A global phylogenomic analysis of the shiitake genus Lentinula

Sean Sierra-Patev, Byoungnam Min, Miguel Naranjo-Ortiz, Brian Looney, Zachary Konkel, Jason C. Slot, Yuichi Sakamoto, Jacob L. Steenwyk, Antonis Rokas, Juan Carro, Susana Camarero, Patricia Ferreira, Gonzalo Molpeceres, Francisco J. Ruiz-Dueñas, Ana Serrano, Bernard Henrissat, Elodie Drula, Karen W. Hughes, Juan L. Mata, Noemia Kazue IshikawaRuby Vargas-Isla, Shuji Ushijima, Chris A. Smith, John Donoghue, Steven Ahrendt, William Andreopoulos, Guifen He, Kurt LaButti, Anna Lipzen, Vivian Ng, Robert Riley, Laura Sandor, Kerrie Barry, Angel T. Martínez, Yang Xiao, John G. Gibbons, Kazuhisa Terashima, Igor V. Grigoriev, David Hibbett*

*Corresponding author for this work

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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.
Original languageEnglish
Article numbere2214076120
JournalProceedings of the National Academy of Sciences of the United States of America
Volume120
Issue number10
Number of pages10
ISSN0027-8424
DOIs
Publication statusPublished - 2023

Keywords

  • Fungi
  • Domestication
  • Mushrooms
  • Evolution
  • Population genomics

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