
==== Front
Open Life Sci
Open Life Sci
biol
Open Life Sciences
2391-5412
De Gruyter

biol-2022-0962
10.1515/biol-2022-0962
Research Article
Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
Bashir Shimaa y_basher@yahoo.com

Behiry Said said.behiry@alexu.edu.eg

Al-Askar Abdulaziz A. aalaskara@ksu.edu.sa

Kowalczewski Przemysław Łukasz przemyslaw.kowalczewski@up.poznan.pl

Emaish Haitham H. drhaitham1976@alexu.edu.eg

Abdelkhalek Ahmed aabdelkhalek@srtacity.sci.eg

Plant Protection and Biomolecular Diagnosis Department, Arid Lands Cultivation Research Institute, City of Scientific Research and Technological Applications, Alexandria, 21934, Egypt
Agricultural Botany Department, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria, 21531, Egypt
Department of Botany and Microbiology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia
Department of Food Technology of Plant Origin, Poznań University of Life Sciences, Poznań, Poland
Department of Soils and Agricultural Chemistry, Biosystem Engineering, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria, 21531, Egypt
tel: +20-10-0755-6883
03 9 2024
2024
19 1 2022096224 4 2024
25 7 2024
19 8 2024
© 2024 the author(s), published by De Gruyter
2024
the author(s), published by De Gruyter
https://creativecommons.org/licenses/by/4.0/ This work is licensed under the Creative Commons Attribution 4.0 International License.

Abstract

The research into the use of plants as plentiful reservoirs of bioactive chemicals shows significant potential for agricultural uses. This study focused on analyzing the chemical composition and potency of an ethanolic extract obtained from the aerial parts (leaves and stems) of Salsola kali against potato pathogenic fungal and bacterial pathogens. The isolated fungal isolates were unequivocally identified as Fusarium oxysporum and Rhizoctonia solani based on morphological characteristics and internal transcribed spacer genetic sequencing data. The antifungal activity of the extract revealed good inhibition efficacy against R. solani (60.4%) and weak activity against F. oxysporum (11.1%) at a concentration of 5,000 µg/mL. The S. kali extract exhibited strong antibacterial activity, as evidenced by the significant inhibition zone diameter (mm) observed in all three strains of bacteria that were tested: Pectobacterium carotovorum (13.33), Pectobacterium atrosepticum (9.00), and Ralstonia solanacearum (9.33), at a concentration of 10,000 µg/mL. High-performance liquid chromatography analysis revealed the presence of several polyphenolic compounds (μg/g), with gallic acid (2942.8), caffeic acid (2110.2), cinnamic acid (1943.1), and chlorogenic acid (858.4) being the predominant ones. Quercetin and hesperetin were the predominant flavonoid components, with concentrations of 1110.3 and 1059.3 μg/g, respectively. Gas chromatography-mass spectrometry analysis revealed the presence of many bioactive compounds, such as saturated and unsaturated fatty acids, diterpenes, and phytosterols. The most abundant compound detected was n-hexadecanoic acid, which accounted for 28.1%. The results emphasize the potential of S. kali extract as a valuable source of bioactive substances that possess good antifungal and antibacterial effects, which highlights its potential for many agricultural uses.

Keywords

Salsola kali
antifungal activity
antibacterial activity
phytochemical
HPLC
GC-MS
==== Body
pmc1 Introduction

Plants are continually exposed to a wide range of pests and microbial pathogens in their environment. Plant diseases significantly reduce crop quality and yield or limit production, causing severe agricultural losses [1,2]. In tropical and subtropical regions, fungi are the primary cause of many plant diseases, which leads to a substantial reduction in agricultural output [3]. Pathogenic fungi may cause serious diseases in a wide variety of flowering plants. Some fungal species have a wide host range, while others are extremely host-specific [4]. Based on their relationship with the host, fungal pathogens are divided into three categories: biotrophic, which feeds on living cells; necrotrophic, which kills and feeds on dead cells; and hemibiotrophic, which follows a biphasic strategy [5]. There is evidence that necrotrophic fungi are more economically harmful than biotrophic ones. Both Rhizoctonia solani and Botrytis cinerea are typical examples of necrotrophic pathogens that infect a wide range of dicot plants, and they are linked closely to symptoms of gray mold and root or rot disease [6,7,8]. On the contrary, Fusarium oxysporum is a host-specific hemibiotrophic pathogen that infects plant vascular tissue, causing Fusarium wilt disease [9].

Although bacterial diseases of plants are less common than fungal ones, the economic loss caused by these diseases is massive [10]. Bacterial plant pathogens are worldwide in disruption and have wide host ranges. The majority of agriculturally important crops, such as potatoes, tomatoes, eggplants, peppers, etc., are susceptible to a variety of bacterial infections [11]. There are over 150 bacterial species that cause various plant diseases, and they have been divided into the following three families: Xantomonadaceae, Pseudomonaceae, and Enterobacteriaceae [12]. Dickeya, Pectobacterium, Ralstonia, and Xanthomonas are the most common genera that cause blackleg, bacterial soft rot, brown rot, and spot diseases, respectively [13,14]. Pathogenic bacteria penetrate plant tissue and cause cell death by secreting lytic enzymes that degrade and destroy cellular structure. In addition to these enzymes, bacteria also produce exopolysaccharides, toxins, and phytohormones, which are all virulence factors that help them cause disease [15].

Chemical pesticides are the primary method for controlling plant diseases [16]. The continued use of pesticides has a negative influence on the surrounding environment and public health. These harmful effects are a result of the high toxicity and lack of biodegradability of pesticides [17,18]. Therefore, using natural materials as a form of disease management is a novel approach to agricultural development. Biopesticides are a term that refers to pesticides made from natural sources. In comparison to synthetic pesticides, biopesticides have a shorter half-life in the environment, thus reducing possible environmental effects and delaying pathogen resistance development [19].

The Salsola genus, from the Amaranthaceae family (previously Chenopodiaceae), is an annual and perennial herb, shrub, and semi-shrub plant that grows in places with low annual rainfall and saline soils [20]. The genus names originate from the Latin words “salsus” or “sallere,” which means “to salt.” This genus, which consists of about 100–150 species, is common along seashores, in grasslands, and in semiarid and arid regions. Salsola species are resistant to pH, heat, water, and salt stresses, and they represent approximately 45% of desert plants [21]. Several plants belonging to the genus Salsola are used in the pharmaceutical and cosmetic industries to treat cough, influenza, and skin diseases, as well as traditional medicine. The aqueous ethanolic extract of Salsola cyclophylla exhibited the most significant analgesic effect, reducing pain by 89.86, 87.50, and 99.66% after 60, 90, and 120 min, respectively. Additionally, this extract showed the highest anti-inflammatory activity, with reductions of 41.07, 34.51, and 24.82% after 2, 3, and 6 h of administration, respectively. Because of its relatively high crude protein content, the plant is also utilized as animal feed during times of difficulty and drought [22,23]. Additionally, some species of the genus Salsola have been described as having industrial benefits. For example, Salsola soda and Salsola kali were used to make sodium carbonate, linin, cotton bleaching, glass, and soap [20,24]. The Salsola genus contains an abundance of different types of phytoconstituents, the majority of which are flavonoids, phenolic compounds, nitrogenous compounds, saponins, triterpenes, sterols, fatty acids, and volatile constituents [21,25,26]. Plants in the genus Salsola have antimicrobial and antioxidant effects that are generally attributed to secondary metabolic products. The plant extracts of Salsola vermiculata and Salsola cyclophylla, which contain a high concentration of flavonoids, steroids, and alkaloids, showed significant antimicrobial activity against Staphylococcus aureus, Klebsiella pneumonia, and Candida albicans [27,28]. Oueslati et al. [26] stated that the chloroform fractions of Salsola villosa displayed promising activity against Gram-positive and Gram-negative bacteria. Recently, nine organic compounds were detected as major constituents of the aerial part of S. kali, which is shown to have antimicrobial activity against S. aureus, Staphylococcus epidermidis, and Candida kefyr [29]. The utilization of extracts derived from Salsola plants as biocontrol agents for plant diseases is now in its nascent phase. This investigation aims to analyze the phytochemical composition of Salsola kali extract utilizing high-performance liquid chromatography (HPLC) and gas chromatography-mass spectrometry (GC-MS) techniques, with the objective of assessing its potential efficacy against three bacterial and two fungal plant pathogens.

2 Materials and methods

2.1 Collection and plant identification

The S. kali plant was collected from Borg El-Arab City, Alexandria, Egypt, at coordinates 30°54′25.9ʺN 29°32′41.3ʺE. The plant material was taxonomically identified at the Plant Production Department, Faculty of Agriculture (Saba Basha), Alexandria University, Egypt. We also performed a molecular identification to confirm the plant taxonomy’s identity. Fresh plant tissue was collected, and genomic DNA was extracted using the cetyltrimethylammonium-bromide method [30]. The tissue was ground to a fine powder in liquid nitrogen, and an extraction buffer was added to facilitate DNA extraction. Following extraction, DNA purification was performed using phenol/chloroform/isoamyl alcohol, and the DNA was precipitated with isopropanol. The DNA pellet was washed with ethanol, air-dried, and resuspended in tris-ethylenediaminetetraacetic acid (EDTA) buffer (10 mM Tris–HCl, 1 mM EDTA, pH 8.0). DNA quality and quantity were assessed using agarose gel electrophoresis and a spectrophotometer. The internal transcribed spacer (ITS) region of nuclear ribosomal DNA was amplified using the primers ITS1 (5′-TCCGTAGGTGAACCTGCGG-3′) and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′). A polymerase chain reaction (PCR) mix was prepared containing genomic DNA, 10× Taq buffer, 25 mM MgCl2, 2.5 mM dNTP mix, 10 µM of each primer, and Taq DNA polymerase. The PCR conditions included an initial denaturation at 95°C for 2 min, followed by 35 cycles of denaturation at 95°C for 1 min, annealing at 55°C for 45 s, and extension at 72°C for 1 min. The amplification was completed with a final extension step at 72°C for 5 min. The PCR product size was confirmed by running it on a 1% agarose gel stained with redsafe stain. For the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit (rbcL) gene, the primers rbcL1 (5′-ATGTCACCACAAACAGAAAC-3′) and rbcL724R (5′-TCGCATGTACCTGCAGTAGC-3′) were used. A PCR reaction mix similar to that used for the ITS region was prepared. The thermal cycling conditions were: initial denaturation at 94°C for 3 min, followed by 35 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s, and extension at 72°C for 1 min. A final extension at 72°C for 10 min was performed. Gel electrophoresis was used to validate amplification. Purification of the PCR products was carried out using a PCR purification kit from QIAquick (Cat. No.28104, Hilden, Germany). The purified products were sequenced using the Sanger sequencing method, with the same primers used for PCR amplification. The sequencing results were analyzed using bioinformatic tools. BLAST was used to find matches between sequences and GenBank reference databases in order to identify plant species based on the ITS region and rbcL gene sequences.

