Document Type : Original Article

Authors

1 Department of Animal Health Management, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

2 Department of Food Hygiene and Public Health, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

Abstract

Purpose: Berberis integerrima Bunge and Berberis vulgaris L. are traditional plants known for their many health benefits. The aim of this study was to investigate the antifungal potential of B. vulgaris and B. integerrima fruit extracts against Fusarium spp. pathogens as an environmentally compatible natural antifungal compound. Research methods: The antifungal activity of methanolic fruit extracts of B. vulgaris and B. integerrima against Fusarium solani, and Fusarium graminearum was investigated using the microdilution method, growth area measurement, and morphological Changes were studied using scanning electron microscopy analysis. Findings: The methanolic fruit extracts of B. vulgaris and B. integerrima had significant antifungal activity against the studied plant pathogens, with B. integerrima exhibiting a stronger effect. The MIC values of B. vulgaris fruit extract against F. graminearum and F. solani were 150 and 75 mg mL-1, and B. integerrima fruit extract had 100 and 75mg mL-1, respectively. F. graminearum was the most resistant fungal species. Scanning electron microscopy analysis showed that the extracts of both medicinal plants changed the structure and morphology of mycelia and, dose-dependently, inhibited conidia formation. Research limitations: There were no limitations. Originality/Value: The study showed that fruit extracts of B. vulgaris and B. integerrima have the potential to be used as natural and environmentally friendly agents against Fusarium species.

Graphical Abstract

In vitro antifungal activity of barberry fruit extract (Berberis spp.) against Fusarium spp.

