with 0.2 % [Fe-urea] nano complex. The highest antioxidant activity (21.98 ± 1.3 mg AAE g−1) was displayed by the sweet basil treated with 0.2 % [Fe-urea] nano complex, whereas the lowest antioxidant activity (9.31 ± 1 mg AAE g−1) was found in the control treatment (Table 5). Plant antioxidants can prevent many diseases such as diabetes, liver disorders, cancer, cardiovascular disease and inflammation (Uttara et al., 2009). There are many factors affecting the formation and retention of antioxidant compounds which one of them is the appropriate nutrition (Kevers et al., 2011). Catalase is a large enzyme containing haem-bound iron at its active sites (Fridovich, 1978). The activity of catalase, peroxidase and ascorbate peroxidase can be reduced in conditions of iron deficiency. Because these enzymes contain iron porphyrin and have a special role in plant metabolism as prosthetic groups (Sun et al., 2007). The results of Javanmardi et al. (2003) showed that the phenolic compounds of basil have high antioxidant activity, which is in consistent with the results of this research. Based on our results, this antioxidant activity is attributed to the high level of carvacrol and rosmarinic acid. Antioxidant activity of carvacrol (Jaberian et al., 2013) and rosmarinic acid (Swarup et al., 2007) has been proven in previous studies. Researches show that there is a positive linear relationship between antioxidant activity and phenolic compounds (Javanmardi et al., 2003). 6

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Plants protect themselves against oxidative damage through the antioxidant defense systems (Gill and Tuteja, 2010). Antioxidants are substances that can reduce the oxidative stress in cells and can inhibit free radicals, prevent oxidation and strengthen the immune system. Also, antioxidants have antimicrobial, anticancer and anti-diabetic activities (Mohajerani, 2012; Ebrahimzadeh et al., 2008). 3.6. Antimicrobial activity The minimum inhibitory concentration (MIC) was defined as the lowest essential oils concentration that induced more than 90 percent growth depletion in comparison with the growth in the control treatment. In this study MIC for fungi (Aspergillus niger and Candida albicans) growth, Gram-positive (Bacillus subtilis and Staphylococcus aureus) and Gram-negative (Escherichia coli and Salmonella typhimurium) bacteria was determined. Generally, the application of iron and urea sources significantly increased the antibacterial and antifungal activity of essential oils compared to the control treatment (p < 0.05) (Table 6). The lowest minimal inhibitory concentration for Bacillus subtilis, Staphylococcus aureus, Escherichia coli, Salmonella typhimurium, Aspergillus niger, and Candida albicans were 0.042 ± 0.008, 0.016 ± 0.003, 0.238 ± 0.024, 0.166 ± 0.025, 0.101 ± 0.021 and 0.129 ± 0.011 mg mL−1 of essential oil derived from treated basils with 0.2 % Fe-urea nano complex foliar spraying, respectively. Essential oil of basil has been used for a wide range of applications such as cooking spices, medicinal treatments, pesticides, aromatherapy, perfumery and food preservatives (Li and Chang, 2016). Extracts and essential oils have antibacterial, antifungal, antioxidant and anticancer activity and can control the growth of pathogens and the production of toxin by microorganisms (Tajkarimi et al., 2010). Given to the number of chemical compounds in the essential oil, we cannot consider a single mechanism for their antibacterial effects, but they will have several targets in the cell (Burt, 2004). One of the important properties of essential oil and their constituent parts are their hydrophobic effect, which leads their influence on the membrane lipids of bacterial cells and disrupts their structures and increases their permeability (Burt, 2004). Different bacterial and fungal species exhibit various sensitivities to phenolic compounds. These compounds include carvacrol, eugenol and thymol. Possibly, the mechanism of the effect of these compounds like other phenolic compounds, includes the following: disruption of the cytoplasmic membrane, disrupting proton dynamics and energy metabolism and coagulation of cellular contents (Burt, 2004; Tajkarimi et al., 2010). The chemical structure of essential oils also affects its mechanism of action. The importance of the presence of hydroxyl group in phenolic compounds such as carvacrol and thymol has been confirmed. However, the position of the hydroxyl group in the phenolic ring has a little effect on its antibacterial activities (Burt, 2004). Our results showed that the application of iron and urea sources increases the content of carvacrol in essential oil. Carvacrol and some other phenolic compounds, such as thymol, are able to disintegrate the outer membrane of gram-negative bacteria and cause the release of lipopolysaccharides (LPS) and increase the permeability of the cytoplasmic membrane. In addition to inhibiting the growth of bacteria cells, carvacrol is also able to inhibit the production of toxin by bacteria (Chavan and Tupe, 2014). Antimicrobial properties of carvacrol have been reported in previous studies (Mahboubi and Kazempour, 2011). Carvacrol inhibits the growth of some bacteria, including Escherichia coli and Bacillus cereus (Du et al., 2008). The results of Ultee and Smid (2001) showed that carvacrol can inhibit the production of toxin from Bacillus cereus that causes diarrhea. There are two theories: first due to the interference of carvacrol with the production of ATP, ATP may not be sufficiently ready to remove toxin from the cell, which is an active and energy-dependent process, and second, by lowering the specific growth rate, it may be possible that the cell spends its entire energy to survive (Burt, 2004).

