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Potential impacts of Pinus halepensis Miller trees as a source of phytochemical compounds: antibacterial activity of the cones essential oil and n-butanol extract

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Abstract

The Aleppo pine (Pinus halepensis Miller) trees grown in the agricultural lands with high biodiversity, and considered as a potential source for chemical and therapeutic compounds. Essential oil (EO) and n-butanol fraction (But-fr) of Aleppo pine cones were evaluated against the growth of four plant bacterial pathogens (Dickeya solani, Pectobacterium atrosepticum, Ralstonia solanacearum, and Agrobacterium tumefaciens) and four human pathogenic bacteria (Bacillus subtilis ATCC 6633, Sarcina lutea ATCC 9341, Escherichia coli ATCC 8739, and Staphylococcus aureus ATCC 6538). The diameter of the inhibition zone (IZ) and the minimum inhibitory concentrations (MICs) were measured. At 2000 μg/mL, But-fr showed the strongest activity against D. solani, P. atrosepticum, and R. solanacearum with inhibition zones (IZs) of 14.33 mm, 12.33 mm, and 15.33 mm, respectively. At 2000 μg/mL, EO showed the best activity against A. tumefaciens with an IZ value of 12.67 mm. Weak activity was observed by applying the EO and But-fr against B. subtilis and S. lutea, while good activity was recorded by But-fr against E. coli and S. aureus with IZs values of 13.67 mm and 11.33 mm, respectively, at 2000 μg/mL. Gas chromatography-mass spectrometry (GC/MS) analysis reported that the EO from cones contained mainly caryophyllene (15.17%), α-pinene (13.51%), and caryophyllene oxide (12.57%); But-fr contained 3,4-dimethyldihydrofuran-2,5-dione (36.25%), and 2-methylenecholestan-3-ol (18.12%). The phytochemical But-fr extract of Aleppo pine cones demonstrated moderate antibacterial effects against the studied bacteria.

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References

  • Abi-Ayad M, Abi-Ayad FZ, Lazzouni HA, Rebiahi SA, Ziani-Cherif C, Bessiere JM (2010a) Chemical composition and antifungal activity of Aleppo pine essential oil. J Med Plant Res 5(22):5433–5436

    Google Scholar 

  • Abi-Ayad M, Abi-Ayad FZ, Lazzouni HA, Rebiahi SA (2010b) Antibacterial activity of Pinus halepensis essential oil from Algeria (Tlemcen). J Nat Prod Plant Resour 1(1):33–36

    Google Scholar 

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing, Carol Stream

    Google Scholar 

  • Alrababah MA, Tadros MJ, Samarah NH, Ghosheh H (2009) Allelopathic effects of Pinus halepensis and Quercus coccifera on the germination of Mediterranean crop seeds. New Forest 38:261–272

    Google Scholar 

  • Amri I, Hamrouni L, Hanana M, Gargouri S, Fezzani T, Jamoussi B (2013) Chemical composition, physico-chemical properties, antifungal and herbicidal activities of Pinus halepensis Miller essential oils. Biol Agric Hortic 29(2):91–106

    Google Scholar 

  • Ashmawy NA, Behiry SI, Ali HM, Salem MZM (2014) Evaluation of Tecoma stans and Callistemon viminalis extracts against potato soft rot bacteria in vitro. J Pure App Microbiol 8(2):667–673

    Google Scholar 

  • Ashmawy NA, Behiry SI, Younes HA, Khaled AE (2015) Development of polyclonal rabbit serum-based ELISA for detection of Pectobacterium carotovorum subsp. carotovorum and its specificity against other causing soft rot bacteria. Asian J Plant Pathol 9(3):135–141

    Google Scholar 

  • Ashmawy NA, Salem MZM, El-Hefny M, Abd El-Kareem MSM, El-Shanhorey NA, Mohamed AA, Salem AZM (2018) Antibacterial activity of the bioactive molecules identified in three woody plants against some pathogenic bacteria. Microb Pathog 12:331–340