Keywords

Main Subjects

Adeyeye, S. A. (2016). Fungal mycotoxins in foods: A review. Cogent Food & Agriculture 2, 1213127. https://doi.org/10.1080/23311932.2016.1213127
Al-Nazwani, M. S., Aboshosha, S. S., El-Saedy, M. A., Ghareeb, R. Y. & Komeil, D. A. (2021). Antifungal activities of Chlorella vulgaris extract on black scurf disease, growth performance and quality of potato. Archives of Phytopathology and Plant Protection, 54, 2171-2190. https://doi.org/10.1080/03235408.2021.1925434
Al-Wakeel, S., Gabr, M., Abu-El-Soud, W. & Saleh, A. (2013). Coumarin and salicylic acid activate resistance to Macrophomina phaseolina in Helianthus annuus. Acta Agronomica Hungarica, 61, 23-35. https://doi.org/10.1556/AAgr.61.2013.1.3
Aoki, T., O’Donnell, K. & Geiser, D. M. (2014). Systematics of key phytopathogenic Fusarium species: current status and future challenges. Journal of General Plant Pathology, 80, 189-201. https://doi.org/10.1007/s10327-014-0509-3
Ardestani, S. B., Sahari, M. A. & Barzegar, M. (2015). Effect of extraction and processing conditions on organic acids of barberry fruits. Journal of Food Biochemistry, 39, 554-565. https://doi.org/10.1111/jfbc.12158
Bhandari, S., Yadav, P. K. & Sarhan, A. (2021). Botanical fungicides; current status, fungicidal properties and challenges for wide scale adoption: a review. Reviews in Food and Agriculture, 2, 63-68. http://doi.org/10.26480/rfna.02.2021.63.68
Bowman, S. M. & Free, S. J. (2006). The structure and synthesis of the fungal cell wall. Bioessays, 28, 799-808. https://doi.org/10.1002/bies.20441
Dang-Minh-Chanh, N., Seo, D., Lee, H., Kim, I., Kim, K., Park, R. & Jung, W. (2013). Antifungal activity of gallic acid purified from Terminalia nigrovenulosa bark against Fusarium solani. Microbial Pathogenesis, 56, 8-15. https://doi.org/10.1016/j.micpath.2013.01.001
Daradka, H. M., Saleem, A. & Obaid, W. A. (2021). Antifungal effect of different plant extracts against phytopathogenic fungi alternaria alternata and fusarium oxysporum isolated from tomato plant. Journal of Pharmaceutical Research International, 33, 188-197. https://doi.org/10.9734/jpri/2021/v33i31A31681
Ene, I. V., Walker, L. A., Schiavone, M., Lee, K. K., Martin-Yken, H., Dague, E., Gow, N. A., Munro, C. A. & Brown, A. J. (2015). Cell wall remodeling enzymes modulate fungal cell wall elasticity and osmotic stress resistance. MBio 6, e00986-00915. https://doi.org/10.1128/mbio.00986-15
Ghahramanlu, A., Rezaei, M., Heidari, P. & Balandari, A. (2023). Species Survey of Iranian Barberry Genotypes Using ITS2 Sequences and Basic Local Alignment Search Tools. Erwerbs-Obstbau, 1-9. https://doi.org/10.1007/s10341-023-00933-5
Goodarzi, S., Khadivi, A., Abbasifar, A. & Akramian, M. (2018). Phenotypic, pomological and chemical variations of the seedless barberry (Berberis vulgaris L. var. asperma). Scientia Horticulturae, 238, 38-50. https://doi.org/10.1016/j.scienta.2018.04.040
Gow, N. A. & Lenardon, M. D. (2023). Architecture of the dynamic fungal cell wall. Nature Reviews Microbiology, 21, 248-259. https://doi.org/10.1038/s41579-022-00796-9
Hasim, S. & Coleman, J. J. (2019). Targeting the fungal cell wall: current therapies and implications for development of alternative antifungal agents. Future Medicinal Chemistry, 11, 869-883. https://doi.org/10.4155%2Ffmc-2018-0465
Kang, Z., Huang, L., Krieg, U., Mauler‐Machnik, A. & Buchenauer, H. (2001). Effects of tebuconazole on morphology, structure, cell wall components and trichothecene production of Fusarium culmorum in vitro. Pest Management Science: formerly Pesticide Science, 57, 491-500. https://doi.org/10.1002/ps.310
Khan, R. U., Naz, S., Raziq, F., Qudratullah, Q., Khan, N. A., Laudadio, V., Tufarelli, V. & Ragni, M. (2022). Prospects of organic acids as safe alternative to antibiotics in broiler chickens diet. Environmental Science and Pollution Research, 29, 32594-32604. https://doi.org/10.1007/s11356-022-19241-8
Korukluoglu, M., Sahan, Y. & Yigit, A. (2008). Antifungal properties of olive leaf extracts and their phenolic compounds. Journal of Food Safety 28, 76-87.     https://doi.org/10.1111/j.1745-4565.2007.00096.x
Kumar, K. N., Venkataramana, M., Allen, J. A., Chandranayaka, S., Murali, H. S. & Batra, H. V. (2016). Role of Curcuma longa L. essential oil in controlling the growth and zearalenone production of Fusarium graminearum. LWT-Food Science and Technology, 69, 522-528. https://doi.org/10.1016/j.lwt.2016.02.005
Lengai, G. M., Muthomi, J. W. & Mbega, E. R. (2020). Phytochemical activity and role of botanical pesticides in pest management for sustainable agricultural crop production. Scientific African, 7, e00239. https://doi.org/10.1016/j.sciaf.2019.e00239
Moein, M., Sabahi, Z. & Salim, H. (2020). A glance at Berberis integerimma pharmacological effects and its active constituents. Trends in Pharmaceutical Sciences 6, 1-10. https://doi.org/10.30476/tips.2020.83414.1024
Munkvold, G. P. (2017). Fusarium species and their associated mycotoxins. In A. Moretti (Ed.), Mycotoxigenic fungi: methods and protocols (Vol. 1542, pp. 51-106): Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6707-0_4
