Absence of induced resistance in Agaricus bisporus against Lecanicillium fungicola
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Abstract
Lecanicillium fungicola causes dry bubble disease and is an important problem in the cultivation of Agaricus bisporus. Little is known about the defense of mushrooms against pathogens in general and L. fungicola in particular. In plants and animals, a first attack by a pathogen often induces a systemic response that results in an acquired resistance to subsequent attacks by the same pathogen. The development of functionally similar responses in these two eukaryotic kingdoms indicates that they are important to all multi-cellular organisms. We investigated if such responses also occur in the interaction between the white button mushroom and L. fungicola. A first infection of mushrooms of the commercial A. bisporus strain Sylvan A15 by L. fungicola did not induce systemic resistance against a subsequent infection. Similar results were obtained with the A. bisporus strain MES01497, which was demonstrated to be more resistant to dry bubble disease. Apparently, fruiting bodies of A. bisporus do not express induced resistance against L. fungicola.
Keywords
Lecanicillium fungicola Agaricus bisporus Induced resistance Dry bubble disease Systemic acquired resistanceNotes
Acknowledgments
The work was supported by the Dutch Technology Foundation STW, Applied Science division of NWO and the Technology Program of the Ministry of Economic Affairs.
Supplementary material
References
- Ahmad S, Gordon-Weeks R, Pickett J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol Plant Pathol 11:817–827PubMedGoogle Scholar
- Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
- Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6:973–979PubMedCrossRefGoogle Scholar
- 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 11:585–595PubMedGoogle 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 50:729–735PubMedCrossRefGoogle Scholar
- Braaksma A, Schaap DJ (2005) Kwaliteit van champignons: geremde hoedopening en meer smaak. Agrotechnology & Food Innovations B.V., WageningenGoogle Scholar
- Braaksma A, Schaap DJ, Donkers JW, Schipper CMA (2001) Effect of cytokinin on cap opening in Agaricus bisporus during storage. Postharvest Biol Technol 23:171–173CrossRefGoogle Scholar
- Camazine S (1983) Mushroom chemical defense: food aversion learning induced by hallucinogenic toxin, muscimol. J Chem Ecol 9:1473–1481CrossRefGoogle Scholar
- Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216PubMedCrossRefGoogle Scholar
- Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B, Grp P-A-P (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071PubMedCrossRefGoogle Scholar
- Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
- Foulongne-Oriol M, Rodier A, Rousseau T, Largeteau M, Savoie J-M (2011) Quantitative genetics to dissect the fungal–fungal interaction between Lecanicillium verticillium and the white button mushroom Agaricus bisporus. Fungal Biol 115:421–431PubMedCrossRefGoogle Scholar
- Foulongne-Oriol M, Rodier A, Savoie J-M (2012) Relationship between yield components and partial resistance to Lecanicillium fungicola in the button mushroom, Agaricus bisporus, assessed by quantitative trait locus mapping. Appl Environ Microbiol 78:2435–2442PubMedCrossRefGoogle Scholar
- Grechkin A (1998) Recent developments in biochemistry of the plant lipoxygenase pathway. Prog Lipid Res 37:317–352PubMedCrossRefGoogle Scholar
- Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67PubMedCrossRefGoogle Scholar
- Heil M, Hilpert A, Kaiser W, Linsenmair KE (2000) Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? J Ecol 88:645–654CrossRefGoogle Scholar
- Henrion B, Chevalier G, Martin F (1994) Typing truffle species by PCR amplification of the ribosomal DNA spacers. Mycol Res 98:37–43CrossRefGoogle Scholar
- Jolivet S, Arpin N, Wichers HJ, Pellon GP (1998) Agaricus bisporus browning: a review. Mycol Res 102:1459–1483CrossRefGoogle Scholar
- Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
- Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91PubMedCrossRefGoogle Scholar
- Largeteau ML, Rodier A, Rousseau T, Juarez del Carmen S, Védie R, Savoie JM (2004) Agaricus susceptibility to Verticillium fungicola. Mushroom Sci 16:504–522Google Scholar