2.2 Crude extract preparation

Before the extraction process, the aerial parts of the plant (leaves and stems) were washed with water to remove soil particles and air-dried at room temperature. The dried plant materials were then powdered using a blender and sieved through a 100-mesh stainless steel sieve. The maceration procedure extracted approximately 50 g of powdered aerial portions of the S. kali plant with 150 mL of absolute ethanol as a solvent [31]. The combination was allowed to soak for 3 days under laboratory conditions and darkness. To eliminate any plant debris, the extract was filtered through Whatman filter paper No. 1, and the solvent was evaporated with a rotary evaporator to yield the S. kali extract. The crude extract was generated in different concentrations and emulsified using dimethyl sulfoxide (DMSO).

2.3 Source of the phytopathogenic microorganisms and their identification

Bacterial strains used in this study are listed in Table 1. Meanwhile, the fungal isolates were isolated from potato plants and tubers that showed dry rot or black scurf. The infected potato tissues were washed with tap water to eliminate soil particles. We subjected decaying tuber fragments to a 2% sodium hypochlorite solution for a duration of 5 min. Subsequently, we rinsed the samples three times with sterile distilled water, each rinse lasting 5 min. Finally, we dried the samples using sterile filter paper. About 0.5-cm fragments that had been disinfected were placed on potato dextrose agar (PDA) media. Each plate contained four pieces, which were then cultivated at a temperature of 25°C for 5–7 days. Multiple fungal colonies were identified on the PDA medium; however, only colonies resembling Fusarium or Rhizoctonia-like were selected. For Fusarium, the fungal isolate was initially identified based on its physical characteristics using the morphological criteria outlined by Leslie and Summerell [32]. Following the steps outlined by Stefańczyk and Sobkowiak [33], the subcultures that came from the outermost part of the colony were separated by letting the conidia germinate on water agar at 16°C for 1–2 days. Rhizoctonia-like colonies were identified based on their morphological characteristics, as outlined by Rliizoctonja and Solan [34]. The ITS amplification region was used to confirm the species molecular characterization of the fungal isolates that were collected [35]. These were then sequenced at Macrogen Company in Seoul, Korea. The sequences were submitted to the GenBank website and aligned with the most related strains. To obtain the accession numbers, the identified isolates were deposited at the NCBI.

Table 1 List of phytopathogenic microorganisms used in this study

Classification	Strain	Accession number	References	
Phytopathogenic fungi	F. oxysporum	This study	—	
R. solani	This study	
Phytopathogenic bacteria	Pectobacterium carotovorum	HF674984	[36]	
Pectobacterium atrosepticum	MG706146	
Ralstonia solanacearum	GH425351	

2.4 Antifungal assay of the plant extract

The mycelia growth rate method was employed to investigate the antifungal efficacy of S. kali extract against three phytopathogenic fungi [37]. The fungal strains were grown on PDA medium for 7 days at 25°C. After this, 5 mm plugs of fungus cut from the edge of the fungus colony were put in the middle of the PDA plates, which have a gradient of plant extract concentrations from 1,000 to 5,000 µg/mL. There are three replicates for each treatment. One set of the plates was used as negative controls, in which DMSO was used instead of the plant extract, while the fungicide carbendazim 50 WP (250 µg/mL) was used in another set as a positive control. In the dark, the cultures were incubated at 25°C for 7 days. For each replicate, the average of two perpendicular mycelia-growth diameters was used to calculate radial mycelial growth. The following formula was used to convert the radial growth rate to a percentage of inhibition. Growth inhibition (%) = [(C − T)/C] × 100, where C is the radial growth in the control (mm) and T is the radial growth in the presence of plant extract (mm).

2.5 Antibacterial assay of the plant extract

The plant extract was screened for antibacterial activity using the well agar method as described by Balouiri et al. [38]. The bacterial strains were pre-cultured in Luria–Bertani broth overnight in a shaking incubator at 30°C. Then, a 0.5 McFarland standard was used to dilute each strain to a concentration of 108 cells/mL. Using a cotton swab, sterile Luria–Bertani agar plates were streaked uniformly with the standardized bacterial broth culture. Wells of equal size (6 mm in diameter) were made into each plate using a sterile cork borer and filled with 50 µL of 3,000, 5,000, 7,000, and 10,000 µg/mL of S. kali extract. The positive and negative controls consisted of vancomycin (30 μg/mL) and DMSO (50 µL/well), respectively. All the plates were kept in the refrigerator for 2 h to allow the extracts to diffuse into the agar and then incubated at 30°C overnight. By measuring the diameters of inhibitory zones (including well diameter) on the agar surface around the wells, the sensitivity of the bacterial strains to the plant extracts was calculated.

2.6 HPLC analysis of phenolic and flavonoid compounds of the plant extract

The HPLC profile of phenolics and flavonoids in S. kali extract was performed using an Agilent 1260 Infinity HPLC Series system with a quaternary pump. The separation was achieved using a Zorbax Eclipse Plus C18 column, 100 mm in length and 4.6 mm in width. A 20 µL of plant extract was filtered through a 0.2 µm syringe filter and then injected into the system. A gradient of 0.2% (v/v) phosphoric acid in HPLC-grade water (mobile phase A), methanol (mobile phase B), and acetonitrile (mobile phase C) was used to separate the substances. The flow rate was kept at 0.7 ml/min, and the absorbance of detection was 273 nm at 30°C [39]. In order to measure the amount of phenolic and flavonoid compounds, the following standards were used: methyl gallate, caffeic acid, syringic acid, pyrocatechol, rutin, ellagic acid, coumaric acid, vanillin, ferulic acid, naringenin, daidzein, quercetin, cinnamic acid, apigenin, kaempferol, and hesperetin.

2.7 GC-MS analysis

The chemical composition of the extract from S. kali was analyzed using a GC-MS instrument with an Agilent 7000D instrument from Technologies in Santa Clara, CA, USA. The GC-MS instrument was equipped with a column composed of a combination of 5% diphenyl and 95% dimethylpolysiloxane, as well as an HP-5MS capillary column. The carrier gas, composed of 99.99% helium, was controlled to flow at a rate of 1 mL per minute. The scanning duration for ionization energy was set to 70 eV, with a rate of 0.2 s. The fragment detection ranged from 40 to 600 m/z. The sample was injected into 1 μL aliquots and split in a 10:1 ratio at 250°C. The starting oven temperatures of the column were set at 50°C with a rate of increase of 3 min. They were then gradually increased by 10°C per minute until reaching 280°C. Finally, the temperatures were raised to 300°C with a rate of growth of 10 min. The phytochemical components that were identified were compared to the authentic chemicals found in the Wiley Registry 8E, Replib, and Mainlib libraries [40].

2.8 Statistical analysis

The antimicrobial inhibition % and diameter of the inhibition zone were tested three times, and the average was calculated. The data were then examined statistically with a one-way analysis of variance (ANOVA) in the CoStat program, substantially distinguishing the means at the LSD 0.05 level.

3 Results

3.1 Identification of S. kali plant

The examined plant sample was recognized based on its morphology as S. kali (Figure 1) and has been stored in the repository of Alexandria University with the assigned number 7709. The genomic DNA extracted from the plant sample was successfully amplified using PCR for both the ITS region and the rbcL gene. Gel electrophoresis confirmed the presence of PCR products of expected sizes for both markers. Sequencing of the PCR products yielded high-quality sequences for the ITS region and rbcL gene. The sequences were analyzed using bioinformatics tools and compared to reference sequences in GenBank. Based on sequence similarity, the plant sample was identified as S. kali and accessioned with numbers PP948524 and PP955420 for ITS region and rbcL, respectively.

Figure 1 Overview of the S. kali whole plant.

3.2 Fusarium and Rhizoctonia isolates identification

The morphological characteristics of the isolated fungi were investigated by observing their growth attributes on PDA and using a light microscope (Figure 2). The isolated Fusarium had fast-growing colonies on PDA that were initially white but turned pink to violet with age, presenting a cottony or woolly appearance. Its conidiophores were simple or branched, bearing both monophialides and polyphialides. The macroconidia were fusiform to sickle-shaped, typically 3–5 septate, and slightly curved with pointed ends (Figure 2). The microconidia were ellipsoid to cylindrical, mostly single-celled (Figure 2). All these features correspond to the fungal species F. oxysporum. Rhizoctonia, in other words, formed light brown to dark brown colonies on PDA with dense, crust-like growth and a smooth, slightly shiny texture. In its hyphae, there were right-angle branching with septa close to the branching point, cells with more than one nucleus, and no clamp connections (Figure 2). All these phenotypic characters indicated that the fungal isolate was R. solani. Following this, these isolates were molecularly identified using Sanger sequencing’s ITS region recognition. After alignment in the GenBank database, the fungal isolates were definitively identified as F. oxysporum and R. solani, and they were deposited under accession numbers OR116509 and OR116529, respectively.