ND: Not detected. † Means followed by the same letter within a column are not significantly different according to Duncan’s multiple range test at P < 0.05. *Calculated mean amount of the flavonoids and polyphenols (mg g−1 DM) based on the weight of the ground dry plant in eight replicates ± sd (standard deviation).

3.81 ± 0.15b 4.10 ± 0.16b 3.96 ± 0.18b 4.41 ± 0.15a 3.19 ± 0.15 cd 3.24 ± 0.16c 2.99 ± 0.15d 4.14 ± 0.17c 4.47 ± 0.16b 4.22 ± 0.14c 4.71 ± 0.14a 1.73 ± 0.11d 1.99 ± 0.12d ND 5.18 ± 0.21c 5.51 ± 0.22b 5.62 ± 0.22ab 5.81 ± 0.18a 3.23 ± 0.19e 3.61 ± 0.19d 2.43 ± 0.12f % % % % Fe-EDDHA 0.1 Fe-EDDHA 0.2 n[Fe-urea] 0.1 n[Fe-urea] 0.2 Urea 0.1 % Urea 0.2 % Control

3.89 ± 0.14c 4.34 ± 0.13a 4.11 ± 0.10b 4.48 ± 0.12a 3.61 ± 0.12e 3.84 ± 0.11d 2.56 ± 0.09f

3.81 ± 0.16d 4.52 ± 0.18b 4.03 ± 0.15c 4.75 ± 0.13a 3.29 ± 0.16f 3.58 ± 0.14e 2.45 ± 0.10 g

2.43 ± 0.09a 2.50 ± 0.11a 2.37 ± 0.11a 2.55 ± 0.13a 1.79 ± 0.10b 2.02 ± 0.09b ND

3.35 ± 0.19b 3.48 ± 0.15ab 3.47 ± 0.17ab 3.56 ± 0.18a 2.05 ± 0.14c 2.11 ± 0.16c ND

3.34 ± 0.15c 3.66 ± 0.14b 3.76 ± 0.18ab 3.92 ± 0.15a 2.99 ± 0.14d 3.24 ± 0.15c 2.21 ± 0.09e

0.86 ± 0.05b 1.06 ± 0.08a 0.82 ± 0.07b 0.97 ± 0.06ab ND ND ND

2.24 ± 0.08b 2.73 ± 0.10a 2.39 ± 0.09b 2.75 ± 0.07a ND ND ND

Quercetin Carvacrol Gallic acid Catechin Rosmarinic acid Treatments

Table 4 Flavonoids and phenolic compounds of sweet basil as affected by iron and nitrogen sources.

Kaempferol

Cinnamic acid

Luteolin

Rutin

Ferulic acid

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Table 5 Radical scavenging activity of sweet basil’s essential oils affected by iron and nitrogen sources. Properties −1 a

Antioxidant (mg AAE g ) IC50 for RNS scavenging (mg mL−1)b IC50 for ROS scavenging (mg mL−1)c IC50 for TBARS scavenging (mg mL−1)d IC50 for H2O2 scavenging (mg mL−1)e a b c d e

