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Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche Public

Emmanuelle Morin,Annegret Kohler,Adam R. Baker,Marie Foulongne-Oriol,Vincent Lombard,Laszlo G. Nagy,Robin A. Ohm,Aleksandrina Patyshakuliyeva,Annick Brun,Andrea L. Aerts,Andrew M. Bailey,Christophe Billette,Pedro M. Coutinho,Greg Deaking,Harshavardhan Doddapaneni,Dimitrios Floudas,Jane Grimwood,Kristina Hildén,Ursula Kües,Kurt M. LaButti,Alla Lapidus,Erika A. Lindquist,Susan M. Lucas,Claude Murat,Robert W. Riley,Asaf A. Salamov,Jeremy Schmutz,Venkataramanan Subramanian,Han A.B. Wösten,Jianping Xu,Daniel C. Eastwood,Gary D. Foster,Anton S.M. Sonnenberg,Dan Cullen,Ronald P. de Vries,Taina Lundell,David S. Hibbett,Bernard Henrissat,Kerry S. Burton,Richard W. Kerrigan,Michael P. Challen,Igor V. Grigoriev,Francis Martin 2012 October 08 PNAS USA 109(43): 17501-17506 Correction: 110(10) 4146-4148

Abstract

Agaricus bisporus is the model fungus for the adaptation,persistence, and growth in the humic-rich leaf-litter environment. Aside from its ecological role, A. bisporus has been an important component of the human diet for over 200 y and worldwide cultivation of the “button mushroom” forms a multibillion dollar industry. We present two A. bisporus genomes, their gene repertoires and transcript profiles on compost and during mushroom formation.The genomes encode a full repertoire of polysaccharide-degrading enzymes similar to that of wood-decayers. Comparative transcriptomics of mycelium grown on defined medium, casing-soil, and compost revealed genes encoding enzymes involved in xylan, cellulose, pectin, and protein degradation are more highly expressed in compost. The striking expansion of heme-thiolate peroxidases and β-etherases is distinctive from Agaricomycotina wood-decayers and suggests a broad attack on decaying lignin and related metabolites found in humic acid-rich environment. Similarly, up-regulation of these genes together with a lignolytic manganese peroxidase, multiple copper radical oxidases, and cytochrome P450s is consistent with challenges posed by complex humic-rich substrates. The gene repertoire and expression of hydrolytic enzymes in A. bisporus is substantially different from the taxonomically related ectomycorrhizal symbiont Laccaria bicolor. A common promoter motif was also identified in genes very highly expressed in humic-rich substrates. These observations reveal genetic and enzymatic mechanisms governing adaptation to the humic-rich ecological niche formed during plant degradation, further defining the critical role such fungi contribute to soil structure and carbon sequestration in terrestrial ecosystems. Genome sequence will expedite mushroom breeding for improved agronomic characteristics.

Citation

Emmanuelle Morin, Annegret Kohler, Adam R. Baker, Marie Foulongne-Oriol, Vincent Lombard, Laszlo G. Nagy, Robin A. Ohm,Aleksandrina Patyshakuliyeva, Annick Brun, Andrea L. Aerts Andrew M. Bailey, Christophe Billette, Pedro M. Coutinho, Greg Deakin, Harshavardhan Doddapaneni, Dimitrios Floudas, Jane Grimwood, Kristiina Hildén, Ursula Kües, Kurt M. LaButti, Alla Lapidus, Erika A. Lindquist, Susan M. Lucas, Claude Murat, Robert W. Riley, Asaf A. Salamov, Jeremy Schmutz, Venkataramanan Subramanian, Han A. B. Wösten, Jianping Xu, Daniel C. Eastwood, Gary D. Foster, Anton S. M. Sonnenberg, Dan Cullen, Ronald P. de Vries, Taina Lundell, David S. Hibbett Bernard Henrissat, Kerry S. Burton, Richard W. Kerrigan, Michael P. Challen, Igor V. Grigoriev, and Francis Martin. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche PNAS 2012 ; published ahead of print October 8, 2012, doi:10.1073/pnas.1206847109


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Comments

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AEOK00000000 and AEOL00000000).