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Neg Imane, Bouda Said, Zaggoumi Hasna, Mardoume Ibtissam, Haddioui Abdelmajid
Keywords: n Juniperus oxycedrus subsp. oxycedrusn , Antioxidant activity, Antimicrobial activity, Phytochemical variability, environmental correlation
This study aimed to quantify the phenolic, flavonoid, and tannin contents, and to evaluate the antioxidant, antimicrobial, and antifungal activities of twig extracts from eleven Moroccan populations of Juniperus oxycedrus subsp. oxycedrus. Furthermore, the research investigated the correlation between environmental factors and these phytochemical parameters to determine the influence of biogeographical conditions on the plant’s biological potential. The biochemical profile and biological potential of eleven Moroccan populations were evaluated in relation to environmental factors. Total polyphenols, flavonoids, and condensed tannins were quantified via spectrophotometry, while antioxidant capacity was assessed using DPPH and ABTS assays. Antibacterial and antifungal activities were evaluated against eleven bacterial species and two fungal strains using disk diffusion, well diffusion, and microdilution methods. Scientific precision was ensured by determining the minimum inhibitory (MIC) and minimum bactericidal (MBC) concentrations. Statistical analyses were employed to determine the correlation between biogeographical variables and the observed variability in phytochemical content and biological efficacy across the populations. Twig extracts from eleven Juniperus oxycedrus subsp. oxycedrus populations exhibited significant variability in extraction yield (8.40 ± 2.60%), total phenolic content (13.16 ± 5.03 mg GAE/g DW), and total flavonoid content (1.63 ± 0.83 mg QE/g DW). Potent antioxidant activity was observed (mean DPPH IC₅₀ = 170 ± 80.36 µg/mL), with TPC identified as the primary driver of radical scavenging capacity (r = -0.938, p < 0.01). The extracts demonstrated broad-spectrum antimicrobial efficacy, particularly against Gram-positive bacteria (S. aureus MIC = 0.024 mg/mL) and Fusarium species (inhibition > 60%), although resistant strains remained recalcitrant. Environmental factors significantly influenced these profiles; altitude correlated positively with TPC (r = 0.705), while rainfall exhibited a strong negative correlation with yield (r = -0.841). Principal Component Analysis (62.83% total variance) clustered the populations into three distinct groups corresponding to their geographical mountain ranges, underscoring the influence of provenance and bioclimatic conditions on the phytochemical and biological potency of Juniperus oxycedrus subsp. oxycedrus. These findings highlight the biochemical diversity of Moroccan Juniperus oxycedrus subsp. oxycedrus, emphasizing its potential as a source of natural antioxidants and antimicrobials. The results advocate for targeted conservation strategies to preserve biochemically rich populations for medicinal and aromatic applications.
