Home Physical Sciences Copper oxide nanoparticles-mediated Heliotropium bacciferum leaf extract: Antifungal activity and molecular docking assays against strawberry pathogens
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Copper oxide nanoparticles-mediated Heliotropium bacciferum leaf extract: Antifungal activity and molecular docking assays against strawberry pathogens

  • Esraa Hamdy , Hamada El-Gendi , Abdulaziz Al-Askar , Ali El-Far , Przemysław Kowalczewski , Said Behiry and Ahmed Abdelkhalek EMAIL logo
Published/Copyright: May 6, 2024
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Open Chemistry
From the journal Open Chemistry Volume 22 Issue 1

Abstract

In the current study, Heliotropium bacciferum leaf extract was used to biosynthesize copper oxide nanoparticles (CuO-NPs). Various analytical techniques were used to characterize the produced CuO-NPs. Transmission electron microscope investigation indicated well-distributed spherical particles in various development phases. The particles’ diameters ranged from 22.15 to 37.01 nm, with an average of 24.8 ± 6.1 nm. Energy dispersive X-ray examination confirmed the presence of nanoscale Cu ions at a high concentration, as seen by the strong signal peak at 1 keV. Fourier transform infrared spectrum revealed various functional groups on the green-produced CuO-NPs, as evidenced by multiple absorption beaks. The bands found at 3,195 and 2,916 cm−1 revealed that phenolic and flavonoid compounds’ alcohols and alkanes were stretching C–H. Also, a band at 1,034 cm−1 is typically attributed to CuO production. CuO-NPs exhibited significant bioactivity against isolated and molecularly identified fungal strains, including Rhizoctonia solani (OR116528), Fusarium oxysporum (OR116508), and Botrytis cinerea (OR116491). Remarkably, the highest inhibition percentages were recorded at 100 µg/mL, with values 81.48, 71.11, and 50.74% for R. solani, F. oxysporum, and B. cinerea, respectively. Molecular docking interactions revealed that the highest binding affinity of CuO-NPs was −5.1 for the oxidoreductase of B. cinerea and −5.2 and −5.4 for the chitin synthase of R. solani and F. oxysporum, respectively. Consequentially, the biosynthesized CuO-NPs could be employed as antifungal biocontrol agents, as well as using H. bacciferum leaf extract for the synthesis of nanoparticles for various sustainable agricultural applications.

Keywords: copper oxide nanoparticles; Heliotropium bacciferum ; green synthesis; antifungal activity; plant disease; molecular docking

1 Introduction

Nanotechnology is an important field of study in medicine, food, health, the chemical industry, electronics, energy science, cosmetics, space exploration, and environmental sciences [1,2]. The demand for nanotechnology-derived products is increasing, and this emerging technology has the potential to benefit human health [3]. Nanoparticle (NP) biosynthesis has recently emerged as a more cost-effective and environmentally friendly alternative to chemical and physical methods [4,5]. Plant-based extracts are the most promising biological alternative [6,7], where they are inexpensive “chemical factories” that require minimal maintenance. However, applying phyto-NPs in medical, pharmaceutical, cosmetic, and agricultural fields still has a long way to go. Green chemistry-based NP synthesis is a single-step process requiring less energy to fabricate eco-friendly NPs that can convert agricultural waste and food into energy and other useful products [8]. The process of converting metal ions into NPs is greatly aided by plant-derived compounds, including terpenoids, tannins, alkaloids, steroids, saponins, and polyphenols [9]. The investigation of functional groups found in aqueous plant leaf extracts has previously been conducted to assess their potential utility as reducing agents. As a result, various functional groups, including amines, polyphenols, and carboxylic acids, present in plant leaf extracts have been employed as reducing agents in synthesizing silver NPs [10].

Copper oxide NPs possess unique crystal structures and high surface areas, making them highly valuable antimicrobial agents. These NPs are robust and stable and have a longer shelf life than other organic antimicrobial agents [11]. Various methods of CuO synthesis exist, such as chemical precipitation, microwave irradiation, and thermal decomposition. The chemical method, on the other hand, uses dangerous chemicals that limit its uses. This has led to more interest in biological methods for synthesizing CuO-NPs, which are better for the environment and easier to handle and do not require cell culture [12]. Thus, researchers have already reported using plant extracts such as Punica granatum [13], Ficus sycomorus [7], Malva sylvestris [14], and Ocimum basilicum [15] for the synthesis of oxide NPs. The biosynthesized CuO-NPs were subjected to characterization using a range of physicochemical techniques, such as Fourier-transform infrared spectroscopy (FTIR), X-ray diffraction, and electron microscopes. Furthermore, the synthesized CuO-NPs were employed in diverse applications, including antibacterial and antifungal activities [16,17,18,19,20].