Figure 2 (a) Upper view of hyphal growth of R. solani on PDA medium contained black sclerotia. (b) Microscopic features of R. solani, showing angle branching of septate hyphae. (c) Upper view hyphal growth of F. oxysporum on PDA medium. (d) Microscopic traits of F. oxysporum, showing macroconidia and microconidia. (e) Microscopic view of F. oxysporum, showing chlamydospores.

3.3 The yield of the S. kali extract and its antifungal activity

The aerial parts of S. kali were extracted with ethanol, resulting in 87.4 mg/g of dry matter. The plant extract’s in vitro antifungal activity was assessed by measuring its inhibitory effects on F. oxysporum and R. solani (Figure 3). Table 2 compares the growth inhibition percentage of fungal strains when exposed to various amounts of the extract with an untreated control for comparison. Out of the fungal strains that were examined, R. solani was shown to be the most susceptible to the S. kali extract. At a concentration of 5,000 µg/mL, the extract inhibited R. solani growth by 60.4%.

Figure 3 Antifungal activity of the S. kali extract against F. oxysporum and R. solani at 1,000, 2,000, 3,000, 4,000, and 5,000 µg/mL concentrations compared to the positive and negative controls.

Table 2 Effect of the S. kali extract on fungal growth

Concentration (µg/mL)	Growth inhibition (%)	
F. oxysporum	R. solani	
1,000	5.6 ± 0.22e	32.9 ± 0.56e	
2,000	6.9 ± 0.32d*	47.8 ± 0.72d	
3,000	8.2 ± 0.42c	55.5 ± 0.39c	
4,000	11.1 ± 0.53b	56.2 ± 0.72c	
5,000	11.1 ± 0.49b	60.4 ± 0.86b	
Negative control	0.0 ± 0.00f	0.0 ± 0.00f	
Positive control**	53.1 ± 0.89a	89.8 ± 0.97a	
*Averages followed by the same letter in each column mean no significant differences. **Carbendazim 50 Wp (250 µg/mL).

3.4 Antibacterial activity of S. kali extract

The antibacterial activity of plant extract was assessed by measuring its inhibitory effects on Pectobacterium carotovorum, Pectobacterium atrosepticum, and Ralstonia solanacearum (Figure 4). Table 3 demonstrates that the S. kali extract, at different doses, had significant efficacy against all the bacterial strains tested, surpassing the positive control. The plant extract had an inhibitory effect on a range of 6.00–13.33 mm, and at a concentration of 10,000 µg/mL, it had the strongest effect on the bacterial strain P. carotovorum (13.33 mm). In general, the findings indicated that there was a statistically significant distinction observed when comparing the impacts of S. kali extract at concentrations of 7,000 and 10,000 µg/mL.

Figure 4 Antibacterial activity of the S. kali extract against P. carotovorum, P. atrosepticum, and R. solanacearum at 3,000, 5,000, 7,000, and 10,000 µg/mL concentrations compared to the positive and two negative controls.

Table 3 Antibacterial activity of S. kali extracts against plant pathogenic bacteria

Concentration (µg/mL)	Inhibition zone diameter (mm) ± standard deviation	
P. carotovorum	P. atrosepticum	R. solanacearum	
3,000	8.33 ± 0.47d*	7.67 ± 0.47c	0.00 ± 0.00c	
5,000	9.00 ± 0.00cd	8.33 ± 0.47bc	9.00 ± 0.00b	
7,000	9.33 ± 0.47c	9.00 ± 0.00b	9.00 ± 0.00b	
10,000	13.33 ± 0.47b	9.00 ± 0.00b	9.33 ± 0.47b	
Negative control	0.00 ± 0.00e	0.00 ± 0.00d	0.00 ± 0.00c	
Positive control**	14.33 ± 0.47a	18.67 ± 0.47a	12.67 ± 0.47a	
*Averages followed by the same letter in each column mean no significant differences. **Vancomycin (30 μg/mL).

3.5 HPLC analysis of S. kali extract

An HPLC analysis was conducted on the fractions of S. kali to determine the presence of 10 phenolic compounds. These compounds include gallic acid, chlorogenic acid, methyl gallate, caffeic acid, syringic acid, pyrocatechol, ellagic acid, coumaric acid, ferulic acid, and cinnamic acid. According to the data presented in Figure 5 and Table 4, gallic acid had the highest concentration at 2942.8 μg/g, followed by caffeic acid at 2110.2 μg/g, cinnamic acid at 1943.1 μg/g, chlorogenic acid at 858.4 μg/g, and coumaric acid at 517.5 μg/g. Conversely, ferulic acid had a lower concentration at 84.2 μg/g, and pyrocatechol had the lowest concentration at 34.2 μg/g. Table 4 shows the results of our analysis of nine flavonoid compounds in the plant extract. The detected flavonoid compounds were quercetin (1110.3 μg/g), hesperetin (1059.3 μg/g), daidzein (314.3 μg/g), vanillin (163.3 μg/g), naringenin (104.1 μg/g), and rutin (14.1 μg/g). However, catechin, apigenin, and kaempferol were not identified.

Figure 5 HPLC chromatogram of S. kali extract.

Table 4 Retention times (RT, min) and concentrations (μg/g) of phenolic and flavonoid compounds present in S. kali extract using the HPLC system

Phenolic compounds	Flavonoid compounds	
Compound	RT*	(μg/g)	Compound	RT	(μg/g)	
Gallic acid	3.380	2942.845	Catechin	4.549	ND**	
Chlorogenic acid	4.238	858.4283	Rutin	7.961	14.1286	
Methyl gallate	5.509	266.4428	Vanillin	9.611	163.2905	
Caffeic acid	5.855	2110.179	Naringenin	10.290	104.0414	
Syringic acid	6.571	435.6735	Daidzein	12.345	314.3267	
Pyrocatechol	6.865	34.23431	Quercetin	12.817	1110.315	
Ellagic acid	8.542	405.438	Apigenin	14.469	ND	
Coumaric acid	9.218	517.4836	Kaempferol	14.948	ND	
Ferulic acid	10.077	84.15188	Hesperetin	15.265	1059.257	
Cinnamic acid	14.131	1943.147				
*RT = retention time, **ND = not detected.

3.6 GC-MS analysis of S. kali extract

GC-MS was used to find the bioactive compounds in S. kali extract. The compounds were matched chemically by looking at their retention time, peak areas, molecular weight, and molecular formula against known compounds from various mass spectral libraries. The mass spectra of the phytochemicals identified in S. kali extract are shown in Figure 6 and listed in Table 5 in more detail. The identified phytochemicals fell into various classes, including saturated and unsaturated fatty acids, fatty acid esters, dialkyl ethers, diterpenes, triterpenoid derivatives, and phytosterol. Of the 23 compounds identified, the major compound identified was n-hexadecanoic acid, which represents 28.03% of the total area, followed by ursolic acid methyl ester (13.22%), 9,12-octadecadienoic acid (12.31%), á-sitosterol (11.14%), and trans-13-octadecenoic acid (5.86%).

Figure 6 Chromatograms of GC-MS analysis of S. kali extract.

Table 5 Phytochemical constituents identified in the extract of S. kali using gas chromatography-mass spectrometry

RT	Area %	Compound	Molecular formula	Compound class	
16.65	0.64	Phenol, 2,4-bis(1,1-bimethylethyl)	C14H22O	Phenol	
22.31	1.12	Tetradecanoic acid	C14H28O2	Saturate FA*	
24.16	1.31	Ethanol, 2-(9-octadecenyloxy)-, (Z)-	C20H40O2	Dialkyl ethers	
25.61	1.26	Palmitic acid methyl ester	C17H34O2	FA ester	
26.34	28.03	n-Hexadecanoic acid	C16H32O2	Saturated FA	
26.52	0.54	Vitamin A palmitate	C36H60O2	Retinyl esters	
28.15	0.84	Hexadecanoic acid	C19H38O4	Saturated FA	
28.79	0.60	Methyl 9,9-dideutero octadecanoate	C19H36D2O2	FA	
29.11	0.98	Tetraneurin-A-diol	C15H20O5	Sesquiterpene lactone	
29.31	12.31	9,12-Octadecadienoic acid	C18H32O2	Unsaturated FA	
29.47	5.86	trans-13-Octadecenoic acid	C18H34O2	Unsaturated FA	
29.56	1.96	cis-Vaccenic acid	C18H34O2	Unsaturated FA	
29.96	3.49	Octadecanoic acid	C18H36O2	Saturated FA	
31.30	0.53	Tributyl acetylcitrate	C20H34O8	citric acid esters	
36.88	3.28	Phorbol	C20H28O6	Diterpenes	
37.96	0.74	4-Hexyl-1-(7-methoxycarbonylheptyl) bicyclo[4.4.0]deca-2,5,7-triene	C25H40O2	FA methyl ester	
41.06	13.22	Ursolic acid methyl ester	C31H50O3	Triterpenoids	
42.24	0.54	9,12-Octadecadienoic acid (Z,Z)-	C27H54O4Si2	Unsaturated FA	
42.47	0.67	5-Fluoro ADB metabolite 7	C19H26FN3O3	Cannabinoid	
42.88	3.26	Oleanolic acid	C30H48O3	Triterpenoid	
43.94	4.71	Betulin	C30H50O2	Triterpenoid	
44.32	2.98	Stigmasterol	C29H48O	Phytosterol	
45.17	11.14	á-Sitosterol	C29H50O	Phytosterol	
*FA = fatty acid.

4 Discussion

Traditional pesticides have proven to be effective in reducing pest damage in agricultural areas. However, they come with a number of serious dangers to human health and the environment [41]. Pesticide overuse has the potential to have devastating effects on biodiversity due to the toxicity it may cause in non-target organisms. Residues from pesticides can transfer to groundwater or accumulate in plant tissue, causing gastrointestinal, neurological, and carcinogenic issues in humans [42,43]. As a result, the production and use of biopesticides have increased, gradually replacing some synthetic chemical pesticides. S. kali is an annual halophytic plant that grows naturally in environments with high salt concentrations, such as coasts and desert areas. Some species of the genus Salsola, including S. kali, have a long history of use in traditional Chinese and North African medicine to treat hypertension, inflammation, and gastrointestinal diseases [22,44]. Recent studies have looked at the antimicrobial effects of Salsola species extracts on clinically important pathogenic bacterial and fungal strains. However, as far as we know, no studies have been done on the effect of S. kali extracts on phytopathogenic microorganisms.

