Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity

Research output: Contribution to journalResearch articleContributedpeer-review


  • Francisco J. Ruiz-Dueñas - , Spanish National Research Council (Author)
  • José M. Barrasa - , University of Alcalá (Author)
  • Marisol Sánchez-García - , Clark University (Author)
  • Susana Camarero - , Spanish National Research Council (Author)
  • Shingo Miyauchi - , Laboratory of Excellence ARBRE (Author)
  • Ana Serrano - , Spanish National Research Council (Author)
  • Dolores Linde - , Spanish National Research Council (Author)
  • Rashid Babiker - , Spanish National Research Council (Author)
  • Elodie Drula - , Aix-Marseille Université (Author)
  • Iván Ayuso-Fernández - , Spanish National Research Council (Author)
  • Remedios Pacheco - , Spanish National Research Council (Author)
  • Guillermo Padilla - , Spanish National Research Council (Author)
  • Patricia Ferreira - , University of Zaragoza (Author)
  • Jorge Barriuso - , Spanish National Research Council (Author)
  • Harald Kellner - , Chair of Environmental Biotechnology (Author)
  • Raúl Castanera - , Public University of Navarre (UPNA) (Author)
  • Manuel Alfaro - , Public University of Navarre (UPNA) (Author)
  • Lucía Ramírez - , Public University of Navarre (UPNA) (Author)
  • Antonio G. Pisabarro - , Public University of Navarre (UPNA) (Author)
  • Robert Riley - , United States Department of Energy (Author)
  • Alan Kuo - , United States Department of Energy (Author)
  • William Andreopoulos - , United States Department of Energy (Author)
  • Kurt LaButti - , United States Department of Energy (Author)
  • Jasmyn Pangilinan - , United States Department of Energy (Author)
  • Andrew Tritt - , United States Department of Energy (Author)
  • Anna Lipzen - , United States Department of Energy (Author)
  • Guifen He - , United States Department of Energy (Author)
  • Mi Yan - , United States Department of Energy (Author)
  • Vivian Ng - , United States Department of Energy (Author)
  • Igor V. Grigoriev - , University of California at Berkeley (Author)
  • Daniel Cullen - , United States Department of Agriculture (Author)
  • Francis Martin - , Laboratory of Excellence ARBRE (Author)
  • Marie Noëlle Rosso - , Aix-Marseille Université (Author)
  • Bernard Henrissat - , Aix-Marseille Université, King Abdulaziz University (Author)
  • David Hibbett - , Clark University (Author)
  • Angel T. Martínez - , Spanish National Research Council (Author)


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.


Original languageEnglish
Pages (from-to)1428-1446
Number of pages19
JournalMolecular biology and evolution
Issue number4
Publication statusPublished - 13 Apr 2021

External IDs

PubMed 33211093
ORCID /0000-0002-0026-2145/work/149204730



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