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Indian Journal of Agricultural Research

  • Chief EditorV. Geethalakshmi

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Full Research Article

Essential Oils of Zygophyllum coccineum L. Chemical Characterization, Antioxidant, Antibacterial and Cytotoxic Activity on Human Breast Adenocarcinoma (MCF-7)

Hanan Ali Kareem1, Ahmed Ali Hussein1, Zahraa Isam Jameel1,*
1Department of Biology, College of Science, Al-Qasim Green University, Al Qasim, Babylon 51013, Iraq.

ABSTRACT

Background: Zygophyllum coccineum L., a halophytic plant from the Zygophyllaceae family, has traditional medicinal uses. Its essential oil (EO) contains diverse bioactive compounds with potential therapeutic value. This study investigates the chemical composition of Z. coccineum EO and evaluates its antioxidant, antibacterial and cytotoxic activities.

Methods: EO was extracted from the aerial parts of Z. coccineum via hydro-distillation and analyzed using GC-MS. Antioxidant activity was assessed using DPPH and ABTS assays, while antibacterial effects were tested against Gram-positive and Gram-negative bacteria using the agar diffusion method. Cytotoxicity was evaluated against MCF-7 breast cancer cells using the MTT assay.

Result: GC-MS analysis identified 22 compounds in Z. coccineum EO, with palmitic acid (20.36%), 1-(2,3,6-trimethylphenyl)-2-butanone (15.62%) and (E)-3-(2,6,6-trimethylcyclohex-1-en-1-yl) acrylaldehyde (11.47%) as major constituents. The EO exhibited significant antioxidant potency, with IC50 values of 19.96 µL/L (DPPH) and 16.70 µL/L (ABTS). It showed strong antibacterial activity, particularly against Salmonella typhimurium (20.88 mm inhibition zone). Additionally, the EO also demonstrated cytotoxic towards MCF-7 cells with an IC50 of 48.26 µg/mL while exhibiting minimal toxicity toward normal WI-38 cells. Conclusion, Z. coccineum EO has a satisfactory bioactive molecule reservoir with potent antioxidant, antibacterial and discriminative anticancer activities. The findings validate its potential pharmaceutical uses.

INTRODUCTION

Traditional medicine is still well integrated into cultural healthcare systems in the majority of developing countries. All therapeutic medicines were originally produced from plants, whether raw plant components or refined crude extracts, mixes, etc. There are more than a thousand known plant species with therapeutic potential and interest in plant-based, eco-friendly medicinal resources increases worldwide (Qadir and Raja, 2021). Essential oils (EOs) with their highly diverse bioactive components represent a significant source of natural therapeutics. European Pharmacopoeia lists several important EOs for treating many disorders (Al-Khaial  et al., 2025). EOs have antioxidants, antifungal, antibacterial, antiviral, allelopathic and insecticidal properties (Abd El-Gawed  et al., 2020). EOs are also applications in food preservation, aromatherapy, aroma, medication, cosmetic and agricultural. Chemically, EOs consist of complex blend of volatile elements such mono-, sesquit- and diterpenes, phenylpropanoids, hyrdocarbons and others with distinct odours and economic value (Razni et al., 2019).
       
Halophytes are salt-tolerant plants found in saline environments like salt marshes and the coasts. They possess specialized physiological and biochemical adaptations that enable them to thrive under salt stress (Zahran and El-Amier, 2013). Among them, Zygophyllum species play a vital ecological and economic role in arid environment, particularly of the Arabian Peninsula and Saharo-Sindian regions. Zygophyllum coccineum, a halophyte within the family Zygophyllaceae known as the “bean caper,” is native to regions like North Africa, the Middle East and the Saharo-sindian area. It naturally grows in harsh environments by producing primary and secondary metabolites that function as antioxidants, phytoalexins and stress mediators (Porter, 1974; Zhang et al., 2017). Various parts of Zygophyllum plants are abundant in bioactive substances such as phenolic compounds, alkaloids, terpenoids, polysaccharides and fatty acids (Amin et al., 2012; Mohammed et al., 2021). These phytochemicals are associated with therapeutic properties such as antimicrobial, anti-inflammatory and cytotoxic activities (Abd El Raheim  et al., 2016; Mohammed et al., 2021). Moreover, in ancient medicines they were used in the treatment of disorders such as skin diseases, diabetes, high blood pressure, wound healing, anthelmintic, diuretic and gastrointestinal disorders (Gibbons and Orio, 2001). This work aims to describe the biochemical substance of Z. coccineum EO and assess its antioxidant, antibacterial and cytotoxic activities.

