Antifungal Effects of Funneliformis mosseae and Plant Essential Oils in the Biological Management of Fusarium Wilt in Pepper (Capsicum annuum L.)

Hasret Güneş

doi:10.18016/ksutarimdoga.vi.1779458

TR EN

Biberde (Capsicum annuum L.) Fusarium Solgunluğunun Biyolojik Mücadelesinde Funneliformis mosseae ve Bitki Uçucu Yağların Antifungal Etkinlikleri

Öz

Bu çalışma, biberde Fusarium oxysporum’un biyolojik kontrolünde Funneliformis mosseae ile bitki uçucu yağları arasındaki sinerjistik ve antogonistik etkileşimleri bütüncül bir şekilde değerlendiren ilk araştırmadır. Bu araştırma, patojen Fusarium oxysporum (Fo) karşı uygulanabilir bir biyolojik mücadele yaklaşımı oluşturmak amacıyla iki ayrı aşamada gerçekleştirilmiştir. İlk olarak, in vivo koşullar altında, argan yağı (Ao), çörek otu yağı (Bo) ve ardıç yağı (Jo) 'nun hastalık azaltma potansiyeli %1 ve %3 konsantrasyonlarda değerlendirilmiş ve sonraki aşama için en etkili konsantrasyon belirlenmiştir. Kontrollü iklimlendirme kabininde (23 ± 2 °C sıcaklık, %60–70 bağıl nem ve 14/10 saatlik aydınlık-karanlık döngü koşullarında) yürütülen çalışmada, Arbusküler Mikorizal Fungi Funneliformis mosseae (Fm)’nin, tek başına ve seçilen uçucu yağlarla kombinasyon halinde, biber (Capsicum annuum L.) bitkilerinin büyüme performansı ve hastalık şiddeti üzerindeki etkileri incelenmiştir. Ayrıca, uygulamalar sonucunda toprakta mikorizal kolonizasyon oranı ve spor yoğunluğunda belirgin artışlar kaydedilmiştir. Elde edilen veriler, F. mosseae inokülasyonu ve %3 çörek otu, ardıç ve argan yağı uygulamaları, Fusarium oxysporum stresi altındaki biber bitkilerinin büyümesini ve biyokütlesini önemli ölçüde artırdı. Fo+Fm uygulaması hastalık şiddetini %77 oranında azaltmış ve kök kolonizasyonu, klorofil içeriği ile besin alımını artırmıştır. Buna karşılık Fo+Bo+Fm kombinasyonu yalnızca %54 oranında baskılama sağlamış, bu durum, uçucu yağın (Bo) AMF’nin performansını artırmak yerine antagonize ettiğini, dolayısıyla kök kolonizasyonu, klorofil içeriği ve besin alımını Fo+Fm uygulamasına kıyasla daha düşük seviyelere indirdiğini göstermektedir. Mevcut bulgular, F. mosseae ile bitkisel uçucu yağlar arasındaki etkileşimin çoğu zaman sinerjik olmadığını ortaya koymaktadır. Bu etkileşim spesifik bileşiğe bağlıdır ve kimi durumlarda antagonistik dahi olabilmektedir. Fo+Bo+Fm kombinasyonu, Fo+Fm uygulamasına kıyasla daha düşük hastalık baskılama ve daha zayıf fizyolojik kazanımlar sağlamıştır. Bu durum, çörek otu yağının etkileşim dinamiğini tamamlayıcıdan rekabetçiye dönüştürebildiğini göstermektedir. Bu değişken yanıtlar, AMF–uçucu yağ kombinasyonlarının ekolojik performansının önceden genellenemeyeceğini vurgulamaktadır. Dolayısıyla, her bir uçucu yağ türü ve konsantrasyonu, ilgili bitki–patojen etkileşim koşullarında ayrı ayrı doğrulanmalı ve değerlendirilmelidir. Bu bulgular, sürdürülebilir tarım uygulamalarının ve biyolojik mücadele stratejilerinin optimize edilmesi için rehberlik sağlar ve moleküler ve ekolojik düzeylerde gelecekteki çalışmaların temelini oluşturur.

