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Inhibitory and stimulatory effects of essential oils and individual monoterpenoids on growth and sporulation of four soil-borne fungal isolates of Aspergillus terreus, Fusarium oxysporum, Penicillium expansum, and Verticillium dahliae

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Abstract

The effect of essential oils and individual monoterpenoids on soil-borne fungi, in pure and mixed cultures, in growth media and in the soil environment, was investigated. Essential oils were extracted from lavender (Lavandula stoechas), oregano (Origanum vulgare subsp. hirtum), sage (Salvia fruticosa) and spearmint (Mentha spicata). The monoterpenoids tested were fenchone, carvacrol, 1,8-cineole, carvone, α-pinene and terpinen-4-ol. Their effect was examined on growth and sporulation of Aspergillus terreus, Fusarium oxysporum, Penicillium expansum and Verticillium dahliae isolated from an organic cultivation of tomato. All tested essential oils and individual monoterpenoids inhibited mycelial growth in all fungi and conidial production in most fungi. The strongest inhibitory activity on mycelial growth was exhibited by oregano and spearmint oils and by carvacrol and carvone, respectively their main constituents. The inhibitory activity was clearly fungistatic in A. terreus and F. oxysporum but fungicidal in V. dahliae. On sporulation, clearly stimulatory effects were observed alongside inhibitory ones. Conidial production was always promoted by α-pinene in P. expansum and by sage oil in F. oxysporum. At certain dosages it was promoted by cineole and carvone in F. oxysporum, and by lavender oil in A. terreus and V. dahliae. Experiments with carvone and carvacrol against mixed fungal cultures in a soil environment showed that V. dahliae was the most sensitive and A. terreus the most tolerant of the four fungi. Our results demonstrate strong but divergent effects and selectivity of action of the lower terpenoids on fungal strains that can become serious pests of tomato. Of special importance is the complete inhibition of growth and conidial production of V. dahliae, a pathogen otherwise very resistant to chemical control.

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Abbreviations

CDA:

Czapek dox agar

CFU:

colony forming units

RMGR:

recovery of mycelial growth

WA:

water agar

References

  • Angioni, A., Barra, A., Coroneo, V., Dessi, S., & Cabras, P. (2006). Chemical composition, seasonal variability, and antifungal activity of Lavandula stoechas L. ssp. stoechas essential oils from stem/leaves and flowers. Journal of Agricultural and Food Chemistry, 54, 4364–4370.

    Article  PubMed  CAS  Google Scholar 

  • Bång, U. (2007). Screening natural plant volatiles to control the potato (Solanum tuberosum) pathogens Helminthosporium solani, Fusarium solani, Phoma foveata, and Rhizoctonia solani. Potato Research, 50, 185–203.

    Article  Google Scholar 

  • Basílico, M. Z., & Basílico, J. C. (1999). Inhibitory effects of some spice essential oils on Aspergillus ochraceus NRRL 3174 growth and ochratoxin A production. Letters in Applied Microbiology, 29(4), 238–241.

    Article  PubMed  Google Scholar 

  • Calvo, A. M., Wilson, R. A., Bok, J. W., & Keller, N. P. (2002). Relationship between secondary metabolism and fungal development. Microbiology and Molecular Biology Reviews, 66, 447–459.

    Article  PubMed  CAS  Google Scholar 

  • Chalkos, D., Kadoglidou, K., Karamanoli, K., Fotiou, C., Pavlatou-Ve, A. S., Eleftherohorinos, I. G., et al. (2010). Mentha spicata and Salvia fruticosa composts as soil amendments in tomato cultivation. Plant and Soil, 332, 495–509.

    Article  CAS  Google Scholar 

  • Daferera, D. J., Ziogas, B. N., & Polissiou, M. G. (2000). GC-MS analysis of essential oils from some Greek aromatic plants and their fungitoxicity on Penicillium digitatum. Journal of Agricultural and Food Chemistry, 48, 2576–2581.

    Article  PubMed  CAS  Google Scholar 

  • Daferera, D. J., Ziogas, B. N., & Polissiou, M. G. (2003). The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Protection, 22, 39–44.

    Article  CAS  Google Scholar 

  • Farag, R. S., Daw, Z. Y., & Abo-Raya, S. H. (1989). Influence of some spice essential oils on Aspergillus parasiticus growth and production of alfatoxins in a synthetic medium. Journal of Food Science, 54, 74–76.

    Article  CAS  Google Scholar 

  • Goud, J. C., Termorshuizen, A. J., & Gams, W. (2003). Morphology of Verticillium dahliae and V. tricorpus on semi-selective media used for the detection of V. dahliae in soil. Mycological Research, 107, 822–830.

    Article  PubMed  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis. Nucleic Acids Symposium Series, 4, 95–98.

    Google Scholar 

  • Hountondji, F. C. C., Hanna, R., & Sabelis, M. W. (2006). Does methyl salicylate, a component of herbivore-induced plant odour, promote sporulation of the mite-pathogenic fungus Neozygites tanajoae? Experimental and Applied Acarology, 39, 63–74.

    Article  CAS  Google Scholar 

  • Kalemba, D., & Kunicka, A. (2003). Antibacterial and antifungal properties of essential oils. Current Medicinal Chemistry, 10, 813–829.

    Article  PubMed  CAS  Google Scholar 

  • Karamanoli, K., Vokou, D., Menkissoglu, O., & Constantinidou, H.-I. (2000). Bacterial colonization of phyllosphere of Mediterranean aromatic plants. Journal of Chemical Ecology, 26, 2035–2048.