Green NP production with Heliotropium bacciferum leaf extract is an intriguing strategy that takes advantage of the natural features of plant extracts to produce NPs. H. bacciferum (Boraginaceae family), sometimes known as the “Cherry Heliotrope,” is a medicinal plant that contains several bioactive chemicals, including polyphenols, flavonoids, alkaloids, and terpenoids [21]. These chemicals can be used as reducing agents and stabilizers in the manufacture of NPs. The Boraginaceae family has a wide range of flavonoids and polyphenols, which have been shown to have a variety of pharmacological actions, including antibacterial, antioxidant, anti-inflammatory, antiviral, and hepatoprotective characteristics [22]. H. bacciferum has been recognized as a rich reservoir of various phytochemicals, with notable efficiency in scavenging diphenyl picryl hydrazyl radicals, as described in previous investigations [23]. A recent investigation showed that the aerial components of H. bacciferum have significant antibacterial and antifungal activities [24]. The antifungal capabilities of specific components of the H. bacciferum plant are not well researched. As a result, the primary goal of this research was to determine the efficacy of copper NPs generated from H. bacciferum leaf extract in preventing fungal development. Furthermore, the characterization of biogenic NPs for research purposes necessitates the use of a variety of instruments and analytical procedures. In addition, the CuO-NPs were molecularly docked with fungal chitin synthase, cutinase agglutinin, trypsin, and oxidoreductase.

2 Materials and methods

2.1 Green synthesis of CuO-NPs through H. bacciferum leaves extract

The green synthesis of CuO-NPs was mediated through H. bacciferum leaf extract using cupric sulfate (CuSO4, Sigma-Aldrich, USA) as a precursor according to the method described by Chen et al. [25] with simple modifications. Briefly, the plant extract was homogenized (150 rpm) for 3 h at 50°C in 100 mM phosphate buffer with a final solid-to-liquid ratio of 10%. Afterward, the clear supernatant was separated through centrifugation for 15 min at 10,000 rpm and used as a source for reduction power. The CuSO4 reduction was carried out by mixing CuSO4 solution (10 mM) with clear plant extract in a ratio of 1:1 for 5 h under shaking at 50°C. After cooling at room temperature, the CuO-NPs formation was indicated by a dark brownish-to-black color developing in the reduction mixer. The developed CuO-NPs were separated through centrifugation at 10,000 rpm for 15 min. To assure purity, the precipitated CuO-NPs were washed several times with double distilled water (ddH2O) and finally with 95% ethanol before being dried at 80°C for 24 h before any further processing.

2.2 Characterization of prepared CuO-NPs

The surface morphology and size of the eco-friendly synthesized CuO-NPs were studied through transmission electron microscopy (TEM) using the JSM-6360 microscope (JEOL, Tokyo, Japan), operating at 15 kV as an acceleration voltage with a carbon-coated copper grid used for sample loading. The energy dispersive X-ray (EDX) unit of TEM (JSM-6360 microscope; JEOL, Tokyo, Japan) was used to evaluate the elemental analysis of the prepared CuO-NPs. The net surface charge (zeta potential) of the prepared NPs was evaluated through Zetasizer nanoseries (ZS, Malvern, Germany). The hydrodynamic size of the prepared CuO-NPs in colloidal solution was evaluated at two angles, 11 and 90°, through Malvern Zetasizer (ZS). Furthermore, the surface functional groups of CuO-NPs were examined utilizing the KBr-disc technique for FTIR spectroscopy at 400–4,000 cm−1.

2.3 Plant pathogens’ isolation and preliminary identification

The isolation and identification of pathogenic fungi from strawberry plants were performed in different steps. First, plants exhibiting symptoms such as wilting, yellowing, discoloration, lesions, or abnormal growth were collected, and the roots or fruits were separated and cut into pieces. Then, a 1% (v/v) aqueous solution of sodium hypochlorite was used to sterilize the symptomatic pieces. Afterward, the small pieces were placed on potato dextrose agar (PDA) plates and incubated at 25–28°C for a week. Any plate exhibiting fungal growth was then purified and subjected to macroscopic examination, including color, texture, shape, and growth patterns, to identify the fungal species.

2.4 Molecular identification

For molecular identification, the ITS region was amplified from the isolated fungi. The extraction process began with 4-day fungal cultures, from which fungal DNA was extracted using the CTAB-DNA extraction method [26,27]. Following DNA extraction, a polymerase chain reaction (PCR) was performed to amplify the ITS region of the fungal ribosomal DNA using ITS1 and ITS4 primers [28]. Gel electrophoresis was carried out to separate the PCR products. After gel electrophoresis, the fungal-PCR amplicons were purified using a commercial purification kit (ChargeSwitch™ gDNA Plant Kit, Thermo Fisher Scientific, Carlsbad, CA, USA). The purified fragments were subsequently sent to a sequencing service provider (Macrogen Co., Seoul, Korea) for DNA sequencing utilizing Sanger sequencing technology. Upon obtaining the ITS-DNA sequence data, it underwent analysis and comparison with the reference database GenBank using sequence alignment algorithms. The BLAST tool (https://blast.ncbi.nlm.nih.gov/Blast.cgi) assisted in fungal species identification based on sequence similarity. The identified pathogenic fungi from strawberry plants were further studied to understand potential control measures.