Anahtar Kelimeler

Antifungal Effects of Funneliformis mosseae and Plant Essential Oils in the Biological Management of Fusarium Wilt in Pepper (Capsicum annuum L.)

Abstract

This study presents the first comprehensive evaluation of the synergistic and antagonistic interactions between Funneliformis mosseae and plant essential oils in the biological control of Fusarium oxysporum in pepper. This research was conducted in two distinct stages, aiming to establish a viable biocontrol approach against the pathogen Fusarium oxysporum (Fo). Initially, under in vivo conditions, the disease mitigation potential of argan oil (Ao), black seed oil (Bo), and juniper oil (Jo) was assessed at concentrations of 1% and 3%, identifying the most potent concentration for subsequent experimentation. This study was conducted in a controlled climate chamber (temperature: 23 ± 2 °C, relative humidity: 60–70%, light-dark cycle: 14/10 h). Researchers investigated the effects of Funneliformis mosseae (Fm), alone and combined with selected essential oils, on the growth and disease severity of pepper (Capsicum annuum L.) plants. The treatments also resulted in significant increases in mycorrhizal colonization rates and spore densities in the soil. The data obtained showed that F. mosseae inoculation and the application of 3% black seed, juniper, and argan oil significantly increased the growth and biomass of pepper plants under Fusarium oxysporum stress. The Fo+Fm application reduced disease severity by 77% and increased root colonization, chlorophyll content, and nutrient uptake. However, the Fo+Bo+Fm combination only provided 54% suppression, demonstrating that the essential oil (Bo) antagonized AMF performance rather than enhancing it, resulting in lower root colonization, reduced chlorophyll content, and diminished nutrient uptake compared to Fo+Fm. Current findings show that the interaction between F. mosseae and plant essential oils is usually not synergistic. It depends on the specific compound and can even be antagonistic. The Fo+Bo+Fm combination resulted in less disease suppression and fewer physiological gains than Fo+Fm. This suggests that black cumin oil can change the interaction from complementary to competitive. These variable responses emphasize that the ecological performance of AMF-essential oil combinations cannot be predicted in advance. Therefore, each essential oil type and concentration should be individually validated and evaluated under the specific plant–pathogen interaction conditions. These findings inform the optimization of sustainable agricultural practices and biological control strategies, laying the foundation for future studies at both the molecular and ecological levels.