    Article  CAS  Google Scholar 

  • Karamanoli, K., Kadoglidou, K., Tananaki, C., Thrasyvoulou, A., Constantinidou, H.-I. A., & Vokou, D. (2008). Transformations of Mentha spicata essential oil in the soil environment. Planta Medica, 74, 1201.

    Article  Google Scholar 

  • Karousou, R., Vokou, D., & Kokkini, S. (1998). Variation of Salvia fruticosa essential oils on the island of Crete (Greece). Botanica Acta, 111, 250–254.

    CAS  Google Scholar 

  • Khaddor, M., Lamarti, A., Tantaoui-Elaraki, A., Ezziyyani, M., Castillo, M. E. C., & Badoc, A. (2006). Antifungal activity of three essential oils on growth and toxigenesis of Penicillium aurantiogriseum and Penicillium viridicatum. Journal of Essential Oil Research, 18, 586–589.

    CAS  Google Scholar 

  • Kim, Y. K., & Xiao, C. L. (2010). Influence of environmental factors on conidial germination and survival of Sphaeropsis pyriputrescens. European Journal of Plant Pathology, 126, 153–163.

    Article  Google Scholar 

  • Kokkini, S., & Vokou, D. (1989). Mentha spicata (Lamiaceae) chemotypes grown wild in Greece. Economic Botany, 43, 192–202.

    Article  CAS  Google Scholar 

  • Kuate, J., Foko, J., Ndindeng, S. A., Jazet-Dongmo, P. M., Fouré, E., Damesse, F., et al. (2006). Effect of essential oils from citrus varieties on in vitro growth and sporulation of Phaeoramularia angolensis causing citrus leaf and fruit spot disease. European Journal of Plant Pathology, 161, 114–151.

    Google Scholar 

  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 2, 2947–2948.

    Article  Google Scholar 

  • Müller-Riebau, F., Berger, B., & Yegen, O. (1995). Chemical composition and fungitoxic properties to phytopathogenic fungi of essential oils of selected aromatic plants growing wild in Turkey. Journal of Agricultural and Food Chemistry, 43, 2262–2266.

    Article  Google Scholar 

  • Olanya, O. M., & Larkin, R. P. (2006). Efficacy of essential oils and biopesticides on Phytopthora infestans suppression in laboratory and growth chamber studies. Biocontrol Science and Technology, 16(9), 901–917.

    Article  Google Scholar 

  • Pawar, V. C., & Thaker, V. S. (2007). Evaluation of the anti-Fusarium oxysporum f. sp cicer and anti-Alternaria porri effects of some essential oils. World Journal of Microbiology and Biotechnology, 23, 1099–1109.

    Article  CAS  Google Scholar 

  • Pitarokili, D., Tzakou, O., Loukis, A., & Harvala, C. (2003). Volatile metabolites from Salvia fruticosa as antifungal agents in soilborne pathogens. Journal of Agricultural and Food Chemistry, 51, 3294–3301.

    Article  PubMed  CAS  Google Scholar 

  • Pradhanag, P. M., Momol, M. T., Olson, S. M., & Jones, J. B. (2003). Effects of plant essential oils on Ralstonia solanacearum population density and bacterial wilt incidence in tomato. Plant Disease, 87, 423–427.

    Article  Google Scholar 

  • Rahmani, M., Ling, C. Y., Meon, S., Ismail, H. B. M., & Sucari, M. A. (2004). The antifungal activity of Glycosmis calcicola and G. rupestris extracts. Pharmaceutical Biology, 42, 430–433.

    Article  Google Scholar 

  • Soković, M., & Van Griensven, L. J. L. D. (2006). Antimicrobial activity of essential oils and their components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. European Journal of Plant Pathology, 116, 211–224.

    Article  Google Scholar 

  • Thompson, D. P. (1989). Fungitoxic activity of essential oil components on food storage fungi. Mycologia, 81, 151–153.

    Article  CAS  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882.

    Article  Google Scholar 

  • Toothaker, L. (1993). Multiple comparison procedures. Newbury Park: Sage.

    Google Scholar 

  • Vokou, D. (1999). Essential oils as allelochemicals: Research advances in Greece. In S. S. Narwal (Ed.), Allelopathy update: Basic and applied aspects (pp. 47–63). Enfield: Science.

    Google Scholar 

  • Vokou, D., & Margaris, N. S. (1986). Autoallelopathy of Thymus capitatus. Acta Oecologica Oecol. Plant, 7, 157–163.

    Google Scholar 

  • Vokou, D., Kokkini, S., & Bessière, J. M. (1993). Geographic variation of Greek oregano (Origanum vulgare subsp. hirtum) essential oils. Biochemical Systematic. Ecology, 21, 287–295.

    CAS  Google Scholar 

  • Vokou, D., Chalkos, D., Yangou, M., & Karamanlidou, G. (2002). Activation of soil respiration and shift of the microbial population balance in soil as a response to Lavandula stoechas essential oil. Journal of Chemical Ecology, 28, 755–768.

    Article  PubMed  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfaund, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic.

    Google Scholar 

  • Zhang, Z., Schwartz, S., Wagner, L., & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Computational Biology, 7, 203–214.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the General Secretariat for Research and Technology, Ministry of Development, Greece (Programme 2001 ED 317).

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Correspondence to Helen-Isis A. Constantinidou.

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Kadoglidou, K., Lagopodi, A., Karamanoli, K. et al. Inhibitory and stimulatory effects of essential oils and individual monoterpenoids on growth and sporulation of four soil-borne fungal isolates of Aspergillus terreus, Fusarium oxysporum, Penicillium expansum, and Verticillium dahliae . Eur J Plant Pathol 130, 297–309 (2011). https://doi.org/10.1007/s10658-011-9754-x

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