2.5 Antimicrobial activities of the synthesized NPs

The food poison technique [29] was used to evaluate the antifungal activity of potential antifungal agents against the isolated fungi from strawberry plants. The biosynthesized CuO-NPs were prepared at 25, 50, 75, and 100 µg/mL in final concentrations. They were incorporated into a suitable solid culture medium, PDA, by being thoroughly mixed while the medium was still in a liquid state, after which the medium was poured into Petri dishes and allowed to solidify. A small plug of the isolated fungal strains was transferred onto the center of the agar plates containing the CuO-NPs using a sterile toothpick. For comparison purposes, control plates containing the culture PDA medium without the CuO-NPs were inoculated. The plates were incubated under appropriate conditions for fungal growth (25–28°C) for 7 days until sufficient fungal growth was observed in the control plates. The plates were examined, and the growth of the test fungi on the plates containing the synthesized CuO-NPs was compared with that on the control plates. The degree of inhibition was evaluated by measuring the diameter of the fungal colonies and comparing them to the control colonies. The inhibition percentage (IP) was calculated as IP% = [(control-fungal treatment)/control] × 100.

2.6 Molecular docking

Before docking, the target proteins were retrieved from the RCSB Protein Data Bank (https://www.rcsb.org/) and AlphaFold Protein Structure (https://alphafold.ebi.ac.uk/) databases. Furthermore, the target proteins were prepared by removing water molecules and attaching ligands by the UCSF Chimera software package. At the same time, the CuO structure was retrieved in the crystallographic information framework from the Material Project database (https://next-gen.materialsproject.org/) and converted to PDB format using Open Babel software. The molecular docking interaction of CuO and target proteins in Rhizoctonia solani (chitin synthase, cutinase, and agglutinin), Fusarium oxysporum (chitin synthase, cutinase, and trypsin), and Botrytis cinerea (chitin synthase, cutinase, and oxidoreductase) were done using AutoDock 4.2 tool and UCSF Chimera, while visualized by BIOVIA Discovery Studio software.

3 Results and discussion

3.1 Particle morphology, size, and elemental analysis through TEM

The surface morphology and size of the prepared CuO-NPs were evaluated through TEM. Figure 1a shows that the prepared CuO-NPs revealed well-dispersed spherical particles in different growth phases. The prepared particles revealed varied sizes ranging from 22.15 to 37.01 nm with an average size of 24.8 ± 6.1 nm (Figure 1b), which asserted the ability of H. bacciferum leaf extract to reduce Cu ions to nanoscale. The CuO-NPs of the same size were reported in other studies [30,31]. The TEM results also indicated a significant separation of all particles from each other with limited aggregation. Furthermore, all particles were surrounded with secondary material in a cap-like shape, which could be attributed to the organic material from plant extract as reported in several studies [32,33,34]. Additionally, the EDX analysis was applied to evaluate the elemental nature of the prepared CuO-NPs. The analysis (Figure 1c) revealed the existence of copper (Cu) and oxygen (O) constituents in copper oxide NPs. The occurrence of strong and narrow diffraction peaks in the EDS spectrum indicates the crystalline quality of the product [35]. The peak observed at 0.5 keV indicates the presence of oxygen, whereas the peaks observed at binding energy values of 1.0, 8.0, and 9.0 keV provide confirmation of the presence of copper [19,35,36]. In addition, the presence of a carbon atom was seen at an energy level of around 0.2 keV, which can be attributed to the organic layer present in the synthesized CuO-NPs [36]. The presence of sulfur may be attributed to the utilization of copper sulfate as the initial substance [37].

Figure 1 Surface morphology of the green synthesized CuO-NPs (a) as illustrated through transmission electron microscopy (TEM) with corresponding average particle size (b) calculated through ImageJ software. The prepared NPs’ elemental analysis is illustrated through EDX unit (c).
Figure 1

Surface morphology of the green synthesized CuO-NPs (a) as illustrated through transmission electron microscopy (TEM) with corresponding average particle size (b) calculated through ImageJ software. The prepared NPs’ elemental analysis is illustrated through EDX unit (c).

3.2 Zeta potential and particle distribution

The surface charge of NPs is an important characteristic that directly mediates the particle’s stability, biosafety, and bioactivity [38]. Hence, the net surface charge of the prepared CuO-NPs was evaluated through Zetasizer. The results indicated in Figure 2a revealed positively charged CuO-NPs with an average zeta potential of about 24.8 ± 3.23 mV, which points to the stability of the prepared particles in the biological systems as the measured zeta potential within +30 and −30 mV [39,40]. The positively charged CuO-NPs were previously reported in several CuO-NPs prepared by various plant extracts, including Stachys lavandulifolia [41] and Mussaenda frondosa L. [39]. On the other hand, the Zetasizer was used to analyze the particle size distribution of the greenly synthesized CuO-NPs. As indicated in Figure 2b, the CuO-NPs ranged between 38.4 and 192.9 nm as measured at 11° and 90°, respectively. The particle size range is significantly higher than that detected through TEM analysis, which could be accredited to the non-homogeneous particle size (polydisperse nature) of the prepared particles and the fact that DSL measures particle size in the wet state. In contrast, the TEM measures the particle size in a dried condition [42,43].

