A global phylogenomic analysis of the shiitake genus Lentinula

Author:

Sierra-Patev Sean1,Min Byoungnam2ORCID,Naranjo-Ortiz Miguel1,Looney Brian1,Konkel Zachary3ORCID,Slot Jason C.3ORCID,Sakamoto Yuichi4,Steenwyk Jacob L.5ORCID,Rokas Antonis5ORCID,Carro Juan6ORCID,Camarero Susana6ORCID,Ferreira Patricia78ORCID,Molpeceres Gonzalo6ORCID,Ruiz-Dueñas Francisco J.6ORCID,Serrano Ana6,Henrissat Bernard910,Drula Elodie1112ORCID,Hughes Karen W.13ORCID,Mata Juan L.14ORCID,Ishikawa Noemia Kazue15ORCID,Vargas-Isla Ruby15ORCID,Ushijima Shuji16,Smith Chris A.17,Donoghue John18ORCID,Ahrendt Steven2,Andreopoulos William2ORCID,He Guifen2,LaButti Kurt2ORCID,Lipzen Anna2ORCID,Ng Vivian2ORCID,Riley Robert2ORCID,Sandor Laura2,Barry Kerrie2,Martínez Angel T.6ORCID,Xiao Yang19ORCID,Gibbons John G.20ORCID,Terashima Kazuhisa16,Grigoriev Igor V.221ORCID,Hibbett David1ORCID

Affiliation:

1. Biology Department, Clark University, Worcester, MA 01610

2. U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720

3. Department of Plant Pathology, Ohio State University, Columbus, OH 43210

4. Iwate Biotechnology Research Center, Kitakami, Iwate 024-0003, Japan

5. Department of Biological Sciences and Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235

6. Centro de Investigaciones Biológicas “Margarita Salas,” Consejo Superior de Investigaciones Científicas, Madrid E-28040, Spain

7. Department of Biochemistry and Molecular and Cellular Biology, University of Zaragoza, 50009 Zaragoza, Spain

8. Institute of Biocomputation and Physics of Complex Systems, University of Zaragoza, 50018 Zaragoza, Spain

9. DTU Bioengineering, Technical University of Denmark 2800, Kgs. Lyngby, Denmark

10. Department of Biological Sciences, King Abdulaziz University, Jeddah 21589, Saudi Arabia

11. Architecture et Fonction des Macromolécules Biologiques, CNRS, Université 13288, Marseille, France

12. INRAE, UMR 1163, Biodiversité et Biotechnologie Fongiques 13009, Marseille, France

13. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996

14. Department of Biology, University of South Alabama, Mobile, AL 36688

15. Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Petrópolis, Manaus AM 69067-375, Brazil

16. The Tottori Mycological Institute, Japan Kinoko Research Center Foundation, Tottori 689-1125, Japan

17. Manaaki Whenua - Landcare Research, Auckland 1072, New Zealand

18. Northwest Mycological Consultants, Corvallis, OR 97330

19. Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei 430070, China

20. Department of Food Science, University of Massachusetts, Amherst, MA 01003

21. Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720

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.

Funder

National Science Foundation

U.S. Department of Energy

Spanish Ministry of Science & Innovation

HHS | National Institutes of Health

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

Reference82 articles.

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2. The biogeographical speciations of shiitake Lentinula edodes and a new species Lentinula platinedodes sp. nov. found in Cat Tien, South Vietnam;Tham L. X.;Acad. J. Biol.,2012

3. Lentinula madagasikarensis sp. nov., a relative of shiitake mushrooms from Madagascar;Looney B. P.;Fungal Syst. Evol.,2021

4. A new species of Lentinula (Agaricales) from Central America

5. The genus Lentinula in the Americas

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