    Google Scholar 

  • Baba Aissa F (1991) Medicinal plants in Algeria. Identification, description of active ingredient properties and traditional use of common plants in Algeria. Algiers, Bouchene and Ad. Diwan, p 181

    Google Scholar 

  • Behiry SI, Ashmawy NA, Abdelkhalek AA, Younes HA, Khaled AE, Hafez EE (2018) Compatible and incompatible type interactions related to defense genes in potato elucidation by Pectobacterium carotovorum. J Plant Dis Prot 125(2):197–204

    Google Scholar 

  • Chakotiya AS, Tanwar A, Narula A, Sharma RK (2017) Zingiber officinale: its antibacterial activity on Pseudomonas aeruginosa and mode of action evaluated by flow cytometry. Microb Pathog 107(6):254–260

    CAS  PubMed  Google Scholar 

  • Cheikh-Rouhou S, Hentati B, Besbes S, Blecker C, Deroanne C, Attia H (2006) Chemical composition and lipid fraction characteristics of Alleppo pine (Pinus halepensis Mill.) seeds cultivated in Tunisia. Food Sci Technol Int 12(5):407–415

    CAS  Google Scholar 

  • Cowan ST, Steel KJ (1974) Manual for the identification of medical bacteria, 2nd edn. Cambridge University Press, London

    Google Scholar 

  • Czajkowski R, Pérombelon M, Jafra S, Lojkowska E, Potrykus M, van der Wolf J, Sledz W (2015) Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: a review. Ann Appl Biol 166(1):18–38

    CAS  PubMed  Google Scholar 

  • De Cleene M, De Ley J (1976) The host range of crown gall. Bot Rev 42(4):389–466

    Google Scholar 

  • de Silva T (1997) In: Bodeker G, Bhat KKS, Burley J, Vantomme P (eds) Medicinal plants for forest conservation and healthcare. Non-wood forest products no. 11. FAO, Rome, pp 38–48

    Google Scholar 

  • Dığrak M, İlçim A, Alma MH (1999) Antimicrobial activities of several parts of Pinus brutia, Juniperus oxycedrus, Abies cilicia, Cedrus libani and Pinus nigra. Phytother Res 13(7):584–587

    PubMed  Google Scholar 

  • Djerrad Z, Djouahri A, Kadik L (2017) Variability of Pinus halepensis Mill. Essential oils and their antioxidant activities depending on the stage of growth during vegetative cycle. Chem Biodivers 14(4):e1600340

    Google Scholar 

  • Dob T, Berramdane T, Chelgoum C (2005) Chemical composition of essential oil of Pinus halepensis Miller growing in Algeria. C R Chimie 8(11–12):1939–1945

    CAS  Google Scholar 

  • Dob T, Berramdane T, Chelghoum C (2007) Essential oil composition of Pinus halepensis Mill. from three different regions of Algeria. J Essent Oil Res 19:40–43

    CAS  Google Scholar 

  • EL-Hefny M, Ali HM, Ashmawy NA, Salem MZM (2017a) Chemical composition and bioactivity of Salvadora persica extracts against some potato bacterial pathogens. BioRes 12(1):1835–1849

    Google Scholar 

  • El-Hefny M, Ashmawy NA, Salem MZM, Salem AZM (2017b) Antibacterial activity of the phytochemicals-characterized extracts of Callistemon viminalis, Eucalyptus camaldulensis and Conyza dioscoridis against the growth of some phytopathogenic bacteria. Microb Pathog 113(12):348–356

    CAS  PubMed  Google Scholar 

  • Eloff JN (1998) A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 64(8):711–713

    CAS  PubMed  Google Scholar 

  • FAO (2003) State of the World’s Forests. FAO, Rome, p 153

    Google Scholar 

  • Fekih N, Allali H, Merghache S, Chaïb F, Merghache D, El Amine M, Djabou N, Muselli A, Tabti B, Costa J (2014) Chemical composition and antibacterial activity of Pinus halepensis Miller growing in West Northern of Algeria. Asian Pac J Trop Dis 4(2):97–103

