Phytochemical and antioxidant activity of male and female buds and pollen grains of Pistacia atlantica

Authors

  • Asmaâ Dich, Waffa Abdelmoumene, Larbi Belyagoubi, Assia Benmahieddine, Imad Abdelhamid El Haci, Ikram Belhocine, Imane Nabib, Nabila Belyagoubi‑Benhammou 1.Laboratory of Natural Products, Department of Biology, Faculty of Natural and Life Sciences, Earth and Universe Sciences, University Abou-Bekr Belkaïd, Tlemcen, 13000, Algeria. 2.Center of Scientific and Technical Research in Physico-Chemical Analyses (CRAPC), BP 384 Bou-Ismail, 42004 Tipaza, Algeria

DOI:

https://doi.org/10.46325/1y2ya545

Keywords:

Pistacia atlantica, Buds, Pollen grains, Phytochemical study, Antioxidant activity.

Abstract

To enhance the different parts of Pistacia atlantica, male and female buds, and pollen grains were selected to quantify the levels of phenolic compounds and evaluate their antioxidant properties. The results showed that the best yield (30.60 ± 2.82%) was in male buds. Noting that the crude extracts of male and female buds were rich in total phenols (636.83 ± 4.72 and 648.97 ± 4.80 mg GAE/g DM) and condensed tannins (4.10 ± 0.53 and 6.02 ± 0.62 mg CE/g DM), respectively, while the crude extract of pollen grains was rich in flavonoids (15.53 ± 1.20 mg CE/g DM). The study of antioxidant power revealed that the crude extract of male buds has the best total antioxidant capacity (TAC) (115.08 ± 3.38 mg AAE/g DM), and the best effects of reducing power (EC50 = 0.094 ± 0.003 mg/mL) and β-carotene bleaching (EC50 = 0.533 ± 0.14 mg/mL). HPLC-DAD analyses revealed the presence of rutin in pollen grains and male bud extracts and catechin in female bud extract. These findings highlight the male buds of P. atlantica as the most promising part of the plant, suggesting their valuable use in phytopharmaceutical and nutraceutical applications.

References

Abdenbi, A., Touati, B., Bouazza, M., Tail, N., Boutercha, M. (2016). Antibacterial activity and physicochemical characteristics of Pistacia atlantica extracts. Der Pharma Chemica, 8(12): 162-168.

Achili, I., Amrani, A., Bensouici, C., Gül, F., Altun, M., Demirtas, I., Benayache, S. (2020). Chemical constituents, antioxidant, anticholinesterase, and antiproliferative effects of Algerian Pistacia atlantica Desf. extracts. Recent Patents on Food, Nutrition and Agriculture, 11(3): 249-256. https://doi.org/10.2174/2212798411666200207101502

Ait Said, S., Fernandez, C., Greff, S., Derridj, A., Gauquelin, T., Mevy, J.P. (2011). Inter-population variability of leaf morpho-anatomical and terpenoid patterns of Pistacia atlantica Desf. ssp. atlantica growing along an aridity gradient in Algeria. Flora-Morphology, Distribution, Functional Ecology of Plants, 206(4): 397-405. https://doi.org/10.1016/j.flora.2010.08.002

Amri, O., Zekhnini, A., Bouhaimi, A., Tahrouch, S., Hatimi, A. (2018). Anti-inflammatory activity of methanolic extract from Pistacia atlantica Desf. leaves. Pharmacognosy Journal, 10(1): 71-76. http://doi.org/10.5530/pj.2018.1.14

Anusuya, N., Gomathi, R., Manian, S., Sivaram, V., Menon, A. (2012). Evaluation of Basella rubra L., Rumex nepalensis Spreng., and Commelina benghalensis L. for antioxidant activity. International Journal of Pharmacy and Pharmaceutical Sciences, 4(3): 714–720.

Barreca, D., Laganà, G., Leuzzi, U., Smeriglio, A., Trombetta, D., Bellocco, E. (2016). Evaluation of the nutraceutical, antioxidant, and cytoprotective properties of ripe pistachio (Pistachia vera L. variety Bronte) hulls. Food Chemistry, 196: 493– 502. https://doi.org/10.1016/j.foodchem.2015.09.077

Belhadj, S., Derridj, A., Auda, Y., Gers, C., Gauquelin, T. (2008). Analyse de la variabilité morphologique chez huit populations spontanées de Pistacia atlantica en Algérie. Botany, 86(5): 520-532. https://doi.org/10.1139/B08-008

Belyagoubi, L., Belyagoubi-Benhammou, N., Atik-Bekkara, F., Coustard, J.M. (2016). Effects of extraction solvents on phenolic content and antioxidant properties of Pistacia atlantica Desf fruits from Algeria. International Food Research Journal, 23(3): 948-953.

