We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives. Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae. Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay. This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes.

Architecture et Fonction des Macromolécules Biologiques CNRS Aix Marseille Université Marseille 13009 France

Architecture et Fonction des Macromolécules Biologiques INRAE Marseille 13009 France

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design Beijing Forestry University Beijing 100083 China

CAS Key Laboratory for Plant Diversity and Biogeography of East Asia Kunming Institute of Botany Chinese Academy of Sciences Kunming 650201 Yunnan China

Chemical and Biological Processes Development Group Pacific Northwest National Laboratory Richland WA 99354 USA

Department of Aquatic Microbial Ecology Institute of Hydrobiology Biology Centre of the Czech Academy of Sciences 370 05 České Budějovice Czech Republic

Department of Biological Sciences King Abdulaziz University Jeddah 21589 Saudi Arabia

Department of Biology McMaster University Hamilton ON L8S 4K1 Canada

Department of Biotechnology College of Life Sciences and Biotechnology Korea University 02841 Seoul Korea

Department of Botany and Plant Pathology Oregon State University Corvallis OR 97331 USA

Department of Plant Anatomy Institute of Biology Eötvös Loránd University Budapest 1117 Hungary

Department of Plant and Microbial Biology University of California Berkeley CA 94720 USA

Hawkesbury Institute for the Environment Western Sydney University Richmond NSW 2753 Australia

Lawrence Berkeley National Laboratory US Department of Energy Berkeley CA 94720 USA

Synthetic and Systems Biology Unit Biological Research Centre Szeged 6726 Hungary

Université de Lorraine INRAE UMR Interactions Arbres Microorganismes Centre INRAE Grand Est Nancy Champenoux 54 280 France

Yunnan Institute of Tropic Crops Jinghong Yunnan 666100 China

Yunnan Key Laboratory for Fungal Diversity and Green Development Kunming Yunnan 650201 China

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