Figure 2 The surface net charge (zeta potential) of the prepared CuO-NPs (a) and hydrodynamic size at two different angles (b) as illustrated through Zetasizer.
Figure 2

The surface net charge (zeta potential) of the prepared CuO-NPs (a) and hydrodynamic size at two different angles (b) as illustrated through Zetasizer.

3.3 FTIR analysis for prepared CuO-NPs

The functional groups on the CuO-NPs were evaluated through FTIR analysis, as shown in Figure 3 and Table 1. The FTIR spectrum revealed several functional groups on the green synthesized CuO-NPs indicated by several absorption beaks in the scanning range (4,000–400 cm−1). The bands detected at 3,195 and 2,916 cm−1 showed the C–H stretching of alcohols and alkanes of phenolic and flavonoid compounds [32,44]. Two small bands were also observed at 2,338 and 1,699 cm−1, indicating O═C═O stretching and amide I bond of proteins/enzymes [45]. The three bands detected at 1,582, 1,426, and 1,325 cm−1 indicated the C═O stretching of alkanes, OH phenolic bending, and C–N stretching, respectively [32,44,46]. The band detected at 1,178 cm−1 indicated the observance of C–OH stretching and C–C stretching of alkanes [32]. The FTIR spectrum indicated a band around 1,034 cm−1, which is usually attributed to CuO formation [36,47], whereas the band at 784 cm−1 is usually attributed to M–O vibration in the CuO structure [48]. Overall, the FTIR results demonstrated the presence of various phenolic substances, terpenoids, or proteins attached to the CuO NPs’ surface, which are in line with the TEM results. The free amino and carboxylic groups that have interacted with the copper surface (as an organic coat) may cause the stability of the green synthesized CuO-NPs to prevent their agglomeration [32,49].

Figure 3 The FTIR spectra of green-synthesized CuO-NPs show various bands corresponding to distinct functional groups on the NP surface.
Figure 3

The FTIR spectra of green-synthesized CuO-NPs show various bands corresponding to distinct functional groups on the NP surface.

Table 1

FTIR spectra list of band positions for CuO-NPs in this study

Wave number (cm−1) Band Functional group References
3,195 C–H stretch Polyphenolic compounds [50]
2,916 C–H stretch Alkanes [34,51]
2,338 O═C═O stretch Carbon dioxide [34]
1,699 –C═C– stretch Alkenes [51,52]
1,582 N–H bend Amide I bonds (NH) of proteins [32,53,54]
1,426 C–O stretch Ester and aliphatic ether [54,55]
1,325 O–H stretch Phenolic group [54]
1,178 C–OH bending Alkanes [32,51,52]
1,034 C–N stretch Aliphatic and aromatic amines [32,34]
784 Cu–O vibrations Corroborating the formation of CuO-NPs [48,56,57]

3.4 Isolation and identification of the pathogenic fungi

The fungal isolates that had been obtained from infected strawberry plants were identified using morphological and molecular identification methods.

3.4.1 Symptoms and morphological identification

The morphological features of fungal colonies isolated from the plants were indicative of root rot symptoms, typically including a white to light brown color, irregular growth patterns, and a cottony to fluffy texture. Under the microscope, the fungus was characterized by its multinucleate hyphae without septa (aseptate) and the presence of sclerotia, which were compact masses of hyphae that appeared dark brown to black. All these features corresponded to the fungus R. solani [58,59].

The isolation trials conducted on symptomatic plants exhibiting wilt and yellowing of leaves revealed fungal colonies characterized by a cottony texture and white color. Microscopic analysis unveiled the presence of macroconidia, which displayed a sickle-shaped morphology with multicellular characteristics, exhibiting a curved and tapered appearance. Additionally, microconidia (small, oval, unicellular spores) and chlamydospores (thick-walled, round, survival structures) were evident. These morphological attributes were consistent with those associated with the fungus F. oxysporum as reported in previous studies [60,61]

The afflicted plants exhibited symptoms of fruit rot, commonly referred to as gray mold, with fungal colonies presenting a characteristic gray-to-brown coloration and a velvety to a fluffy texture. Microscopic examination revealed septate hyphae and the presence of conidiophores, which were branched structures responsible for bearing conidia (asexual spores). The conidia, typically oval-shaped, were produced in chains, delineating the characteristic features of B. cinerea [62,63].