Akkol EK, Orhan I, Kartal M, Yeşilada E (2010) Bioactivity guided evaluation of anti-inflammatory and antinociceptive activities of Arceuthobium oxycedri (DC) M. Bieb. J Ethnopharmacol 128(1):79–84
Amrani O, Karim A, Marghich M, Beyi L, Bouknana S, Aziz M (2024) Antispasmodic and antidiarrheal effects of Juniperus oxycedrus L. on the jejunum in rodents. J Smooth Muscle Res 60:10–22. https://doi.org/10.1540/JSMR.60.1
Antasionasti I, Datu OS, Lestari US, Abdullah SS, Jayanto I (2021) Correlation Analysis of Antioxidant Activities with Tannin, Total Flavonoid, and Total Phenolic Contents of Nutmeg (Myristica fragrans Houtt) Fruit Precipitated by Egg white. Borneo J Pharm 4:301–310. https://doi.org/10.33084/bjop.v4i4.2497
Araujo RDC, Da Costa ALP, Pinto JB, Da Silva LMA, Da Silva GA. Seasonal and pluviometric effects on the phenolic compound compositionand antioxidant potential of licania macrophylla benth (Chrysobalanaceae), a medicinal plant from the amazon rainforest. Brazilian J Pharm Sci2022;58. https://doi.org/10.1590/s2175-97902022e19558
Aziz EE, Badawy EM, Zheljazkov VD, Nicola SM, Fouad H (2019) Yield and chemical composition of essential oil of achillea millefolium L. As affected by harvest time. Egypt J Chem 62(3):933. https://doi.org/10.21608/ejchem.2018.5129.145
Ba K, Tine E, Destain J, Cissé N, Thonart P (2010) Étude comparative des composés phénoliques, du pouvoir antioxydant de différentes variétés de sorgho sénégalais et des enzymes amylolytiques de leur malt. Biotechnol Agron Soc Envir, 14(1)
Barbieri F, Montanari C, Šimat V, Skroza D, Čagalj M, Smole-Možina S et al (2022) Effects of Rubus fruticosus and Juniperus oxycedrus derivatives on culturability and viability of Listeria monocytogenes. Sci Rep 12:13158. https://doi.org/10.1038/s41598-022-17408-4
Bellakhdar J (1997) La pharmacopee marocaine traditionnelle. Medecine arabe ancienne et savoirs populaires. Ibis, Paris
Benabid A (2000) Flore et écosystèmes du Maroc Évaluation et préservation de la biodiversité. Ibis, Paris,France
Bouhlal K, Meynadier JM, Peyron JL, Peyron L, Marion JP, Bonetti G (1988) Le cade en dermatologie. Parfums cosmétiques arômes 83:73–82
Brighente IMC, Dias M, Verdi LG, Pizzolatti MG (2007) Antioxidant activity and total phenolic content of some Brazilian species. Pharma biol 45(2):156–161. https://doi.org/10.1080/13880200601113131
Cherrat L, Espina L, Bakkali M, Pagán R, Laglaoui A (2014) Chemical composition, antioxidant and antimicrobial properties of Mentha pulegium, Lavandula stoechas and Satureja calamintha Scheele essential oils and an evaluation of their bactericidal effect in combined processes. IFSET 22:221–229. https://doi.org/10.1016/j.ifset.2013.12.016
Cosentino S, Barra A, Pisano B, Cabizza M, Pirisi FM, Palmas F (2003) Composition and antimicrobial properties of Sardinian Juniperus essential oils against foodborne pathogens and spoilage microorganisms. JFB 66(7):1288–1291. https://doi.org/10.4315/0362-028X-66.7.1288Get rights and content
Diep T, Pook C, Yoo M (2020) Phenolic and anthocyanin compounds and antioxidant activity of Tamarillo (Solanum betaceum Cav). Antioxidants 9(2):1–21. https://doi.org/10.3390/antiox9020169
Djellouli S, Larbi KS, Meddah B, Rebiai A, Touil AT, Sonnet P (2022) Chemical composition, in vitro antioxidant and anti-inflammatory activities of Juniperus oxycedrus subsp. oxycedrus extracts from Algeria. Eur J Biol Res 12(2):271–281
Dob T, Dahmane D, Chelghoum C (2006) Essential oil composition of Juniperus oxycedrus. growing in Algeria. Pharm biol 1(1):1–6. https://doi.org/10.1080/13880200500530922
