Skip to main content
SpringerLink
Log in

Characterization and pathogenicity of Cladobotryum mycophilum in Spanish Pleurotus eryngii mushroom crops and its sensitivity to fungicides

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

In 2010, symptoms of cobweb disease were observed on cultivated Pleurotus eryngii crops in Spain. Based on morphological and genetic analyses, the causal agent of cobweb was identified as Cladobotryum mycophilum. Pathogenicity tests on fruit bodies were performed using conidial suspensions of three C. mycophilum isolates. The causal agent was re-isolated in 80–85 % of the fruit bodies inoculated internally and 15–40 % of those fruit bodies inoculated on the cap surface. The results pointed to a certain resistance of the P. eryngii cap surface to the mycelium of C. mycophilum. Two cropping trials inoculated with C. mycophilum were set up to evaluate the pathogenicity of the causal agent of cobweb in two casings. At the end of the growth cycle, 50–60 % of the inoculated blocks cased with mineral soil, and 20–33 % of the inoculated blocks cased with black peat showed cobweb symptoms. This difference in the appearance of the disease and its aggressiveness may be partly explained by different electrical conductivity values of the casing materials used. In vitro sensitivity of the C. mycophilum isolates and P. eryngii strains against four fungicides (chlorothalonil, prochloraz-Mn, thiabendazole and thiophanate-methyl) was assessed in radial growth experiments on fungicide-amended media. The most effective fungicides for inhibiting the in vitro growth of C. mycophilum were prochloraz-Mn and chlorothalonil, while prochloraz-Mn was also the most selective fungicide between P. eryngii and C. mycophilum, and chlorothalonil was the most toxic fungicide against the P. eryngii mycelium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Back, C. G., Kim, Y. H., Jo, W. S., Chung, H., & Jung, H. Y. (2010). Cobweb disease on Agaricus bisporus caused by Cladobotryum mycophilum in Korea. Journal of General Plant Pathology, 76, 232–235.

    Article  Google Scholar 

  • Back, C. G., Lee, C. Y., Seo, G. S., & Jung, H. Y. (2012). Characterization of species of Cladobotryum which cause cobweb disease in edible mushrooms grown in Korea. Mycobiology, 40, 189–194.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bidartondo, M. I., Burghardt, B., Gebauer, G., Bruns, T. D., & Read, D. J. (2004). Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proceedings of the Royal Society of London. Series B, 271, 1799–1806.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrasco, J., Navarro, M. J., Santos, M., Diánez, F., & Gea, F. J. (2016). Identification, incidence and pathogenicity of Cladobotryum mycophilum, causal agent of cobweb disease on Agaricus bisporus mushroom crops in Spain. Annals of Applied Biology, 168, 214–224.

    Article  Google Scholar 

  • Chrysayi-Tokousbalides, M., Kastanias, M. A., Philippoussis, A., & Diamantopoulou, P. (2007). Selective fungitoxicity of famoxadone, tebuconazole and trifloxistrobin between Verticillium fungicola and Agaricus bisporus. Crop Protection, 26, 469–475.

    Article  CAS  Google Scholar 

  • Cole, G. T., & Kendrick, B. (1971). Conidium ontogeny in hyphomycetes. Development and morphology of Cladobotryum. Canadian Journal of Botany, 49, 595–599.

    Article  Google Scholar 

  • Finney, D. J. (1971). Probit analysis. Cambridge: University Press.

    Google Scholar 

  • Fletcher, J. T., & Gaze, R. H. (2008). Mushroom pest and disease control. London: Manson Publishing.

    Google Scholar 

  • Gams, W., & Hoozemans, A. C. M. (1970). Cladobotryum-Konidienformen von Hypomyces-Arten. Persoonia, 6, 95–110.

    Google Scholar 

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Gea, F. J., Navarro, M. J., & Suz, L. M. (2011). First report of Cladobotryum mycophilum causing cobweb on cultivated king oyster mushroom in Spain. Plant Disease, 95, 1030.

    Article  Google Scholar 

  • Gea, F. J., Navarro, M. J., Carrasco, J., González, A. J., & Suz, L. M. (2012a). First report of cobweb on white button mushroom (Agaricus bisporus) in Spain caused by Cladobotryum mycophilum. Plant Disease, 96, 1067.

    Google Scholar 

  • Gea, F. J., Santos, M., Diánez, F., Tello, J. C., & Navarro, M. J. (2012b). Effect of spent mushroom compost tea on mycelial growth and yield of button mushroom (Agaricus bisporus). World Journal of Microbiology and Biotechnology, 28, 2765–2769.

