Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes
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 adaptatio...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-05-01
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| Series: | Journal of Advanced Research |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2090123221001892 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Jingcheng Zhang |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T11:31:35Z |
| format | Article |
| id | doaj.art-f5b4a974288c40aeaa10d3f25646c23e |
| institution | Directory Open Access Journal |
| issn | 2090-1232 |
| language | English |
| last_indexed | 2024-04-12T11:31:35Z |
| publishDate | 2022-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Advanced Research |
| spelling | doaj.art-f5b4a974288c40aeaa10d3f25646c23e2022-12-22T03:35:01ZengElsevierJournal of Advanced Research2090-12322022-05-013891106Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodesJingcheng Zhang0Nan Shen1Chuang Li2Xingjie Xiang3Gaolei Liu4Ying Gui5Sean Patev6David S. Hibbett7Kerrie Barry8William Andreopoulos9Anna Lipzen10Robert Riley11Guifen He12Mi Yan13Igor V. Grigoriev14Hoi Shan Kwan15Man Kit Cheung16Yinbing Bian17Yang Xiao18Institute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaDepartment of Biology, Clark University, Worcester, MA, USADepartment of Biology, Clark University, Worcester, MA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA; Department of Plant and Microbial Biology, University of California, Berkeley, CA, USASchool of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative RegionSchool of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative RegionInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, ChinaInstitute of Applied Mycology, Huazhong Agricultural University, Wuhan, Hubei, China; Corresponding author.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.http://www.sciencedirect.com/science/article/pii/S2090123221001892ShiitakePopulation genomicsAdaptationGenetic divergenceGWASPhenotypic differentiation |
| spellingShingle | 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 Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes Journal of Advanced Research Shiitake Population genomics Adaptation Genetic divergence GWAS Phenotypic differentiation |
| title | Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
| title_full | Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
| title_fullStr | Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
| title_full_unstemmed | Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
| title_short | Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
| title_sort | population genomics provides insights into the genetic basis of adaptive evolution in the mushroom forming fungus lentinula edodes |
| topic | Shiitake Population genomics Adaptation Genetic divergence GWAS Phenotypic differentiation |
| url | http://www.sciencedirect.com/science/article/pii/S2090123221001892 |
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