Keywords

References

Abbas, M., Gururani, M. A., Ali, A., Bajwa, S., Hassan, R., Batool, S. W., ... & Wei, D. (2024). Antimicrobial properties and therapeutic potential of bioactive compounds in Nigella sativa: A review. Molecules, 29(20), 4914. https://doi.org/10.3390/molecules29204914
Abdel Latef, A.A.H., & Miransari, M. (2014). The role of arbuscular mycorrhizal fungi in alleviation of salt stress. In: Use of Microbes for the Alleviation of Soil Stresses: Volume 2: Alleviation of Soil Stress by PGPR and Mycorrhizal Fungi, Springer, New York, NY, pp. 23–38. https://doi.org/10.1007/978-1-4939-0721-2_2
Abkenar, M.B., Mozafari, H., Karimzadeh, K., Rajabzadeh, F., & Azimi, R. (2024). Arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria (PGPR) as an alternative to mineral fertilizers to improve the growth, essential oil profile, and phenolic content of Satureja macrantha L. Journal of Crop Health, 76, 347–356. https://doi.org/10.1007/s10343-023-00934-0
Ahmad, A., Sripong, K., Uthairatanakij, A., Photchanachai, S., Pankasemsuk, T., & Jitareerat, P. (2022). Decontamination of seed-borne disease in pepper (Capsicum annuum L.) seed and the enhancement of seed quality by the emulated plasma technology. Scientia Horticulturae, 291, 110568. https://doi.org/10.1016/j.scienta.2021.110568
Ahmad, N., Abbas, A., Shamsullah, S., Jabran, M., & Ali, M.A. (2023). Fusarium wilt disease of chili: pathogen, its mechanism of infection, eradication, and impacts. Phytopathogenom. Dis. Control, 2, 95–110. https://doi.org/10.22194/Pdc/2.1024
Ahmed, A.F. & Shehata, A.M. (2023). Improving growth, yield, and oil productivity of rosemary plants grown in sandy calcareous soil by using some manures organic tea and salicylic acid. International Journal of Plant Production, 14, 479–487. 10.21608/jpp.2023.234844.1269
Alaoui, M.M. (2020). Antifungal effect of natural extracts on fungal contamination in the vitro culture of Calodendrum capense (Lf.) Thunberg. Journal of Materials and Environmental Science,11, 647–657.
Al Raish, S.M., Sourani, O.M., & Abu-Elsaoud, A.M. (2025). Plant growth-promoting microorganisms as biocontrol agents: Mechanisms, challenges, and future prospects. Applied Microbiology, 5(2), 44.. https://doi.org/10.3390/applmicrobiol5020044