3.4.2 Molecular identification

For molecular identification purposes, the ITS region of the ribosomal RNA gene cluster served as a common target. This region’s widespread adoption stemmed from its high sequence variability across fungal species, rendering it instrumental for fungal identification and phylogenetic analyses. The PCR was employed to amplify the ITS region of fungal DNA, followed by DNA sequencing and subsequent comparison with known sequences within the GenBank public database. Sequencing of the PCR-amplified ITS region was conducted for each isolate, and the resulting sequences were juxtaposed with reference sequences in the database, affirming the identities of R. solani, F. oxysporum, and B. cinerea in the infected strawberry samples. These sequences were deposited in the GenBank database under accession numbers OR116528, OR116508, and OR116491, respectively. PCR is widely recognized for its exceptional accuracy in detecting and identifying diverse organisms, encompassing pathogenic and non-pathogenic fungi, such as Alternaria alternata, F. solani, R. solani, and Aspergillus spp. [64,65]. The nuclear ribosomal internal transcribed spacer (ITS) region has been accepted as the authoritative fungal barcode and represents mycology’s most frequently examined genetic marker. The average length of the ITS region within the fungi kingdom is around 550 base pairs (bp). However, it is essential to note that this length may differ substantially among various species [66]. The geographical area under consideration encompasses two distinct regions, referred to as ITS1 and ITS2, characterized by their variability. These regions are separated by the presence of the 5.8S ribosomal gene, which is conserved to a high degree. Including a chimera, control is essential in ITS-based mycological investigations due to the crucial role played by the 5.8S gene in facilitating chimeric elongation in mixed-template PCR [67]. In conclusion, the combination of morphological and molecular identification techniques confirmed the presence of the detected fungal strains in the infected strawberry samples. This information was crucial for understanding the diseases caused by these pathogens and developing effective control strategies for strawberry production.

3.5 Antimicrobial activities against the isolated fungi

Table 2 and Figure 4 show the inhibitory percentages of the three fungi (R. solani, F. oxysporum, and B. cinerea) at four different concentrations (25, 50, 75, and 100 µg/mL) of CuO-NPs biosynthesized from H. bacciferum leaf extract. A negative control group is included, indicating no inhibition of fungal growth. At the lowest 25 µg/mL concentration, R. solani showed 78.15% inhibition, F. oxysporum exhibited 70.00% inhibition, and B. cinerea displayed 40.37% inhibition. As the concentration of CuO-NPs increased to 50 µg/mL, the IPs for R. solani, F. oxysporum, and B. cinerea were 80.00, 70.37, and 44.44%, respectively. At 75 µg/mL concentration, R. solani had 80.37% inhibition, F. oxysporum showed 70.74% inhibition, and B. cinerea demonstrated 48.52% inhibition. Finally, at the highest 100 µg/mL concentration, the IPs were 81.48% for R. solani, 71.11% for F. oxysporum, and 50.74% for B. cinerea. The data suggest that the biosynthesized CuO-NPs from H. bacciferum leaf extract can potentially suppress the growth of plant pathogenic fungi. The IPs generally increased with higher concentrations of CuO-NPs, indicating a dose-dependent effect.

Table 2

Percentage of in vitro growth suppression of plant pathogenic fungi subjected to CuO-NPs biosynthesized from H. bacciferum leaf extract

Concentrations (µg/mL) IP (%)
R. solani* F. oxysporum B. cinerea
25 78.15c 70.00a 40.37c
50 80.00b 70.37a 44.44bc
75 80.37b 70.74a 48.52ab
100 81.48a 71.11a 50.74a
Negative control 00.00d 00.00b 00.00d

*The different letters beside the antifungal means in each column indicate that the data were significantly other at probability level 0.05.

Figure 4 The antifungal activity of the CuO-NPs biosynthesized from H. bacciferum leaf extract against three fungi (R. solani, F. oxysporum, and B. cinerea).
Figure 4

The antifungal activity of the CuO-NPs biosynthesized from H. bacciferum leaf extract against three fungi (R. solani, F. oxysporum, and B. cinerea).

Nanomaterial synthesis typically employs three distinct approaches: physical, chemical, and biological processes. Plant-based nanotechnology has the potential to be cost-effective, biocompatible, dependable, and environmentally friendly. Green methods have recently gained prominence as a significant aspect of nanotechnology. Green-mediated production of nanomaterials is emerging as an alternative approach. Various green sources have been documented, such as microorganisms, fungi, viruses, and plant extracts. Jebril et al. [68] utilized Melia azedarach leaf extract as a reducing agent to green synthesize silver nanoparticles (Ag-NPs). The synthesized Ag-NPs demonstrated antifungal activity by inhibiting the growth of Verticillium dahlia [68]. Mali et al. [17] employed Celastrus paniculatus leaf extract to produce cost-effective and eco-friendly copper nanoparticles (Cu-NPs) for copper reduction. The Cu-NPs displayed significant antifungal properties against F. oxysporum [17]. Zhu et al. [69] used Cinnamomum camphora leaf extract for the green synthesis of zinc nanoparticles (Zn-NPs). The synthesized Zn-NPs exhibited antifungal activity against Alternaria alternate, inhibiting spore germination and causing cell membrane disruption. This disruption resulted in the leakage of essential proteins and nucleic acids, leading to the death of the fungal pathogen [69].

