Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity
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- Francisco J Ruiz-Dueñas
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- José M Barrasa
- Life Sciences Department, Alcalá University, Alcalá de Henares, Spain
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- Marisol Sánchez-García
- Biology Department, Clark University, Worcester, MA, USA
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- Susana Camarero
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Shingo Miyauchi
- INRAE, Laboratory of Excellence ARBRE, Champenoux, France
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- Ana Serrano
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Dolores Linde
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Rashid Babiker
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Elodie Drula
- Architecture et Fonction des Macromolécules Biologiques, CNRS/Aix-Marseille University, Marseille, France
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- Iván Ayuso-Fernández
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Remedios Pacheco
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Guillermo Padilla
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Patricia Ferreira
- Biochemistry and Molecular and Cellular Biology Department and BIFI, Zaragoza University, Zaragoza, Spain
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- Jorge Barriuso
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Harald Kellner
- International Institute Zittau, Technische Universität Dresden, Zittau, Germany
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- Raúl Castanera
- Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
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- Manuel Alfaro
- Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
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- Lucía Ramírez
- Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
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- Antonio G Pisabarro
- Institute for Multidisciplinary Research in Applied Biology, IMAB-UPNA, Pamplona, Spain
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- Robert Riley
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Alan Kuo
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- William Andreopoulos
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Kurt LaButti
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Jasmyn Pangilinan
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Andrew Tritt
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Anna Lipzen
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Guifen He
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Mi Yan
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Vivian Ng
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Igor V Grigoriev
- US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA, USA
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- Daniel Cullen
- Forest Products Laboratory, US Department of Agriculture, Madison, WI, USA
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- Francis Martin
- INRAE, Laboratory of Excellence ARBRE, Champenoux, France
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- Marie-Noëlle Rosso
- INRAE, Biodiversité et Biotechnologie Fongiques, Aix-Marseille University, Marseille, France
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- Bernard Henrissat
- Architecture et Fonction des Macromolécules Biologiques, CNRS/Aix-Marseille University, Marseille, France
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- David Hibbett
- Biology Department, Clark University, Worcester, MA, USA
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- Angel T Martínez
- Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain
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- Julian Echave
- editor
抄録
<jats:title>Abstract</jats:title> <jats:p>As actors of global carbon cycle, Agaricomycetes (Basidiomycota) have developed complex enzymatic machineries that allow them to decompose all plant polymers, including lignin. Among them, saprotrophic Agaricales are characterized by an unparalleled diversity of habitats and lifestyles. Comparative analysis of 52 Agaricomycetes genomes (14 of them sequenced de novo) reveals that Agaricales possess a large diversity of hydrolytic and oxidative enzymes for lignocellulose decay. Based on the gene families with the predicted highest evolutionary rates—namely cellulose-binding CBM1, glycoside hydrolase GH43, lytic polysaccharide monooxygenase AA9, class-II peroxidases, glucose–methanol–choline oxidase/dehydrogenases, laccases, and unspecific peroxygenases—we reconstructed the lifestyles of the ancestors that led to the extant lignocellulose-decomposing Agaricomycetes. The changes in the enzymatic toolkit of ancestral Agaricales are correlated with the evolution of their ability to grow not only on wood but also on leaf litter and decayed wood, with grass-litter decomposers as the most recent eco-physiological group. In this context, the above families were analyzed in detail in connection with lifestyle diversity. Peroxidases appear as a central component of the enzymatic toolkit of saprotrophic Agaricomycetes, consistent with their essential role in lignin degradation and high evolutionary rates. This includes not only expansions/losses in peroxidase genes common to other basidiomycetes but also the widespread presence in Agaricales (and Russulales) of new peroxidases types not found in wood-rotting Polyporales, and other Agaricomycetes orders. Therefore, we analyzed the peroxidase evolution in Agaricomycetes by ancestral-sequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.</jats:p>
収録刊行物
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- Molecular Biology and Evolution
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Molecular Biology and Evolution 38 (4), 1428-1446, 2020-11-19
Oxford University Press (OUP)