MATERIALS AND METHODS

Plant material
Aerial parts of Z. coccineum were gathered during its flowering period in June 2024 from various populations located in the northern Nile Delta region, Egypt (coordinates: 31°17'11.81"N, 32°10'35.08"E). Healthy, flowering specimens were selectively collected for the study. The identification of the plant was conducted in accordance with the taxonomic references provided by Boulos (1999). A voucher plant sample (code ManU.262603008) was created and kept at the Botany Department Herbarium at the Faculty of Science, Mansoura University, Egypt.
 
Extraction of EO and GC-MS analysis
 
The EO was extracted by hydro-distilling 200 g of air-dried Z. coccineum aerial parts for 3 hours using a Clevenger apparatus. The EO was separated with n-hexane, dried over anhydrous Na2SO4  and stored at ±5°C for further analysis. GC-MS analysis was performed as described by Abd-El Gawad et al., (2020) using a TRACE GC Ultra system with a quadrupole mass spectrometer. A 31 m x  0.33 mm column with a 0.26 µm film thickness was used, with helium as the carrier gas at 1.0 mL/min and a split ratio of 1:10. The temperature ramp started at 61°C for 1 min, increasing to 240°C at 4°C/min. Mass spectra were acquired at 71 eV (m/z 41-452). Compound identification was achieved using AMDIS software, NIST and Wiley libraries, retention indices and authentic standards.
 
Antioxidant activity of the EO
 
The antioxidant activity of Z. coccineum EO was evaluated using the DPPH radical scavenging assay (Miguel, 2010). EO concentrations (5-50 mg/L) were prepared in methanol and mixed with an equal volume of 0.3 mM DPPH solution. After 30 minutes of incubation at 25°C, absorbance was measured at ~518 nm using a spectrophotometer (Analytik Jena, Germany). Vitamin C served as a positive control at concentrations of 1-20 mg/L. The radical scavenging (RS) activity was calculated as:
 
     
 
Following Re et al., (1999), the antioxidant activity of Z. coccineum EO was assessed using the ABTS radical scavenging assay. EO concentrations (5-50 mg/mL) were prepared and 2.5 mL of ABTS solution was mixed with 0.3 mL of EO. After 6 minutes of dark incubation, absorbance was measured at ~735 nm. Vitamin C was used as a reference and ABTS inhibition was calculated using a formula similar to that of the DPPH assay.
 
Antibacterial activity of the EO
 
Four Gram-negative bacterial strains Escherichia coli (PQ836611), Pseudomonas aeruginosa (PQ805338), Salmonella typhimurium (PQ836615) and Streptococcus epidermidis (PQ125228) as well as three Gram-positive strains-Bacillus cereus (PQ836613), Staphylococcus aureus (PQ836612) and Staphylococcus haemolyticus (PQ836616)-were used to measure the antibacterial effectiveness of the EO extracted from Z. coccineum aerial parts. Bacterial strains were acquired from the Microbiological Lab., College of Medicine, Mansoura University in Egypt.
       
The antibacterial activity was evaluated using the agar diffusion method (Lorian, 2005). Filter paper discs (5 mm, Whatman no.1) were impregnated with 10 mg L-1 of Z. coccineum EO and placed on nutrient agar plates inoculated with 10v  CFU/mL of each bacterial strain. Plates were sealed with Para-film® and incubated at ~35°C for 36 hours. Inhibition zones (mm) were measured at three random points. Standard antibiotics (tetracycline (TET), azithromycin (AZM), ampicillin (AMP)) were used for comparison.
 
MTT assay
 
Cytotoxic activity of Z. coccineum EO was assessed using the MTT assay (Applichem, USA) as described by Bondock et al., (2012). MCF-7 human breast cancer cells, obtained from ATCC (Cairo), were used with doxorubicin as a standard chemotherapeutic drug. The assay measures the conversion of MTT to blue formazan by mitochondrial enzymes, indicating cell viability. Cells (2x104  cells/mL) were seeded in 96-well plates (200 µL/well) and incubated for ~25 hours before treatment. EO was diluted in 10% DMSO to a final concentration of 4 mg/mL and applied to two cell lines. Treated cells were incubated at 37°C with 5% CO‚  for 72 hours. After 24 hours of treatment, 20 µL of MTT (5 mg/mL in PBS) was added per well. Formazan crystals were dissolved in 100 µL DMSO and absorbance was measured at 540 nm using a microplate reader (Thermo Scientific Multiscan Spectrum). Cytotoxicity was calculated by comparing the optical densities of treated and untreated cells:
 
    
       
The concentration (in μg/mL) that induces 50% cell death is defined as the IC50.
 
