Altered chromatin architecture and gene expression during polyploidization and domestication of soybean

Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes in genomic structure and gene expression. The 3D structure of the genome is intricately linked to gene expression, but its role in transcript...

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Published inThe Plant cell Vol. 33; no. 5; pp. 1430 - 1446
Main Authors Wang, Longfei, Jia, Guanghong, Jiang, Xinyu, Cao, Shuai, Chen, Z Jeffrey, Song, Qingxin
Format Journal Article
LanguageEnglish
Published England Oxford University Press 02.07.2021
Subjects
Chromatin - chemistry
Chromosomes, Plant - genetics
Diploidy
Domestication
Gene Duplication
Gene Expression Regulation, Plant
Genome, Plant
Glycine max - anatomy & histology
Glycine max - genetics
Large-Scale Biology
Phaseolus - genetics
Polyploidy
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Abstract Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes in genomic structure and gene expression. The 3D structure of the genome is intricately linked to gene expression, but its role in transcription regulation following polyploidy and domestication remains unclear. Here, we generated high-resolution (∼2 kb) Hi-C maps for cultivated soybean (Glycine max), wild soybean (Glycine soja), and common bean (Phaseolus vulgaris). We found polyploidization in soybean may induce architecture changes of topologically associating domains and subsequent diploidization led to chromatin topology alteration around chromosome-rearrangement sites. Compared with single-copy and small-scale duplicated genes, WGD genes displayed more long-range chromosomal interactions and were coupled with higher levels of gene expression and chromatin accessibilities but void of DNA methylation. Interestingly, chromatin loop reorganization was involved in expression divergence of the genes during soybean domestication. Genes with chromatin loops were under stronger artificial selection than genes without loops. These findings provide insights into the roles of dynamic chromatin structures on gene expression during polyploidization, diploidization, and domestication of soybean.
AbstractList Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes in genomic structure and gene expression. The 3D structure of the genome is intricately linked to gene expression, but its role in transcription regulation following polyploidy and domestication remains unclear. Here, we generated high-resolution (∼2 kb) Hi-C maps for cultivated soybean ( Glycine max ), wild soybean ( Glycine soja ), and common bean ( Phaseolus vulgaris ). We found polyploidization in soybean may induce architecture changes of topologically associating domains and subsequent diploidization led to chromatin topology alteration around chromosome-rearrangement sites. Compared with single-copy and small-scale duplicated genes, WGD genes displayed more long-range chromosomal interactions and were coupled with higher levels of gene expression and chromatin accessibilities but void of DNA methylation. Interestingly, chromatin loop reorganization was involved in expression divergence of the genes during soybean domestication. Genes with chromatin loops were under stronger artificial selection than genes without loops. These findings provide insights into the roles of dynamic chromatin structures on gene expression during polyploidization, diploidization, and domestication of soybean. Reorganization of chromatin structure was involved in expression divergence during polyploidization, diploidization, and domestication of soybean.
Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes in genomic structure and gene expression. The 3D structure of the genome is intricately linked to gene expression, but its role in transcription regulation following polyploidy and domestication remains unclear. Here, we generated high-resolution (∼2 kb) Hi-C maps for cultivated soybean (Glycine max), wild soybean (Glycine soja), and common bean (Phaseolus vulgaris). We found polyploidization in soybean may induce architecture changes of topologically associating domains and subsequent diploidization led to chromatin topology alteration around chromosome-rearrangement sites. Compared with single-copy and small-scale duplicated genes, WGD genes displayed more long-range chromosomal interactions and were coupled with higher levels of gene expression and chromatin accessibilities but void of DNA methylation. Interestingly, chromatin loop reorganization was involved in expression divergence of the genes during soybean domestication. Genes with chromatin loops were under stronger artificial selection than genes without loops. These findings provide insights into the roles of dynamic chromatin structures on gene expression during polyploidization, diploidization, and domestication of soybean.
Abstract Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes in genomic structure and gene expression. The 3D structure of the genome is intricately linked to gene expression, but its role in transcription regulation following polyploidy and domestication remains unclear. Here, we generated high-resolution (∼2 kb) Hi-C maps for cultivated soybean (Glycine max), wild soybean (Glycine soja), and common bean (Phaseolus vulgaris). We found polyploidization in soybean may induce architecture changes of topologically associating domains and subsequent diploidization led to chromatin topology alteration around chromosome-rearrangement sites. Compared with single-copy and small-scale duplicated genes, WGD genes displayed more long-range chromosomal interactions and were coupled with higher levels of gene expression and chromatin accessibilities but void of DNA methylation. Interestingly, chromatin loop reorganization was involved in expression divergence of the genes during soybean domestication. Genes with chromatin loops were under stronger artificial selection than genes without loops. These findings provide insights into the roles of dynamic chromatin structures on gene expression during polyploidization, diploidization, and domestication of soybean.
Author Jiang, Xinyu
Chen, Z Jeffrey
Cao, Shuai
Song, Qingxin
Wang, Longfei
Jia, Guanghong
AuthorAffiliation 2 Department of Molecular Biosciences, The University of Texas at Austin , Austin, Texas 78712, USA
1 State Key Laboratory of Crop Genetics and Germplasm Enhancement, Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University , No. 1 Weigang, Nanjing, Jiangsu 210095, China
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  publication-title: Cell
  doi: 10.1016/j.cell.2013.04.053
  contributor:
    fullname: Phillips-Cremins
– volume: 49
  start-page: 579
  year: 2017
  ident: 2023011109351621200_koab081-B61
  article-title: Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication
  publication-title: Nat Genet
  doi: 10.1038/ng.3807
  contributor:
    fullname: Wang
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Snippet Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic changes...
Abstract Polyploidy or whole-genome duplication (WGD) is widespread in plants and is a key driver of evolution and speciation, accompanied by rapid and dynamic...
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StartPage 1430
SubjectTerms Chromatin - chemistry
Chromosomes, Plant - genetics
Diploidy
Domestication
Gene Duplication
Gene Expression Regulation, Plant
Genome, Plant
Glycine max - anatomy & histology
Glycine max - genetics
Large-Scale Biology
Phaseolus - genetics
Polyploidy
Title Altered chromatin architecture and gene expression during polyploidization and domestication of soybean
URI https://www.ncbi.nlm.nih.gov/pubmed/33730165
https://pubmed.ncbi.nlm.nih.gov/PMC8254482
Volume 33
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