The current study conducted an in vitro experiment, which demonstrated that Gram-negative bacteria, P. carotovorum, P. atrosepticum, and R. solanacearum exhibited greater sensitivity compared to the control. Differences in sensitivity between the two bacterial groups, Gram-positive and Gram-negative bacteria, have been observed in several studies. Elisha et al. [45] discovered that leaf extracts from nine distinct plant species were more effective against E. coli, Salmonella typhimurium, and Pseudomonas aeruginosa than S. aureus, Enterococcus faecalis, and Bacillus cereus. Makhafola et al. [46] also said that the Ochna pretoriensis crude extract had higher average minimum inhibitory concentration (MIC) values against Gram-negative bacteria than against Gram-positive bacteria in their study. However, other previous investigations obtained opposite results [47,48]. This may be attributed to the fact that the efficacy of the plant extract against bacterial pathogens depends on several factors, such as the polarity of the solvent used in the extraction process, the nature of bioactive components, and the variation in cell wall structure between Gram-positive and Gram-negative bacteria [45,49]. Regarding the antifungal study, our findings show that the S. kali extract works better against R. solani than the other tested F. oxysporum fungus. Zhao et al. [50] showed that the Moutan cortex extract had a higher inhibitory effect against R. solani and Fusarium spp. than Alternaria spp. and B. cinerea. The fungicidal activity of the plant extract depended on the type and concentration of the bioactive compounds, as found by Alotibi et al. [51], who evaluated the antifungal activity of Rumex vesicarius L. and Ziziphus spina-christi (L.) Desf. aqueous extracts at 1, 10, and 50 mg/mL and found that the increase in concentrations of plant extract had a positive relationship with the growth of fungi such as F. oxysporum and Alternaria spp. and a negative relationship with R. solani. The species-specific differences in the composition of the cell wall and/or membrane might also be responsible for these variations in antifungal efficacy.

There are several secondary metabolites produced by plants that have the potential to act as antibacterial agents. Polyphenols are one of the most abundant secondary metabolites in the class and are classified into four main groups: phenolic acids, flavonoids, stilbenes, and lignans [52,53]. Our research showed the presence of several bioactive phenolic and flavonoid components in the S. kali extract using HPLC analysis. Gallic acid was identified as the major phenolic compound in the plant extract, followed by caffeic acid and cinnamic acid. The antimicrobial capability of numerous bioactive substances is typically closely related to the presence of phenolic compounds. Gallic acid has been proven to possess potent bactericidal properties against multi-drug-resistant E. coli and effectively hinder the production of bacterial biofilm [54]. Pinho et al. [55] found that gallic acid and caffeic acid from various wild plants can stop the growth of three types of bacteria: S. epidermidis, S. aureus, and K. pneumoniae. Wang et al. [56] demonstrated that the antifungal properties of cinnamic acid against Sclerotinia sclerotiorum extend to preventing sclerotia formation as well as mycelial growth. The phenolic acids caused the bacterial cell to explode due to hyperacidification of the plasma membrane and the efflux pump. In the present study, we also observed a significant number of flavonoid compounds in the S. kali extract. These bioactive components in the plant extract may be responsible for its antibacterial properties. Flavonoids have the potential to influence protein and RNA production by reducing energy consumption and DNA synthesis. Flavonoids may also inhibit various cellular enzyme synthases involving nucleic acid synthesis, the bacterial respiratory chain, or cell envelope synthesis [57,58].

GC-MS is a proven method for identifying and quantifying bioactive chemicals in plants. The qualitative phytochemical analysis of S. kali extract revealed the presence of numerous compounds belonging to different organic classes. Fatty acids, saturated and unsaturated, were the most abundant hydrocarbon compounds identified in this extract. Numerous plant species use fatty acids as a defense mechanism against pathogenic bacteria. Fatty acids’ primary goal is to interfere with the electron transport chain. Furthermore, they decrease nutrition absorption and inhibit enzyme function [59]. The most abundant phytochemical compound found in the GC-MS analysis was the fatty acid n-hexadecanoic acid, which has antioxidant and antifungal properties against Alternaria alternata [31,60]. The n-hexadecanoic acid exhibited considerable antimicrobial properties against S. aureus, B. subtilis, E. coli, and K. pneumoniae, with inhibition zones of 7.96, 10.96, 11.10, and 11.93 mm, respectively, at a maximum concentration of 50 µg/mL [61]. The presence of n-hexadecanoic acid has been detected in plant extracts of Benincasa hispida, Carissa congesta, Allium nigrum, Kielmeyera coriacea, Cyrtocarpa procera, Labisia pumila, and Rosa indica. It has been claimed that this compound has antibacterial properties [62]. Furthermore, the in silico technology has been employed to utilize n-hexadecanoic acid in the development of phospholipase A (2) inhibitors that are specifically designed. This was achieved by comparing it with other established inhibitors that function as anti-inflammatory medicines [63,64]. The primary target of its activity is the bacterial cell membranes. Furthermore, it impedes cellular energy production, hinders enzyme function, and ultimately leads to bacterial cell destruction. Due to its high level of safety and effectiveness, this antibacterial therapeutic drug has enormous promise [65].

Ursolic acid methyl ester, also known as urs-12-en-28-oic acid or 3-hydroxy-methyl ester, is the second most bioactive compound in our extract. It is a natural triterpenoid compound that has been suggested to have antioxidant properties [66]. Terpenoids have antioxidant properties because they eliminate free radicals. They also have antibacterial or bactericidal properties because they can inhibit oxygen uptake and oxidative phosphorylation [67]. In a study by dos Santos et al. [68], they looked at the antibacterial activity of ursolic acid or its combination with other tripenoid such as oleanolic acid. They found that the mix of ursolic and oleanolic acids (1 + 2) was the most effective against Bacteroides fragilis, with an MIC value of 20 μg/mL. The combination had higher activity than ursolic acid alone (MIC = 80 μg/mL), suggesting a potential synergistic effect. The 1 + 2 combination was potent against Actinomyces naeslundii and Porphyromonas gingivalis, with MIC values of 20 and 40 μg/mL, respectively. Andrade et al. [69] found that ursolic acid was effective against most bacteria tested, with MIC values of 20 μg/mL for A. naeslundii and P. gingivalis, 80 μg/mL for B. fragilis, and 90 μg/mL for Prevotella nigrescens. Oleanolic acid successfully inhibited A. naeslundii and P. gingivalis strains, with MIC values of 20 and 40 μg/mL, respectively [70].

Mallavadhani et al. [71] have demonstrated that lipophilicity plays a crucial role in the development of biological agents. The scientists stated that molecules with carbon chains exceeding C-10 are highly lipophilic and so well-suited for pharmacological testing. Based on these discoveries, two lipophilic derivatives of ursolic acid with 3-O-fatty acid ester chains (1b and 1c) were synthesized [68]. The 3β-dodecanoate (1b) and 3β-octadecanoate (1c) derivatives of ursolic acid did not result in decreased MIC values against the tested bacteria, while the C-28 methyl ester derivative (1d) improved the activity against B. fragilis only, with an MIC value of 20 μg/mL. The discrepancies in results could be attributed to the varied bacteria species used in the experiments and to the processes involved in the action. 9,12-Octadecadienoic acid was the third most common compound in our ethanolic extract. It was found in large amounts in many parts of plants, like the n-hexane extract of B. hispida and Cucurbita moschata seeds, which had two main components in large amounts. The most abundant ingredient was 9, 12-octadecadienoic acid (ZZ) with a concentration of 79.88 and 59.71%, respectively. The second major molecule was n-hexadecanoic acid, which accounted for 16.95 and 37.38% of the two plant extracts, respectively [72]. Krishnaveni et al. [73] reported that Gossypium seed powder GCMS contained 9,12-octadecadienoic acid as an abundant phytochemical compound, and the authors evaluated the ethanolic extract of the Gossypium seed powder against fungal and bacterial strains and found that Gossypium seed powder has fungicidal properties against Aspergillus niger and Aspergillus flavus. In addition, it exhibits activity against Escherichia coli and S. aureus. The seed powder exhibits antifungal and antibacterial properties at concentrations of 50 and 100 μg. It was discovered to have a higher level of bactericidal activity. The suggested antibacterial action seen in Gossypium seed powder is attributed to the presence of phytochemicals in it. Additionally, á-sitosterol and stigmasterol, phytosterol compounds that are present in high concentrations in the studied plant extract, have been shown to exhibit antimicrobial effects. Prior research has shown that stigmasterol and β-sitosterol, which were extracted from the stems of Neocarya macrophylla and Punica granatum, possess antibacterial properties [74,75]. Because of their similarity to the sterols naturally present in bacterial cells, phytosterols can be used to kill bacteria by replacing the regular sterols in the bacterial cell membrane. Disruption of the cell membrane is one of the potential processes that might explain the activity of sterols on microorganisms [76].

5 Conclusion

In conclusion, the ethanolic extract from the S. kali aerial parts effectively fought against the tested bacterial and fungal strains, as well as inhibiting their growth. Because of its high phenolic and flavonoid content, the extract had a significant inhibitory effect on R. solani, as well as other bacterial strains such as P. carotovorum, P. atrosepticum, and Ralstonia solanacearum. The findings highlight the value of S. kali extract as a bioactive chemical reservoir for agricultural applications, particularly in plant disease management and crop protection.

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.

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

Author contributions: Sh.B., A.A., and A.Al. devised the project, the main conceptual ideas, and proof outline. S.B. worked out almost all of the technical details and performed the numerical statical calculations with help from P.K. and H.H.A. verified the results. Sh.B., S.B., and A.A. proposed the experiments in discussions. All the authors wrote the manuscript.