    CAS  PubMed Central  Google Scholar 

  • Fernandez C, Voiriot S, Mévy JP, Vila B, Ormeño E, Dupouyet S et al (2008) Regeneration failure of Pinus halepensis Mill.: the role of autotoxicity and some abiotic environmental parameters. For Ecol Manag 255(7):2928–2936

    Google Scholar 

  • Gardan L, Gouy C, Christen R, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Microbiol 53(Pt 2):381–391

    CAS  PubMed  Google Scholar 

  • Hamrouni L, Hanan M, Amri I, Romane AE, Gargouri S, Jamoussi B (2015) Allelopathic effects of essential oils of Pinus halepensis Miller: chemical composition and study of their antifungal and herbicidal activities. Arch Phytopathol PFL 48(2):145–158

    CAS  Google Scholar 

  • Hijmans RJ, Forbes GA, Walker TS (2000a) Estimating the global severity of potato late blight with a GIS-linked disease forecaster. Plant Pathol 49:697–705

    Google Scholar 

  • Hijmans RJ, Garrett KA, Huamán Z, Zhang DP, Schreuder M, Bonierbale M (2000b) Assessing the geographic representativeness of genebank collections: the case of Bolivian wild potatoes. Conserv Biol 14:1755–1765

    Google Scholar 

  • Hmamouchi M, Hamamouchi J, Zouhdi M, Bessiere JM (2001) Chemical and antimicrobial properties of essential oils of five Moroccan Pinaceae. J Essent Oil Res 13(4):298–302

    CAS  Google Scholar 

  • Joshi DN, Rawat GS (1997) Need for conservation and propagation of alpine and sub-alpine medicinal plants of northwest Himalayas. Indian Forester 123:811–814

    Google Scholar 

  • Kabeil SS, Lashin SM, El-Masry MH (2008) Potato brown rot disease in Egypt. J Agric Environ Sci 4(1):44–54

    Google Scholar 

  • Kainulainen P, Holopainen JK (2002) Concentrations of secondary compounds in Scots pine needles at different stages of decomposition. Soil Biol Biochem 34:37–42

    CAS  Google Scholar 

  • Kerr A, Brisbane PG (1983) Agrobacterium. In: Fahy PC, Persley GJ (eds) Plant bacterial disease: a diagnostic guide. Academic Press, New York, pp 27–43

    Google Scholar 

  • Klement K, Rudolph K, Sands DC (1990) Methods in phytobacteriology, vol 810. Akedemiai Kiado, Budapest

    Google Scholar 

  • Macchioni F, Cioni PL, Flamini G, Morelli I, Maccioni S, Ansaldi M (2003) Chemical composition of essential oils from needles, branches and cones of Pinus pinea, P. halepensis, P. pinaster and P. nigra from central Italy. Flavour Fragr J 18(2):139–143

    CAS  Google Scholar 

  • Marti R, Cubero J, Daza A, Piquer J, Salcedo CI, Morente C, Lòpez MM (1998) Evidence of migration and endophytic presence of Agrobacterium tumefaciens in rose plant. Eur J Plant Pathogen 50:1–12

    Google Scholar 

  • Matasyoh JC, Kiplimo JJ, Karubiu NM, Hailstorks TP (2007) Chemical composition and antimicrobial activity of essential oil of Tarchonanthus camphoratus. Food Chem 101(3):1183–1187

    CAS  Google Scholar 

  • Mohareb ASO, Kherallah IEA, Badawy MEI, Salem MZM, Hameda AY (2017) Chemical composition and activity of bark and leaf extracts of pinus halepensis and Olea europaea grown in AL-Jabel AL-Akhdar region, Libya against some plant phytopathogens. J Appl Biotechnol Bioeng 3(3):331–342

    Google Scholar 

  • Moore LW, Kado CI, Bouzar H (2011) Agrobacterium. In: Schaad NW, Jones JB, Chun W (eds) Laboratory guide for identification of plant pathogenic bacteria. APS Press, St. Paul, pp 17–35

