Sean Sierra-Patev et al.

PNAS February 27, 2023; 120 (10) e2214076120; https://doi.org/10.1073/pnas.2214076120

Significance

Lentinula is an economically important group of fungi that includes the cultivated shiitake mushroom. We performed a comparative analysis of shiitake and related species, including 24 new genomes from Asia, Australasia, and the Americas. Lentinula is roughly 28 My old and includes four major groups, three in the Americas and one in Asia–Australasia. Lentinula edodes (shiitake) comprises three independent lineages that may warrant recognition as species. One lineage of L. edodes is represented by a single Nepalese isolate, while the others are broadly distributed across East and Southeast Asia and show evidence of hybridization. Genes that encode enzymes responsible for biosynthesis of sulfur-containing compounds have expanded in Lentinula and may contribute to the distinctive flavor of shiitake mushrooms.

Abstract

Lentinula is 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 of Lentinula from 15 countries on four continents. Lentinula 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 L. edodes from China that were previously published as raw Illumina reads and added them to our dataset. Lentinula edodes 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 L. edodes 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 (lecsl) and γ-glutamyl transpeptidase (leggt), which are implicated in biosynthesis of the organosulfur flavor compound lenthionine, have diversified in Lentinula. Paralogs of both genes that are unique to Lentinula (lecsl 3 and leggt 5b) are coordinately up-regulated in fruiting bodies of L. edodes. The pangenome of L. edodes 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.

See https://www.pnas.org/doi/10.1073/pnas.2214076120

Figure 1: Genome characteristics of Lentinula. (A) Nonrepeat regions and number of genes. The vertical lines indicate the average sizes of the groups. (B) Repeat contents of the eight PacBio assemblies. Repeat regions were estimated using the JGI annotation pipeline. LTR: long terminal repeats.