    Article  PubMed  Google Scholar 

  • Gioia, T., Figliuolo, G., Rana, G. L., & Sisto, D. (2007). Morpho-productive comparison among some wild and commercial strains of Pleurotus eryngii (D.C.: Fr.) Quél., in protected cultivation. Micologia Italiana, 36, 35–46.

    Google Scholar 

  • González, A. J., González-Varela, G., & Gea, F. J. (2009). Brown blotch caused by Pseudomonas tolaasii on cultivated Pleurotus eryngii in Spain. Plant Disease, 93, 667.

    Article  Google Scholar 

  • Grogan, H. M. (2005). Cobweb confusion – cobweb isolates explained. Mushroom Journal, 660, 21–33.

    Google Scholar 

  • Grogan, H. M. (2006). Fungicide control of mushroom cobweb disease caused by Cladobotryum strains with different benzimidazole resistance profiles. Pest Management Science, 62, 153–161.

    Article  CAS  PubMed  Google Scholar 

  • Grogan, H. M., & Gaze, R. H. (2000). Fungicide resistance among Cladobotryum spp. – causal agents of cobweb disease of the edible mushroom Agaricus bisporus. Mycological Research, 104, 357–364.

    Article  CAS  Google Scholar 

  • Kim, M. K., Lee, Y. H., Cho, K. M., & Lee, J. Y. (2012). First report of cobweb disease caused by Cladobotryum mycophilum on the edible mushroom Pleurotus eryngii in Korea. Plant Disease, 96, 1374.

    Article  Google Scholar 

  • Kim, M. K., Seuk, S. W., Lee, Y. H., Kim, H. R., & Cho, K. M. (2014). Fungicide sensitivity and characterization of cobweb disease on a Pleurotus eryngii mushroom crop caused by Cladobotryum mycophilum. Plant Pathology Journal, 30, 82–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane, C. R., Cooke, R. C., & Burden, L. J. (1991). Ecophysiology of Dactylium dendroides – the causal agent of cobweb mould. In T. J. Elliott (Ed.), Science and cultivation of edible fungi, Proceedings of the 14th International Congress on the Science and Cultivation of Edible Fungi (Vol. 1, pp. 365–372). Rotterdam: Balkema.

    Google Scholar 

  • McKay, G. J., Egan, D., Morris, E., Scott, C., & Brown, A. E. (1998). Identification of benzimidazole resistance in Cladobottryum dendroides using a PCR-based method. Mycological Research, 102, 671–676.

    Article  CAS  Google Scholar 

  • McKay, G. J., Egan, D., Morris, E., Scott, C., & Brown, A. E. (1999). Genetic and morphological characterization of Cladobotryum species causing cobweb disease of mushrooms. Applied and Environmental Microbiology, 65, 606–610.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mignucci, J. S., Hernández-Bacó, C., Rivera-Vargas, L., Betancourt, C., & Alameda, M. (2000). Diseases and pests research on oyster mushrooms (Pleurotus spp.) in Puerto Rico. International Journal of Mushroom Sciences, 3, 21–26.

    Google Scholar 

  • Põldmaa, K. (2011). Tropical species of Cladobotryum and Hypomyces producing red pigments. Studies in Mycology, 68, 1–34.

    Article  PubMed  PubMed Central  Google Scholar 

  • Potočnik, I., Rekanović, E., Milijašević, S., Todorović, B., & Stepanović, M. (2008). Morphological and pathogenic characteristics of the fungus Cladobotryum dendroides, the causal agent of cobweb disease of the cultivated mushroom Agaricus bisporus in Serbia. Pesticides and Phytomedicine, 23, 175–181.

    Article  Google Scholar 

  • Potočnik, I., Vukojević, J., Stajić, M., Rekanović, E., Milijašević, S., Todorović, B., & Stepanović, M. (2009a). In vitro toxicity of selected fungicides from the groups of benzimidazoles and demethylation inhibitors to Cladobotryum dendroides and Agaricus bisporus. Journal of Environmental Science and Health. Part. B, 44, 365–370.

    Article  Google Scholar 

  • Potočnik, I., Vukojević, J., Stajić, M., Rekanović, E., Milijašević, S., Todorović, B., & Stepanović, M. (2009b). Toxicity of fungicides with different modes of action to Cladobotryum dendroides and Agaricus bisporus. Journal of Environmental Science and Health. Part. B, 44, 823–827.