Nazarov, P. A., Baleev, D. N., Ivanova, M. I., Sokolova, L. M. & Karakozova, M. V. (2020). Infectious plant diseases: Etiology, current status, problems and prospects in plant protection. Acta Naturae, 12, 46. https://doi.org/10.32607%2Factanaturae.11026
Nehra, S., Gothwal, R. K., Varshney, A. K., Solanki, P. S., Chandra, S., Meena, P., Trivedi, P. & Ghosh, P. (2021). Biomanagement of Fusarium spp. associated with oil crops. In Microbiome Stimulants for Crops (pp. 453-474): Elsevier. https://doi.org/10.1016/B978-0-12-822122-8.00026-1
Nisar, M., Khan, I., Ahmad, B., Ali, I., Ahmad, W. & Choudhary, M. I. (2008). Antifungal and antibacterial activities of Taxus wallichiana Zucc. Journal of Enzyme Inhibition and Medicinal Chemistry, 23, 256-260. https://doi.org/10.1080/14756360701505336
Nosratabadi, M., Akhtari, J., Faeli, L., Haghani, I., Aghili, S. R., Shokohi, T., Hedayati, M. T., Zarrinfar, H., Mohammadi, R. & Najafzadeh, M. J. (2022). In vitro antifungal susceptibility profile of Miltefosine against a collection of azole and echinocandins resistant Fusarium strains. Journal of Fungi, 8, 709. https://doi.org/10.3390/jof8070709
Pârvu, M. & Pârvu, A. E. (2011). Antifungal plant extracts. Science against microbial pathogens: communicating current research and technological advances. Formatex Research Center, Badajoz, Spain, 2, 1055-1062.
Perveen, K., Bukhari, N. A., Al Masoudi, L. M., Alqahtani, A. N., Alruways, M. W. & Alkhattaf, F. S. (2022). Antifungal potential, chemical composition of Chlorella vulgaris and SEM analysis of morphological changes in Fusarium oxysporum. Saudi Journal of Biological Sciences, 29, 2501-2505. https://doi.org/10.1016/j.sjbs.2021.12.033
Rahimi-Madiseh, M., Lorigoini, Z., Zamani-Gharaghoshi, H. & Rafieian-Kopaei, M. (2017). Berberis vulgaris: specifications and traditional uses. Iranian Journal of Basic Medical Sciences, 20, 569. https://doi.org/10.22038%2FIJBMS.2017.8690
Rezaei, M., Ebadi, A., Reim, S., Fatahi, R., Balandary, A., Farrokhi, N. & Hanke, M.-V. (2011). Molecular analysis of Iranian seedless barberries via SSR. Scientia Horticulturae, 129, 702-709. https://doi.org/10.1016/j.scienta.2011.05.021
Rongai, D., Milano, F. & Sciò, E. (2012). Inhibitory effect of plant extracts on conidial germination of the phytopathogenic fungus Fusarium oxysporum. American Journal of Plant Sciences 3, 1693-1698.  http://doi.org/10.4236/ajps.2012.312207
Salehi, B., Selamoglu, Z., Sener, B., Kilic, M., Kumar Jugran, A., de Tommasi, N., Sinisgalli, C., Milella, L., Rajkovic, J. & Flaviana B. Morais-Braga, M. (2019). Berberis plants—drifting from farm to food applications, phytotherapy, and phytopharmacology. Foods, 8, 522. https://doi.org/10.3390/foods8100522
Salem, M. Z., Mohamed, A. A., Ali, H. M. & Al Farraj, D. A. (2021). Characterization of phytoconstituents from alcoholic extracts of four woody species and their potential uses for management of six Fusarium oxysporum isolates identified from some plant hosts. Plants, 10, 1325. https://doi.org/10.3390/plants10071325
Samie, A. & Mashau, F. (2013). Antifungal activities of fifteen Southern African medicinal plants against five Fusarium species. Journal of Medicinal Plants Studies, 7, 1839-1848. http://dx.doi.org/10.5897/JMPR11.1212
Sellamani, M., Kalagatur, N. K., Siddaiah, C., Mudili, V., Krishna, K., Natarajan, G. & Rao Putcha, V. L. (2016). Antifungal and zearalenone inhibitory activity of Pediococcus pentosaceus isolated from dairy products on Fusarium graminearum. Frontiers in Microbiology, 7, 890. https://doi.org/10.3389/fmicb.2016.00890
Seo, D.-J., Lee, H.-B., Kim, I.-S., Kim, K.-Y., Park, R.-D. & Jung, W.-J. (2013). Antifungal activity of gallic acid purified from Terminalia nigrovenulosa bark against Fusarium solani. Microbial Pathogenesis, 56, 8-15. https://doi.org/10.1016/j.micpath.2013.01.001
Tavakoli, A., Sahari, M. A. & Barzegar, M. (2017). Antioxidant activity of Berberis integerrima seed oil as a natural antioxidant on the oxidative stability of soybean oil. International Journal of Food Properties, 20, S2914-S2925. http://dx.doi.org/10.1080/10942912.2017.1382509
Xie, Y., Liu, X. & Zhou, P. (2020). In vitro antifungal effects of berberine against Candida spp. in planktonic and biofilm conditions. Drug Design, Development and Therapy, 87-101. https://doi.org/10.2147/DDDT.S230857
Yazgi, M., Awad, D. & Jreikous, B. (2015). Screening of the antifungal activity of plant Mentha longifolia crude extracts against two fungi Alternaria citri and Fusarium moniliforme. Journal of Entomology and Zoology Studies, 3, 359-364. Retrieved from https://www.entomoljournal.com/archives/2015/vol3issue2/PartG/3-3-86-898.pdf
Zhou, L., Zhou, H., Hou, G., Ji, F. & Wang, D. (2023). Antifungal activity and metabolomics analysis of Piper sarmentosum extracts against Fusarium graminearum. Journal of Applied Microbiology, 134, 3, lxad019. https://doi.org/10.1093/jambio/lxad019