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Article

Phytochemical Compounds of Branches from P. halepensis Oily Liquid Extract and S. terebinthifolius Essential Oil and Their Potential Antifungal Activity

by
Abeer A. Mohamed
1,
Said I. Behiry
2,
Hayssam M. Ali
3,4,*,
Mervat EL-Hefny
5,
Mohamed Z.M. Salem
6,* and
Nader A. Ashmawy
7
1
Plant Pathology Institute, Agriculture Research Center (ARC), Alexandria 21616, Egypt
2
Agricultural Botany Department, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria 21531, Egypt
3
Botany and Microbiology Department, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
4
Timber Trees Research Department, Sabahia Horticulture Research Station, Horticulture Research Institute, Agriculture Research Center, Alexandria 21526, Egypt
5
Department of Floriculture, Ornamental Horticulture and Garden Design, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria 21545, Egypt
6
Forestry and Wood Technology Department, Faculty of Agriculture (EL-Shatby), Alexandria University, Alexandria 21545, Egypt
7
Department of Plant Pathology, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria 21545, Egypt
*
Authors to whom correspondence should be addressed.
Processes 2020, 8(3), 330; https://doi.org/10.3390/pr8030330
Submission received: 28 January 2020 / Revised: 3 March 2020 / Accepted: 6 March 2020 / Published: 11 March 2020
(This article belongs to the Special Issue Green Separation and Extraction Processes)
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Abstract

:
In the present study, the antifungal activity of wood treated with Pinus halepensis branch n-hexane oily liquid extract (OLE) and Schinus terebinthifolius branch essential oil (EO) was evaluated against the growth of four phytopathogenic fungi—Bipolaris oryzae, Fusarium oxysporum, Fusarium solani, and Rhizoctonia solani. Air-dried wood samples of Pinus roxburghii were autoclaved, and each wood received 100 µL of the concentrated oils from P. halepensis and S. terebinthifolius. The main compounds identified in S. terebinthifolius branch EO were terpinen-4-ol (18.25%), cis-β-terpineol (15.60%), γ-terpinene (12.46%), sabinene (9.83%), α-terpinene (8.56%), and 4-thujanol (6.71%), while the main compounds in P. halepensis branch HeO were 2-undecenal (22.25%), 4-hydroxy-10-methyl-3,4,7,8,9,10-hexahydro-2H-oxecin-2-one (8.43%), (Z)-2-decenal (6.88%), nonanal (5.85%), (2E)-2-decenal (4.65%), (E,E)-2,4-decadienal (4.41%), arachidonic acid methyl ester (4.36%), and 2-(7-heptadecynyloxy)tetrahydro-2H-pyran (4.22%). P. halepensis OLE at a concentration of 3% showed the highest inhibition percentage of fungal growth (IPFG) of B. oryzae, followed by S. terebinthifolius EO at 3% and 2%, with IPFG values of 80%, 74.44%, and 71.66%, respectively. At a concentration of 3%, branch oils from S. terebinthifolius and P. halepensis were found to have the highest IPFG values with 45.55% and 40.55%, respectively, against F. oxysporum growth. Moderate to weak activity was found against F. solani when S. terebinthifolius EO and P. halepensis OLE were applied to wood. EO and OLE-treated wood samples at 3% produced inhibitions of 54.44% and 41.11%, respectively, against R. solani.