Conflict of interest: Przemysław Kowalczewski is a current Editor of Open Life Sciences. This fact did not affect the peer-review process.

Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
==== Refs
References

[1] Ghalem BR. Essential oils as antimicrobial agents against some important plant pathogenic bacteria and fungi. Plant-Microbe Interact An Approach to Sustain Agric. Singapore: Springer; 2017. p. 271–96. 10.1007/978-981-10-2854-0_13.
Ghalem BR Essential oils as antimicrobial agents against some important plant pathogenic bacteria and fungi Plant-Microbe Interact An Approach to Sustain Agric Singapore: Springer 2017 p. 271 96 10.1007/978-981-10-2854-0_13
[2] Behiry SI, Ashmawy NA, Abdelkhalek AA, Younes HA, Khaled AE, Hafez EE. Compatible- and incompatible-type interactions related to defense genes in potato elucidation by Pectobacterium carotovorum. J Plant Dis Prot. 2018;125:197–204. 10.1007/s41348-017-0125-5.
Behiry SI Ashmawy NA Abdelkhalek AA Younes HA Khaled AE Hafez EE Compatible- and incompatible-type interactions related to defense genes in potato elucidation by Pectobacterium carotovorum J Plant Dis Prot 2018 125 197 204 10.1007/s41348-017-0125-5
[3] Peng Y, Li SJ, Yan J, Tang Y, Cheng JP, Gao AJ, et al. Research progress on phytopathogenic fungi and their role as biocontrol agents. Front Microbiol. 2021;12:670135. 10.3389/fmicb.2021.670135.
Peng Y Li SJ Yan J Tang Y Cheng JP Gao AJ Research progress on phytopathogenic fungi and their role as biocontrol agents Front Microbiol 2021 12 670135 10.3389/fmicb.2021.670135 34122383
[4] Newman TE, Derbyshire MC. The evolutionary and molecular features of broad host-range necrotrophy in plant pathogenic fungi. Front Plant Sci. 2020;11:591733. 10.3389/fpls.2020.591733.
Newman TE Derbyshire MC The evolutionary and molecular features of broad host-range necrotrophy in plant pathogenic fungi Front Plant Sci 2020 11 591733 10.3389/fpls.2020.591733 33304369
[5] Kumar P, Sharma R, Kumar K. A perspective on varied fungal virulence factors causing infection in host plants. Mol Biol Rep. 2024;51:392. 10.1007/s11033-024-09314-x.
Kumar P Sharma R Kumar K A perspective on varied fungal virulence factors causing infection in host plants Mol Biol Rep 2024 51 392 10.1007/s11033-024-09314-x 38446264
[6] Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L. Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection. Proc Natl Acad Sci U S A. 2017;114:12267–72. 10.1073/pnas.1714916114.
Andika IB Wei S Cao C Salaipeth L Kondo H Sun L Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection Proc Natl Acad Sci U S A 2017 114 12267 72 10.1073/pnas.1714916114 29087346
[7] Behiry S, Soliman SA, Massoud MA, Abdelbary M, Kordy AM, Abdelkhalek A, et al. Trichoderma pubescens elicit induced systemic resistance in tomato challenged by Rhizoctonia solani. J Fungi. 2023;9(2):167. 10.3390/jof9020167.
Behiry S Soliman SA Massoud MA Abdelbary M Kordy AM Abdelkhalek A Trichoderma pubescens elicit induced systemic resistance in tomato challenged by Rhizoctonia solani J Fungi 2023 9 2 167 10.3390/jof9020167
[8] Christova PKK, Dobreva AM, Dzhurmanski AG, Dincheva IN, Dimkova SD, Zapryanova NG. The impact of plant essential oils on the growth of the pathogens Botrytis cinerea, Fusarium solani, and Phytophthora pseudocryptogea. Life. 2024;14:817.
Christova PKK Dobreva AM Dzhurmanski AG Dincheva IN Dimkova SD Zapryanova NG The impact of plant essential oils on the growth of the pathogens Botrytis cinerea, Fusarium solani, and Phytophthora pseudocryptogea Life 2024 14 817 39063571
[9] Jain A, Sarsaiya S, Wu Q, Lu Y, Shi J. A review of plant leaf fungal diseases and its environment speciation. Bioengineered. 2019;10:409–24. 10.1080/21655979.2019.1649520.
Jain A Sarsaiya S Wu Q Lu Y Shi J A review of plant leaf fungal diseases and its environment speciation Bioengineered 2019 10 409 24 10.1080/21655979.2019.1649520 31502497
[10] Ravikumar MR, Mahesha HS, Vinay JU, Dinesh K. Recent advances in management of bacterial diseases of crops. In: Singh KP, Jahagirdar S, Sarma BK, editors. Emerging trends in plant pathology. Singapore: Springer; 2021. p. 197–210. 10.1007/978-981-15-6275-4_9.
Ravikumar MR Mahesha HS Vinay JU Dinesh K Recent advances in management of bacterial diseases of crops In: Singh KP, Jahagirdar S, Sarma BK, editors. Emerging trends in plant pathology Singapore: Springer 2021 p. 197 210 10.1007/978-981-15-6275-4_9
[11] Tripathi AN, Tiwari SK, Sharma SK, Sharma PK, Behera TK. Current status of bacterial diseases of vegetable crops. Veg Sci. 2024;51:106–17. 10.61180/vegsci.2024.v51.spl.10.
Tripathi AN Tiwari SK Sharma SK Sharma PK Behera TK Current status of bacterial diseases of vegetable crops Veg Sci 2024 51 106 17 10.61180/vegsci.2024.v51.spl.10
[12] Mamphogoro TP, Babalola OO, Aiyegoro OA. Sustainable management strategies for bacterial wilt of sweet peppers (Capsicum annuum) and other Solanaceous crops. J Appl Microbiol. 2020;129:496–508. 10.1111/jam.14653.
Mamphogoro TP Babalola OO Aiyegoro OA Sustainable management strategies for bacterial wilt of sweet peppers (Capsicum annuum) and other Solanaceous crops J Appl Microbiol 2020 129 496 508 10.1111/jam.14653 32248611
[13] Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13:614–29. 10.1111/j.1364-3703.2012.00804.x.
Mansfield J Genin S Magori S Citovsky V Sriariyanum M Ronald P Top 10 plant pathogenic bacteria in molecular plant pathology Mol Plant Pathol 2012 13 614 29 10.1111/j.1364-3703.2012.00804.x 22672649
[14] Czajkowski R, Pérombelon MCM, Jafra S, Lojkowska E, Potrykus M, Van Der Wolf JM, et al. Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: A review. Ann Appl Biol. 2015;166:18–38. 10.1111/aab.12166.
Czajkowski R Pérombelon MCM Jafra S Lojkowska E Potrykus M Van Der Wolf JM Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: A review Ann Appl Biol 2015 166 18 38 10.1111/aab.12166 25684775
[15] Pfeilmeier S, Caly DL, Malone JG. Bacterial pathogenesis of plants: future challenges from a microbial perspective: Challenges in bacterial molecular plant pathology. Mol Plant Pathol. 2016;17:1298–313. 10.1111/mpp.12427.
Pfeilmeier S Caly DL Malone JG Bacterial pathogenesis of plants: future challenges from a microbial perspective: Challenges in bacterial molecular plant pathology Mol Plant Pathol 2016 17 1298 313 10.1111/mpp.12427 27170435
[16] Abdelkhalek A, Hafez E. Plant viral diseases in Egypt and their control. Cottag. Ind. Biocontrol Agents Their Appl. Pract. Asp. to Deal Biol. with Pests Stress. Facing Strateg. Crop. Cham, Switzerland: Springer; 2019. p. 403–21. 10.1007/978-3-030-33161-0_13.
Abdelkhalek A Hafez E Plant viral diseases in Egypt and their control Cottag. Ind. Biocontrol Agents Their Appl. Pract. Asp. to Deal Biol. with Pests Stress. Facing Strateg. Crop Cham, Switzerland: Springer 2019 p. 403 21 10.1007/978-3-030-33161-0_13
[17] El-Mohamedy RSR. Plant essential oils for controlling plant pathogenic fungi. Volatiles Food Secur Role Volatiles Agro-Ecosystems. Singapore: Springer; 2017. p. 171–98. 10.1007/978-981-10-5553-9_9.
El-Mohamedy RSR Plant essential oils for controlling plant pathogenic fungi Volatiles Food Secur Role Volatiles Agro-Ecosystems Singapore: Springer 2017 p. 171 98 10.1007/978-981-10-5553-9_9
[18] Kannojia P, Choudhary KK, Srivastava AK, Singh AK. Chapter four - PGPR bioelicitors: Induced systemic resistance (ISR) and proteomic perspective on biocontrol. PGPR amelioration in sustainable agriculture. Cambridge, UK: Woodhead Publishing; 2019. p. 67–84.
Kannojia P Choudhary KK Srivastava AK Singh AK Chapter four - PGPR bioelicitors: Induced systemic resistance (ISR) and proteomic perspective on biocontrol PGPR amelioration in sustainable agriculture Cambridge, UK: Woodhead Publishing 2019 p. 67 84
[19] Marrone PG. Pesticidal natural products – status and future potential. Pest Manag Sci. 2019;75:2325–40. 10.1002/ps.5433.
Marrone PG Pesticidal natural products – status and future potential Pest Manag Sci 2019 75 2325 40 10.1002/ps.5433 30941861
[20] ElNaggar MH, Eldehna WM, Abourehab MAS, Abdel Bar FM. The old world salsola as a source of valuable secondary metabolites endowed with diverse pharmacological activities: A review. J Enzyme Inhib Med Chem. 2022;37:2036–62. 10.1080/14756366.2022.2102005.
