Chromatin loop anchors contain core structural components of the gene expression machinery in maize
Abstract Background Three-dimensional chromatin loop structures connect regulatory elements to their target genes in regions known as anchors. In complex plant genomes, such as maize, it has been proposed that loops span heterochromatic regions marked by higher repeat content, but little is known on...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2021-01-01
|
Series: | BMC Genomics |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12864-020-07324-0 |
id |
doaj-9a1084fd569f4e07bd8950facbe5ee31 |
---|---|
record_format |
Article |
spelling |
doaj-9a1084fd569f4e07bd8950facbe5ee312021-01-10T12:33:57ZengBMCBMC Genomics1471-21642021-01-0122111210.1186/s12864-020-07324-0Chromatin loop anchors contain core structural components of the gene expression machinery in maizeStéphane Deschamps0John A. Crow1Nadia Chaidir2Brooke Peterson-Burch3Sunil Kumar4Haining Lin5Gina Zastrow-Hayes6Gregory D. May7Corteva AgriscienceCorteva AgriscienceCorteva AgriscienceCorteva AgriscienceCorteva Agriscience, The V-AcendasCorteva AgriscienceCorteva AgriscienceCorteva AgriscienceAbstract Background Three-dimensional chromatin loop structures connect regulatory elements to their target genes in regions known as anchors. In complex plant genomes, such as maize, it has been proposed that loops span heterochromatic regions marked by higher repeat content, but little is known on their spatial organization and genome-wide occurrence in relation to transcriptional activity. Results Here, ultra-deep Hi-C sequencing of maize B73 leaf tissue was combined with gene expression and open chromatin sequencing for chromatin loop discovery and correlation with hierarchical topologically-associating domains (TADs) and transcriptional activity. A majority of all anchors are shared between multiple loops from previous public maize high-resolution interactome datasets, suggesting a highly dynamic environment, with a conserved set of anchors involved in multiple interaction networks. Chromatin loop interiors are marked by higher repeat contents than the anchors flanking them. A small fraction of high-resolution interaction anchors, fully embedded in larger chromatin loops, co-locate with active genes and putative protein-binding sites. Combinatorial analyses indicate that all anchors studied here co-locate with at least 81.5% of expressed genes and 74% of open chromatin regions. Approximately 38% of all Hi-C chromatin loops are fully embedded within hierarchical TAD-like domains, while the remaining ones share anchors with domain boundaries or with distinct domains. Those various loop types exhibit specific patterns of overlap for open chromatin regions and expressed genes, but no apparent pattern of gene expression. In addition, up to 63% of all unique variants derived from a prior public maize eQTL dataset overlap with Hi-C loop anchors. Anchor annotation suggests that < 7% of all loops detected here are potentially devoid of any genes or regulatory elements. The overall organization of chromatin loop anchors in the maize genome suggest a loop modeling system hypothesized to resemble phase separation of repeat-rich regions. Conclusions Sets of conserved chromatin loop anchors mapping to hierarchical domains contains core structural components of the gene expression machinery in maize. The data presented here will be a useful reference to further investigate their function in regard to the formation of transcriptional complexes and the regulation of transcriptional activity in the maize genome.https://doi.org/10.1186/s12864-020-07324-0MaizeChromatinLoopAnchorTADDomain |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Stéphane Deschamps John A. Crow Nadia Chaidir Brooke Peterson-Burch Sunil Kumar Haining Lin Gina Zastrow-Hayes Gregory D. May |
spellingShingle |
Stéphane Deschamps John A. Crow Nadia Chaidir Brooke Peterson-Burch Sunil Kumar Haining Lin Gina Zastrow-Hayes Gregory D. May Chromatin loop anchors contain core structural components of the gene expression machinery in maize BMC Genomics Maize Chromatin Loop Anchor TAD Domain |
author_facet |
Stéphane Deschamps John A. Crow Nadia Chaidir Brooke Peterson-Burch Sunil Kumar Haining Lin Gina Zastrow-Hayes Gregory D. May |
author_sort |
Stéphane Deschamps |
title |
Chromatin loop anchors contain core structural components of the gene expression machinery in maize |
title_short |
Chromatin loop anchors contain core structural components of the gene expression machinery in maize |
title_full |
Chromatin loop anchors contain core structural components of the gene expression machinery in maize |
title_fullStr |
Chromatin loop anchors contain core structural components of the gene expression machinery in maize |
title_full_unstemmed |
Chromatin loop anchors contain core structural components of the gene expression machinery in maize |
title_sort |
chromatin loop anchors contain core structural components of the gene expression machinery in maize |
publisher |
BMC |
series |
BMC Genomics |
issn |
1471-2164 |
publishDate |
2021-01-01 |
description |
Abstract Background Three-dimensional chromatin loop structures connect regulatory elements to their target genes in regions known as anchors. In complex plant genomes, such as maize, it has been proposed that loops span heterochromatic regions marked by higher repeat content, but little is known on their spatial organization and genome-wide occurrence in relation to transcriptional activity. Results Here, ultra-deep Hi-C sequencing of maize B73 leaf tissue was combined with gene expression and open chromatin sequencing for chromatin loop discovery and correlation with hierarchical topologically-associating domains (TADs) and transcriptional activity. A majority of all anchors are shared between multiple loops from previous public maize high-resolution interactome datasets, suggesting a highly dynamic environment, with a conserved set of anchors involved in multiple interaction networks. Chromatin loop interiors are marked by higher repeat contents than the anchors flanking them. A small fraction of high-resolution interaction anchors, fully embedded in larger chromatin loops, co-locate with active genes and putative protein-binding sites. Combinatorial analyses indicate that all anchors studied here co-locate with at least 81.5% of expressed genes and 74% of open chromatin regions. Approximately 38% of all Hi-C chromatin loops are fully embedded within hierarchical TAD-like domains, while the remaining ones share anchors with domain boundaries or with distinct domains. Those various loop types exhibit specific patterns of overlap for open chromatin regions and expressed genes, but no apparent pattern of gene expression. In addition, up to 63% of all unique variants derived from a prior public maize eQTL dataset overlap with Hi-C loop anchors. Anchor annotation suggests that < 7% of all loops detected here are potentially devoid of any genes or regulatory elements. The overall organization of chromatin loop anchors in the maize genome suggest a loop modeling system hypothesized to resemble phase separation of repeat-rich regions. Conclusions Sets of conserved chromatin loop anchors mapping to hierarchical domains contains core structural components of the gene expression machinery in maize. The data presented here will be a useful reference to further investigate their function in regard to the formation of transcriptional complexes and the regulation of transcriptional activity in the maize genome. |
topic |
Maize Chromatin Loop Anchor TAD Domain |
url |
https://doi.org/10.1186/s12864-020-07324-0 |
work_keys_str_mv |
AT stephanedeschamps chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT johnacrow chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT nadiachaidir chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT brookepetersonburch chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT sunilkumar chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT haininglin chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT ginazastrowhayes chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize AT gregorydmay chromatinloopanchorscontaincorestructuralcomponentsofthegeneexpressionmachineryinmaize |
_version_ |
1724342681369313280 |