1. Introduction

Natural products extracted from forestry trees have a sustainable source of natural products from their different parts (wood, bark, roots, leaves, flowers, branches, seeds, and fruits). These natural products, such as essential oils (EOs), fixed oils, and polyphenolic and flavonoid compounds, have great effects in terms of their antimicrobial activities [1,2,3,4,5,6,7,8,9].
Bipolaris oryzae is the causal agent of rice brown spot disease and is responsible for significant economic losses, and in Egypt the disease is ranked second, coming next after blast disease [10]. Fusaria are common soil saprophytes; however, they are also known as phytopathogens—especially Fusarium oxysporum—that cause root or blight diseases in many host plants [11,12,13]. Two Fusarium species were recently included in the list of the top ten plant pathogenic fungi with both economic and scientific importance, with one of them being F. solani, which causes vascular wilt or root rot in more than 100 plant species [14,15]. Rhizoctonia solani is considered a distractive soil-borne disease of rice production worldwide, causing rice sheath blight disease. The initiation of an integrated disease management procedure is important to keep the disease under control [16].
Phytochemicals from all of the parts of Aleppo pine, P. halepensis Miller, have shown the presence of EOs, phenolic compounds, turpentine, and terpenes with valuable medicinal uses and antimicrobial agents [9,10,11,12,13,14,15,16,17,18,19,20,21]. Needle EOs have been shown to have many bioactive compounds, such as α-humulene, aromadendrin, and β-caryophyllene [22]; caryophyllene oxide, myrcene, α-pinene, and β-caryophyllene were also identified [23,24].
Schinus terebinthifolius Raddi produces resin that contains monoterpenes acting as a defense against attacking pathogenic agents [25]. Extracts and EOs, especially from fruits, have been studied extensively in dozens of works, e.g., oleic acid, δ-cadinene, α-phellandrene, 1b,5,5,6α-tetramethyloctahydro-6H-indeno[1,2-b]oxiren-6-one, aromadendrene, hexadecanoic acid-2,3-dihydroxypropyl ester, α-caryophyllene, and germacrene D were the main compounds found in the ethyl ether extract of S. terebinthifolius fruits with good antifungal activity against T. harzianum and A. niger [2]. Acetone extract from ripened fruits with oleic acid, α-phellandrene, and δ-cadinene as main compounds had observed antibacterial activity [26]. Other compounds such as flavonoids, phenols, tannins, anthraquinones, quercetin, kaempferol, biphenyl esters, and steroids were isolated from the fruits of S. terebinthifolius [27,28,29,30,31], with potential antimicrobial activities. Methanol and Aqueous extracts of S. terebinthifolius showed potential activity against C. albicans [32,33]. Extracts of the stem of the plant showed the isolated compounds of schinol and biphenyl 4′-ethyl-4-methyl-2,2′,6,6′-tetrahydroxy[1,1′-biphenyl]-4,4′-dicarboxylate with potential antifungal activity against P. brasiliensis [34].
Lignocellulosic materials such as wood can be affected or deteriorated by fungi in moist conditions, causing a loss in the overall quality or the surface quality of the wood, as well as some environmental problems as a result of their excretion of toxins [35,36,37,38]. Some works have been carried out to preserve or protect some commercial wood species from deterioration by fungi using natural extracts, and the results showed good antifungal activity, either inhibiting or preventing their growth [2,3,7,8]. No fungal growth of A. tenuissima and F. culmorum occurred on the Acacia saligna wood surface treated with the methanol extract of Maclura pomifera bark [39]. Recently, the treated wood samples of Melia azedarach with the water extract of A. saligna flowers, the ethanol extract of Musa paradisiaca peels, the n-hexane oily extracts from Eucalyptus camaldulensis and Vitex agnus-castus, or with Withania somnifera fruit acetone extract showed good antifungal activity against several molds, such as F. culmorum, P. chrysogenum, and R. solani [3,7,8,40]. Furthermore, new green pesticides that act as alternatives, such as natural product-based pesticides, are being developed to replace compounds lost due to the new regulations [41].
EOs are an interesting option for use as new pesticides reserving as anti; fungi, insects, and weeds. Moreover, many EOs can directly act as a natural insect repellent to provide protection against mosquitoes and other harmful arthropods, or to provide antifeedant activity against herbivores, such as eucalyptus oil [42,43]. MyggA® or Natural or Citriodiol® and Buzz away are other mosquito repellent products based on p-Menthane-3,8-diol and citronellal monoterpene extracted from lemon eucalyptus E, which are marketed to use against public health pests and can help avoid ticks or biting flies [44,45,46,47]. Many researchers have reported that EO applications should be considered as resistance inducers and could affect pathogens through the production of phytoalexins and biochemical plant defense [48]. Indeed, even little amounts of EOs applied on plants in vivo have been shown to produce a greater reduction in disease severity [49]. There are many reasons that may contribute to the greater effect of EOs in vivo than in vitro, such as variation of the optimum temperature of fungal growth and the presence of microorganisms on the plant surface [50]. The present work aimed to evaluate the bioactivity of P. halepensis n-hexane oily liquid extract and S. terebinthifolius essential oil as wood-biofungicides.