ElNaggar MH Eldehna WM Abourehab MAS Abdel Bar FM The old world salsola as a source of valuable secondary metabolites endowed with diverse pharmacological activities: A review J Enzyme Inhib Med Chem 2022 37 2036 62 10.1080/14756366.2022.2102005 35875938
[21] Altay V, Ozturk M. The genera salsola and suaeda (Amaranthaceae) and their value as fodder. Handbook of Halophytes: From Molecules to Ecosystems towards Biosaline Agriculture. Cham, Switzerland: Springer; 2021. p. 2333–44. 10.1007/978-3-030-57635-6_97.
Altay V Ozturk M The genera salsola and suaeda (Amaranthaceae) and their value as fodder Handbook of Halophytes: From Molecules to Ecosystems towards Biosaline Agriculture Cham, Switzerland: Springer 2021 p. 2333 44 10.1007/978-3-030-57635-6_97
[22] Seo JH, Jin MH, Chang YH. Anti-inflammatory effect of Salsola komarovii extract with dissociated glucocorticoid activity. BMC Complement Med Ther. 2020;20:1–9.
Seo JH Jin MH Chang YH Anti-inflammatory effect of Salsola komarovii extract with dissociated glucocorticoid activity BMC Complement Med Ther 2020 20 1 9 32020859
[23] Mohammed HA, Al-Omar MS, Mohammed SAA, Alhowail AH, Eldeeb HM, Sajid MSM, et al. Phytochemical analysis, pharmacological and safety evaluations of halophytic plant, salsola cyclophylla. Molecules. 2021;26:2384. 10.3390/molecules26082384.
Mohammed HA Al-Omar MS Mohammed SAA Alhowail AH Eldeeb HM Sajid MSM Phytochemical analysis, pharmacological and safety evaluations of halophytic plant, salsola cyclophylla Molecules 2021 26 2384 10.3390/molecules26082384 33923964
[24] Tite MS, Shortland A, Maniatis Y, Kavoussanaki D, Harris SA. The composition of the soda-rich and mixed alkali plant ashes used in the production of glass. J Archaeol Sci. 2006;33:1284–92. 10.1016/j.jas.2006.01.004.
Tite MS Shortland A Maniatis Y Kavoussanaki D Harris SA The composition of the soda-rich and mixed alkali plant ashes used in the production of glass J Archaeol Sci 2006 33 1284 92 10.1016/j.jas.2006.01.004
[25] Murshid SSA, Atoum D, Abou-Hussein DR, Abdallah HM, Hareeri RH, Almukadi H, et al. Genus Salsola: Chemistry, biological activities and future prospective—A review. Plants. 2022;11:714. 10.3390/plants11060714.
Murshid SSA Atoum D Abou-Hussein DR Abdallah HM Hareeri RH Almukadi H Genus Salsola: Chemistry, biological activities and future prospective—A review Plants 2022 11 714 10.3390/plants11060714 35336596
[26] Oueslati MH, Al-Ghamdi FA, Noubigh A. Two new bioactive salsolanol and biphenylsalsinol from the aerial parts of Salsola villosa Delile. ex Schul. (Chenopodiaceae) growing in Saudi Arabia. Asian Pac J Trop Biomed. 2015;5:624–8. 10.1016/j.apjtb.2015.05.012.
Oueslati MH Al-Ghamdi FA Noubigh A Two new bioactive salsolanol and biphenylsalsinol from the aerial parts of Salsola villosa Delile. ex Schul. (Chenopodiaceae) growing in Saudi Arabia Asian Pac J Trop Biomed 2015 5 624 8 10.1016/j.apjtb.2015.05.012
[27] Al-Tohamy R, Ali SS, Saad-Allah K, Fareed M, Ali A, El-Badry A, et al. Phytochemical analysis and assessment of antioxidant and antimicrobial activities of some medicinal plant species from Egyptian flora. J Appl Biomed. 2018;16:289–300. 10.1016/j.jab.2018.08.001.
Al-Tohamy R Ali SS Saad-Allah K Fareed M Ali A El-Badry A Phytochemical analysis and assessment of antioxidant and antimicrobial activities of some medicinal plant species from Egyptian flora J Appl Biomed 2018 16 289 300 10.1016/j.jab.2018.08.001
[28] Mohammed HA, Al-Omar MS, Aly MSA, Hegazy MM. Essential oil constituents and biological activities of the halophytic plants, Suaeda Vermiculata Forssk and Salsola Cyclophylla bakera growing in Saudi Arabia. J Essent Oil-Bearing Plants. 2019;22:82–93. 10.1080/0972060X.2019.1574611.
Mohammed HA Al-Omar MS Aly MSA Hegazy MM Essential oil constituents and biological activities of the halophytic plants, Suaeda Vermiculata Forssk and Salsola Cyclophylla bakera growing in Saudi Arabia J Essent Oil-Bearing Plants 2019 22 82 93 10.1080/0972060X.2019.1574611
[29] Boulaaba M, Medini F, Hajlaoui H, Mkadmini K, Falleh H, Ksouri R, et al. Biological activities and phytochemical analysis of phenolic extracts from Salsola kali L. Role of endogenous factors in the selection of the best plant extracts. South Afr J Bot. 2019;123:193–9. 10.1016/j.sajb.2019.03.003.
Boulaaba M Medini F Hajlaoui H Mkadmini K Falleh H Ksouri R Biological activities and phytochemical analysis of phenolic extracts from Salsola kali L. Role of endogenous factors in the selection of the best plant extracts South Afr J Bot 2019 123 193 9 10.1016/j.sajb.2019.03.003
[30] Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987;19:11–5.
Doyle JJ Doyle JL A rapid DNA isolation procedure for small quantities of fresh leaf tissue Phytochem Bull 1987 19 11 5
[31] Youssef NH, Qari SH, Behiry SI, Dessoky ES, El-Hallous EI, Elshaer MM, et al. Antimycotoxigenic activity of beetroot extracts against altenaria alternata mycotoxins on potato crop. Appl Sci. 2021;11:4239. 10.3390/app11094239.
Youssef NH Qari SH Behiry SI Dessoky ES El-Hallous EI Elshaer MM Antimycotoxigenic activity of beetroot extracts against altenaria alternata mycotoxins on potato crop Appl Sci 2021 11 4239 10.3390/app11094239
[32] Leslie JF, Summerell BA. The Fusarium laboratory manual. Ames, IA, USA: Blackwell Publishing; 2007. 10.1002/9780470278376.
Leslie JF Summerell BA The Fusarium laboratory manual Ames, IA USA: Blackwell Publishing 2007 10.1002/9780470278376
[33] Stefańczyk E, Sobkowiak S. Isolation, identification and preservation of Fusarium Spp. causing dry rot of potato tubers. Plant Breed Seed Sci. 2018;76:45–51. 10.1515/plass-2017-0020.
Stefańczyk E Sobkowiak S Isolation, identification and preservation of Fusarium Spp. causing dry rot of potato tubers Plant Breed Seed Sci 2018 76 45 51 10.1515/plass-2017-0020
[34] Rliizoctonja I, Solan R. Introduction-the genus Rhizoctonia Akiraogosid. Rhizoctonia Species: Taxonomy, molecular biology, ecology, pathology and disease control. Dordrecht, The Netherlands: Springer; 1996. p. 1–9.
Rliizoctonja I Solan R Introduction-the genus Rhizoctonia Akiraogosid Rhizoctonia Species: Taxonomy, molecular biology, ecology, pathology and disease control Dordrecht, The Netherlands: Springer 1996 p. 1 9
[35] White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc. 1990;18:315–22. 10.1016/b978-0-12-372180-8.50042-1.
White TJ Bruns T Lee S Taylor J Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics PCR Protoc 1990 18 315 22 10.1016/b978-0-12-372180-8.50042-1
[36] Ashmawy NA, Salem MZM, El Shanhorey N, Al-Huqail AA, Ali HM, Behiry SI. Eco-friendly wood-biofungicidal and antibacterial activities of various Coccoloba uvifera L. Leaf Extracts: HPLC analysis of phenolic and flavonoid compounds. BioResources. 2020;15:4165–87. 10.15376/biores.15.2.4165-4187.
Ashmawy NA Salem MZM El Shanhorey N Al-Huqail AA Ali HM Behiry SI Eco-friendly wood-biofungicidal and antibacterial activities of various Coccoloba uvifera L. Leaf Extracts: HPLC analysis of phenolic and flavonoid compounds BioResources 2020 15 4165 87 10.15376/biores.15.2.4165-4187
[37] Agarwal M, Walia S, Dhingra S, Khambay BPS. Insect growth inhibition, antifeedant and antifungal activity of compounds isolated/derived from Zingiber officinale Roscoe (ginger) rhizomes. Pest Manag Sci. 2001;57:289–300. 10.1002/ps.263.
Agarwal M Walia S Dhingra S Khambay BPS Insect growth inhibition, antifeedant and antifungal activity of compounds isolated/derived from Zingiber officinale Roscoe (ginger) rhizomes Pest Manag Sci 2001 57 289 300 10.1002/ps.263 11455660
[38] Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal. 2016;6:71–9. 10.1016/j.jpha.2015.11.005.
Balouiri M Sadiki M Ibnsouda SK Methods for in vitro evaluating antimicrobial activity: A review J Pharm Anal 2016 6 71 9 10.1016/j.jpha.2015.11.005 29403965
[39] Hamzah KA, Al-Askar A, Kowalczewski P, Abdelkhalek A, Emaish HH, Behiry S. A comparative study of the antifungal efficacy and phytochemical composition of date palm leaflet extracts. Open Chem. 2024;22:20240044. 10.1515/chem-2024-0044.
Hamzah KA Al-Askar A Kowalczewski P Abdelkhalek A Emaish HH Behiry S A comparative study of the antifungal efficacy and phytochemical composition of date palm leaflet extracts Open Chem 2024 22 20240044 10.1515/chem-2024-0044
