The landscape of accessible chromatin in bovine oocytes and early embryos

Chromatin reorganization governs the regulation of gene expression during preimplantation development. However, the landscape of chromatin dynamics in this period has not been explored in bovine. In this study, we constructed a genome-wide map of accessible chromatin in bovine oocytes and early embr...

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Main Authors: Hao Ming, Jiangwen Sun, Rolando Pasquariello, Lauren Gatenby, Jason R Herrick, Ye Yuan, Carlos R Pinto, Kenneth R Bondioli, Rebecca L Krisher, Zongliang Jiang
Format: Article
Language:English
Published: Taylor & Francis Group 2021-03-01
Series:Epigenetics
Subjects:
Online Access:http://dx.doi.org/10.1080/15592294.2020.1795602
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author Hao Ming
Jiangwen Sun
Rolando Pasquariello
Lauren Gatenby
Jason R Herrick
Ye Yuan
Carlos R Pinto
Kenneth R Bondioli
Rebecca L Krisher
Zongliang Jiang
author_facet Hao Ming
Jiangwen Sun
Rolando Pasquariello
Lauren Gatenby
Jason R Herrick
Ye Yuan
Carlos R Pinto
Kenneth R Bondioli
Rebecca L Krisher
Zongliang Jiang
author_sort Hao Ming
collection DOAJ
description Chromatin reorganization governs the regulation of gene expression during preimplantation development. However, the landscape of chromatin dynamics in this period has not been explored in bovine. In this study, we constructed a genome-wide map of accessible chromatin in bovine oocytes and early embryos using an improved assay for transposase-accessible chromatin with high-throughput sequencing (ATAC-seq) which revealed unique features of the accessible chromatin during bovine early embryo development. We found that chromatin accessibility is low in oocytes and 2-/4-cell embryos, followed by a significant increase in embryos during major embryonic genome activation (EGA), and peaked in elongating day 14 embryos. Genome-wide characteristics of open chromatin showed that ATAC-seq signals in both transcription start sites (TSS) and transcription end sites (TES) were strong. Additionally, the distal ATAC-seq peaks were enriched in repeat elements in a type-specific and stage-specific manner. We further unveiled a series of transcription factor (TF) motifs with distinct variation of enrichment from distal ATAC-seq peaks. By integrated analysis of chromatin accessibility with transcriptomes and DNA methylomes in bovine early embryos, we showed that promoter accessibility was positively correlated with gene expression, especially during major EGA, and was strongly correlated to DNA methylation and CpG density. Finally, we identified the critical chromatin signatures and TFs that differ between in vivo and in vitro derived blastocysts, which provides insights to the potential mechanisms leading to low quality of embryos produced in vitro. Together, this comprehensive analysis revealed critical features of chromatin landscape and epigenetic reprogramming during bovine preimplantation embryo development.
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spelling doaj.art-a2d65c2e14ac4293bb22320ab2aa6e162023-09-21T13:09:24ZengTaylor & Francis GroupEpigenetics1559-22941559-23082021-03-0116330031210.1080/15592294.2020.17956021795602The landscape of accessible chromatin in bovine oocytes and early embryosHao Ming0Jiangwen Sun1Rolando Pasquariello2Lauren Gatenby3Jason R Herrick4Ye Yuan5Carlos R Pinto6Kenneth R Bondioli7Rebecca L Krisher8Zongliang Jiang9AgCenter, Louisiana State UniversityOld Dominion UniversityColorado Center for Reproductive MedicineAgCenter, Louisiana State UniversityColorado Center for Reproductive MedicineColorado Center for Reproductive MedicineSchool of Veterinary Medicine, Louisiana State UniversityAgCenter, Louisiana State UniversityColorado Center for Reproductive MedicineAgCenter, Louisiana State UniversityChromatin reorganization governs the regulation of gene expression during preimplantation development. However, the landscape of chromatin dynamics in this period has not been explored in bovine. In this study, we constructed a genome-wide map of accessible chromatin in bovine oocytes and early embryos using an improved assay for transposase-accessible chromatin with high-throughput sequencing (ATAC-seq) which revealed unique features of the accessible chromatin during bovine early embryo development. We found that chromatin accessibility is low in oocytes and 2-/4-cell embryos, followed by a significant increase in embryos during major embryonic genome activation (EGA), and peaked in elongating day 14 embryos. Genome-wide characteristics of open chromatin showed that ATAC-seq signals in both transcription start sites (TSS) and transcription end sites (TES) were strong. Additionally, the distal ATAC-seq peaks were enriched in repeat elements in a type-specific and stage-specific manner. We further unveiled a series of transcription factor (TF) motifs with distinct variation of enrichment from distal ATAC-seq peaks. By integrated analysis of chromatin accessibility with transcriptomes and DNA methylomes in bovine early embryos, we showed that promoter accessibility was positively correlated with gene expression, especially during major EGA, and was strongly correlated to DNA methylation and CpG density. Finally, we identified the critical chromatin signatures and TFs that differ between in vivo and in vitro derived blastocysts, which provides insights to the potential mechanisms leading to low quality of embryos produced in vitro. Together, this comprehensive analysis revealed critical features of chromatin landscape and epigenetic reprogramming during bovine preimplantation embryo development.http://dx.doi.org/10.1080/15592294.2020.1795602accessible chromatinatac-seqoocytesembryosbovine
spellingShingle Hao Ming
Jiangwen Sun
Rolando Pasquariello
Lauren Gatenby
Jason R Herrick
Ye Yuan
Carlos R Pinto
Kenneth R Bondioli
Rebecca L Krisher
Zongliang Jiang
The landscape of accessible chromatin in bovine oocytes and early embryos
Epigenetics
accessible chromatin
atac-seq
oocytes
embryos
bovine
title The landscape of accessible chromatin in bovine oocytes and early embryos
title_full The landscape of accessible chromatin in bovine oocytes and early embryos
title_fullStr The landscape of accessible chromatin in bovine oocytes and early embryos
title_full_unstemmed The landscape of accessible chromatin in bovine oocytes and early embryos
title_short The landscape of accessible chromatin in bovine oocytes and early embryos
title_sort landscape of accessible chromatin in bovine oocytes and early embryos
topic accessible chromatin
atac-seq
oocytes
embryos
bovine
url http://dx.doi.org/10.1080/15592294.2020.1795602
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