2. Materials and Methods

2.1. Preparation of Essntial Oil and n-Hexane Oily Liquid Extract

Green branches (wood and bark) of Brazilian Peppertree, Schinus terebinthifolius Raddi (Anacardiaceae), were rapidly washed by tap water to remove the dust, then smoothly dried with paper towel and cut into small pieces. About 100 g of the cut branches underwent extraction of their essential oil (EO) using the hydrodistillation method of the Clevenger apparatus for 3 h [51]. Meanwhile, the green branches (wood and bark) of Aleppo pine, Pinus halepensis Miller (Pinaceae), after being cut into small pieces, underwent extraction via the soaking method, where about 100 g of the branch sample was soaked in n-hexane solvent (200 mL) for 6 h under shaking. The n-hexane oily liquid extract (OLE) was separated by filtration with Whatman No. 1 filter paper under suction pressure then the OLE concentrated by evaporating the n-hexane solvent under vacuum using a rotary evaporator at 45 °C. EO and OLE were stored in brown tubes until use.

2.2. The Antifungal Activity of Wood Treated with Essential Oil and Oily Lquid Extract

Wood samples of P. roxburghii Sarg were prepared at the approximate dimensions of 2 × 1 × 0.5 cm, autoclaved at 121 °C for 20 min, and then left to cool. The four fungi of Bipolaris oryzae, Fusarium oxysporum, Fusarium solani, and Rhizoctonia solani were used for the bioassay. S. terebinthifolius (EO) and P. halepensis (OLE) were prepared at the concentrations of 1%, 2%, and 3%. For every wood sample, 100 µL of the concentrated EO or OLE was applied. The antifungal activity of the treated wood samples was compared with wood samples without oil treatments, which were used as a control. The fungal inhibition percentage was calculated with the formula of inhibition percentage of fungal growth (IPFG) ( % ) = [ DC − DT DC ] × 100 , where DC is the diameter of fungal control and DT is the diameter of treatment. Four replicates were carried out for all of the treatments. The antifungal activities of the treated wood were measured following the method of our previous works [3,52,53,54,55] with minor modification, namely, ensuring that each wood sample examined for its antifungal activity had received the tested amount of EO or OLE.

2.3. Gas Chromatography-Mass Spectrometry (GC/MS) Analysis of the EO and OLE

The chemical compositions of the EO and OLE were analyzed using the Focus GC-DSQ Mass Spectrometer (Thermo Scientific, Austin, TX, USA) with a direct capillary column TG–5MS (30 m × 0.25 mm × 0.25 µm film thickness) apparatus at the Atomic and Molecular Physics Unit, Experimental Nuclear Physics Department, Nuclear Research Centre, Egyptian Atomic Energy Authority, Inshas, Cairo, Egypt. The column oven temperature was initially held at 45 °C, and then increased by 5 °C/min to 200 °C, held for 5 min, then increased again to 300 °C by 5 °C/min. Other conditions and identification of the compounds using the WILEY 09 and NIST 14 mass spectral databases can be found in previous works [1,2,3,4,5,56,57].

2.4. Statistical Analysis

Data of the antifungal activity were statistically analyzed with two factors [(type of oil (EO and OLE) and the concentration)] using the SAS system [58]. The differences among the means of the treatments were recorded using Fisher’s least significant difference (LSD0.05).

3. Results

3.1. Visual Observations of the Fungal Growth

Figure 1 shows the antifungal activity of the treated Pinus roxburghii wood with the n-hexane oily extract (OLE) from Pinus halepensis and the essential oil (EO) of S. terebinthifolius against the growth of Bipolaris oryzae. In the control treatment (wood without EO or OLE), the fungal growth almost reached full linear growth, but for the wood treated with both oils, the fungal mycelia were suspended and the inhibition was found at all of the concentrations used (1%, 2%, and 3%). Additionally, the fungal growth was found to grow on the side opposite to the treated wood with both EO and OLE.
Compared to the control condition, Fusarium oxysporum growth was inhibited and did not reach the treated wood with both EO and OLE, especially at the concentrations of 2% and 3% (Figure 2). On the other hand, the treated wood with both EO and OLE showed weak activity against Fusarium solani (Figure 3); however, P. halepensis OLE at 3% showed inhibition against its growth. Figure 4 shows that, in the control treatment, the fungal mycelia of Rhizoctonia solani covered and grew over the wood samples after the incubation period. Meanwhile, either the growth did not completely reach the direction of the treated wood, or no growth was found at all.
Furthermore, as shown in Figure 4, the fungal growth of R. solani was found in the opposite direction of the treated wood with the P. halepensis OLE and Schinus terebinthifolius EO.