El Azzouzi F, Zidane L (2015) La flore médicinale traditionnelle de la région de Béni- Mellal (Maroc). J Appl Biosci 91:8493. https://doi.org/10.4314/jab.v91i1.8
El Hajjouji H, Rahhal R, Gmouh S, Hsaine M, Fougrach H, Badri W (2019) Chemical composition, antioxidant and antibacterial activities of the essential oils of Juniperus phoenicea, Juniperus thurifera and Juniperus oxycedrus. Mediterr J Chem 9:190–198. https://doi.org/10.13171/mjc93191002145heh
Fromard F, Gauquelin T (1993) Thuriferous juniper stands in Morocco: research and conservation for an endangered environment and species
Gaamouche S, Arakrak A, Bakkali M, Laglaoui A (2021) Combined antimicrobial effect of bacteriocins of LAB isolated from a traditional brine table olives and essential oils against foodborne pathogens. Moroccan J Chem 9(3):J–Chem. https://doi.org/10.48317/IMIST.PRSM/morjchem-v9i3.22091
Guerroudj S, Maatoug M, Naceur K, Chaibi R, Khene M, Boualem A (2021) Extraction, yield and chemical composition of essential oils of Juniperus oxycedrus L. from Tiaret region (Algeria). Ukr J Ecol 11(10):105–111
Hatano T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem Pharm Bull 36(6):2090–2097
Kalogiouri NP, Kritikou E, Martakos IC, Lazarou C, Pentogennis M, Thomaidis NS (2021) Characterization of the phenolic fingerprint of kolovi extra virgin olive oils from lesvos with regard to altitude and farming system analyzed by uhplc-qtof‐ms. Molecules. https://doi.org/10.3390/molecules26185634
Karaman I, Şahin F, Güllüce M, Öǧütçü H, Şengül M, Adigüzel A (2003) Antimicrobial activity of aqueous and methanol extracts of Juniperus oxycedrus L. J Ethnopharmacol 85:231–235. https://doi.org/10.1016/S0378-8741(03)00006-0
Kiani R, Arzani A, Mirmohammady Maibody SAM (2021) Polyphenols, Flavonoids, and Antioxidant Activity Involved in Salt Tolerance in Wheat, Aegilops cylindrica and Their Amphidiploids. Front Plant Sci 12:1–13. https://doi.org/10.3389/fpls.2021.646221
Leung AY, Foster S (1996) Encyclopedia of common natural ingredients used in food, drugs, and cosmetics, New York
Magaldi S, Mata-Essayag S, De Capriles CH, Pérez C, Colella MT, Olaizola C, Ontiveros Y (2004) Well diffusion for antifungal susceptibility testing. IJID 8(1):39–45. https://doi.org/10.1016/j.ijid.2003.03.002
Mërtiri I, Păcularu-Burada B, Stănciuc N (2024a) Phytochemical characterization and antibacterial activity of Albanian Juniperus communis and Juniperus oxycedrus berries and needle leaves extracts. Antioxidants 13(3):345
Miceli N, Trovato A, Marino A, Bellinghieri V, Melchini A, Dugo P (2011) Phenolic composition and biological activities of Juniperus drupacea Labill. berries from Turkey. Food Chem Toxicol 49:2600–2608. https://doi.org/10.1016/j.fct.2011.07.004
Moreno L, Bello R, Beltran B, Calatayud S, Primo-Yúfera E, Esplugues J (1998) Pharmacological screening of different Juniperus oxycedrus L. extracts. Pharmacol toxicol 82(2):108–112
Mrid RB, Bouchmaa N, Bouargalne Y, Ramdan B, Karrouchi K, Kabach I, Karbane M, El, Idir A, Zyad A, Nhiri M (2019) Phytochemical characterization, antioxidant and in vitro cytotoxic activity evaluation of juniperus oxycedrus subsp oxycedrus needles and berries. Molecules. https://doi.org/10.3390/molecules24030502
Muflihah YM, Gollavelli G, Ling YC (2021) Correlation study of antioxidant activity with phenolic and flavonoid compounds in 12 indonesian indigenous herbs. Antioxidants 10(10):1–15. https://doi.org/10.3390/antiox10101530