Numerous research teams have used plant leaf extracts to biosynthesize Ag-NPs and explored their antibacterial applications [70,71,72]. Ravichandran et al. discovered that Parkia speciosa leaf extract could be utilized for the green chemistry-based synthesis of Ag-NPs with antimicrobial properties, which may be employed to treat various diseases [73]. Punniyakotti et al. [74] produced Cu-NPs using Cardiospermum halicacabum leaf extracts and found that Cu-NPs possess antibacterial properties, disrupting the bacterial cell wall and hindering their growth within the host body [74]. Mukherjee et al. [75] showed that Olax scandens leaf extract could be used to make Ag-NPs using green chemistry. They revealed that the Ag-NPs can be applied in four distinct areas: antibacterial properties, anticancer, cell imaging, and as a biocompatible delivery system [75].

3.6 Molecular docking interaction

Molecular docking interaction and scores are represented in Table 3 and Figure 5. CuO bound to the binding site of chitin synthase (Figure 5a), cutinase (Figure 6a), and agglutinin (Figure 7a) in R. solani by energy of −5.2, −4.3, and −4.7 kcal/mol, respectively. By −5.4, −5.1, and −5.0 kcal/mol, CuO interacted with the binding site of chitin synthase (Figure 5b), cutinase (Figure 6b), and trypsin (Figure 7b) in F. oxysporum, respectively. Regarding the B. cinerea’s chitin synthase (Figure 5c), cutinase (Figure 6c), and oxidoreductase (Figure 7c), CuO bound with their binding sites by −4.4, −4.8, and −5.1 kcal/mol, respectively.

Table 3

Molecular docking interaction of CuO and target proteins in R. solani, F. oxysporum, and B. cinerea

Fungi Targets Binding energy (kcal/mol) Interactions
R. solani Chitin synthase −5.2 Hydrogen bonds: SER778, ARG781, TYR894, GLY905, and GLU906
Cutinase −4.3 Hydrogen bonds: THR11, LYS13, SER39, GLY41, and GLN45
Agglutinin −4.7 Hydrogen bonds: ARG88, ALA128, GLU131, and ASN155
F. oxysporum Chitin synthase −5.4 Hydrogen bonds: ASP385, PHE386, TYR389, SER395, and GLN497
Cutinase −5.1 Hydrogen bonds: SER43, ASN85, SER121, and GLN122
Trypsin −5.0 Hydrogen bonds: SER190, CYS191, SER214, TRP215, and VAL227
B. cinerea Chitin synthase −4.4 Hydrogen bonds: ASP385, PHE386, TYR389, SER395, and GLN497
Cutinase −4.8 Hydrogen bonds: ALA30, CYS31, SER32, SER67, and THR70
Oxidoreductase −5.1 Hydrogen bonds: THR35, PRO36, GLN38, GLN143, and GLN427
Figure 5 Molecular interaction of CuO-NPs and chitin synthase of R. solani (a), F. oxysporum (b), and B. cinerea (c).
Figure 5

Molecular interaction of CuO-NPs and chitin synthase of R. solani (a), F. oxysporum (b), and B. cinerea (c).

Figure 6 Molecular interaction of CuO-NPs and cutinase of R. solani (a), F. oxysporum (b), and B. cinerea (c).
Figure 6

Molecular interaction of CuO-NPs and cutinase of R. solani (a), F. oxysporum (b), and B. cinerea (c).

Figure 7 Molecular interaction of CuO-NPs and R. solani agglutinin (a), F. oxysporum trypsin (b), and B. cinerea oxidoreductase (c).
Figure 7

Molecular interaction of CuO-NPs and R. solani agglutinin (a), F. oxysporum trypsin (b), and B. cinerea oxidoreductase (c).

Targeting of fungal chitin synthase leads to loss of chitin in the fungal cell membrane and finally fungal death. Therefore, chitin synthesis is considered a promising target for antifungal drugs [76]. In addition, targeting oxidoreductases led to disturbances in fungal viability. Besides, fungal oxidoreductases play a major role in the pathogenicity and protection of fungi against host defense [77]. Fungal cutinase acts on cutin in the cuticle that covers all plant leaves, stems, flowers, and fruit [78]. Also, some antifungal agents possess trypsin inhibition and plant resistance against fungal attack [79]. Fungal agglutinin is a lectin accumulated in the mycelium and sclerotia fungi and serves as a storage protein [80]. In the current study, the molecular docking technique demonstrated that CuO has binding affinities for fungal trypsin. Furthermore, CuO exhibited binding affinities for fungal trypsin. Cutinase and agglutinin prevent the spreading of fungus on the infected strawberries.

4 Conclusions

Using an extract from H. bacciferum leaves, this study was able to make copper oxide nanoparticles (CuO-NPs). The CuO-NPs exhibited well-dispersed spherical particles with an average size of 24.8 ± 6.1 nm. The synthesized NPs displayed high concentrations of nanoscale copper ions, as confirmed by EDX analysis. Copper oxide nanoparticles produced with the help of H. bacciferum leaf extract have shown promising antifungal action against strawberry infections. The current work used molecular docking experiments to examine the interactions between the NPs and the target pathogens, revealing important details about their mechanism of action. The molecular docking model demonstrated CuO’s affinity for engaging the binding sites of fungal target proteins, allowing researchers to investigate its antifungal potential. These interactions shed light on the putative mechanisms by which NPs exercise their antifungal effects. This information is critical for understanding the underlying mechanisms and enhancing the design of future antifungal NPs. Our findings show that copper oxide nanoparticles mediated by H. bacciferum leaf extract have the potential to be a practical and effective antifungal agent against strawberry infections. Further research and development in this area may result in the development of novel solutions for long-term crop protection and disease management in strawberry agriculture.