Data analysis
 
Each treatment was tested in triplicate for antibacterial and antioxidant activities. Data was analyzed using ANOVA, followed by Duncan’s test for mean differences. Results are presented as mean ± standard error. IC50 values were calculated using Microsoft Excel 2016.

RESULTS AND DISCUSSION

Chemical composition of Z. coccineum EO
 
Hydrodistillation of Z. coccineum aerial portions yielded a pale yellowish EO with a percentage of 0.049% (v/w), comparable to the 0.044% yield reported for Z. album (Kchaou et al., 2016). The extracted EO was investigated utilizing GC-MS to establish its chemical composition (Fig 1). GC-MS analysis identified 22 components, representing 99.97% of the total oil composition (Table 1), a number similar to those identified in the EO of Z. album (Kchaou et al., 2016).

Fig 1: The GC-MS chromatogram of the EO isolated from the shore sample of Z. coccineum highlights the major compounds, with their peaks distinctly numbered (1-5).



Table 1: The essential oil constituents of the coastal Z. coccineum were identified through GC-MS analysis.


       
The EO constituents of Z. coccineum were analyzed, revealing a diverse range of chemical compounds classified into different groups (Table 1). Monoterpenes were present in moderate amounts, with limonene (7.31%) being the most abundant (Fig 2), followed by β-pinene (2.31%), thymol (2.14%) and safranal (1.13%). The phenolic compounds included 4-vinylphenol (1.06%) and eugenol (2.27%). Caryophyllene oxide, a sesquiterpene, accounted for 4.23% of the total composition. The alkyl benzene group was represented by (E)-2-(buta-1,3-dien-1-yl)-1,3,4-trimethylbenzene (3.04%) and 1-(2,3,6-trimethylphenyl)-2-butanone (15.62%), the latter being the second most abundant compound overall (Figure 2). Aldehydes were dominated by (E)-3-(2,6,6-trimethylcyclohex-1-en-1-yl) acrylaldehyde (11.47%), with nonanal contributing 1.68%.

Fig 2: The biochemical structures of the primary detected substances in the EO of Z. coccineum were determined through GC-MS analysis.


       
Fatty acids and their derivatives constituted a significant portion, with palmitic acid (20.36%) being the maximum abundant substance in the oil (Fig 2), followed by oleic acid (7.31%), docosanoic acid (3.28%), 2-mono-linolein (3.42%) and 2-mono-olein (2.8%). Steroids were detected in lower amounts, including β-sitosterol-3-O-β-D-glucopyranoside (0.91%), β-sitosterol (0.76%) and stigmasterol (1.57%). Additionally, the hydrocarbon cyclic alcohol 3,3a,7,7-tetramethyl-3a,5,6,7-tetrahydro-4H-inden-4-ol was present at 3.87% (Table 1).
       
Palmitic acid was found in a superior concentration (20.36%) in the EO of Z. eichwaldii (Mazoochi et al., 2021). Additionally, several identified compounds, including thymol and oleic acid, were also reported as constituents of Z. eichwaldii EO. Kchaou et al., (2016) reported that nonanal, safranal, thymol and eugenol are commonly dispersed compounds in EOs of Zygophyllum album. In this study, oleic acid was found in moderate amounts (7.31%) in the plant extracts, consistent with its presence in the EOs of Z. oxianum and Z. eichwaldii as reported by previous studies (Sasmakov et al., 2012; Mazoochi et al., 2021). Additionally, Mazoochi et al., (2021) documented caryophyllene oxide in Z. eichwaldii. Furthermore, limonene, β-pinene, docosanoic acid, 2-mono-linolein and 1-(2,3,6-trimethylphenyl)-2-butanone are commonly found compounds in EOs of various plants, including Moringa oleifera (Kuete, 2017), Pistacia atlantica (Tahir et al., 2019) and Cannabis sativa (Judzentienë  et al., 2023).
       
With the exception of the presence of palmitic and oleic acids, the chemical makeup of the EO in this investigation was completely different from that reported for Z. eichwaldii EO (Mazoochi et al., 2021).  The genetic distinctions between the two species might be the cause of this variance (Abd-ElGawad  et al., 2021).  Furthermore, it has been established that climatic and ecological variables have exert a substantial influence on the composition of EO (Abd-El Gawad  et al., 2020). The EO of Z. coccineum contains various chemical classes, with fatty acids and derivatives making up 40.91% of the composition. Alkyl benzenes account for 18.66%, followed by aldehydes and monoterpenes at 13.15% and 13.14%, respectively. Monoterpenes, known for their fragrance, may aid in plant defense and therapeutic uses. Sesquiterpenes (4.53%), hydrocarbons (3.87%), phenols (3.33%) and steroids (3.24%) are also present, contributing to the oil’s stability and pharmacological activities, including antioxidant and anti-inflammatory properties (Salama et al., 2022).