3.2. Antifungal Activity of the Oils

Statistically, there was a significance effect of EO and OLE in terms of antifungal activity against B. oryzae, F. oxysporum, F. solani, and R. solani (Figure 5a), where P. halepensis OLE had the highest effect against the growth of F. oxysporum and F. solani. Meanwhile, S. terebinthifolius EO was found to have good activity against B. oryzae and R. solani. Furthermore, when increasing the EO or OLE concentration from 0% (control) to 3%, the inhibition percentage of fungal growth (IPFG) was increased (Figure 5b).
For the effect of EO/OLE-treated wood as affected by the interaction between the EO/OLE type and their concentrations (Table 1), the highest activity against B. oryzae growth was found for P. halepensis OLE applied at a concentration of 3%, followed by S. terebinthifolius EO at 3% and 2%, with IPFG values of 80%, 74.44%, and 71.66%, respectively. S. terebinthifolius EO and P. halepensis OLE at a concentration of 3% observed the highest IPFG, with values of 45.55% and 40.55%, respectively, against F. oxysporum growth.
Wood treated with P. halepensis OLE at the 3% and 2% concentration levels showed significant activity against the growth of F. solani, with IPFG values of 30.55% and 29.44%, respectively. Also, S. terebinthifolius EO (2%) and P. halepensis OLE (1%) showed IPFG values of 21.11% and 20%, respectively. The highest activity against the growth of R. solani was observed for wood treated with S. terebinthifolius EO and P. halepensis OLE at 3%, with IPFG values of 54.44% and 41.11%, respectively. However, S. terebinthifolius EO and P. halepensis OLE at 2% showed IPFG values of 35% and 30.55%, respectively, against R. solani.

3.3. Chemical Composition of Branches from S. terebinthifolius Eessntial Oil and P. halepensis Oily Liquid Extract

The chemical composition of the EO identified in S. terebinthifolius branch is shown in Table 2. The main compounds were terpinen-4-ol (18.25%), cis-β-terpineol (15.60%), γ-terpinene (12.46%), sabinene (9.83%), α-terpinene (8.56%), 4-thujanol (6.71%), (-)-α-terpineol (4.34%), o-cymene (4.05%), D-limonene (2.79%), α-phellandrene (2.46%), and β-caryophyllene (2.34%). The chemical compounds of P. halepensis branch OLE are presented in Table 3. The main compounds were 2-undecenal (22.25%), 4-hydroxy-10-methyl-3,4,7,8,9,10-hexahydro-2H-oxecin-2-one (8.43%), (Z)-2-decenal (6.88%), nonanal (5.85%), (2E)-2-decenal (4.65%), (E,E)-2,4-decadienal (4.41%), arachidonic acid methyl ester (4.36%), 2-(7-heptadecynyloxy)tetrahydro-2H-pyran (4.22%), 1-nonadecene (3.50%), 12,15-octadecadiynoic acid, methyl ester (3.1%), Z-(13,14-epoxy)tetradec-11-en-1-ol acetate (3.04%), 7-methyl-Z-tetradecen-1-ol acetate (3.01%), (Z)-2-tridecenal (2.9%), O-benzylserine (2.22%), methyl octadeca-13,16-diynoate (2.21%), myristyl chloride (1.97%), (Z)-oleic acid (1.48%), n-caprylaldehyde (1.31%), and 1-heptatriacotanol (1.15%).

