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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...
Autores principales: | , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Elsevier
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9091725/ https://www.ncbi.nlm.nih.gov/pubmed/35572413 http://dx.doi.org/10.1016/j.jare.2021.09.008 |
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author | Zhang, Jingcheng Shen, Nan Li, Chuang Xiang, Xingjie Liu, Gaolei Gui, Ying Patev, Sean Hibbett, David S. Barry, Kerrie Andreopoulos, William Lipzen, Anna Riley, Robert He, Guifen Yan, Mi Grigoriev, Igor V. Shan Kwan, Hoi Kit Cheung, Man Bian, Yinbing Xiao, Yang |
author_facet | Zhang, Jingcheng Shen, Nan Li, Chuang Xiang, Xingjie Liu, Gaolei Gui, Ying Patev, Sean Hibbett, David S. Barry, Kerrie Andreopoulos, William Lipzen, Anna Riley, Robert He, Guifen Yan, Mi Grigoriev, Igor V. Shan Kwan, Hoi Kit Cheung, Man Bian, Yinbing Xiao, Yang |
author_sort | Zhang, Jingcheng |
collection | PubMed |
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. |
format | Online Article Text |
id | pubmed-9091725 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Elsevier |
record_format | MEDLINE/PubMed |
spelling | pubmed-90917252022-05-12 Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes Zhang, Jingcheng Shen, Nan Li, Chuang Xiang, Xingjie Liu, Gaolei Gui, Ying Patev, Sean Hibbett, David S. Barry, Kerrie Andreopoulos, William Lipzen, Anna Riley, Robert He, Guifen Yan, Mi Grigoriev, Igor V. Shan Kwan, Hoi Kit Cheung, Man Bian, Yinbing Xiao, Yang J Adv Res Basic and Biological Science 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. Elsevier 2021-09-28 /pmc/articles/PMC9091725/ /pubmed/35572413 http://dx.doi.org/10.1016/j.jare.2021.09.008 Text en © 2022 The Authors. Published by Elsevier B.V. on behalf of Cairo University. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Basic and Biological Science Zhang, Jingcheng Shen, Nan Li, Chuang Xiang, Xingjie Liu, Gaolei Gui, Ying Patev, Sean Hibbett, David S. Barry, Kerrie Andreopoulos, William Lipzen, Anna Riley, Robert He, Guifen Yan, Mi Grigoriev, Igor V. Shan Kwan, Hoi Kit Cheung, Man Bian, Yinbing Xiao, Yang Population genomics provides insights into the genetic basis of adaptive evolution in the mushroom-forming fungus Lentinula edodes |
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 | Basic and Biological Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9091725/ https://www.ncbi.nlm.nih.gov/pubmed/35572413 http://dx.doi.org/10.1016/j.jare.2021.09.008 |
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