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Acknowledgments

The authors express their sincere thanks to the City of Scientific Research and Technological Applications (SRTA-City) and the Faculty of Agriculture (Saba Basha), Alexandria University, Egypt, for providing the necessary research facilities. The authors would like to extend their appreciation to the Researchers Supporting Project number (RSP2024R505), King Saud University, Riyadh, Saudi Arabia.

  1. Funding information: The research was financially supported by Researchers Supporting Project number (RSP2024R505), King Saud University, Riyadh, Saudi Arabia.

  2. Author contributions: Study conception and design: A.A. and S.B.; data collection: E.H.l; analysis and interpretation of results: H.El., A.Al., P.K., and A.El.; and draft manuscript preparation: A.A., S.B., H.El., A.Al., and A.El. All authors reviewed the results and approved the final version of the manuscript.

  3. Conflict of interest: The authors declare no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animals use.

  5. Data availability statement: The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-03-16
Revised: 2024-03-31
Accepted: 2024-04-10
Published Online: 2024-05-06

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  88. Preparation, characterization, and determination of the therapeutic effects of copper nanoparticles green-formulated by Pistacia atlantica in diabetes-induced cardiac dysfunction in rat
  89. Antioxidant and antidiabetic potentials of methoxy-substituted Schiff bases using in vitro, in vivo, and molecular simulation approaches
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  96. Fabrication of β-cyclodextrin-based microgels for enhancing solubility of Terbinafine: An in-vitro and in-vivo toxicological evaluation
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  99. Quality control analyses of selected honey samples from Serbia based on their mineral and flavonoid profiles, and the invertase activity
  100. Eco-friendly synthesis of silver nanoparticles using Phyllanthus niruri leaf extract: Assessment of antimicrobial activity, effectiveness on tropical neglected mosquito vector control, and biocompatibility using a fibroblast cell line model
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  102. Quality changes of durian pulp (Durio ziberhinus Murr.) in cold storage
  103. Study on recrystallization process of nitroguanidine by directly adding cold water to control temperature
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  112. Torilis arvensis ethanolic extract: Phytochemical analysis, antifungal efficacy, and cytotoxicity properties
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  114. HPLC and GC–MS analyses of phytochemical compounds in Haloxylon salicornicum extract: Antibacterial and antifungal activity assessment of phytopathogens
  115. Efficient and stable to coking catalysts of ethanol steam reforming comprised of Ni + Ru loaded on MgAl2O4 + LnFe0.7Ni0.3O3 (Ln = La, Pr) nanocomposites prepared via cost-effective procedure with Pluronic P123 copolymer
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  128. Special Issue on Recent Trends in Green Chemistry
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  135. Green synthesis, characterization, and application of iron and molybdenum nanoparticles and their composites for enhancing the growth of Solanum lycopersicum
  136. Green synthesis of silver nanoparticles from Olea europaea L. extracted polysaccharides, characterization, and its assessment as an antimicrobial agent against multiple pathogenic microbes
  137. Photocatalytic treatment of organic dyes using metal oxides and nanocomposites: A quantitative study
  138. Antifungal, antioxidant, and photocatalytic activities of greenly synthesized iron oxide nanoparticles
  139. Special Issue on Phytochemical and Pharmacological Scrutinization of Medicinal Plants
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  141. Chemical composition and biological properties of Thymus capitatus plants from Algerian high plains: A comparative and analytical study
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  143. In vivo protective effects of vitamin C against cyto-genotoxicity induced by Dysphania ambrosioides aqueous extract
  144. Insights about the deleterious impact of a carbamate pesticide on some metabolic immune and antioxidant functions and a focus on the protective ability of a Saharan shrub and its anti-edematous property
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  146. A study to investigate the anticancer potential of carvacrol via targeting Notch signaling in breast cancer
  147. Assessment of anti-diabetic properties of Ziziphus oenopolia (L.) wild edible fruit extract: In vitro and in silico investigations through molecular docking analysis
  148. Optimization of polyphenol extraction, phenolic profile by LC-ESI-MS/MS, antioxidant, anti-enzymatic, and cytotoxic activities of Physalis acutifolia
  149. Phytochemical screening, antioxidant properties, and photo-protective activities of Salvia balansae de Noé ex Coss
  150. Antihyperglycemic, antiglycation, anti-hypercholesteremic, and toxicity evaluation with gas chromatography mass spectrometry profiling for Aloe armatissima leaves
  151. Phyto-fabrication and characterization of gold nanoparticles by using Timur (Zanthoxylum armatum DC) and their effect on wound healing
  152. Does Erodium trifolium (Cav.) Guitt exhibit medicinal properties? Response elements from phytochemical profiling, enzyme-inhibiting, and antioxidant and antimicrobial activities
  153. Integrative in silico evaluation of the antiviral potential of terpenoids and its metal complexes derived from Homalomena aromatica based on main protease of SARS-CoV-2
  154. 6-Methoxyflavone improves anxiety, depression, and memory by increasing monoamines in mice brain: HPLC analysis and in silico studies
  155. Simultaneous extraction and quantification of hydrophilic and lipophilic antioxidants in Solanum lycopersicum L. varieties marketed in Saudi Arabia
  156. Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models
https://doi.org/10.1515/chem-2024-0028
Keywords for this article
copper oxide nanoparticles; Heliotropium bacciferum; green synthesis; antifungal activity; plant disease; molecular docking
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BY 4.0