Belyagoubi-Benhammou, N., Belyagoubi, L., Atik-Bekkara, F. (2014). Phenolic contents and activities in vitro of some selected Algerian plants. Journal of Medicinal Plant Research, 8(40): 1198-1207. https://doi.org/10.5897/JMPR2014.5554

Belyagoubi-Benhammou, N., Belyagoubi, L., Benmahieddine, A., El Zerey-Belaskri, A., Di Marco, G., D’Agostino, A., Canini, A., Gismondi, A. (2024). Nutraceutical content and biological properties of lipophilic and hydrophilic fractions of the phytocomplex from Pistacia atlantica Desf. buds, roots, and fruits. Plants, 13(5): 611. https://doi.org/10.3390/plants13050611

Ben Ahmed, Z., Yousfi, M., Viaene, J., Dejaegher, B., Demeyer, K., Mangelings, D., Heyden, Y.V. (2017). Seasonal, gender, and regional variations in total phenolic, flavonoid, and condensed tannin contents and in antioxidant properties from Pistacia atlantica ssp. leaves. Pharmaceutical Biology, 55(1): 1185–1194. https://doi.org/10.1080/13880209.2017.1291690

Ben Ahmed, Z., Yousfi, M., Viaene, J., Dejaegher, B., Demeyer, K., Mangelings, D., Heyden, Y.V. (2018). Potentially antidiabetic and antihypertensive compounds identified from Pistacia atlantica leaf extracts by LC fingerprinting. Journal of Pharmaceutical and Biomedical Analysis, 149: 547-556. https://doi.org/10.1016/j.jpba.2017.11.049

Benamar, H., Marouf, A., Bennaceur, M. (2018). Phytochemical composition, antioxidant, and acetylcholinesterase inhibitory activities of aqueous extract and fractions of Pistacia atlantica subsp. atlantica from Algeria. Journal of Herbs, Spices and Medicinal Plants, 24(3): 229-244. https://doi.org/10.1080/10496475.2018.1446204

Bozorgi, M., Memariani, Z., Mobli, M., Salehi Surmaghi, M.H., Shams-Ardekani, M.R., Rahimi, R. (2013). Five Pistacia species (P. vera, P. atlantica, P. terebinthus, P. khinjuk, and P. lentiscus): a review of their traditional uses, phytochemistry, and pharmacology. The Scientific World Journal, 1-33. https://doi.org/10.1155/2013/219815

Chelghoum, M., Guenane, H., Tahri, D., Laggoun, I., Marfoua, F.Z., Rahmani, F.Z., Khenifer, F., Yousfi, M. (2021). Influence of altitude, precipitation, and temperature factors on the phytoconstituents, antioxidant, and α-amylase inhibitory activities of Pistacia atlantica. Journal of Food Measurement and Characterization, 15(5): 4411-4425. https://doi.org/10.1007/s11694-021-01006-5

Eghbali-Feriz, S., Taleghani, A., Al-Najjar, H., Emami, S.A., Rahimi, H., Asili, J., Tayarani-Najaran, Z. (2018). Anti-melanogenesis and anti-tyrosinase properties of Pistacia atlantica subsp. mutica extracts on B16F10 murine melanoma cells. Research in Pharmaceutical Sciences, 13(6): 533-545. https://doi.org/10.4103/1735-5362.245965

El Haci, I.A., Mazari, W., Atik-Bekkara, F., Mouttas-Bendimerad, F., Hassani, F. (2020). Bioactive compounds from the flower part of Polygonum maritimum L. collected from Algerian coast. Current Bioactive Compounds, 16(04): 543-545. https://doi.org/10.2174/1573407214666181116120901

El Zerey-Belaskri, A., Belyagoubi-Benhammou, N., Benhassaini, H. (2022). From traditional knowledge to modern formulation: potential and prospects of Pistacia atlantica desf. essential and fixed oils uses in cosmetics. Cosmetics, 9(6): 109. https://doi.org/10.3390/cosmetics9060109

Hatamnia, A.A., Abbaspour, N., Darvishzadeh, R. (2014). Antioxidant activity and phenolic profile of different parts of Bene (Pistacia atlantica subsp. kurdica) fruits. Food Chemistry, 145: 306-311. https://doi.org/10.1016/j.foodchem.2013.08.031

