A global phylogenomic analysis of the shiitake genus <i>Lentinula</i>

<i>Lentinula</i> is a broadly distributed group of fungi that contains the cultivated shiitake mushroom, <i>L. edodes</i>. We sequenced 24 genomes representing eight described species and several unnamed lineages of <i>Lentinula</i> from 15 countries on four continents. <i>Lentinula</i> comprises 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 of <i>L. edodes</i> from China that were previously published as raw Illumina reads and added them to our dataset. <i>Lentinula edodes</i> sensu 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 of <i>L. edodes</i> s. 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 (<i>lecsl</i>) and γ-glutamyl transpeptidase (<i>leggt</i>), which are implicated in biosynthesis of the organosulfur flavor compound lenthionine, have diversified in <i>Lentinula</i>. Paralogs of both genes that are unique to <i>Lentinula</i> (<i>lecsl</i> 3 and <i>leggt</i> 5b) are coordinately up-regulated in fruiting bodies of <i>L. edodes</i>. The pangenome of <i>L. edodes</i> s. 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.