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Lentinulais a broadly distributed group of fungi that contains the cultivated shiitake mushroom,L. edodes. We sequenced 24 genomes representing eight described species and several unnamed lineages ofLentinulafrom 15 countries on four continents.Lentinulacomprises four major clades that arose in the Oligocene, three in the Americas and one in Asia–Australasia. To expand sampling of shiitake mushrooms, we assembled 60 genomes ofL. edodesfrom China that were previously published as raw Illumina reads and added them to our dataset.Lentinula edodessensu lato (s. lat.) contains three lineages that may warrant recognition as species, one including a single isolate from Nepal that is the sister group to the rest ofL. edodess. lat., a second with 20 cultivars and 12 wild isolates from China, Japan, Korea, and the Russian Far East, and a third with 28 wild isolates from China, Thailand, and Vietnam. Two additional lineages in China have arisen by hybridization among the second and third groups. Genes encoding cysteine sulfoxide lyase (lecsl) and γ-glutamyl transpeptidase (leggt), which are implicated in biosynthesis of the organosulfur flavor compound lenthionine, have diversified inLentinula. Paralogs of both genes that are unique toLentinula(lecsl3 andleggt5b) are coordinately up-regulated in fruiting bodies ofL. edodes. The pangenome ofL. edodess. lat. contains 20,308 groups of orthologous genes, but only 6,438 orthogroups (32%) are shared among all strains, whereas 3,444 orthogroups (17%) are found only in wild populations, which should be targeted for conservation. 

Summary The ectomycorrhizal (ECM) symbiosis has independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic signatures of the transition to the ECM habit within the hyperdiverse Russulaceae.We present comparative analyses of the genomic architecture and the total and secreted gene repertoires of 18 species across the order Russulales, of which 13 are newly sequenced, including a representative of a saprotrophic member of Russulaceae,Gloeopeniophorella convolvens.The genomes of ECM Russulaceae are characterized by a loss of genes for plant cell wall‐degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of small secreted proteins (SSPs) with TE ‘nests’, or dense aggregations of TEs. Some PCWDEs have been retained or even expanded, mostly in a species‐specific manner. The genome ofG. convolvenspossesses some characteristics of ECM genomes (e.g. loss of some PCWDEs, TE expansion, reduction in secondary metabolism clusters).Functional specialization in ECM decomposition may drive diversification. Accelerated gene evolution predates the evolution of the ECM habit, indicating that changes in genome architecture and gene content may be necessary to prime the evolutionary switch. 

Abstract Multi‐locus sequence data are widely used in fungal systematic and taxonomic studies to delimit species and infer evolutionary relationships. We developed and assessed the efficacy of a multi‐locus pooled sequencing method using PacBio long‐read high‐throughput sequencing. Samples included fresh and dried voucher specimens, cultures and archival DNA extracts of Agaricomycetes with an emphasis on the order Cantharellales. Of the 283 specimens sequenced, 93.6% successfully amplified at one or more loci with a mean of 3.3 loci amplified. Our method recovered multiple sequence variants representing alleles of rDNA loci and single copy protein‐coding genesrpb1,rpb2 andtef1. Within‐sample genetic variation differed by locus and taxonomic group, with the greatest genetic divergence observed among sequence variants ofrpb2 andtef1 from corticioid Cantharellales. Our method is a cost‐effective approach for generating accurate multi‐locus sequence data coupled with recovery of alleles from polymorphic samples and multi‐organism specimens. These results have important implications for understanding intra‐individual genomic variation among genetic loci commonly used in species delimitation of fungi.