Hatamnia, A.A., Rostamzad, A., Hosseini, M., Abbaspour, N., Darvishzadeh, R., Malekzadeh, P., Aminzadeh, B.M. (2015). Antioxidant capacity and phenolic composition of leaves from 10 Bene (Pistacia atlantica subsp. kurdica) genotypes. Natural Product Research, 30(5): 600-604. https://doi.org/10.1080/14786419.2015.1028060

Julkunen-Titto, R. (1985). Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. Journal of Agricultural and Food Chemistry, (33): 213-217. https://doi.org/10.1021/jf00062a013

Kawashty, S.A., Mosharrafa, S.A.M., El-Gibali, M., Saleh, N.A.M. (2000). The flavonoids of four Pistacia species in Egypt. Biochemical Systematics and Ecology, 28(9): 915-917.

Khiya, Z., Oualcadi, Y., Gamar, A., Amalich, S., Fabre, K., Zair, T., Hilali, F.E. (2019). In vitro evaluation of antioxidant activity of the methanol and ethanol extracts of Pistacia atlantica Desf from Morocco. Phytothérapie, 17(6): 321-333. https://doi.org/10.3166/phyto-2018-0100

Labdelli, A., Rebiai, A., Tahirine, M., Adda, A., Merah, O. (2020). Nutritional content and antioxidant capacity of the seed and the epicarp in different ecotypes of Pistacia atlantica Desf. subsp. atlantica. Plants, 9(9): 1065. https://doi.org/10.3390/plants9091065

Malekzadeh, P., Hatamnia, A.A.H., Nourollahi, K. (2015). Total phenolic content and antioxidant activity of fruit and leaf of Bene (Pistacia atlantica subsp. kurdica) in Ilam province. Iranian Journal of Plant Physiology, 6 (1): 1543-1549.

Nachvak, S.M., Hosseini, S., Nili-Ahmadabadi, A., Dastan, D., Rezaei, M. (2018). Chemical composition and antioxidant activity of Pistacia atlantica subsp. Kurdica from Awraman. Journal of Reports in Pharmaceutical Sciences, 7(3): 222-230

Nejabat, M., Negahdarsaber, M., Ghahari, G. (2017). Range of soil and climate characteristics appropriate for Pistacia atlantica forest development and rehabilitation (case study: Fars province, Iran). Journal of Water and Land Development, 32(1): 71-78. https://doi.org/10.1515/jwld-2017-0008

Oyaizu, M. (1986). Studies on products of browning reaction prepared from glucose amine. Japanese Journal of Nutrition, 44: 307–315. https://doi.org/10.5264/eiyogakuzashi.44.307

Peksel, A., Arisan, I., Yanardag, R. (2013). Radical scavenging and anti-acetylcholinesterase activities of aqueous extract of wild pistachio (Pistacia atlantica Desf.) leaves. Food Science and Biotechnology, 22(2): 515–522. https://doi.org/10.1007/s10068-013-0109-6

Peksel, A., Arisan-Atac, I., Yanardag, R. (2010). Evaluation of antioxidant and antiacetylcholinesterase activities of the extracts of Pistacia atlantica Desf. leaves. Journal of Food Biochemistry, 34(3): 451-476. https://doi.org/10.1111/j.1745-4514.2009.00290.x

Pérez, M., Dominguez-López, I., Lamuela-Raventós, R.M. (2023). The chemistry behind the Folin–Ciocalteu method for the estimation of (poly)phenol content in food: Total phenolic intake in a Mediterranean dietary pattern. Journal of Agricultural and Food Chemistry, 71(46): 17543-17553. https://doi.org/10.1021/acs.jafc.3c04022

Prieto, P., Pineda, M., Aguilar, M. (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phospho-molybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry, 269: 337–341. https://doi.org/10.1006/abio.1999.4019

Rezaei, P.F., Fouladdel, S., Hassani, S., Yousefbeyk, F., Ghaffari, S.M., Amin, G., Azizi, E. (2012). Induction of apoptosis and cell cycle arrest by pericarp polyphenol-rich extract of Baneh in human colon carcinoma HT29 cells. Food and Chemical Toxicology, 50: 1054-1059. https://doi.org/10.1016/j.fct.2011.11.012

Rezaie, M., Farhoosh, R., Iranshahi, M., Sharif, A., Golmohamadzadeh, S. (2015). Ultrasonic-assisted extraction of antioxidative compounds from Bene (Pistacia atlantica subsp. mutica) hull using various solvents of different physicochemical properties. Food Chemistry, 173: 577-583. https://doi.org/10.1016/j.foodchem.2014.10.081