[40] Yassin Y, Aseel D, Khalil A, Abdel-Megeed A, Al-Askar A, Elbeaino T, et al. Foliar application of Rhizobium leguminosarum bv. viciae strain 33504-Borg201 promotes faba bean growth and enhances systemic resistance against bean yellow mosaic virus infection. Curr Microbiol. 2024;81:220. 10.1007/s00284-024-03733-6.
Yassin Y Aseel D Khalil A Abdel-Megeed A Al-Askar A Elbeaino T Foliar application of Rhizobium leguminosarum bv. viciae strain 33504-Borg201 promotes faba bean growth and enhances systemic resistance against bean yellow mosaic virus infection Curr Microbiol 2024 81 220 10.1007/s00284-024-03733-6 38867024
[41] Kumar J, Ramlal A, Mallick D, Mishra V. An overview of some biopesticides and their importance in plant protection for commercial acceptance. Plants. 2021;10:1185. 10.3390/plants10061185.
Kumar J Ramlal A Mallick D Mishra V An overview of some biopesticides and their importance in plant protection for commercial acceptance Plants 2021 10 1185 10.3390/plants10061185 34200860
[42] Moawad H, Abd El-Rahim WM. Bioremediation of irrigation water contaminated with textile dyes. Fresenius Env Bull. 2003;12:786–92.
Moawad H Abd El-Rahim WM Bioremediation of irrigation water contaminated with textile dyes Fresenius Env Bull 2003 12 786 92
[43] Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L. Chemical pesticides and human health: The urgent need for a new concept in agriculture. Front Public Heal. 2016;4:148. 10.3389/fpubh.2016.00148.
Nicolopoulou-Stamati P Maipas S Kotampasi C Stamatis P Hens L Chemical pesticides and human health: The urgent need for a new concept in agriculture Front Public Heal 2016 4 148 10.3389/fpubh.2016.00148
[44] Selim DA, Shawky E, Ghareeb DA, Abdulmalek SA, Abu El-Khair RM. Comparative metabolomics of the different fractions of two saltwort (Salsola L.) species in relation to their anti-inflammatory activity. Food Biosci. 2023;51:102306. 10.1016/j.fbio.2022.102306.
Selim DA Shawky E Ghareeb DA Abdulmalek SA Abu El-Khair RM Comparative metabolomics of the different fractions of two saltwort (Salsola L.) species in relation to their anti-inflammatory activity Food Biosci 2023 51 102306 10.1016/j.fbio.2022.102306
[45] Elisha IL, Botha FS, McGaw LJ, Eloff JN. The antibacterial activity of extracts of nine plant species with good activity against Escherichia coli against five other bacteria and cytotoxicity of extracts. BMC Complement Altern Med. 2017;17:133. 10.1186/s12906-017-1645-z.
Elisha IL Botha FS McGaw LJ Eloff JN The antibacterial activity of extracts of nine plant species with good activity against Escherichia coli against five other bacteria and cytotoxicity of extracts BMC Complement Altern Med 2017 17 133 10.1186/s12906-017-1645-z 28241818
[46] Makhafola TJ, Samuel BB, Elgorashi EE, Eloff JN. Ochnaflavone and ochnaflavone 7-O-methyl ether two antibacterial biflavonoids from Ochna pretoriensis (Ochnaceae). Nat Prod Commun. 2012;7:1601–4. 10.1177/1934578x1200701216.
Makhafola TJ Samuel BB Elgorashi EE Eloff JN Ochnaflavone and ochnaflavone 7-O-methyl ether two antibacterial biflavonoids from Ochna pretoriensis (Ochnaceae) Nat Prod Commun 2012 7 1601 4 10.1177/1934578x1200701216 23413563
[47] Koohsari H, Ghaemi EA, Sadegh Sheshpoli M, Jahedi M, Zahiri M. The investigation of antibacterial activity of selected native plants from North of Iran. J Med Life. 2015;8:38–42.
Koohsari H Ghaemi EA Sadegh Sheshpoli M Jahedi M Zahiri M The investigation of antibacterial activity of selected native plants from North of Iran J Med Life 2015 8 38 42
[48] Chhetry AK, Dhakal S, Chaudhary L, Karki K, Khadka RB, Chaudhary GP, et al. Study of antibacterial activity of root bark, leaves, and pericarp extracts of Diploknema butyracea and evaluation of prospective antioxidant activity. J Trop Med. 2022;2022:6814901. 10.1155/2022/6814901.
Chhetry AK Dhakal S Chaudhary L Karki K Khadka RB Chaudhary GP Study of antibacterial activity of root bark, leaves, and pericarp extracts of Diploknema butyracea and evaluation of prospective antioxidant activity J Trop Med 2022 2022 6814901 10.1155/2022/6814901 35371266
[49] Khan AV, Ahmed QU, Shukla I, Khan AA. Antibacterial activity of leaves extracts of Trifolium alexandrinum Linn, against pathogenic bacteria causing tropical diseases. Asian Pac J Trop Biomed. 2012;2:189–94. 10.1016/S2221-1691(12)60040-9.
Khan AV Ahmed QU Shukla I Khan AA Antibacterial activity of leaves extracts of Trifolium alexandrinum Linn, against pathogenic bacteria causing tropical diseases Asian Pac J Trop Biomed 2012 2 189 94 10.1016/S2221-1691(12)60040-9 23569896
[50] Zhao Y, Wang X, Zhang L, Wang K, Wu Y, Yao J, et al. Anti-fungal activity of moutan cortex extracts against rice sheath blight (Rhizoctonia solani) and its action on the pathogen’s cell membrane. ACS Omega. 2022;7:47048–55. 10.1021/acsomega.2c06150.
Zhao Y Wang X Zhang L Wang K Wu Y Yao J Anti-fungal activity of moutan cortex extracts against rice sheath blight (Rhizoctonia solani) and its action on the pathogen’s cell membrane ACS Omega 2022 7 47048 55 10.1021/acsomega.2c06150 36570206
[51] Alotibi FO, Ashour EH, Al-Basher G. Evaluation of the antifungal activity Rumex vesicarius of L. and Ziziphus spina-christi (L) Desf. Aqueous extracts and assessment of the morphological changes induced to certain myco-phytopathogens. Saudi J Biol Sci. 2020;27:2818–28. 10.1016/j.sjbs.2020.06.051.
Alotibi FO Ashour EH Al-Basher G Evaluation of the antifungal activity Rumex vesicarius of L. and Ziziphus spina-christi (L) Desf. Aqueous extracts and assessment of the morphological changes induced to certain myco-phytopathogens Saudi J Biol Sci 2020 27 2818 28 10.1016/j.sjbs.2020.06.051 32994742
[52] Pandey KB, Rizvi SI. Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev. 2009;2:270–8. 10.4161/oxim.2.5.9498.
Pandey KB Rizvi SI Plant polyphenols as dietary antioxidants in human health and disease Oxid Med Cell Longev 2009 2 270 8 10.4161/oxim.2.5.9498 20716914
[53] Othman L, Sleiman A, Abdel-Massih RM. Antimicrobial activity of polyphenols and alkaloids in middle eastern plants. Front Microbiol. 2019;10:911. 10.3389/fmicb.2019.00911.
Othman L Sleiman A Abdel-Massih RM Antimicrobial activity of polyphenols and alkaloids in middle eastern plants Front Microbiol 2019 10 911 10.3389/fmicb.2019.00911 31156565
[54] Tian QM, Wei SM, Su HR, Zheng SM, Xu SY, Liu MJ, et al. Bactericidal activity of gallic acid against multi-drug resistance Escherichia coli. Microb Pathog. 2022;173:105824. 10.1016/j.micpath.2022.105824.
Tian QM Wei SM Su HR Zheng SM Xu SY Liu MJ Bactericidal activity of gallic acid against multi-drug resistance Escherichia coli Microb Pathog 2022 173 105824 10.1016/j.micpath.2022.105824 36243382
[55] Pinho E, Ferreira ICFR, Barros L, Carvalho AM, Soares G, Henriques M. Antibacterial potential of northeastern portugal wild plant extracts and respective phenolic compounds. Biomed Res Int. 2014;2014:814590. 10.1155/2014/814590.
Pinho E Ferreira ICFR Barros L Carvalho AM Soares G Henriques M Antibacterial potential of northeastern portugal wild plant extracts and respective phenolic compounds Biomed Res Int 2014 2014 814590 10.1155/2014/814590 24804249
[56] Wang Y, Sun Y, Wang J, Zhou M, Wang M, Feng J. Antifungal activity and action mechanism of the natural product cinnamic acid against Sclerotinia sclerotiorum. Plant Dis. 2019;103:944–50. 10.1094/PDIS-08-18-1355-RE.
Wang Y Sun Y Wang J Zhou M Wang M Feng J Antifungal activity and action mechanism of the natural product cinnamic acid against Sclerotinia sclerotiorum Plant Dis 2019 103 944 50 10.1094/PDIS-08-18-1355-RE 30895869
[57] Bouarab-Chibane L, Forquet V, Lantéri P, Clément Y, Léonard-Akkari L, Oulahal N, et al. Antibacterial properties of polyphenols: Characterization and QSAR (Quantitative structure-activity relationship) models. Front Microbiol. 2019;10:440698. 10.3389/fmicb.2019.00829.
Bouarab-Chibane L Forquet V Lantéri P Clément Y Léonard-Akkari L Oulahal N Antibacterial properties of polyphenols: Characterization and QSAR (Quantitative structure-activity relationship) models Front Microbiol 2019 10 440698 10.3389/fmicb.2019.00829
[58] Yuan G, Guan Y, Yi H, Lai S, Sun Y, Cao S. Antibacterial activity and mechanism of plant flavonoids to gram-positive bacteria predicted from their lipophilicities. Sci Rep. 2021;11:10471. 10.1038/s41598-021-90035-7.
Yuan G Guan Y Yi H Lai S Sun Y Cao S Antibacterial activity and mechanism of plant flavonoids to gram-positive bacteria predicted from their lipophilicities Sci Rep 2021 11 10471 10.1038/s41598-021-90035-7 34006930