Fe-EDDHA 0.1 %

Fe-EDDHA 0.2 %

n[Fe-urea] 0.1 %

n[Fe-urea] 0.2 %

Urea 0.1 %

Urea 0.2 %

Control

18.11 ± 1.3 2.11 ± 0.09 1.31 ± 0.2 3.81 ± 0.2 2.44 ± 0.2

20.21 ± 1.5 1.82 ± 0.09 1.19 ± 0.2 3.29 ± 0.2 2.18 ± 0.2

19.44 ± 1.1 1.76 ± 0.1 1.24 ± 0.2 3.64 ± 0.2 2.36 ± 0.2

21.98 ± 1.3 1.50 ± 0.2 1.11 ± 0.3 3.03 ± 0.2 1.98 ± 0.3

11.10 ± 1.1 3.44 ± 0.2 2.18 ± 0.3 4.44 ± 0.1 3.98 ± 0.2

13.22 ± 1.1 3.12 ± 0.09 1.91 ± 0.2 4.14 ± 0.2 3.71 ± 0.4

9.31 ± 1.0 4.98 ± 0.4 3.77 ± 0.6 5.86 ± 0.3 5.11 ± 0.5

Data are presented as milligrams ascorbic acid equivalents per gram of essential oil. IC50 is concentration of essential oil to scavenge RNS (reactive nitrogen species) by 50 %. IC50 is concentration of essential oil required to scavenge ROS (reactive oxygen species) by 50 %. IC50 is concentration of essential oil to scavenge TBARS (thiobarbituric acid reactive substances) by 50 %. IC50 is concentration of essential oil to scavenge H2O2 by 50 %.

Table 6 Antimicrobial activity of sweet basil’s essential oils affected by iron and nitrogen sources. MIC (mg mL−1)

Fe-EDDHA 0.1 %

Fe-EDDHA 0.2 %

n[Fe-urea] 0.1 %

n[Fe-urea] 0.2 %

Urea0.1 %

Urea0.2 %

Control

Bacillus subtilis Staphylococcus aureus Escherichia coli Salmonella typhimurium Aspergillus niger Candida albicans

0.092 ± 0.004 0.025 ± 0.002 0.328 ± 0.021 0.295 ± 0.015 0.145 ± 0.008 0.161 ± 0.005

0.067 ± 0.003 0.015 ± 0.0005 0.292 ± 0.018 0.217 ± 0.011 0.118 ± 0.045 0.150 ± 0.005

0.061 ± 0.009 0.024 ± 0.004 0.275 ± 0.025 0.201 ± 0.027 0.132 ± 0.008 0.152 ± 0.016

0.042 ± 0.008 0.016 ± 0.003 0.238 ± 0.024 0.166 ± 0.025 0.101 ± 0.021 0.129 ± 0.011

0.133 ± 0.011 0.056 ± 0.003 0.613 ± 0.030 0.445 ± 0.037 0.173 ± 0.028 0.224 ± 0.018

0.125 ± 0.011 0.052 ± 0.002 0.596 ± 0.031 0.418 ± 0.035 0.165 ± 0.032 0.219 ± 0.016

0.154 ± 0.013 0.068 ± 0.005 0.761 ± 0.047 0.749 ± 0.052 0.208 ± 0.040 0.240 ± 0.022

Values are means of MIC in eight replicates ± sd (standard deviation). MIC: Minimal Inhibitory Concentration.

proteins present in the bacterial cell, can directly inhibit cell proliferation and protein enzyme function. It has been shown that chemical interactions between iron and Escherichia coli cells are primarily responsible for the destruction of the cell membrane. Iron is a strong reducing and induces the decomposition of external membrane proteins and polysaccharides of the bacterial cells. On the other hand, the iron existed in the iron-urea complex may be oxidized by intracellular oxygen after being isolated, which results in oxidative damage. Iron nanoparticles showed stronger bactericidal activity than other nanoparticles such as silver nanoparticles (Lee et al., 2008). Previous studies have shown that the chemical and biological reactivity of iron-containing nanoparticles is related to the size and surface of the nanoparticles (Waldman et al., 2007). Rod-shaped iron nanoparticles are more soluble in comparison with rod-shaped iron microparticles due to their larger surface and chemical activity (Rubasinghege et al., 2010). In addition, the shape and crystalline structure of nanomaterials can affect toxicological responses. Barzan et al. (2014) examined the antimicrobial and genotoxicity properties of iron nanoparticles on gram-positive bacterial systems of Bacillus cereus and Streptomyces and gram-negative of Erwinia amylovora and Xanthomonas oryzae. The results showed that the minimum inhibitory concentration (MIC) which inhibits the growth of Erwinia amylovora, Xanthomonas oryzae, Bacillus cereus and Streptomyces, are 625, 550, 1250, and 1280 ppm, respectively. In this experiment, the antifungal activity of essential oil of sweet basil on Aspergillus niger and Candida albicans was confirmed (Table 6). In a study conducted on thymoquinone as an active ingredient of Nigella sativa seeds, the effect of inhibiting 100 % of this substance was obtained on Aspergillus niger in a concentration of 2 mg ml−1 (Al Jabre et al., 2003). Mohammadi et al. (2014) examined the antifungal activity of essential oil of thymus kostschyanus on Aspergillus flavus, Fusarium oxysporum and Alternaria alternata. The results showed that the minimum inhibitory concentration, which inhibits the growth of Aspergillus flavus, Fusarium oxysporum and Alternaria alternata, are 0.5, 1, and 0.5 μg ml−1, respectively.