- Largeteau ML, Regnault-Roger C, Savoie JM (2007) Verticillium disease of Agaricus bisporus: variations in host contribution to total fungal DNA in relation to symptom heterogeneity. Eur J Plant Pathol 118:155–164CrossRefGoogle Scholar
- Largeteau M, Latapy C, Minvielle N, Regnault-Roger C, Savoie J-M (2010) Expression of phenol oxidase and heat-shock genes during the development of Agaricus bisporus fruiting bodies, healthy and infected by Lecanicillium fungicola. Appl Microbiol Biotechnol 85:1499–1507PubMedCrossRefGoogle Scholar
- Little TJ, Kraaijeveld AR (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19:58–60PubMedCrossRefGoogle Scholar
- Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403PubMedCrossRefGoogle Scholar
- Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Ann Rev Immun 27:229–265CrossRefGoogle Scholar
- Moore D (1991) Perception and response to gravity in higher fungi--a critical appraisal. New Phytol 117:3–23PubMedCrossRefGoogle Scholar
- North LH, Wuest PJ (1993) The infection process and symptom expression of Verticillium disease of Agaricus bisporus. Can J Plant Pathol 15:74–80CrossRefGoogle Scholar
- Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
- Pan Z, Camara B, Gardner HW, Backhaus RA (1998) Aspirin inhibition and acetylation of the plant cytochrome P450, allene oxide synthase, resembles that of animal prostaglandin endoperoxide H synthase. J Biol Chem 273:18139–18145PubMedCrossRefGoogle Scholar
- Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3:1–8CrossRefGoogle Scholar
- Reverberi M, Ricelli A, Zjalic S, Fabbri A, Fanelli C (2010) Natural functions of mycotoxins and control of their biosynthesis in fungi. App Microbiol Biotechnol 87:899–911CrossRefGoogle Scholar
- Rohlfs M, Albert M, Keller NP, Kempken F (2007) Secondary chemicals protect mould from fungivory. Biol Lett 3:523–525PubMedCrossRefGoogle Scholar
- Roth O, Sadd BM, Schmid-Hempel P, Kurtz J (2009) Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc R Soc B Biol Sci 276:145–151CrossRefGoogle Scholar
- Savoie JM, Largeteau ML (2004) Hydrogen peroxide concentrations detected in Agaricus bisporus sporocarps and relation with their susceptibility to the pathogen Verticillium fungicola. FEMS Microbiol Lett 237:311–315PubMedGoogle Scholar
- Schultz JC (2002) Shared signals and the potential for phylogenetic espionage between plants and animals. Integr Comp Biol 42:454–462PubMedCrossRefGoogle Scholar
- Sherratt TN, Wilkinson DM, Bain RS (2005) Explaining Dioscorides’ “double differences”: why are some mushrooms poisonous, and do they signal their unprofitability? Am Nat 166:767–775PubMedCrossRefGoogle Scholar
- Silar P (2005) Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant. Mycol Res 109:137–149PubMedCrossRefGoogle Scholar
- Soanes DM, Talbot NJ (2010) Comparative genome analysis reveals an absence of leucine-rich repeat pattern-recognition receptor proteins in the kingdom fungi. PLoS ONE 5:1–10CrossRefGoogle Scholar
- Soler-Rivas C, Möller AC, Arpin N, Olivier JM, Wichers HJ (2001) Induction of a tyrosinase mRNA in Agaricus bisporus upon treatment with a tolaasin preparation from Pseudomonas tolaasii. Physiol Mol Plant Pathol 58:95–99CrossRefGoogle Scholar
- Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5:1–11Google Scholar
- Spiteller P (2008) Chemical defence strategies of higher fungi. Chemistry 14:9100–9110PubMedCrossRefGoogle Scholar
- Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100PubMedCrossRefGoogle Scholar
- Thomas J, Sergeant M, Costa A, Collopy P, Bailey A, Foster G, Mills P, Challen M (2007) Molecular characterisation of the interaction between Agaricus bisporus and its mycopathogen Verticillium fungicola. Mushroom Sci 17:123–130Google Scholar
- Torres MA (2009) ROS in biotic interactions. Physiol Plant 138:414–429PubMedCrossRefGoogle Scholar
- Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588PubMedCrossRefGoogle Scholar
- Van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. P Natl Acad Sci Biol 103:5602–5607CrossRefGoogle Scholar
- Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483PubMedCrossRefGoogle Scholar
- Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas strain WCS417r. Phytopathology 81:728–734CrossRefGoogle Scholar