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Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease

  • Applied microbial and cell physiology
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Abstract

Dry bubble disease caused by Lecanicillium fungicola is a persistent problem in the cultivation of the white button mushroom (Agaricus bisporus). Because control is hampered by chemicals becoming less effective, new ways to control dry bubble disease are urgently required. 1-Octen-3-ol is a volatile that is produced by A. bisporus and many other fungi. In A. bisporus, it has been implicated in self-inhibition of fruiting body formation while it was shown to inhibit spore germination in ascomycetes. Here, we show that 1-octen-3-ol inhibits germination of L. fungicola and that enhanced levels of 1-octen-3-ol can effectively control the malady. In addition, application of 1-octen-3-ol stimulates growth of bacterial populations in the casing and of Pseudomonas spp. specifically. Pseudomonas spp. and other bacteria have been demonstrated to play part in both the onset of mushroom formation in A. bisporus, as well as the inhibition of L. fungicola spore germination. A potential role of 1-octen-3-ol in the ecology of L. fungicola is discussed.

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References

  • Berendsen RL, Baars JPP, Kalkhove SIC, Lugones LG, Wösten HAB, Bakker PAHM (2010) Lecanicillium fungicola: causal agent of dry bubble disease in white-button mushroom. Mol Plant Pathol 11:585–595

    Google Scholar 

  • Berendsen RL, Kalkhove SIC, Lugones LG, Baars JJP, Wösten HAB, Bakker PAHM (2012a) Effects of fluorescent Pseudomonas spp. isolated from mushroom cultures on Lecanicillium fungicola. Biol Control 63:210–221

    Article  CAS  Google Scholar 

  • Berendsen RL, Kalkhove SIC, Lugones LG, Wösten HAB, Bakker PAHM (2012b) Germination of Lecanicillium fungicola in the mycosphere of Agaricus bisporus. Environ Microbiol Rep 4:227–233

    Article  CAS  Google Scholar 

  • Berendsen RL, Schrier N, Kalkhove SIC, Lugones LG, Baars JJP, Zijlstra C, de Weerdt M, Wösten HAB, Bakker PAHM (2013) Absence of induced resistance in Agaricus bisporus against Lecanicillium fungicola. Anton Leeuw Int J G 13:539–550

    Article  Google Scholar 

  • Bernardo D, Cabo AP, Novaes-Ledieu M, Mendoza CG (2004) Verticillium disease or “dry bubble” of cultivated mushrooms: the Agaricus bisporus lectin recognizes and binds the Verticillium fungicola cell wall glucogalactomannan. Can J Microbiol 50:729–735

    Article  CAS  Google Scholar 

  • Bollen GJ, van Zaayen A (1975) Resistance to benzimidazole fungicides in pathogenic strains of Verticillium fungicola. Neth J Pl Path 81:157–167

    Article  CAS  Google Scholar 

  • Calonje M, Mendoza CG, Cabo AP, Bernardo D, Novaes-Ledieu M (2000) Interaction between the mycoparasite Verticillium fungicola and the vegetative mycelial phase of Agaricus bisporus. Mycol Res 104:988–992

    Article  Google Scholar 

  • Chitarra GS, Abee T, Rombouts FM, Dijksterhuis J (2005) 1-Octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition. FEMS Microbiol Ecol 54:67–75

    Article  CAS  Google Scholar 

  • Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J (2004) Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol 70:2823–2829

    Article  CAS  Google Scholar 

  • Combet E, Henderson J, Eastwood DC, Burton KS (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326

    Article  CAS  Google Scholar 

  • Combet E, Henderson J, Eastwood DC, Burton KS (2009) Influence of sporophore development, damage, storage, and tissue specificity on the enzymic formation of volatiles in mushrooms (Agaricus bisporus). J Agr Food Chem 57:3709–3717

    Article  CAS  Google Scholar 

  • Cross MJ, Jacobs L (1968) Some observations on the biology of spores of Verticillium malthousei. Mushroom Sci 7:239–244

    Google Scholar 

  • de Beaufort F, Voilley A (1995) Methyl cellulose-based edible films and coatings I. Effect of plasticizer content on water and 1-octen-3-ol sorption and transport. Cellulose 2:205–213

    Article  Google Scholar 

  • Doornbos RF, Geraats BPJ, Kuramae EE, Van Loon LC, Bakker PAHM (2011) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microbe In 24:395–407

    Article  CAS  Google Scholar 

  • Eger G (1961) Untersuchungen über die Funktion der Deckschicht bei der Fruchtkörperbildung des Kulturchampignon, Psalliota bispora Lange. Arch Mikrobiol 39:313–334

    Article  Google Scholar 

  • Fekete K (1967) Über Morphologie, Biologie und Bekämpfung von Verticillium malthousei, einem Parasiten des Kulturchampignons. Phytopathol Z 59:1–32

    Article  Google Scholar 

  • Fletcher JT, Gaze RH (2008) Mushroom pest and disease control. Academic Press, San Diego, CA