Amani Machiani, M., Javanmard, A., Ostadi, A., & Alizadeh, K. (2023). Improvement in essential oil quantity and quality of thyme (Thymus vulgaris L.) by integrative application of chitosan nanoparticles and arbuscular mycorrhizal fungi under water stress conditions. Plants, 12(7), 1422... https://doi.org/10.3390/plants12071422
Andrino, A., Guggenberger, G., Kernchen, S., Mikutta, R., Sauheitl, L., & Boy, J. (2021). Production of organic acids by arbuscular mycorrhizal fungi and their contribution in the mobilization of phosphorus bound to iron oxides. Frontiers in Plant Science, 12, 661842. https://doi.org/10.3389/fpls.2021.661842
Atay, M., & Soylu, S. (2023). Kurutmalık Biber meyvelerinde iç çürüklüğüne neden olan fungal etmenlere karşı bitki uçucu yağlarının in vitro antifungal etkileri. KSU Tarım ve Doğa Dergisi, 26(1), 76-89. https://doi.org/10.18016/ksutarimdoga.vi.1085859
Basaid, K., & Furze, J.N. (2024). Botanical-microbial synergy—fundamentals of untapped potential of sustainable agriculture. Journal of Crop Health,76, 1263–1280. https://doi.org/10.1007/s10343-024-01008-5
Begum, N., Qin, C., Ahanger, M.A., Raza, S., Khan, M.I., Ashraf, M., & Zhang, L. (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science,10, 1068. https://doi.org/10.3389/fpls.2019.01068
Bona, E., Lingua, G., & Todeschini, V. (2016). Effect of bioinoculants on the quality of crops. In: Bioformulations: for Sustainable Agriculture, Springer, New Delhi, pp. 93–124. https://doi.org/10.1007/978-81-322-2779-3_5
Cerkauskas, R.F. (2017). Etiology and management of Fusarium crown and root rot (Fusarium oxysporum) on greenhouse pepper in Ontario, Canada. Can. J. Plant Pathol. 39(2), 121–132. https://doi.org/10.1080/07060661.2017.1321044
Da Silva, J.K.R., Silva, J.R.A., Nascimento, S.B., Da Luz, S.F., Meireles, E.N., Alves, C.N., & Maia, J.G.S. (2014). Antifungal activity and computational study of constituents from Piper divaricatum essential oil against Fusarium infection in black pepper. Molecules, 19(11), 17926–17942. https://doi.org/10.3390/molecules191117926
Declerck, S., Plenchette, C., & Strullu, D.G. (1995). Mycorrhizal dependency of banana (Musa acuminate, AAA group) cultivar. Plant Soil, 176, 183–187. https://doi.org/10.1007/BF00017688
De Lamo, F.J., & Takken, F.L. (2020). Biocontrol by Fusarium oxysporum using endophyte-mediated resistance. Front. Plant Science, 11, 37. https://doi.org/10.3389/fpls.2020.00037
Frans, M., Aerts, R., Van Laethem, S., & Ceusters, J. (2017). Environmental effects on growth and sporulation of Fusarium spp. Causing internal fruit rot in bell pepper. European Journal of Plant Pathology, 149, 875–883. https://doi.org/10.1007/s10658-017-1235-4
Gerdemann, L.W., & Nicholson, T.H. (1963). Spores of mycorrhizal endogene extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society,46, 235–244.
Giovanetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist,84, 489–500. https://www.jstor.org/stable/2432123
Güneş, H., Demir, S., Durak, E.D., & Boyno, G. (2024). The effect of arbuscular mycorrhizal fungal species Funneliformis mosseae and biochar against Verticillium dahliae in pepper plants under salt stress. European Journal of Plant Pathology, 170, 669–686. https://doi.org/10.1007/s10658-024-02926-w
Greff, B., Sáhó, A., Lakatos, E., & Varga, L. (2023). Biocontrol activity of aromatic and medicinal plants and their bioactive components against soil-borne pathogens. Plants 12(4), 706. https://doi.org/10.3390/plants12040706
Gruľová, D., Baranová, B., Sedlák, V., De Martino, L., Zheljazkov, V. D., Konečná, M., ... & De Feo, V. (2022). Juniperus horizontalis Moench: Chemical composition, herbicidal and insecticidal activities of its essential oil and of its main component, sabinene. Molecules, 27(23), 8408.
Hashem, A., Almutairi, K.F., Alshaikh, N.A., Kumar, A., Wu, Q.S., Ibramimova, U., & Abd-Allah, E.F. (2025). Role of arbuscular mycorrhizal fungi in plant growth promotion and biotic stress management. In: Management of Mycorrhizal Symbiosis for Mycoremediation and Phytostabilization. Elsevier, pp. 145–155. https://doi.org/10.1016/B978-0-443-24863-4.00008-X
