Abstract
Fusarium spp. are considered as one of the most devastating plant pathogenic fungi worldwide. In this study, the effect of essential oil (EO) of Mentha longifolia, M. spicata, Achillea sp. and Foeniculum vulgare, ethanolic extract of Propolis (EEP), and Trichoderma harzianum T447 and T. hamatum T622 was investigated against five phytopathogenic Fusarium species. The results showed that the fungal species, the type of EO, and concentrations play a substantial role in inhibiting the mycelial growth of Fusarium spp. GC–MS analysis of the EOs showed that the piperitone oxide and cis-piperitone oxide were found as the main components of M. longifolia. Our results also revealed that EEP possessed the growth inhibitory effect against Fusarium spp. It was observed that the extracellular secretions of T. harzianum T447 showed very high inhibition against the fungi. Our results highlighted the need for further research to apply them as a safe alternative to the chemical pesticides.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbaszadeh S, Sharifzadeh A, Shokri H, Khosravi A, Abbaszadeh A (2014) Antifungal efficacy of thymol, carvacrol, eugenol and menthol as alternative agents to control the growth of food-relevant fungi. J Mycol Med 24:e51–e56. https://doi.org/10.1016/j.mycmed.2014.01.063
Adams R (2007) identification of essential oils components by gas chromatography/quadrupole mass spectroscopy., Carol Stream. In. USA
Alizadeh M, Vasebi Y, Safaie N (2020) Microbial antagonists against plant pathogens in Iran: a review. Open Agric 5:404–440. https://doi.org/10.1515/opag-2020-0031
Bariş Ö et al (2006) Biological activities of the essential oil and methanol extract of Achillea biebersteinii Afan. (Asteraceae). Turk J Biol 30:65–73. https://doi.org/10.3906/biy-0603-1
Chang Y, Harmon PF, Treadwell DD, Carrillo D, Sarkhosh A, Brecht JK (2021) Biocontrol potential of essential oils in organic horticulture systems: From farm to fork. Front Nutr. https://doi.org/10.3389/fnut.2021.805138
Curifuta M, Vidal J, Sánchez-Venegas J, Contreras A, Salazar LA, Alvear M (2012) The in vitro antifungal evaluation of a commercial extract of Chilean propolis against six fungi of agricultural importance. Int j Agric Nat Resour 39:347–359. https://doi.org/10.4067/S0718-16202012000200011
Davari M, Ezazi R (2017) Chemical composition and antifungal activity of the essential oil of Zhumeria majdae, Heracleum persicum and Eucalyptus sp. against some important phytopathogenic fungi. J Mycol Med 27:463–468. https://doi.org/10.1016/j.mycmed.2017.06.001
Davari M et al (2013) Geographic differences in trichothecene chemotypes of Fusarium graminearum in the Northwest and North of Iran. World Mycotoxin J 6:137–150. https://doi.org/10.3920/WMJ2012.1493
Dennis C, Webster J (1971a) Antagonistic properties of species-groups of Trichoderma: I. production of non-volatile antibiotics. Trans Br Mycol Soc. https://doi.org/10.1016/S0007-1536(71)80077-3
Dennis C, Webster J (1971b) Antagonistic properties of species-groups of Trichoderma: II. production of volatile antibiotics. Trans Br Mycol Soc. https://doi.org/10.1016/S0007-1536(71)80078-5
Dennis C, Webster J (1971c) Antagonistic properties of species-groups of Trichoderma: III. Hyphal interaction. T Trans Br Mycol Soc. https://doi.org/10.1016/S0007-1536(71)80050-5
Desam NR, Al-Rajab AJ, Sharma M, Mylabathula MM, Gowkanapalli RR, Mohammed A (2017) Chemical composition, antibacterial and antifungal activities of Saudi Arabian Mentha longifolia L. essential oil. J Coast Life Med 5:441–446. https://doi.org/10.5530/ajbls.2019.8.9
Desjardins AE, Hohn TM, McCORMICK SP (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Mol Biol Rev 57:595–604. https://doi.org/10.1128/mr.57.3.595-604.1993
Enayati S, Davari M, Habibi-Yangjeh A, Ebadollahi A, Feizpoor S (2021) Enhancement of the antifungal properties of Zataria multiflora essential oil through nanoencapsulation with ZnO nanomaterial. Toxin Rev. https://doi.org/10.1080/15569543.2021.2007405
Esmaeili Taheri A, Hamel C, Gan Y, Vujanovic V (2011) First report of Fusarium redolens from saskatchewan and its comparative pathogenicity. Can J Plant Pathol 33:559–564. https://doi.org/10.1080/07060661.2011.620631