Our results showed that the effect of essential oil of basil on growth of gram-positive bacteria is slightly higher than their effect on gramnegative bacteria (Table 6). In other words, gram-positive bacteria were more sensitive to the antibacterial effect of the essential oil. The reason for the lower sensitivity of the gram-negative bacteria may be due to the presence of external membrane in these bacteria, which limits the release of the hydrophobic components of the essential oil to the lipopolysaccharide layer (Burt, 2004). However, all studies conducted on the antibacterial activity of essential oils do not indicate a higher sensitivity of gram-positive bacteria. For example, Aeromonas hydrophila, a gram-negative bacterium is one of the most sensitive bacterial species in comparison to the effects of essential oils. Among the gram-negative bacteria, Pseudomonas species, especially Pseudomonas aeruginosa, have the least susceptibility in comparison to the effect of antibacterial activity of essential oils. Successful results have been obtained related to the antimicrobial effect of essential oils (Soliman and Badeaa, 2002; Shahnia et al., 2012; Kim et al., 2004; Nielsen and Rios, 2000; Velluti et al., 2003). In previous studies, antimicrobial effects of Zataria multiflora (Mahmoudabadi et al., 2007), thymus kostschyanus and thymus persicus (Rasooli and Mirmostafa, 2003), Hyssopus officinalis (Letessier, 2001) and Artemisia sieberi (Negahban et al., 2007) have been investigated. In this experiment, Fe-urea nano complex quickly inhibited the Escherichia coli (Table 6). However, in order to inhibition of this bacterium, much higher iron content under oxygen saturation conditions is required. This is due to surface oxidation and rusting of iron nanoparticles by dissolved oxygen in the environment. The bactericidal effect of iron nanoparticles is a unique feature. The results of Lee et al. (2008) showed a direct relationship between the inactivation of Escherichia coli and the use of iron nanoparticles. Selvarani and Prema, 2013, investigated the antibacterial properties of iron nanoparticles against gram-positive bacteria Bacillus cereus, Staphylococcus aureus, Staphylococcus epidermidis and gram-negative Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Salmonella typhimurium and Yersinia pestis. Their results showed that iron nanoparticles had potential antibacterial activity against gram-positive and gram-negative bacteria. The role of iron in bactericidal capacity has not been well understood. It is unknown whether the link of iron to the DNA molecule, or specific

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4. Conclusion

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The effect of nitrogen and iron on plant growth reflects their positive role in photosynthetic activity and metabolism of organic compounds. Application of iron and urea sources improved the growth and biochemical parameters of sweet basil. Vegetative growth, essential oil yields, polyphenols content, antioxidant and antimicrobial activity of the essential oil of sweet basil significantly increased in response to 0.2 % n[Fe-urea] application. The results of this study showed that epi-αcadinol and rosmarinic acid were the predominant terpenoid and phenolic compound of the essential oil and the extract, respectively. Application of 0.2 % n[Fe-urea] compared to other treatments significantly increased the content of these two compounds. The high surface area to volume ratio, the continuous release of nutrients, easy absorption through the leaves and high impact are nano-fertilizers properties. These properties help to increase the efficiency of nutrients in plants. The development of nanotools and nanomaterials can provide new prospects in plant biotechnology and the achievement of sustainable and eco-friendly agriculture. Funding No funding was received for this work. Intellectual property We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing we confirm that we have followed the regulations of our institutions concerning intellectual property. Research ethics We further confirm that any aspect of the work covered in this manuscript that has involved human patients has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the manuscript. IRB approval was obtained (required for studies and series of 3 or more cases). Written consent to publish potentially identifying information, such as details or the case and photographs, was obtained from the patient(s) or their legal guardian(s). Authorship All listed authors meet the ICMJE criteria. We attest that all authors contributed significantly to the creation of this manuscript, each having fulfilled criteria as established by the ICMJE. We confirm that the manuscript has been read and approved by all named authors. We confirm that the order of authors listed in the manuscript has been approved by all named authors. Declaration of Competing Interest The authors confirm that there are no known conflicts of interest associated with this manuscript. References Abbaszadeh, B., Farahani, H.A., Valadabadi, S.A., Darvishi, H.H., 2009. Nitrogenous fertilizer influence on quantity and quality values of balm (Melissa officinalis L.). J. Agric. Ext. Rural. Dev. 1 (1), 31–33. Adams, R.P., 2007. Identification of Essential Oil Components by Gas Chromatography/

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