Antioxidant activity of Z. coccineum EO
 
The EO of Z. coccineum exhibited strong antioxidant capacity in both DPPH and ABTS assays (Table 2). A one-way ANOVA indicated significant differences in scavenging activities across concentrations (p£0.05) and Duncan’s post hoc test revealed that values at 20 and 25 µg/mL were significantly higher than at lower concentrations (p<0.05), confirming a dose-dependent trend. At a concentration of 25 µL/L, Z. coccineum EO reduced the DPPH and ABTS colors by 64.05% and 73.59%, correspondingly. Based on IC50  values, the EO exhibited IC50 values of 19.96 µL/L and 16.70 µL/L for DPPH and ABTS, correspondingly, while vitamin C displayed IC50 values of 0.73 µL/L and 0.41 µL/L for the same assays.

Table 2: DPPH and ABTS scavenging activity along with IC50 values by Z. coccineum essential oil. Duncan’s multiple range test at p£0.05.


       
The pronounced antioxidant potency of Z. coccineum EO in this work may be ascribed to its major constituents, including palmitic acid, oleic acid, 1-(2,3,6-trimethylphenyl)-2-butanone, caryophyllene oxide, limonene and docosanoic acid, which may act either individually or synergistically (Abd-ElGawad et al., 2020; Salama et al., 2022; El Hachlafi et al., 2024). Notably, palmitic acid, the predominant compound, has been reported at a high concentration (14.85%) in Reichardia tingitana, which exhibited strong antioxidant activity (Salama et al., 2022).
 
Antibacterial activity of Z. coccineum EO
 
The EO demonstrated differential antibacterial effects against the tested strains (Table 3). With an inhibitory zone of 20.88 mm, S. typhimurium showed the greatest sensitivity to the EO among the tested bacterial strains, demonstrating its strong antibacterial action. Similarly, E. coli and B. cereus exhibited considerable sensitivity, with clear zones of 16.84 mm and 17.91 mm, correspondingly. These findings suggest that the EO possesses potent antibacterial properties, particularly against certain enteric and foodborne pathogens (Table 3).

Table 3: The antibacterial activity of the EO obtained from the aerial shoot of Z. coccineum was assessed in comparison to selected reference antibiotics.


       
On the other hand, P. aeruginosa exhibited the lowest sensitivity to the EO, with an inhibition zone of only 8.47 mm, suggesting a higher level of resistance. This is consistent with previous reports indicating that P. aeruginosa is often more resistant to plant-derived antimicrobials due to its robust efflux pump system and biofilm formation capabilities. Among the Gram-positive bacteria tested, S. aureus demonstrated moderate sensitivity, with an inhibition zone of 10.97 mm, whereas B. cereus showed a stronger inhibitory response (Table 3). ANOVA confirmed significant differences in bacterial inhibition zones (p≤0.05). Duncan’s test identified S. typhimurium as significantly more susceptible than P. aeruginosa and S. aureus (p<0.05).
       
The selected antibiotics demonstrated varying degrees of activity versus the tested bacterial strains, with Gram -ve bacteria generally exhibiting higher resistance than Gram-positive strains. This trend aligns with findings from previous research (Breijyeh et al., 2020; Salama et al., 2022; Abduljabbara et al., 2024), which attribute the observed resistance to the structural differences in bacterial cell walls (Breijyeh et al., 2020). Gram -ve bacteria’s outer membrane serves as an extra barrier, preventing antibiotics from penetrating and enhancing their resistance. The reference antibiotic tetracycline exhibited the strongest inhibition across all tested bacteria, with MIC values extending from 0.035 to 0.058 mg/ml. Azithromycin and ampicillin, however, showed inconsistent effects, with S. typhimurium and P. aeruginosa being resistant to at least one of these antibiotics. Interestingly, the EO demonstrated higher efficacy against S. typhimurium compared to both azithromycin and ampicillin, indicating its potential as an alternative antimicrobial agent.
       