4. Discussion

Pinus halepensis OLE and Schinus terebinthifolius EO showed the presence of several bioactive compounds, as identified by Gas Chromatography-Mass Spectrometry (GC/MS). 2-undecenal, as well as other compounds such as 4-hydroxy-10-methyl-3,4,7,8,9,10-hexahydro-2H-oxecin-2-one, (Z)-2-decenal, nonanal, (2E)-2-decenal, (E,E)-2,4-decadienal, arachidonic acid methyl ester, and 2-(7-heptadecynyloxy)tetrahydro-2H-pyran, were found in the OLE of P. halepensis.
Several cited chemical compositions of P. halepensis have been published regarding terpenes, fatty acids, aldehydes, and cyclic phenolic compounds [59,60,61]. The lipophilic extractives (resin acids, terpenes, fatty acids, glycerides, steryl esters, sterols) were extracted using n-hexane then the hydrophilic ones (stilbenes, flavanols, monosaccharides, sugar alcohols) with acetone/water from sapwood and heartwood of P. halepensis stem [62]. Additionally, lipophilic and hydrophilic extractives were analyzed with GC-MS that were more abundant in heartwood than in sapwood of P. halepensis [63]. Seed oil of P. halepensis extracted with hexane was rich in fatty acid composition with linoleic and oleic acids accounting for more than 76% [64].
Terpinen-4-ol, cis-β-terpineol, γ-terpinene, sabinene, α-terpinene, and 4-thujanol were identified as the main compounds in S. terebinthifolius branch EO. The EO from S. terebinthifolius showed the presence of several compounds related to monoterpenes, sesquiterpene, and some other organic compounds [65,66,67,68,69,70,71]. Another study showed that the most abundant component of S. terebinthifolius EO was limonene [6]; also, α-phellandrene, β-phellandrene, α-pinene, and limonene were reported in the EO of S. terebinthifolius [69,72].
S. terebinthifolius EO compounds such as α-β-pinene, α-funebrene, Z-salvene, sabinene, and limonene [73] were isolated from fruits, while the compounds β-Longipinene, bicyclogermacrene, germacrene D, and β-pinene were found in leaves [74]. Although, mixed monoterpenes and sesquiterpenes were reported in unripe fruits; namely, α-cadinol, δ-cadinene, elemole, ∆3-carene, germacrene D-4-ol, β-phellandrene, epi-α-cadinol, and germacrene D [67]. On the other hand, the terpenes limonene, sabinene, ∆3-carene, and p-cymene were detected as main components of S. terebinthifolius ripe fruit EO [27].
In the present study, both oils were observed to have potential antimicrobial activity in terms of microbial inhibition when treating wood. The monoterpenic or sesquiterpenic hydrocarbons and their oxygenated derivatives are considered as potential antimicrobial agents by many studies. Thus, these results agree with other previous works [9,18,21,26,75,76].
Recently, schinol and a new biphenyl compound (4′-ethyl-4-methyl-2,2′,6,6′-tetrahydroxyl(1.1′-biphenyl)-4,4′-dicarboxylate), isolated from hexane and dichloromethane fractions obtained from leaves and stems, showed marked antifungal activity against P. brasiliensis [34]. Santos et al. [77] found that EOs from S. terebinthifolius and S. molle could be a possible alternative to control diseases caused by phytopathogenic fungi that affect agricultural production. The EOs from S. terebinthifolius showed a pronounced fungicide effect against Botrytis ssp isolated from “gerberas” and roses [73]. The antifungal activity may be attributed to the presence of the said chemical components in the EO; for instance, O-cymene and limonene have been shown to have strong antifungal properties [78]. Nevertheless, the mechanism of antifungal activity of this EO is still unknown. However, a recent study on the induced damage to the cell membrane structure of yeast and isolated mitochondria suggests that phytoconstituents from the EO of S. terebinthifolius are likely to disrupt the permeability barrier of the cell membranes and thereby inhibit respiration [79,80]. Furthermore, it has been suggested that the differences in susceptibility of tested organisms to monoterpenes and the differences in the efficacy of different monoterpenes may possibly be explained by the variation in the rate of monoterpene penetration and characteristic membrane structure [80].