[59] Desbois AP, Smith VJ. Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol. 2010;85:1629–42. 10.1007/s00253-009-2355-3.
Desbois AP Smith VJ Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential Appl Microbiol Biotechnol 2010 85 1629 42 10.1007/s00253-009-2355-3 19956944
[60] Cho KH, Hong JH, Lee KT. Monoacylglycerol (MAG)-oleic acid has stronger antioxidant, anti-atherosclerotic, and protein glycation inhibitory activities than MAG-palmitic acid. J Med Food. 2010;13:99–107. 10.1089/jmf.2009.1024.
Cho KH Hong JH Lee KT Monoacylglycerol (MAG)-oleic acid has stronger antioxidant, anti-atherosclerotic, and protein glycation inhibitory activities than MAG-palmitic acid J Med Food 2010 13 99 107 10.1089/jmf.2009.1024 20136442
[61] Ganesan T, Subban M, Christopher Leslee DB, Kuppannan SB, Seedevi P. Structural characterization of n-hexadecanoic acid from the leaves of Ipomoea eriocarpa and its antioxidant and antibacterial activities. Biomass Convers Biorefin. 2024;14:14547–58. 10.1007/s13399-022-03576-w.
Ganesan T Subban M Christopher Leslee DB Kuppannan SB Seedevi P Structural characterization of n-hexadecanoic acid from the leaves of Ipomoea eriocarpa and its antioxidant and antibacterial activities Biomass Convers Biorefin 2024 14 14547 58 10.1007/s13399-022-03576-w
[62] Mickymaray S, Al Aboody MS, Rath PK, Annamalai P, Nooruddin T. Screening and antibacterial efficacy of selected Indian medicinal plants. Asian Pac J Trop Biomed. 2016;6:185–91. 10.1016/j.apjtb.2015.12.005.
Mickymaray S Al Aboody MS Rath PK Annamalai P Nooruddin T Screening and antibacterial efficacy of selected Indian medicinal plants Asian Pac J Trop Biomed 2016 6 185 91 10.1016/j.apjtb.2015.12.005
[63] Aparna V, Dileep KV, Mandal PK, Karthe P, Sadasivan C, Haridas M. Anti-inflammatory property of n-hexadecanoic Acid: structural evidence and kinetic assessment. Chem Biol Drug Des. 2012;80:434–9. 10.1111/j.1747-0285.2012.01418.x.
Aparna V Dileep KV Mandal PK Karthe P Sadasivan C Haridas M Anti-inflammatory property of n-hexadecanoic Acid: structural evidence and kinetic assessment Chem Biol Drug Des 2012 80 434 9 10.1111/j.1747-0285.2012.01418.x 22642495
[64] Qureshi T, Memon N, Memon SQ, Ashraf MA. Decontamination of ofloxacin: optimization of removal process onto sawdust using response surface methodology. Desalin Water Treat. 2016;57:221–9. 10.1080/19443994.2015.1006825.
Qureshi T Memon N Memon SQ Ashraf MA Decontamination of ofloxacin: optimization of removal process onto sawdust using response surface methodology Desalin Water Treat 2016 57 221 9 10.1080/19443994.2015.1006825
[65] Shaaban MT, Ghaly MF, Fahmi SM. Antibacterial activities of hexadecanoic acid methyl ester and green-synthesized silver nanoparticles against multidrug-resistant bacteria. J Basic Microbiol. 2021;61:557–68. 10.1002/jobm.202100061.
Shaaban MT Ghaly MF Fahmi SM Antibacterial activities of hexadecanoic acid methyl ester and green-synthesized silver nanoparticles against multidrug-resistant bacteria J Basic Microbiol 2021 61 557 68 10.1002/jobm.202100061 33871873
[66] Abdelaziz R, Tartor YH, Barakat AB, EL-Didamony G, Gado MM, Berbecea A, et al. Bioactive metabolites of Streptomyces misakiensis display broad-spectrum antimicrobial activity against multidrug-resistant bacteria and fungi. Front Cell Infect Microbiol. 2023;13:1162721. 10.3389/fcimb.2023.1162721.
Abdelaziz R Tartor YH Barakat AB EL-Didamony G Gado MM Berbecea A Bioactive metabolites of Streptomyces misakiensis display broad-spectrum antimicrobial activity against multidrug-resistant bacteria and fungi Front Cell Infect Microbiol 2023 13 1162721 10.3389/fcimb.2023.1162721 37168394
[67] Mahizan NA, Yang SK, Moo CL, Song AAL, Chong CM, Chong CW, et al. Terpene derivatives as a potential agent against antimicrobial resistance (AMR) pathogens. Molecules. 2019;24:2631. 10.3390/molecules24142631.
Mahizan NA Yang SK Moo CL Song AAL Chong CM Chong CW Terpene derivatives as a potential agent against antimicrobial resistance (AMR) pathogens Molecules 2019 24 2631 10.3390/molecules24142631 31330955
[68] dos Santos FM, de Souza MG, Miller Crotti AE, Martins CHG, Ambrósio SR, Veneziani RCS, et al. Evaluation of antimicrobial activity of extracts of Tibouchina candolleana (melastomataceae), isolated compounds and semi-synthetic derivatives against endodontic bacteria. Brazilian. J Microbiol. 2012;43:793–9. 10.1590/S1517-83822012000200045.
dos Santos FM de Souza MG Miller Crotti AE Martins CHG Ambrósio SR Veneziani RCS Evaluation of antimicrobial activity of extracts of Tibouchina candolleana (melastomataceae), isolated compounds and semi-synthetic derivatives against endodontic bacteria. Brazilian J Microbiol 2012 43 793 9 10.1590/S1517-83822012000200045
[69] Andrade SF, Da Silva Filho AA, Resende DDO, Silva MLA, Cunha WR, Nanayakkara NPD, et al. Antileishmanial, antimalarial and antimicrobial activities of the extract and isolated compounds from Austroplenckia populnea (Celastraceae). Z Fur Naturforsch - Sect C J Biosci. 2008;63:497–502. 10.1515/znc-2008-7-805.
Andrade SF Da Silva Filho AA Resende DDO Silva MLA Cunha WR Nanayakkara NPD Antileishmanial, antimalarial and antimicrobial activities of the extract and isolated compounds from Austroplenckia populnea (Celastraceae) Z Fur Naturforsch - Sect C J Biosci 2008 63 497 502 10.1515/znc-2008-7-805
[70] Bakri IM, Douglas CWI. Inhibitory effect of garlic extract on oral bacteria. Arch Oral Biol. 2005;50:645–51. 10.1016/j.archoralbio.2004.12.002.
Bakri IM Douglas CWI Inhibitory effect of garlic extract on oral bacteria Arch Oral Biol 2005 50 645 51 10.1016/j.archoralbio.2004.12.002 15892950
[71] Mallavadhani UV, Mahapatra A, Jamil K, Reddy PS. Antimicrobial activity of some pentacyclic triterpenes and their synthesized 3-O-lipophilic chains. Biol Pharm Bull. 2004;27:1576–9. 10.1248/bpb.27.1576.
Mallavadhani UV Mahapatra A Jamil K Reddy PS Antimicrobial activity of some pentacyclic triterpenes and their synthesized 3-O-lipophilic chains Biol Pharm Bull 2004 27 1576 9 10.1248/bpb.27.1576 15467198
[72] Muzahid AA, Sharmin S, Hossain MS, Ahamed KU, Ahmed N, Yeasmin MS, et al. Analysis of bioactive compounds present in different crude extracts of Benincasa hispida and Cucurbita moschata seeds by gas chromatography-mass spectrometry. Heliyon. 2023;9(1):e12702. 10.1016/j.heliyon.2022.e12702.
Muzahid AA Sharmin S Hossain MS Ahamed KU Ahmed N Yeasmin MS Analysis of bioactive compounds present in different crude extracts of Benincasa hispida and Cucurbita moschata seeds by gas chromatography-mass spectrometry Heliyon 2023 9 1 e12702 10.1016/j.heliyon.2022.e12702 36685362
[73] Krishnaveni M, Dhanalakshmi R, Nandhini N. GC-MS analysis of phytochemicals, fatty acid profile, antimicrobial activity of gossypium seeds. Int J Pharm Sci Rev Res. 2014;27:273–6.
Krishnaveni M Dhanalakshmi R Nandhini N GC-MS analysis of phytochemicals, fatty acid profile, antimicrobial activity of gossypium seeds Int J Pharm Sci Rev Res 2014 27 273 6
[74] Nweze C, Ibrahim H, Ndukwe GI. Beta-sitosterol with antimicrobial property from the stem bark of pomegranate (Punica granatum Linn). J Appl Sci Env Manag. 2019;23:1045. 10.4314/jasem.v23i6.7.
Nweze C Ibrahim H Ndukwe GI Beta-sitosterol with antimicrobial property from the stem bark of pomegranate (Punica granatum Linn) J Appl Sci Env Manag 2019 23 1045 10.4314/jasem.v23i6.7
[75] Yusuf AJ, Abdullahi MI, Aleku GA, Ibrahim IAA, Alebiosu CO, Yahaya M, et al. Antimicrobial activity of stigmasterol from the stem bark of Neocarya macrophylla. J Med Plants Econ Dev. 2018;2:1–5. 10.4102/jomped.v2i1.38.
Yusuf AJ Abdullahi MI Aleku GA Ibrahim IAA Alebiosu CO Yahaya M Antimicrobial activity of stigmasterol from the stem bark of Neocarya macrophylla J Med Plants Econ Dev 2018 2 1 5 10.4102/jomped.v2i1.38
[76] Ochieng Nyalo P, Isanda Omwenga G, Piero Ngugi M. GC-MS analysis, antibacterial and antioxidant potential of ethyl acetate leaf extract of Senna singueana (Delile) grown in Kenya. Evid-Based Complement Altern Med. 2022;2022:5436476. 10.1155/2022/5436476.
Ochieng Nyalo P Isanda Omwenga G Piero Ngugi M GC-MS analysis, antibacterial and antioxidant potential of ethyl acetate leaf extract of Senna singueana (Delile) grown in Kenya Evid-Based Complement Altern Med 2022 2022 5436476 10.1155/2022/5436476