    Google Scholar 

  • Fletcher JT, Yarham DJ (1976) The incidence of benomyl tolerance in Verticillium fungicola, Mycogone perniciosa and Hypomyces rosellus in mushroom crops. Ann Appl Biol 83:4898–4903

    Google Scholar 

  • Garbeva P, Hol WHG, Termorshuizen AJ, Kowalchuk GA, de Boer W (2011) Fungistasis and general soil biostasis - A new synthesis. Soil Biol Biochem 43:469–477

    Article  CAS  Google Scholar 

  • Gea FJ, Navarro MJ, Tello JC (2005) Reduced sensitivity of the mushroom pathogen Verticillium fungicola to prochloraz-manganese in vitro. Mycol Res 109:741–745

    Article  CAS  Google Scholar 

  • Grewal SIS, Rainey PB (1991) Phenotypic variation of Pseudomonas putida and P. tolaasii affects the chemotactic response to Agaricus bisporus mycelial exudate. J Gen Microbiol 137:2761–2768

    Article  CAS  Google Scholar 

  • Grove JF, Blight MM (1983) The oviposition attractant for the mushroom phorid Megaselia halterata - the identification of volatiles present in mushroom house air. J Sci Food Agr 34:181–185

    Article  CAS  Google Scholar 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of phycocyanin and fluorescin. J Lab Clin Med 44:301–307

    CAS  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37

    Article  CAS  Google Scholar 

  • Largeteau M, Savoie JM (2010) Microbially induced diseases of Agaricus bisporus: biochemical mechanisms and impact on commercial mushroom production. Appl Microbiol Biotechnol 86:63–73

    Article  CAS  Google Scholar 

  • Miller N, Gillespie JB, Doyle OPE (1995) The involvement of microbiological components of peat based casing materials in fructification of Agaricus bisporus. Mushroom Sci 14:313–321

    Google Scholar 

  • Noble R, Dobrovin-Pennington A, Hobbs PJ, Pederby J, Rodger A (2009) Volatile C8 compounds and pseudomonads influence primordium formation of Agaricus bisporus. Mycologia 101:583–591

    Article  CAS  Google Scholar 

  • Okull DO, Beelman RB, Gourama H (2003) Antifungal activity of 10-oxo-trans-8-decenoic acid and 1-octen-3-ol against Penicillium expansum in potato dextrose agar medium. J Food Protect 66:1503–1505

    CAS  Google Scholar 

  • Spiteller P (2008) Chemical defence strategies of higher fungi. Chemistry 14:9100–9110

    Article  CAS  Google Scholar 

  • Visscher HR (1988) Casing soil. In: van Griensven LJLD (ed) The cultivation of mushrooms. Grafidrukkerij Waalwijk, Waalwijk, the Netherlands, pp 73–90

    Google Scholar 

  • Wu C, Wan Z (2000) Volatile compounds in fresh and processed shiitake mushrooms (Lentinus edodes Sing.). Food Sci Technol Res 6:166–170

    Article  CAS  Google Scholar 

  • Wuest PJ, Cole H, Sanders PL (1974) Tolerance of Verticillium malthousei to benomyl. Phytopathol 64:331–334

    Article  CAS  Google Scholar 

  • Wuest PJ, Forer LB (1975) Temperature, time, and the influence of volatiles of phialospore germination in Verticillium malthousei (Ware). Mycopathol 55:9–12

    Article  CAS  Google Scholar 

  • Wurzenberger M, Grosch W (1982) The enzymic oxidative breakdown of linoleic acid in mushrooms (Psalliota bispora). Z Lebensm Unters Fors 175:186–190

    Article  CAS  Google Scholar 

  • Wurzenberger M, Grosch W (1984) Origin of the oxygen in the products of the enzymatic cleavage reaction of linoleic acid to 1-octen-3-ol and 10-oxo-trans-8-decenoic acid in mushrooms (Psalliota bispora). Biochim Biophys Acta 794:18–24

    Article  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Dutch Technology Foundation (STW), Applied Science Division of NWO and the Technology Program of the Ministry of Economic Affairs. We would like to thank Jo Rutjens, Merlin van Strien, and Sebastian Jianu for excellent technical assistance.

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Authors and Affiliations

  1. Plant-Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Roeland L. Berendsen & Peter A. H. M. Bakker

  2. Molecular Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Stefanie I. C. Kalkhove, Luis G. Lugones & Han A. B. Wösten

  3. Department of Plant Breeding, Plant Research International, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Johan J. P. Baars

Authors
  1. Roeland L. Berendsen
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  2. Stefanie I. C. Kalkhove
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  3. Luis G. Lugones
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  4. Johan J. P. Baars
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  5. Han A. B. Wösten
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  6. Peter A. H. M. Bakker
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Correspondence to Roeland L. Berendsen.

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Berendsen, R.L., Kalkhove, S.I.C., Lugones, L.G. et al. Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease. Appl Microbiol Biotechnol 97, 5535–5543 (2013). https://doi.org/10.1007/s00253-013-4793-1

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  • DOI: https://doi.org/10.1007/s00253-013-4793-1

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