    Google Scholar 

  • Nam AM, Casanova J, Tomi F, Bighelli A (2014) Composition and chemical variability of Corsican Pinus halepensis cone oil. Nat Prod Commun 9(9):1361–1364

    CAS  PubMed  Google Scholar 

  • Nam AM, Tomi F, Gibernau M et al (2016) Composition and chemical variability of the needle oil from Pinus halepensis growing in Corsica. Chem Biodivers 13(4):380–386

    CAS  PubMed  Google Scholar 

  • Nash RJ, Longland AC, Wormald MR (1994) The potential of trees as sources of new drugs and pesticides. In: Singh P, Pathak PS, Roy MM (eds) Agroforestry systems for degraded lands, vol 2. Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, pp 899–910

    Google Scholar 

  • Navarro-Cano JA, Barbera GG, Ruiz-Navarro A, Castillo VM (2009) Pine plantation bands limit seedling recruitment of a perennial grass under semiarid conditions. J Arid Environ 73(1):120–126

    Google Scholar 

  • NCCLS (1997) Performance standards for antimicrobial disk susceptibility tests: approved standard M2–A7. National Committee for Clinical Laboratory Standards, Wayne

    Google Scholar 

  • Panos VR, Petrakis V, Ortiz A, Mazomenos BE (1995) Volatile constituents of needles of five Pinus species grown in Greece. Phytochemistry 39(2):357–361

    Google Scholar 

  • Pérombelon MCM, Van Der Wolf JM (2002) Methods for the Detection and Quantification of Erwinia carotovora subsp. Atroseptica (Pectobacterium carotovorum subsp. Atrosepticum) on potatoes: a laboratory manual. Scottish Crop Research Institute, Invergowrie, p 393

    Google Scholar 

  • Pionnat S, Keller H, Hericher D, Bettachini A, Dessaux Y, Nesme X, Poncet C (1999) Ti plasmids from Agrobacterium characterize rootstock clones that initiated a spread of crown gall disease in Mediterranean countries. Appl Environ Microb 65:4197–4206

    CAS  Google Scholar 

  • Prajapati ND, Purohit SS, Sharma AK, Kumar T (2003) A handbook of medicinal plants. Agribios (India) 553:pp

    Google Scholar 

  • Rao MR, Palada MC, Becker BN (2004) Medicinal and aromatic plants in agroforestry systems. Agroforest Syst 61:107–122

    Google Scholar 

  • Rios JL, Recio MC (2005) Medicinal plants and antimicrobial activity. J Ethnopharmacol 100(1–2):80–84

    CAS  PubMed  Google Scholar 

  • Rusenova N, Parvanov P (2009) Antimicrobial activities of twelve essential oils against microorganisms of veterinary importance. Trakia J Sci 7(1):37–43

    Google Scholar 

  • Saadou NC, Seridi R, Helamia F, Djahoudi A (2013) Chemical composition and antibacterial activities of Algerian Pinus halepensis Mill and Pinus maritima essential oils. Plant Med 79:114. https://doi.org/10.1055/s-0033-1352203

    Article  Google Scholar 

  • Sakagami H, Kawazoe N, Komatsu N, Simpson A, Nonoyama M, Konno K, Yoshida T, Kuroiwa Y, Tanuma S (1991) Antitumor, antiviral and immunopotentiating activities of pine cone extracts: potential medicinal efficacy of natural and synthetic lignin-related materials. Anticancer Res 11(2):881–888

    CAS  PubMed  Google Scholar 

  • Salem MZM, Ali HM, El-Shanhorey NA, Abdel-Megeed A (2013) Evaluation of extracts and essential oil from Callistemon viminalis leaves: antibacterial and antioxidant activities, total phenolic and flavonoid contents. Asian Pac J Trop Med 6(10):785–791

    CAS  PubMed  Google Scholar 

  • Salem MZM, Ali HM, Basalah MO (2014a) Essential oils from wood, bark, and needles of Pinus roxburghii Sarg. from Alexandria, Egypt: antibacterial and antioxidant activities. BioRes 9(4):7454–7466