    Article  Google Scholar 

  • Potočnik, I., Vukojević, J., Stajić, M., Rekanović, E., Stepanović, M., Milijašević, S., & Todorović, B. (2010). Toxicity of biofungicide Timorex 66 EC to Cladobotryum dendroides and Agaricus bisporus. Crop Protection, 29, 290–294.

    Article  Google Scholar 

  • Rana, G. L., Marino, R., Sisto, D., & Candido, V. (2000). Effetti di tre tipi di terreno di copertura sulla comparsa delle verruche sul fungo cardoncello. Agricoltura Ricerca, 188, 113–121.

    Google Scholar 

  • Robertson, J. L., Preisler, H. K., & Russell, R. M. (2003). Polo plus. Probit and logit analysis. User’s guide. Petaluma: LeOra Software.

    Google Scholar 

  • Rodriguez Estrada, A. & Royse, D.J. (2005). Determination of Pseudomonas tolaasii threshold concentrations required to produce symptoms of bacterial blotch disease in Pleurotus eryngii. In Acta Edulis Fungi Vol. 12 (Supplement), Proceedings of the 5th International Conference on Mushroom Biology and Mushroom Products (379–382). Shanghai, China.

  • Rodriguez Estrada, A. E., & Royse, D. J. (2007). Yield, size and bacterial blotch resistance of Pleurotus eryngii grown on cotton seed hulls/oak sawdust supplemented with manganese, copper and whole ground soybean. Bioresource Technology, 98, 1898–1906.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez Estrada, A. E., Jimenez-Gasco, M. M., & Royse, D. J. (2009). Improvement of yield of Pleurotus eryngii var. eryngii by substrate supplementation and use of a casing overlay. Bioresource Technology, 100, 5270–5276.

    Article  CAS  PubMed  Google Scholar 

  • Rogerson, C. T., & Samuels, G. J. (1994). Agaricicolous species of Hypomyces. Mycologia, 86, 839–866.

    Article  Google Scholar 

  • Sharma, V. P., Kumar, S., & Kumari, R. (2006). Symptomatology and management of cobweb disease of oyster mushroom. Mushroom Research, 15, 55–58.

    Google Scholar 

  • Silvestro, D., & Michalak, I. (2012). RaxmlGUI: a graphical front-end for RAxML. Organisms, Diversity and Evolution, 12, 335–337.

    Article  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamm, H. & Põldmaa, K. (2013). Diversity, host associations, and phylogeography of temperate aurofusarin-producing Hypomyces/Cladobotryum including causal agents of cobweb disease of cultivated mushrooms. Fungal Biology, 117, 348–367.

  • 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. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

Download references

Acknowledgments

Funding for this research was provided by Ministerio de Economía y Competitividad (MINECO, Spain) and FEDER (Projects RTA2010-00011-C02-01 and E-RTA2014-00004-C02-01). Jaime Carrasco is the recipient of a fellowship from the FPI-INIA program of MINECO. Authors would like to thank Dr. Bryn Dentinger (Comparative Plant and Fungal Biology, Royal Botanic Gardens Kew, Richmond Surrey, UK) for helpful comments on the phylogenetic analysis.

Author information

Authors and Affiliations

  1. Centro de Investigación, Experimentación y Servicios del Champiñón (CIES), E-16220, Quintanar del Rey, Cuenca, Spain

    Francisco J. Gea, Jaime Carrasco & María J. Navarro

  2. Comparative Plant and Fungal Biology, Royal Botanic Gardens Kew, Richmond, Surrey, TW9 3DS, UK

    Laura M. Suz

Authors
  1. Francisco J. Gea
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaime Carrasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura M. Suz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María J. Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco J. Gea.

Electronic Supplementary Material

ESM 1

Fig Suppl. material. Maximum likelihood tree using nuclear ribosomal internal transcribed spacer (ITS) sequences. Numbers above branches are nonparametric bootstrap values. C. varium is the outgroup. (PDF 118 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gea, F.J., Carrasco, J., Suz, L.M. et al. Characterization and pathogenicity of Cladobotryum mycophilum in Spanish Pleurotus eryngii mushroom crops and its sensitivity to fungicides. Eur J Plant Pathol 147, 129–139 (2017). https://doi.org/10.1007/s10658-016-0986-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-0986-7

Keywords

Search

Navigation