Hegazy, M.M., Mekky, R.H., Ibrahim, A.E., Abouelela, M.E., Kedra, T.A., & Al-Harrasi, A. (2025). Essential Oils: The Science of Extraction and Its Implications for Composition and Biological Activity—A Review. Food Analytical Methods 18, 1483-1513. https://doi.org/10.1007/s12161-025-02808-9
Jojić, A. A., Liga, S., Uţu, D., Ruse, G., Suciu, L., Motoc, A., ... & Tchiakpe-Antal, D. S. (2024). Beyond Essential Oils: Diterpenes, Lignans, and Biflavonoids from Juniperus communis L. as a Source of Multi-Target Lead Compounds. Plants, 13(22), 3233.
Kamal, R., Gusain, Y.S., Kumar, V., & Sharma, A.K. (2015). Disease management through biological control agents: An eco-friendly and cost-effective approach for sustainable agriculture—A Review. Agricultural Reviews 36(1), 37–45. 10.5958/0976-0741.2015.00004.5
Khaitov, B., Umurzokov, M., Cho, K.M., Lee, Y.J., Park, K.W., & Sung, J. (2019). Importance and production of chilli pepper; heat tolerance and efficient nutrient use under climate change conditions. Korean Journal of Agricultural Science 46(4), 769–779. https://doi.org/10.7744/kjoas.20190059
Kim, B.S., & Hwang, B.K. (2007). Microbial fungicides in the control of plant diseases. Journal of Phytopathology 155(11–12), 641–653. https://doi.org/10.1111/j.1439-0434.2007.01314.x
Li, N., Wang, C., Li, X., & Liu, M. (2019). Effects of earthworms and arbuscular mycorrhizal fungi on preventing Fusarium oxysporum infection in the strawberry plant. Plant and Soil, 443(1), 139-153.
Lorito, M., Peterbauer, C., Hayes, C.K., & Harman, G.E. (1994). Synergistic interaction between fungal cell wall-degrading enzymes and different antifungal compounds enhances inhibition of spore germination. Microbiology 140(3), 623–629. https://doi.org/10.1099/00221287-140-3-623
Mai, W., Xue, X., Feng, G., & Tian, C. (2018). Simultaneously maximizing root/mycorrhizal growth and phosphorus uptake by cotton plants by optimizing water and phosphorus management. BMC Plant Biology, 18(1), 334. https://doi.org/10.1186/s12870-018-1550-8
Manjunath, M.S., Koshariya, A.K., Sharma, N., Rajput, A., Pandey, S.K., Singh, S., & Singh, B.V. (2023). Exploring the use of aromatic compounds in crop growth and protection. International Journal of Plant & Soil Science,35(21), 78–89. 10.9734/IJPSS/2023/v35i213948
McGuire, R.G. (1992). Reporting of objective color measurements. HortScience 27, 1254–1255.
Mohammed, S. J., Amin, H. H., Aziz, S. B., Sha, A. M., Hassan, S., Abdul Aziz, J. M., & Rahman, H. S. (2019). Structural characterization, antimicrobial activity, and in vitro cytotoxicity effect of black seed oil. Evidence‐Based Complementary and Alternative Medicine, 2019(1), 6515671. https://doi.org/10.1155/2019/6515671
Moumou, M., Mokhtari, I., Tayebi, A., Milenkovic, D., Amrani, S., & Harnafi, H. (2024). Juniperus oxycedrus L. fruit, leaves, and essential oil: a systematic literature review on bioactive compounds, pharmacological properties, and toxicology. Phytochemistry Reviews, 1–31. https://doi.org/10.1007/s11101-024-10054-w
Moutassem, D., Belabid, L., Bellik, Y., Ziouche, S., & Baali, F. (2019). Efficacy of essential oils of various aromatic plants in the biocontrol of Fusarium wilt and inducing systemic resistance in chickpea seedlings. Plant Protection Science 55(3). 10.17221/134/2018-PPS
Ninkuu, V., Zhang, L., Yan, J., Fu, Z., Yang, T., Zeng, H. (2021). Biochemistry of terpenes and recent advances in plant protection. International Journal of Molecular Sciences 22(11), 5710. https://doi.org/10.3390/ijms22115710
Qian, L., Yu, W.J., Cui, J.Q., Jie, W.G., & Cai, B.Y. (2015). Funneliformis mosseae affects the root rot pathogen Fusarium oxysporum in soybeans. Acta Agriculturae Scandinavica, Section B—Soil & Plant Science 65(4), 321–328. https://doi.org/10.1080/09064710.2015.1009938
