Widespread Enhancer Dememorization and Promoter Priming during Parental-to-Zygotic Transition

Zhang, Bingjie; Wu, Xiaotong; Zhang, Wenhao; Shen, Wei-Min; Sun, Qingrui; Liu, Kaili; Zhang, Yu; Wang, Qiujun; Li, Yuanyuan; Meng, Anming; Xie, Wei

doi:10.1016/j.molcel.2018.10.017

Cited by 66 publications

(109 citation statements)

References 77 publications

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“…Here, we show directly that the increase in accessibility during the earliest stages of zygotic genome activation has a strong predictive value for future transcription. This is in contrast with the absolute level of chromatin accessibility prior to transcription, which does not correlate well with transcription at later stages of zebrafish development [59,63].…”

Section: Pou5f3 Sox19b and Nanog Prime Genes For Activationcontrasting

confidence: 63%

“…Future studies will be required to explore in more detail how Pou5f3, Sox19b and Nanog prime genes for activity. One potential mechanism is that these transcription factors mediate the establishment of H3K27ac at regulatory elements [56,59]. PSN as well as H3K27ac are essential for zygotic genome activation [15,19,59], and the highest H3K27ac enrichment occurs at PSNprimed loci (this study).…”

Section: Pou5f3 Sox19b and Nanog Prime Genes For Activationmentioning

confidence: 82%

“…Our finding that regulatory elements can be accessible prior to transcription of associated genes is in agreement with the establishment of other "active" chromatin features prior to gene expression. At zebrafish promoters, for example, the histone modifications H3K4me3 [57,58] and H3K27ac [56,59], a hypomethylated state ( [25,[60][61][62], and well-positioned nucleosomes [63] can be established prior to the time their associated genes become expressed. Similar observations have been made in other species.…”

Section: Chromatin Accessibility Precedes Transcriptional Activitymentioning

confidence: 99%

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Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

Pálfy

Schulze

Valen

et al. 2019

Preprint

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In many organisms, early embryonic development is driven by maternally provided factors until the controlled onset of transcription during zygotic genome activation. The regulation of chromatin accessibility and its relationship to gene activity during this transition remains poorly understood. Here, we generated chromatin accessibility maps from genome activation until the onset of lineage specification. During this period, chromatin accessibility increases at regulatory elements. This increase is independent of RNA polymerase II-mediated transcription, with the exception of the hyper-transcribed miR-430 locus. Instead, accessibility often precedes the transcription of associated genes. Loss of the maternal transcription factors Pou5f3, Sox19b, and Nanog, which are known to be required for zebrafish genome activation, results in decreased accessibility at regulatory elements. Importantly, the accessibility of regulatory regions, especially when established by Pou5f3, Sox19b and Nanog, is predictive for future transcription.Our results show that the maternally provided transcription factors Pou5f3, Sox19b, and Nanog open up chromatin and prime genes for activity during zygotic genome activation in zebrafish.

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Section: Pou5f3 Sox19b and Nanog Prime Genes For Activationcontrasting

confidence: 63%

Section: Pou5f3 Sox19b and Nanog Prime Genes For Activationmentioning

confidence: 82%

Section: Chromatin Accessibility Precedes Transcriptional Activitymentioning

confidence: 99%

See 1 more Smart Citation

Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

Pálfy

Schulze

Valen

et al. 2019

Preprint

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“…While vertebrate embryogenesis requires extensive erasing and rewriting of active histone marks during developmental transitions (Dahl et al 2016;Zheng et al 2016;Zhang et al 2018), our chromatin maps and enrichment analysis suggest that the histone modification status of early embryonic promoters (4-8 cell, pre-gastrula stage) appear to be retained, not erased, in somatic tissues of differentiated embryos. Despite massive changes in mRNA expression programs during C. elegans development (Levin et al 2012;Hashimshony et al 2015;Packer et al 2019a), a large fraction of accessible chromatin domains in the early embryo are maintained throughout late embryo morphogenesis and even into post-embryonic development (Supp.…”

Section: Stable Maintenance Of Pol II Associated Histone Modificationmentioning

confidence: 80%

Persistent chromatin states, pervasive transcription, and sharedcis-regulatory sequences have shaped theC. elegansgenome

Whitehouse

2019

Preprint

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Despite highly conserved chromatin states and cis-regulatory elements, studies of metazoan genomes reveal that gene organization and the strategies to control mRNA expression can vary widely among animal species. C. elegans gene regulation is often assumed to be similar to that of other model organisms, yet evidence suggests the existence of distinct molecular mechanisms to pattern the developmental transcriptome, including extensive post-transcriptional RNA control pathways, widespread splice leader (SL) trans-splicing of pre-mRNAs, and the organization of genes into operons. Here, we performed ChIP-seq for histone modifications in highly synchronized embryos cohorts representing three major developmental stages, with the goal of better characterizing whether the dynamic changes in embryonic mRNA expression are accompanied by changes to the chromatin state. We were surprised to find that thousands of promoters are persistently marked by active histone modifications, despite a fundamental restructuring of the transcriptome. We employed global run-on sequencing using a long-read nanopore format to map nascent RNA transcription across embryogenesis, finding that the invariant open chromatin regions are persistently transcribed by Pol II at all stages of embryo development, even though the mature mRNA is not produced. By annotating our nascent RNA sequencing reads into directional transcription units, we find extensive evidence of polycistronic RNA transcription genome-wide, suggesting that nearby genes in C. elegans are linked by shared transcriptional regulatory mechanisms. We present data indicating that the sharing of cisregulatory sequences has constrained C. elegans gene positioning and likely explains the remarkable retention of syntenic gene pairs over long evolutionary timescales.

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“…Occupancy of those genes by H3K4me3 prior to ZGA was suggested to pre-pattern developmental gene expression (Lindeman et al, 2011). A recent report has also shown dynamic changes of H3 Lys27 acetylation (H3K27ac) at promoters and enhancers before and after zebrafish ZGA by ChIP-seq (Zhang et al, 2018). However, the spatiotemporal dynamics of transcription and histone modifications remain unclear because appropriate tools are lacking.…”

Section: Introductionmentioning

confidence: 99%

Quantitative measurements of chromatin modification dynamics during zygotic genome activation

Sato

Hilbert

Oda

et al. 2019

Preprint

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Histone posttranslational modifications (PTMs) are key gene expression regulators, but their rapid dynamics during development remain difficult to capture. We describe an approach that images fluorescent antibody fragments to quantify PTM enrichment and active transcription at defined loci during zygotic genome activation in living zebrafish embryos. The technique reveals a drastic increase in histone H3 Lys27 acetylation (H3K27ac) before genome activation both at a specific locus and globally.

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Widespread Enhancer Dememorization and Promoter Priming during Parental-to-Zygotic Transition

Cited by 66 publications

References 77 publications

Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

Persistent chromatin states, pervasive transcription, and sharedcis-regulatory sequences have shaped theC. elegansgenome

Quantitative measurements of chromatin modification dynamics during zygotic genome activation

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