    Google Scholar 

  • Salem MZM, Hatamleh AA, Ali HM (2014b) Efficacy of oily and resinous fractions of cone extracts from Pinus roxburghii Sarg. J Pure Appl Microbiol 8(5):3909–3913

    Google Scholar 

  • Salem MZM, El-Hefny M, Ali HM, Elansary HO, Nasser RA, El-Settawy AAA, El Shanhorey N, Ashmawy NA, Salem AZM (2018a) Antibacterial activity of extracted bioactive molecules of Schinus terebinthifolius ripened fruits against some pathogenic bacteria. Microb Pathog 120:119–127

    CAS  PubMed  Google Scholar 

  • Salem MZM, Behiry SI, Salem AZM (2018b) Effectiveness of root-bark extract from Salvadora persica against the growth of certain molecularly identified pathogenic bacteria. Microb Pathog 117(4):320–326

    CAS  PubMed  Google Scholar 

  • SAS (2001) Users guide: statistics (release 8.02). SAS Institute, Cary

    Google Scholar 

  • Soković M, Griensven LJLD (2006) Antimicrobial activity of essential oils and their components against the three major pathogens of cultivated button mushroom Agaricus bisporus. Eur J Plant Path 116(3):211–224

    Google Scholar 

  • Staley JT, Boone DR, Garrity GM, Devos P, Fellow MG, Rainey FA, Schlifer KH, Brenner DJ, Castenholz RW, Holt JG, Krieg NR, Liston J, Moulder JW, Murray RGE, JrCF Niven, Pfenning N, Sneath PHA, Jully JG, Williams S (2005) Bergey’s manual of systematic bacteriology: the proteobacteria, vol 2. Williams and Wilkins, Baltimore

    Google Scholar 

  • Süntar I, Tumen I, Ustün O, Keles H, Akkol EK (2012) Appraisal on the wound healing and anti-inflammatory activities of the essential oils obtained from the cones and needles of Pinus species by in vivo and in vitro experimental models. J Ethnopharmacol 139(2):533–540

    PubMed  Google Scholar 

  • Toth IK, van der Wolf JM, Saddler G, Lojkowska E, Hélias V, Pirhonen M, Tsror L, Lahkim J, Elphinstone G (2011) Dickeya species: an emerging problem for potato production in Europe. Plant Pathol 60(3):385–399

    Google Scholar 

  • Tumen I, Hafizoglu H, Kilic A, Dönmez IE, Sivrikaya H, Reunanen M (2010) Yields and constituents of essential oil from cones of Pinaceae spp. natively grown in Turkey. Molecules 15(8):5797–5806

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viljoen AM, Subramoney S, Vuuren SF, Başer KHC, Demirci B (2005) The composition, geographical variation and antimicrobial activity of Lippia javanica (Verbenaceae) leaf essential oils. J Ethnopharmacol 96(1–2):271–277

    CAS  PubMed  Google Scholar 

  • Zou X, Sanford RL (1990) Agroforestry systems in China: a survey and classification. Agroforest Syst 11:85–94

    Google Scholar 

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Acknowledgements

The authors would like to thank the Deanship of Scientific Research at King Saud University for funding this work through research Group No. RG 1439-044.

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Authors and Affiliations

  1. Department of Plant Pathology, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria, Egypt

    Nader A. Ashmawy

  2. Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

    Dunia A. Al Farraj, Mohamed S. Elshikh, Roua Al-Kufaidy & Mariyam K. Alshammari

  3. Forestry and Wood Technology Department, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria, Egypt

    Mohamed Z. M. Salem

  4. Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma del Estado de México, Toluca, Estado de México, Mexico

    Abdelfattah Z. M. Salem

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  1. Nader A. Ashmawy
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Ashmawy, N.A., Al Farraj, D.A., Salem, M.Z.M. et al. Potential impacts of Pinus halepensis Miller trees as a source of phytochemical compounds: antibacterial activity of the cones essential oil and n-butanol extract. Agroforest Syst 94, 1403–1413 (2020). https://doi.org/10.1007/s10457-018-0324-5

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