Several authors who have studied the antimicrobial activity of Pinaceae family [81,82,83] report that monoterpenes possess a high antifungal activity. The absence of monoterpenes in our EO can explain the absence of a very high activity of Aleppo pine EO, but aldehydes are often found as constituents of plant products [84] and may play an important role in the observed antimicrobial activity of plant aldehyde-containing material [85]. Their action, very likely due to an alteration in the function of membrane-associated proteins, seems to be exerted mainly at the cell surface. However, the capability to penetrate the outer layer of cells can help to explain the antimicrobial activity of some aldehydes, especially against Gram-negative bacteria [86,87]. On the other hand, the antifungal activity of our EO may due to the presence of n-caprylaldehyde (hexanal) which is commercially used to produce fruity flavors and to prevent fruit spoilage. Meanwhile, another study confirmed that the saturated aldehydes hexanal, nonanal, and (E)-2-octenal showed almost no antimicrobial activity against some clinical bacteria [88], while the same study proved that the complex of long chain aldehydes—which highly presented in our EO—has very good antimicrobial activity, as they stated that α,β-unsaturated aldehydes ((E)-2-eptenal, (E)-2-nonenal, (E)-2-decenal, and (E,E)-2,4-decadienal) were tested together (ratio = 1:1:1:1) against ATCC bacterial isolates and clinically isolated microbial strains, and a strong synergic effect was observed [88]. Moreover, the effectiveness of the aldehydes seems to depend not only on the presence of the α,β-double bond, but also on the chain length from the enal group and on the microorganism tested. Finally these oil α,β-unsaturated aldehydes might be good alternatives to other highly toxic disinfectants, such as glutaraldehyde [89]. In another study [18], the P. halepensis EO was shown to possess antifungal activity against A. flavus, A. niger, F. oxysporum, and R. stolonifera, and thus can be used as a natural treatment for fungal infections, as well as a natural preservative in food.
The treated wood of Acacia saligna at the concentration of 5% with the methanolic extracts of Morus alba heartwood, Cupressus sempervirens wood, and Maclura pomifera bark showed no fungal growth of T. harzianum on the surface of the wood [52]. An inhibition zone was found against T. harzianum for A. saligna wood treated with the methanolic extract of C. sempervirens wood at concentrations of 5%, 10%, and 20% [52]. Wood samples of P. sylvestris, F. sylvatica, and P. rigida treated with the EOs or extracts from E. camaldulensis leaves or P. rigida wood had a potential effect against the growth of some phytopathogenic fungi [54,56].
Acer saccharum bark acetone extract, in combination with citric acid, applied to Leucaena leucocephala wood showed some activities against T. viride, F. subglutinans, and A. niger [4]. No growth of A. flavus and C. gloeosporioides was observed for sheets of Papyrus (Cyperus papyrus L.) strips pre-treated with P. rigida and E. camaldulensis or Salix babylonica extracts [90]. Melia azedarach wood samples treated with A. saligna flowers water extract showed activity and growth inhibition against F. culmorum, R. solani, and P. chrysogenum [8], while the same treated with the methanol extract of Musa paradisiaca peels showed potential antifungal activity against F. culmorum and R. solani [7]. Additionally, the same wood treated with oils extracted with n-hexane from E. camaldulensis and Vitex agnus-castus showed promising antifungal activities against F. culmorum, R. solani, and P. chrysogenum [3].
Among the chemical components of the oils, there are synergistic or antagonistic interaction effects. The mode of action of EOs has been investigated by many authors, who suggested that antimicrobial activity is produced by interactions provoked by terpenes in the enzymatic systems related with energy production and in the synthesis of structural components of the microbial cells [91]. Other reports have suggested that the components of the EOs cross the cell membrane, interacting with the enzymes and proteins of the membrane such as the H+-ATPase pumping membrane, thus producing a flux of protons toward the cell exterior, which induces changes in the cells and, ultimately, their death [92]. Furthermore, several works [93,94,95,96] have explained how the antimicrobial ability of terpenes stop the functions of cell membranes, not only the permeability, how they might penetrate the membrane to the cell interior organs and interact critically with intracellular sites. Moreover, Daferera et al. [97] reported that the antifungal activity of EOs may be due to formation of hydrogen bonds between the hydroxyl group of oil phenols and the active sites of the target enzymes.

