Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes

Jingcheng Zhang; Nan Shen; Chuang Li; Xingjie Xiang; Gaolei Liu; Ying Gui; Sean Patev; David S. Hibbett; Kerrie Barry; William Andreopoulos; Anna Lipzen; Robert Riley; Guifen He; Mi Yan; Igor V. Grigoriev; Hoi Shan Kwan; Man Kit Cheung; Yinbing Bian; Yang Xiao

Journal of Advanced Research (May 2022)

Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes

Jingcheng Zhang,
Nan Shen,
Chuang Li,
Xingjie Xiang,
Gaolei Liu,
Ying Gui,
Sean Patev,
David S. Hibbett,
Kerrie Barry,
William Andreopoulos,
Anna Lipzen,
Robert Riley,
Guifen He,
Mi Yan,
Igor V. Grigoriev,
Hoi Shan Kwan,
Man Kit Cheung,
Yinbing Bian,
Yang Xiao

Affiliations

Jingcheng Zhang: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Nan Shen: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Chuang Li: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Xingjie Xiang: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Gaolei Liu: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Ying Gui: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Sean Patev: Department of Biology, Clark University, Worcester, MA, USA
David S. Hibbett: Department of Biology, Clark University, Worcester, MA, USA
Kerrie Barry: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
William Andreopoulos: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Anna Lipzen: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Robert Riley: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Guifen He: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Mi Yan: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Igor V. Grigoriev: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA; Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
Hoi Shan Kwan: School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative Region
Man Kit Cheung: School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative Region
Yinbing Bian: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China
Yang Xiao: Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China; Corresponding author.

Journal volume & issue: Vol. 38
pp. 91 – 106

Abstract

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Introduction: Mushroom-forming fungi comprise diverse species that develop complex multicellular structures. In cultivated species, both ecological adaptation and artificial selection have driven genome evolution. However, little is known about the connections among genotype, phenotype and adaptation in mushroom-forming fungi. Objectives: This study aimed to (1) uncover the population structure and demographic history of Lentinula edodes, (2) dissect the genetic basis of adaptive evolution in L. edodes, and (3) determine if genes related to fruiting body development are involved in adaptive evolution. Methods: We analyzed genomes and fruiting body-related traits (FBRTs) in 133 L. edodes strains and conducted RNA-seq analysis of fruiting body development in the YS69 strain. Combined methods of genomic scan for divergence, genome-wide association studies (GWAS), and RNA-seq were used to dissect the genetic basis of adaptive evolution. Results: We detected three distinct subgroups of L. edodes via single nucleotide polymorphisms, which showed robust phenotypic and temperature response differentiation and correlation with geographical distribution. Demographic history inference suggests that the subgroups diverged 36,871 generations ago. Moreover, L. edodes cultivars in China may have originated from the vicinity of Northeast China. A total of 942 genes were found to be related to genetic divergence by genomic scan, and 719 genes were identified to be candidates underlying FBRTs by GWAS. Integrating results of genomic scan and GWAS, 80 genes were detected to be related to phenotypic differentiation. A total of 364 genes related to fruiting body development were involved in genetic divergence and phenotypic differentiation. Conclusion: Adaptation to the local environment, especially temperature, triggered genetic divergence and phenotypic differentiation of L. edodes. A general model for genetic divergence and phenotypic differentiation during adaptive evolution in L. edodes, which involves in signal perception and transduction, transcriptional regulation, and fruiting body morphogenesis, was also integrated here.

Published in Journal of Advanced Research

ISSN: 2090-1232 (Print); 2090-1224 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General); Science: Science (General)
Website: http://www.journals.elsevier.com/journal-of-advanced-research/

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