The antibacterial activity of the EO may be attributed to its major bioactive components, including limonene, 1-(2,3,6-trimethylphenyl)-2-butanone. (E)-3-(2,6,6-trimethylcyclohex-1-en-1-yl) acrylaldehyde, palmitic acid and oleic acid. These compounds may exert their antimicrobial effects either individually or through synergistic interactions. A similar study by Han et al., (2021) demonstrated potent inhibitory activity against S. aureus. Additionally, according to Kuete (2017), 1-[2,3,6-trimethylphenyl]-2-butanone is a significant component of Moringa oleifera EO and has strong microbicidal, anti-inflammatory and antidiabetic effects. Moreover, palmitic and oleic acids have also shown antibacterial activity against various Gram-positive and Gram-negative oral pathogens (Huang et al., 2010). Furthermore, Sharma et al., (2021) identified palmitic acid as a major compound (15.57%) in Capsicum annuum oleoresin, where it exhibited antimicrobial potential towards B. subtilis, E. coli, P. aeruginosa and S. aureus.
       
EOs with high concentrations of caryophyllene oxide have also exhibited significant antimicrobial properties (Bhaisare et al., 2016; Abd-ElGawad et al., 2022). Moreover, EOs intense in fatty acids and monoterpenes have been reported to possess substantial antimicrobial activity (Marchese et al., 2017).
 
Cytotoxic activity of Z. coccineum EO
 
The EO of Z. coccineum exhibited dose-dependent cytotoxicity against MCF-7 breast cancer and normal WI-38 cells at different concentrations, with doxorubicin as a standard (Fig 3). The highest inhibition rate was recorded at 70.96% at 800 µg/mL, while the IC50  value for MCF-7 cells was calculated to be 48.26 µg/mL. In contrast, its effect on normal WI-38 cells was minimal, with greatest inhibition of 9.32% at 1000 µg/mL and an IC50 value exceeding 100 µg/mL, indicating selective toxicity toward cancer cells. Doxorubicin exhibited stronger cytotoxicity, achieving complete inhibition (100%) at 800 µg/mL, with an IC50 of 5.24 µg/mL for MCF-7 cells. However, it also affected normal cells, showing 11.61% cytotoxicity at 1000 µg/mL.

Fig 3: The cytotoxic action and IC50 values of Z. coccineum EO were assessed against MCF-7 tumor cells and natural cells at varying concentrations, with doxorubicin used as a control.


       
These findings indicate that EOs exhibits promising anticancer potential with selective cytotoxicity, suggesting its potential as a natural medicinal agent to treat breast cancer. According to published guidelines, cytotoxicity is classified based on IC50 values as follows: IC50  less than 10 µg/mL is considered very toxic, IC50 between 10 and 100 µg/mL is classified as potentially toxic, IC50 ranging from 100 to 1000 µg/mL is deemed hypothetically harmful and IC50  greater than 1000 µg/mL is regarded as potentially non-toxic (Gad-Shayne, 2009). This classification provides a valuable reference for evaluating the cytotoxic potential of phytoconstituents of extracts and essential oils in biomedical applications.
       
The principal chemical substance in the EOs analyzed are responsible for the cytotoxicity of the oils employed in this investigation. Several factors influence the cytotoxic mechanism, such as the sample intensity, nature of the isolated components, phytochemical content, nanoparticle model, size and collection and the nature of the tumor and non-cancerous cell line. Cytotoxicity may also be related to protein loss (El-Amier  et al., 2023).
       
The main component of EOs, palmitic acid, has cytotoxic properties, especially against cancer cells, via a number of pathways, including oxidative stress and apoptosis induction (Biswas et al., 2022). According to Kuete (2017), 1-[2,3,6-trimethylphenyl]-2-butanone, derived from Moringa oleifera essential oil, exhibited anticancer activity. In addition, limonene induced cytotoxic effects on multiple cancer cell lines, including those of the colon, prostate, lung and breast (Chaudhary et al., 2012). Oleic acid and limonene have also been said to enhance the action of conventional chemotherapy drugs such as doxorubicin and paclitaxel (Menendez et al., 2005).

CONCLUSION

This investigation identifies the chemical profile and bioactivity of Z. coccineum essential oil (EO) and its potential pharmaceutical and therapeutic applications. The EO contained high levels of bioactive compounds according to GC-MS analysis, the chief ingredients of which were palmitic acid, 1-(2,3,6-trimethylphenyl)-2-butanone and (E)-3-(2,6,6-trimethylcyclohex-1-en-1-yl) acrylaldehyde. The EO exhibited high antioxidant activity, which suggests its potential as a natural antioxidant agent. Besides, its high antibacterial activity, especially against S. typhimurium, makes it a candidate for use as an alternative antimicrobial agent. In addition, the EO was selectively cytotoxic to MCF-7 human breast cancer cells but exhibited low toxicity toward natural WI-38 cells, showing its promise as a natural anticancer agent. These results indicate that Z. coccineum EO is a satisfactory source of bioactive substances for food preservation, cosmetic and pharmaceutical industries.

CONFLICT OF INTEREST

All authors declared that there is no conflict of interest.

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