Najar B, Pistelli L, Buhagiar J (2020) Volatilomic analyses of Tuscan Juniperus oxycedrus L. and in vitro cytotoxic effect of its essential oils on human cell lines. JEOBP 23(4):756–771. https://doi.org/10.1080/0972060X.2020.1823891
Nemeth E (2005) Changes in essential oil quantity and quality influenced by ontogenetic factors. Acta Hortic. https://doi.org/10.17660/ActaHortic.2005.675.23
Orhan N, Orhan IE, Ergun F (2011) Insights into cholinesterase inhibitory and antioxidant activities of five Juniperus species. FCT 49(9):2305–2312
Özhatay N, Koyuncu M, Atay S, Byfi eld A (1997) Türkiye’nin Doğal Tıbbi Bitkilerinin Ticareti Hakkında Bir Çalışma. Doğal Hayatı Koruma Derneği, İstanbul, Türkiye
Platzer M, Kiese S, Herfellner T, Schweiggert-Weisz U, Miesbauer O, Eisner P (2021) Common trends and differences in antioxidant activity analysis of phenolic substances using single electron transfer based assays. Molecules. https://doi.org/10.3390/molecules26051244
Raho GB, Otsmane M, Sebaa F (2017) Antimicrobial activity of essential oils of Juniperus phoenicea from North Western Algeria. J Med Bot 1:01–7
Rajouani N, Benyamna A, Romane A, Bouamama H (2015) Chemical Composition, Antioxidant and Antibacterial Activity of Juniperus oxycedrus subsp. oxycedrus L. berry, essential oil from Morocco. J ApplChem Envir Prot 1:9–19
Re R, Pellegrini N, Pannala A, Yang M, Rice-Evan C (1999) Antioxidant activity applying an improvrd ABTS radical cation decolorization. Free Radic Biol Med 26(9–10):1231–1237
Sauvage C, Vindt J (1952) Flore de Maroc : Analytique, descriptive et illustrée. Editions Internationales. Rabat.
Sharififar F, Moshafi MH, Mansouri SH, Khodashenas M, Khoshnoodi M (2007) In vitro evaluation of antibacterial and antioxidant activities of the essential oil and methanol extract of endemic Zataria multiflora Boiss. Food Control 18(7):800–805. https://doi.org/10.1016/j.foodcont.2006.04.002
Simonetti G, Brasili E, Pasqua G (2020) Antifungal Activity of Phenolic and Polyphenolic Compounds from Di ff erent Matrices of Vitis vinifera. Molecules 25:1–22
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticult 16(3):144–158
Spengler G, Gajdács M, Donadu MG, Usai M, Marchetti M, Ferrari M (2022) Evaluation of the Antimicrobial and Antivirulent Potential of Essential Oils Isolated from Juniperus oxycedrus L. ssp. macrocarpa Aer Parts Microorganisms 10:1–19. https://doi.org/10.3390/microorganisms10040758
Taviano MF, Marino A, Trovato A, Bellinghieri V, La Barbera TM, Gvenç A (2011) Antioxidant and antimicrobial activities of branches extracts of five Juniperus species from Turkey. Pharm Biol 49:1014–1022. https://doi.org/10.3109/13880209.2011.560161
Taviano MF, Marino A, Trovato A, Bellinghieri V, Melchini A, Dugo P (2013) Juniperus oxycedrus L. subsp. oxycedrus and Juniperus oxycedrus L. subsp. macrocarpa (Sibth. & Sm.) Ball. berries from Turkey: Comparative evaluation of phenolic profile, antioxidant, cytotoxic and antimicrobial activities. Food Chem Toxicol 58:22–29. https://doi.org/10.1016/j.fct.2013.03.049
Theodosi S, Kosma IS, Badeka AV (2021) Quality characteristics of Koroneiki olive oil from Zakynthos island (Greece) and differentiation depending on the altitude level. Eur Food Res Technol 247:1235–1248. https://doi.org/10.1007/s00217-021-03705-1
Valdés B (2002) Catalogue des plantes vasculaires du Nord du Maroc, incluant des clés d’identification. Consejo Superior de Investigaciones Científicas
Laboratory of Agro-Industrial and Medical Biotechnologies, Faculty of Sciences and Technics, Sultan Moulay Slimane University, Beni Mellal, Morocco