Falcão SI, Vilas-Boas M, Estevinho LM, Barros C, Domingues MR, Cardoso SM (2010) Phenolic characterization of Northeast Portuguese propolis: usual and unusual compounds. Anal Bioanal Chem 396:887–897. https://doi.org/10.1007/s00216-009-3232-8
Fallahi M et al (2019) Isolation, molecular identification and mycotoxin profile of Fusarium species isolated from maize kernels in Iran. Toxins 11:297. https://doi.org/10.3390/toxins11050297
Ghiasian SA et al (2005) Fumonisin production by Fusarium species isolated from freshly harvested corn in Iran. Mycopathologia 159:31–40. https://doi.org/10.1007/s11046-004-3899-5
Ghisalberti EL, Rowland CY (1993) Antifungal metabolites from Trichoderma harzianum. J Nat Prod 56:1799–1804. https://doi.org/10.1021/np50100a020
Ghoulami Sd, Idrissi AI, Fkih-Tetouani S (2001) Phytochemical study of Mentha longifolia of Morocco. Fitoterapia 72:596–598. https://doi.org/10.1016/S0367-326X(01)00279-9
Gulluce M et al (2007) Antimicrobial and antioxidant properties of the essential oils and methanol extract from Mentha longifolia L. ssp. longifolia. Food Chem 103:1449–1456. https://doi.org/10.1016/j.foodchem.2006.10.061
Gupta S, Dikshit A (2010) Biopesticides: an ecofriendly approach for pest control. J Biopestic 3:186
Hammer KA, Carson CF (2011) Antibacterial and antifungal activities of essential oils. In: Halldor T (ed) Lipids Essent Oils Antimicrob Agents. Wiley, Hoboken
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797
Howell C (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10. https://doi.org/10.1094/PDIS.2003.87.1.4
Jaimand K, Rezaee M (2002) Chemical constituents of essential oils from Mentha longifolia (L.) Hudson var. asiatica (Boriss.) Rech. f. from Iran. J Essent Oil Res 14:107–108. https://doi.org/10.1080/10412905.2002.9699786
Kalogeropoulos N, Konteles SJ, Troullidou E, Mourtzinos I, Karathanos VT (2009) Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from greece and cyprus. Food Chem 116:452–461. https://doi.org/10.1016/j.foodchem.2009.02.060
Kanatt SR, Chander R, Sharma A (2007) Antioxidant potential of mint (Mentha spicata L.) in radiation-processed lamb meat. Food Chem 100:451–458. https://doi.org/10.1016/j.foodchem.2005.09.066
Karpiński TM (2020) Essential oils of lamiaceae family plants as antifungals. Biomolecules 10:103. https://doi.org/10.3390/biom10010103
Kordali S et al (2009) Antifungal and herbicidal properties of essential oils and n-hexane extracts of Achillea gypsicola Hub-Mor. and Achillea biebersteinii Afan. (Asteraceae). Ind Crops Prod 29:562–570. https://doi.org/10.1016/j.indcrop.2008.11.002
Larsson M, Olofsson J (1994) Prevalence and pathogenicity of spinach root pathogens of the genera Aphanomyces, Phytophthora, Fusarium, Cylindrocarpon, and Rhizoctonia in Sweden. Plant Pathol 43:251–260. https://doi.org/10.1111/j.1365-3059.1994.tb02683.x
Leslie JF, Summerell BA (2008) The Fusarium laboratory manual. Wiley, Hoboken
Mahboubi M, Haghi G (2008) Antimicrobial activity and chemical composition of Mentha pulegium L. essential oil. J Ehnopharmacol 119:325–327. https://doi.org/10.1016/j.jep.2008.07.023
Marei GIK, Rasoul MAA, Abdelgaleil SA (2012) Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi. Pestic Biochem Physiol 103:56–61. https://doi.org/10.1016/j.pestbp.2012.03.004
Mutlu-Ingok A, Devecioglu D, Dikmetas DN, Karbancioglu-Guler F, Capanoglu E (2020) Antibacterial, antifungal, antimycotoxigenic, and antioxidant activities of essential oils: an updated review. Molecules 25:4711. https://doi.org/10.3390/molecules25204711
Ozan F, Sümer Z, Polat ZA, Er K, Ozan U, Deger O (2007) Effect of mouthrinse containing propolis on oral microorganisms and human gingival fibroblasts. Eur J Dent 1:195–201. https://doi.org/10.1055/s-0039-1698339
Papavizas G (1985) Trichoderma and Gliocladium: biology, ecology, and potential for biocontrol. Annu Rev Phytopath 23:23–54. https://doi.org/10.1146/annurev.py.23.090185.000323
Pouralibaba HR, Šatović Z, Cobos MJ, Rubiales D, Fondevilla S (2019) Genetic diversity and structure of Fusarium oxysporum f. sp. lentis isolates from Iran, Syria and Algeria. Eur J Plant Pathol 153:1019–1029. https://doi.org/10.1007/s10658-018-01617-7