Rasouli, F., Nasiri, Y., Hassanpouraghdam, M.B., Asadi, M., Qaderi, T., Trifa, A., & Szczepanek, M. (2023). Seaweed extract and arbuscular mycorrhiza co-application affect the growth responses and essential oil composition of Foeniculum vulgare L. Scientific Reports 13(1), 11902. https://doi.org/10.1038/s41598-023-39194-3
Rasul, S.Z.R. (2019). Biocontrol of Trichoderma spp. and Saccharomyces cerevisiae against Fusarium oxysporum f.sp. Lycopersici in tomato. Master's Thesis. Van Yuzuncu Yil University, Institute of Science, Van.
Raveau, R., Fontaine, J., & Lounès-Hadj Sahraoui, A. (2020). Essential oils as potential alternative biocontrol products against plant pathogens and weeds: A review. Foods 9(3), 365. https://doi.org/10.3390/foods9030365
Rydlová, J., Jelínková, M., Dušek, K., Dušková, E., Vosátka, M., & Püschel, D. (2016). Arbuscular mycorrhiza differentially affects the synthesis of essential oils in coriander and dill. Mycorrhiza, 26(2), 123-131.
Schüßler, A., & Walker, C. (2010). The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University.
Shoresh, M., Harman, G.E., & Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology 48(1), 21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
Singh, V., Naveenkumar, R., & Muthukumar, A. (2019). Arbuscular mycorrhizal fungi and their effectiveness against soil borne diseases. Management 183, 199.
Soussani, F.E., Nilahyane, A., Ikan, C., Ouhaddou, R., Ben-Laouane, R., Salah-Eddine, H., & Meddich, A. (2025). Enhancing sweet pepper tolerance to combined drought and salinity stresses: synergistic role of biochar and arbuscular mycorrhizal fungi. Journal of Crop Health 77(2), 1–17. https://doi.org/10.1007/s10343-025-01145-5
Soylu, E. M., Kurt, Ş., & Soylu, S. (2010). In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. International Journal of Food Microbiology, 143(3), 183-189. https://doi.org/10.1016/j.ijfoodmicro.2010.08.015
Soylu, S., Atay, M., Kara, M., Uysal, A., Soylu, E. M., & Kurt, Ş. (2023). Morphological and molecular characterization of Fusarium incarnatum as a causal disease agent of pepper (Capsicum annuum) fruit rot. Journal of Phytopathology, 171(11-12), 688-699. https://doi.org/10.1111/jph.13228
Tabassum, N., & Vidyasagar, G.M. (2013). Antifungal investigations on plant essential oils. A review. International Journal of Pharmacy and Pharmaceutical Sciences 5(2), 19–28.
Tarraf, W., Ruta, C., De Cillis, F., Tagarelli, A., Tedone, L., & De Mastro, G. (2015). Effects of mycorrhiza on growth and essential oil production in selected aromatic plants. Italian Journal of Agronomy 10(3), 633. https://doi.org/10.4081/ija.2015.633
Umer, M., Anwar, N., Mubeen, M., Li, Y., Ali, A., Alshaharni, M.O., & Liu, P. (2025). Roles of arbuscular mycorrhizal fungi in plant growth and disease management for sustainable agriculture. Frontiers in Microbiology 16, 1616273. https://doi.org/10.3389/fmicb.2025.1616273
Wahab, A., Muhammad, M., Munir, A., Abdi, G., Zaman, W., Ayaz, A., & Reddy, S.P.P. (2023). Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants 12(17), 3102. https://doi.org/10.3390/plants12173102
Wang, H., Hao, Z., Zhang, X., Xie, W., & Chen, B. (2022). Arbuscular mycorrhizal fungi induced plant resistance against Fusarium wilt in jasmonate biosynthesis defective mutant and wild type of tomato. Journal of Fungi 8(5), 422. https://doi.org/10.3390/jof8050422

Details

Primary Language

English

Subjects

Phytopathology

Journal Section

Research Article

Authors

Hasret Güneş ^*
0000-0003-3155-2695
Türkiye

Early Pub Date

January 21, 2026

Publication Date

January 21, 2026

Submission Date

September 7, 2025

Acceptance Date

November 12, 2025

Published in Issue

Year 2026 Volume: 29 Number: 2

DOI

https://doi.org/10.18016/ksutarimdoga.vi.1779458

IZ

https://izlik.org/JA26DA39YC

Cite

RIS / Bibtex

APA

Güneş, H. (2026). Antifungal Effects of Funneliformis mosseae and Plant Essential Oils in the Biological Management of Fusarium Wilt in Pepper (Capsicum annuum L.). Kahramanmaraş Sütçü İmam Üniversitesi Tarım Ve Doğa Dergisi, 29(2), 335-352. https://doi.org/10.18016/ksutarimdoga.vi.1779458