Rigane, G., Ghazghazi, H., Aouadhi, C., Ben Salem, R., Nasr, Z. (2017). Phenolic content, antioxidant capacity, and antimicrobial activity of leaf extracts from Pistacia atlantica. Natural Product Research, 31(6): 696-699. https://doi.org/10.1080/14786419.2016.1212035

Samavati, V., Adeli, M. (2014). Isolation and characterization of hydrophobic compounds from carbohydrate matrix of Pistacia atlantica. Carbohydrate polymers, 101: 890-896. https://doi.org/10.1016/j.carbpol.2013.09.069

Sánchez-Moreno, C., Larrauri, J.A. (1998). Principales métodos para la determinación de la oxidación lipídica Main methods used in lipid oxidation determination. Food Science and Technology International, 4(6):391-399. https://doi.org/10.1177/108201329800400603

Singleton, V.L., Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. The American Journal of Enology and Viticulture, 16: 144–158. https://doi.org/10.5344/ajev.1965.16.3.14

Tahir, N.A., Ahmed, J.O., Azeez, H.A., Palani, W.R.M., Omer, D.A. (2019). Phytochemical, antibacterial, antioxidant, and phytotoxicity screening of the extracts collected from the fruit and root of wild mt. Atlas mastic tree (Pistacia atlantica subsp. Kurdica). Applied Ecology and Environmental Research, 17(2): 4417-4429. http://dx.doi.org/10.15666/aeer/1702_44174429

Tahir, N.A., Azeez, H.A., Hama Amin, H.H., Rashid, J.S., Omer, D.A. (2019). Antibacterial activity and allelopathic effects of extracts from leaf, stem, and bark of Mt. Atlas mastic tree (Pistacia atlantica subsp. kurdica) on crops and weeds. International Allelopathy Foundation Journal, 46 (1): 121-132. https://doi.org/10.26651/allelo.j/2019-46-1-1203

Toul, F., Belyagoubi-Benhammou, N., Zitouni, A., Atik-Bekkara, F. (2017). Antioxidant activity and phenolic profile of different organs of Pistacia atlantica Desf. subsp. atlantica from Algeria. Natural Product Research, 31(6): 718–723. https://doi.org/10.1080/14786419.2016.1217205

Toul, F., Belyagoubi-Benhammou, N., Zitouni, A., Ghembaza, N., Atik-Bekkara, F. (2016). In-vitro antioxidant effects of tannin extracts of Pistacia atlantica. International Journal of Pharmaceutical Sciences and Research, 7(1): 1000-1006. https://doi.org/10.13040/IJPSR.0975-8232.7(1).1000-06

Uçak, A.B. (2023). The Effects of Some Climate Parameters on Yield and Quality of Siirt Pistachio Variety (Pistacia vera, L) Grown in Semi-Arid Climate Conditions. In Innovative Research in Agriculture, Forest and Water Issues, Editors, Uçak, A.A., and Gunes sen, S., Ed. Duvar Publishing, Izmir, Turkey, pp 05-24.

Yousfi, M., Djeridane, A., Bombarda, I., Duhem, B., Gaydou, E.M. (2009). Isolation and characterization of a new hispolone derivative from antioxidant extracts of Pistacia atlantica. Phytotherapy Research, 23(9): 1237-1242. https://doi.org/10.1002/ptr.2543

Zarafshar, M., Rousta, M.J., Matinizadeh, M., Talebi, K.S., Bordbar, S.K., Alizadeh, T., Nouri, I., Bader, M.K.F. (2023). Scattered wild pistachio trees profoundly modify soil quality in semi-arid woodlands. Catena, 224: 106983. https://doi.org/10.1016/j.catena.2023.106983

Zhishen, J., Mengcheng, T., Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry, 64(4): 555-559. https://doi.org/10.1016/S0308-8146(98)00102-2

Zitouni, A., Belyagoubi-Benhammou, N., Ghembaza, N., Toul, F., Atik-Bekkara, F. (2016). Assessment of phytochemical composition and antioxidant properties of extracts from the leaf, stem, fruit, and root of Pistacia lentiscus L. International Journal of Pharmacognosy and Phytochemical Research, 8(4): 627-633.

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Published

2025-11-28

How to Cite

Phytochemical and antioxidant activity of male and female buds and pollen grains of Pistacia atlantica. (2025). Journal of Natural Product Research and Applications, 5(01), 1-14. https://doi.org/10.46325/1y2ya545

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