5. Conclusions

The antifungal activity of the wood of Pinus roxburghii treated with P. halepensis branch n-hexane oily liquid extract and S. terebinthifolius branch essential oil was tested against B. oryzae, F. oxysporum, F. solani, and R. solani. Both the extracted essential oil and oily liquid extract inhibited F. oxysporum isolate growth with a percentage of ca. 40% at a concentration of 3%, and showed good bioactivity against the growth of B. oryzae, F. oxysporum, and R. solani. These activities could be related to monoterpenoids, the most abundant compounds identified in the extracts. Therefore, both natural extracted materials could be considered as a wood-biofungicide agent and for their possible use on a larger scale.

Author Contributions

A.A.M., S.I.B., H.M.A., M.E.-H., M.Z.M.S., and N.A.A. designed the experiments, conducted the laboratory analyses, wrote parts of the manuscript, and interpreted the results; all coauthors contributed to writing and revising the article. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Researchers Supporting Project number (RSP-2019/123) King Saud University, Riyadh, Saudi Arabia.

Acknowledgments

Researchers Supporting Project number (RSP-2019/123) King Saud University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Antifungal bioassay of wood treated with (B) P. halepensis oily liquid extract (OLE) and (F) S. terebinthifolius essential oil (EO) against the growth of B. oryzae. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
Figure 1. Antifungal bioassay of wood treated with (B) P. halepensis oily liquid extract (OLE) and (F) S. terebinthifolius essential oil (EO) against the growth of B. oryzae. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
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Figure 2. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of F. oxysporum. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
Figure 2. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of F. oxysporum. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
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Figure 3. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of F. solani. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
Figure 3. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of F. solani. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
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Figure 4. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of R. solani. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
Figure 4. Antifungal bioassay of wood treated with (B) P. halepensis OLE and (F) S. terebinthifolius EO against the growth of R. solani. B1: 3%; B2: 2%; B3: 1%; F1: 3%; F2: 2%; F3: 1%.
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Figure 5. Overall bioactivity of wood treated with P. halepensis OLE and S. terebinthifolius EO; (a) EO and OLE source and (b) EO and OLE concentration against the fungal linear growth of B. oryzae, F. oxysporum, F. solani, and R. solani.
Figure 5. Overall bioactivity of wood treated with P. halepensis OLE and S. terebinthifolius EO; (a) EO and OLE source and (b) EO and OLE concentration against the fungal linear growth of B. oryzae, F. oxysporum, F. solani, and R. solani.
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Table
Table 1. Inhibition percentages of fungal growth (%) as affected by wood treated with P. halepensis OLE and S. terebinthifolius EO.
Table 1. Inhibition percentages of fungal growth (%) as affected by wood treated with P. halepensis OLE and S. terebinthifolius EO.
Oil/Extract TypeConcentration (%)Fungal Inhibition (%)
B. oryzaeF. oxysporumF. solaniR. solani
P. halepensis OLE0 (control)0.000.000.000.00
150.55 ± 4.9231.11 ± 4.0520 ± 9.0724.44 ± 4.05
270 ± 5.2835.55 ± 6.6029.44 ± 4.2030.55 ± 7.34
380 ± 1.8140.55 ± 4.5830.55 ± 2.1241.11 ± 2.86
S. terebinthifolius EO0 (control)0.000.000.000.00
161.11 ± 2.8623.44 ± 2.9313.88 ± 2.1228.33 ± 3.79
271.66 ± 3.7933.33 ± 1.8121.11 ± 2.8635 ± 2.12
374.44 ± 2.8645.55 ± 2.8623.88 ± 2.1254.44 ± 6.91
p-value ********
**: High significance difference.
Table
Table 2. Phytochemicals of essential oil from S. terebinthifolius branches by gas chromatography-mass spectrometry (GC-MS).
Table 2. Phytochemicals of essential oil from S. terebinthifolius branches by gas chromatography-mass spectrometry (GC-MS).