Qu B et al (2008) Geographic distribution and genetic diversity of Fusarium graminearum and F. asiaticum on wheat spikes throughout China. Plant Pathol 57:15–24. https://doi.org/10.1111/j.1365-3059.2007.01711.x
Quiroga EN, Sampietro DA, Soberon JR, Sgariglia MA, Vattuone MA (2006) Propolis from the northwest of Argentina as a source of antifungal principles. J Appl Microbiol 101:103–110. https://doi.org/10.1111/j.1365-2672.2006.02904.x
Raveau R, Fontaine J, Lounès-Hadj Sahraoui A (2020) Essential oils as potential alternative biocontrol products against plant pathogens and weeds: a review. Foods 9:365. https://doi.org/10.3390/foods9030365
Ruberto G, Baratta MT, Deans SG, Dorman HD (2000) Antioxidant and antimicrobial activity of Foeniculum vulgare and Crithmum maritimum essential oils. Planta Med 66:687–693. https://doi.org/10.1055/s-2000-9773
Saeidnia S, Gohari A, Mokhber-Dezfuli N, Kiuchi F (2011) A review on phytochemistry and medicinal properties of the genus Achillea. DARU J Pharm Sci 19:173
Sarver BA, Ward TJ, Gale LR et al (2011) Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genet Biol 48:1096–1107. https://doi.org/10.1016/j.fgb.2011.09.002
Shuping D, Eloff JN (2017) The use of plants to protect plants and food against fungal pathogens: a review. Afr J Tradit Complement Altern Med 14:120–127. https://doi.org/10.21010/ajtcam.v14i4.14
Soković MD, Vukojević J, Marin PD, Brkić DD, Vajs V, Van Griensven LJ (2009) Chemical composition of essential oilsof thymus and mentha species and their antifungal activities. Molecules 14:238–249. https://doi.org/10.3390/molecules14010238
Soylu S, Yigitbas H, Soylu E, Kurt Ş (2007) Antifungal effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. J Appl Microbiol 103:1021–1030. https://doi.org/10.1111/j.1365-2672.2007.03310.x
Stanisavljević D, Stojicevic S, Djordjevic S et al (2014) Antimicrobial and antioxidant activity of the essential oils obtained from Mentha longifolia L. hudson, dried by three different techniques. Rec Nat Prod 8:61–65
Suga H, Karugia GW, Ward T et al (2008) Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology 98:159–166. https://doi.org/10.1094/PHYTO-98-2-0159
Vigan M (2010) Essential oils: renewal of interest and toxicity. Eur J Dermatol 20:685–692. https://doi.org/10.1684/ejd.2010.1066
Wang K, Jiang S, Pu T, Fan L, Su F, Ye M (2019) Antifungal activity of phenolic monoterpenes and structure-related compounds against plant pathogenic fungi. Nat Prod Res 33:1423–1430. https://doi.org/10.1080/14786419.2017.1419232
Windels CE (2000) Economic and social impacts of Fusarium head blight: changing farms and rural communities in the Northern great plains. Phytopathology 90:17–21. https://doi.org/10.1094/PHYTO.2000.90.1.17
Xiao Y, Liu Z, Gu H, Yang F, Zhang L, Yang L (2021) Improved method to obtain essential oil, asarinin and sesamin from Asarum heterotropoides var mandshuricum using microwave-assisted steam distillation followed by solvent extraction and antifungal activity of essential oil against Fusarium spp. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2021.113295
Yang L, Van der Lee T, Yang X, Yu D, Waalwijk C (2008) Fusarium populations on Chinese barley show a dramatic gradient in mycotoxin profiles. Phytopathology 98:719–727. https://doi.org/10.1094/PHYTO-98-6-0719
Yang S et al (2011) Bioassay-guided isolation and identification of antifungal components from propolis against Penicillium italicum. Food Chem 127:210–215. https://doi.org/10.1016/j.foodchem.2010.12.011
Zeng H, Chen X, Liang J (2015) In vitro antifungal activity and mechanism of essential oil from fennel (Foeniculum vulgare L.) on dermatophyte species. J Med Microbiol 64:93–103. https://doi.org/10.1099/jmm.0.077768-0
Zeppa G, Allegrone G, Barbeni M, Guarda P (1990) Variability in the production of volatile metabolites by Trichoderma viride. Ann Microbiol Enzimol 90:171–176
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Davari, M., Ezazi, R. Mycelial inhibitory effects of antagonistic fungi, plant essential oils and propolis against five phytopathogenic Fusarium species. Arch Microbiol 204, 480 (2022). https://doi.org/10.1007/s00203-022-03102-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03102-6