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  102. Quality changes of durian pulp (Durio ziberhinus Murr.) in cold storage
  103. Study on recrystallization process of nitroguanidine by directly adding cold water to control temperature
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  105. Larvicidal properties of essential oils of three Artemisia species against the chemically insecticide-resistant Nile fever vector Culex pipiens (L.) (Diptera: Culicidae): In vitro and in silico studies
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  114. HPLC and GC–MS analyses of phytochemical compounds in Haloxylon salicornicum extract: Antibacterial and antifungal activity assessment of phytopathogens
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  124. Structural aspects of Pt(η3-X1N1X2)(PL) (X1,2 = O, C, or Se) and Pt(η3-N1N2X1)(PL) (X1 = C, S, or Se) derivatives
  125. Biosurfactants in biocorrosion and corrosion mitigation of metals: An overview
  126. Stimulus-responsive MOF–hydrogel composites: Classification, preparation, characterization, and their advancement in medical treatments
  127. Electrochemical dissolution of titanium under alternating current polarization to obtain its dioxide
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  129. Phytochemical screening and antioxidant activity of Vitex agnus-castus L.
  130. Phytochemical study, antioxidant activity, and dermoprotective activity of Chenopodium ambrosioides (L.)
  131. Exploitation of mangliculous marine fungi, Amarenographium solium, for the green synthesis of silver nanoparticles and their activity against multiple drug-resistant bacteria
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  133. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part III
  134. Impact of biogenic zinc oxide nanoparticles on growth, development, and antioxidant system of high protein content crop (Lablab purpureus L.) sweet
  135. Green synthesis, characterization, and application of iron and molybdenum nanoparticles and their composites for enhancing the growth of Solanum lycopersicum
  136. Green synthesis of silver nanoparticles from Olea europaea L. extracted polysaccharides, characterization, and its assessment as an antimicrobial agent against multiple pathogenic microbes
  137. Photocatalytic treatment of organic dyes using metal oxides and nanocomposites: A quantitative study
  138. Antifungal, antioxidant, and photocatalytic activities of greenly synthesized iron oxide nanoparticles
  139. Special Issue on Phytochemical and Pharmacological Scrutinization of Medicinal Plants
  140. Hepatoprotective effects of safranal on acetaminophen-induced hepatotoxicity in rats
  141. Chemical composition and biological properties of Thymus capitatus plants from Algerian high plains: A comparative and analytical study
  142. Chemical composition and bioactivities of the methanol root extracts of Saussurea costus
  143. In vivo protective effects of vitamin C against cyto-genotoxicity induced by Dysphania ambrosioides aqueous extract
  144. Insights about the deleterious impact of a carbamate pesticide on some metabolic immune and antioxidant functions and a focus on the protective ability of a Saharan shrub and its anti-edematous property
  145. A comprehensive review uncovering the anticancerous potential of genkwanin (plant-derived compound) in several human carcinomas
  146. A study to investigate the anticancer potential of carvacrol via targeting Notch signaling in breast cancer
  147. Assessment of anti-diabetic properties of Ziziphus oenopolia (L.) wild edible fruit extract: In vitro and in silico investigations through molecular docking analysis
  148. Optimization of polyphenol extraction, phenolic profile by LC-ESI-MS/MS, antioxidant, anti-enzymatic, and cytotoxic activities of Physalis acutifolia
  149. Phytochemical screening, antioxidant properties, and photo-protective activities of Salvia balansae de Noé ex Coss
  150. Antihyperglycemic, antiglycation, anti-hypercholesteremic, and toxicity evaluation with gas chromatography mass spectrometry profiling for Aloe armatissima leaves
  151. Phyto-fabrication and characterization of gold nanoparticles by using Timur (Zanthoxylum armatum DC) and their effect on wound healing
  152. Does Erodium trifolium (Cav.) Guitt exhibit medicinal properties? Response elements from phytochemical profiling, enzyme-inhibiting, and antioxidant and antimicrobial activities
  153. Integrative in silico evaluation of the antiviral potential of terpenoids and its metal complexes derived from Homalomena aromatica based on main protease of SARS-CoV-2
  154. 6-Methoxyflavone improves anxiety, depression, and memory by increasing monoamines in mice brain: HPLC analysis and in silico studies
  155. Simultaneous extraction and quantification of hydrophilic and lipophilic antioxidants in Solanum lycopersicum L. varieties marketed in Saudi Arabia
  156. Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models
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