CompoundChemical ClassificationPercentage in the Oil (%)SI 1RSI 2
α-ThujeneMonoterpene0.94935954
α-PineneMonoterpene1.21960962
SabineneMonoterpene9.83961968
β-PineneMonoterpene0.32942952
MyrceneMonoterpene1.88943945
α-TerpineneMonoterpene8.56939944
D-LimoneneMonoterpene2.79926929
α-PhellandreneMonoterpene2.46918921
o-CymeneMonoterpene4.05926937
γ-TerpineneMonoterpene12.46936941
Artemisia ketoneMonoterpene0.33774974
4-ThujanolMonoterpene6.71888890
LinaloolMonoterpene0.74922934
cis-β-TerpineolMonoterpene15.60928937
para-Menth-3-en-1-olMonoterpene1.85888893
cis-para-2-menthen-1-olMonoterpene0.64903918
CamphorMonoterpene0.23765820
Terpinen-4-olMonoterpene18.25931937
(Z)-PiperitolMonoterpene0.28873927
(-)-α-TerpineolMonoterpene4.34941945
trans-PiperitolMonoterpene0.14866925
Linalyl acetateMonoterpene1.63899921
2,2-Dimethyl-3-vinyl-bicyclo[2.2.1]heptaneHydrocarbons0.26748807
ThymolMonoterpene1.19866903
β-CaryophylleneSesquiterpene2.34922941
γ-ElemeneSesquiterpene0.95849885
1 SI: Standard index; 2 RSI: Reverse standard index.
Table
Table 3. Phytochemicals of oily liquid extract from P. halepensis branches by GC/MS.
Table 3. Phytochemicals of oily liquid extract from P. halepensis branches by GC/MS.
CompoundChemical ClassificationPercentage in the Extract (%)SI 1RSI 2
2,7-dimethyl-1-OctanolTerpene hydrocarbon0.70706783
2,6-Dimethyloctane-1,8-diolTerpene hydrocarbon0.25675675
(E)-2-Decen-1-olUnsaturated aldehydes0.57705775
(2-Hexylcyclopropyl)acetic acidHydrocarbons0.29718758
1-DodeceneUnsaturated aldehydes0.47742742
n-CaprylaldehydeAlkyl aldehyde1.31803934
IsopinocarveolPinane monoterpene0.97708748
(E)-9-Tetradecen-1-ol acetateUnsaturated aldehydes0.45751783
trans-2-DecenalUnsaturated aldehydes0.40884921
(Z)-2-DecenalUnsaturated aldehydes6.88901932
(2E)-2-DecenalUnsaturated aldehydes4.65884919
NonanalFatty aldehydes5.85870887
Oxacyclotetradecan-2-oneKetone0.32751752
Methyl octadeca-13,16-diynoateFatty acid methyl ester2.21742750
1-TetradecanolSaturated fatty alcohol0.32767768
(Z)-2-TridecenalUnsaturated aldehydes2.9771814
Undecanoic acid, hydroxy-, lactoneFatty acid0.19740757
1,2-15,16-DiepoxyhexadecaneAlkane hydrocarbon0.74780782
5-heptyldihydro-2(3H)-furanonegamma butyrolactones0.32734745
(E,E)-2,4-DecadienalUnsaturated aldehydes4.41838870
(Z)-Oleic acidFatty acid1.48770770
2-UndecenalUnsaturated aldehydes22.25890903
OlealdehydeAldehydes0.69727792
Arachidonic acid methyl esterFatty acid methyl ester4.36753760
Myristyl chlorideFatty acid1.97735755
Z,Z,Z-1,4,6,9-NonadecatetraeneUnsaturated aldehydes0.68741741
4-Hydroxy-10-methyl-3,4,7,8,9,10-hexahydro-2H-oxecin-2-oneKetone8.43844890
2-methylene-(3β,5α)-Cholestan-3-olSteroids0.87772782
(Z)-7-HexadecenalUnsaturated aldehydes0.46747890
Vitamin A aldehyde (Retinal)Retinoids0.21701771
9-Hexadecenoic acidFatty acid1.08788789
1-HeptatriacotanolFatty alcohol1.15728730
O-BenzylserineAmino acid2.22766776
12,15-Octadecadiynoic acid, methyl esterFatty acid3.1743753
2-(7-heptadecynyloxy)tetrahydro-2H-PyranHydrocarbons4.22697697
1-NonadeceneHydrocarbons3.50724757
Z-(13,14-Epoxy)tetradec-11-en-1-ol acetateHydrocarbons3.04785794
7-Methyl-Z-tetradecen-1-ol acetateHydrocarbons3.01747762
1 SI: Standard index; 2 RSI: Reverse standard index.

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Mohamed, A.A.; Behiry, S.I.; Ali, H.M.; EL-Hefny, M.; Salem, M.Z.M.; Ashmawy, N.A. Phytochemical Compounds of Branches from P. halepensis Oily Liquid Extract and S. terebinthifolius Essential Oil and Their Potential Antifungal Activity. Processes 2020, 8, 330. https://doi.org/10.3390/pr8030330

AMA Style

Mohamed AA, Behiry SI, Ali HM, EL-Hefny M, Salem MZM, Ashmawy NA. Phytochemical Compounds of Branches from P. halepensis Oily Liquid Extract and S. terebinthifolius Essential Oil and Their Potential Antifungal Activity. Processes. 2020; 8(3):330. https://doi.org/10.3390/pr8030330

Chicago/Turabian Style

Mohamed, Abeer A., Said I. Behiry, Hayssam M. Ali, Mervat EL-Hefny, Mohamed Z.M. Salem, and Nader A. Ashmawy. 2020. "Phytochemical Compounds of Branches from P. halepensis Oily Liquid Extract and S. terebinthifolius Essential Oil and Their Potential Antifungal Activity" Processes 8, no. 3: 330. https://doi.org/10.3390/pr8030330

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