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Research article - Peer-reviewed, 2021

Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity

Ruiz-Duenas, Francisco J.; Barrasa, Jose M.; Sanchez-Garcia, Marisol; Camarero, Susana; Miyauchi, Shingo; Serrano, Ana; Linde, Dolores; Babiker, Rashid; Drula, Elodie; Ayuso-Fernandez, Ivan; Pacheco, Remedios; Padilla, Guillermo; Ferreira, Patricia; Barriuso, Jorge; Kellner, Harald; Castanera, Raul; Alfaro, Manuel; Ramirez, Lucia; Pisabarro, Antonio G.; Riley, Robert;
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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 ancestralsequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.


Agaricales; lifestyle evolution; lignocellulose decay; plant cell-wall degrading enzymes; ligninolytic peroxidases; ancestral-sequence reconstruction

Published in

Molecular Biology and Evolution
2021, volume: 38, number: 4, pages: 1428-1446

Authors' information

Ruiz-Duenas, Francisco J.
Consejo Superior de Investigaciones Cientificas (CSIC)
Barrasa, Jose M.
Universidad de Alcala
Clark University
Camarero, Susana
Max Planck Society
Camarero, Susana
Consejo Superior de Investigaciones Cientificas (CSIC)
Miyauchi, Shingo
Serrano, Ana
Consejo Superior de Investigaciones Cientificas (CSIC)
Linde, Dolores
Consejo Superior de Investigaciones Cientificas (CSIC)
Babiker, Rashid
Consejo Superior de Investigaciones Cientificas (CSIC)
Drula, Elodie
Aix-Marseille Universite
Ayuso-Fernandez, Ivan
Consejo Superior de Investigaciones Cientificas (CSIC)
Pacheco, Remedios
Consejo Superior de Investigaciones Cientificas (CSIC)
Padilla, Guillermo
Consejo Superior de Investigaciones Cientificas (CSIC)
Ferreira, Patricia
Zaragoza Univ
Barriuso, Jorge
Consejo Superior de Investigaciones Cientificas (CSIC)
Kellner, Harald
Technische Universitat Dresden
Castanera, Raul
Universidad Publica de Navarra
Alfaro, Manuel
Universidad Publica de Navarra
Ramirez, Lucia
Universidad Publica de Navarra
Pisabarro, Antonio G.
Universidad Publica de Navarra
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UKÄ Subject classification

Evolutionary Biology

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