scholarly journals Establishment of developmental gene silencing by ordered polycomb complex recruitment in early zebrafish embryos

eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Graham JM Hickey ◽  
Candice L Wike ◽  
Xichen Nie ◽  
Yixuan Guo ◽  
Mengyao Tan ◽  
...  
Keyword(s):  
Zebrafish Embryos ◽  
Dna Hypomethylation ◽  
Developmental Gene ◽  
Developmental Genes ◽  
Chromatin States ◽  
Vertebrate Embryos ◽  
Polycomb Repressive Complex 1 ◽  
Genome Activation ◽  
Polycomb Complex ◽  
Zygotic Genome

Vertebrate embryos achieve developmental competency during zygotic genome activation (ZGA) by establishing chromatin states that silence yet poise developmental genes for subsequent lineage-specific activation. Here, we reveal the order of chromatin states in establishing developmental gene poising in preZGA zebrafish embryos. Poising is established at promoters and enhancers that initially contain open/permissive chromatin with 'Placeholder' nucleosomes (bearing H2A.Z, H3K4me1, and H3K27ac), and DNA hypomethylation. Silencing is initiated by the recruitment of Polycomb Repressive Complex 1 (PRC1), and H2Aub1 deposition by catalytic Rnf2 during preZGA and ZGA stages. During postZGA, H2Aub1 enables Aebp2-containing PRC2 recruitment and H3K27me3 deposition. Notably, preventing H2Aub1 (via Rnf2 inhibition) eliminates recruitment of Aebp2-PRC2 and H3K27me3, and elicits transcriptional upregulation of certain developmental genes during ZGA. However, upregulation is independent of H3K27me3 - establishing H2Aub1 as the critical silencing modification at ZGA. Taken together, we reveal the logic and mechanism for establishing poised/silent developmental genes in early vertebrate embryos.

scholarly journals Establishment of Developmental Gene Silencing by Ordered Polycomb Complex Recruitment in Early Zebrafish Embryos

2021 ◽  
Author(s):  
Bradley R Cairns ◽  
Graham J.M. Hickey ◽  
Candice Wike ◽  
Xichen Nie ◽  
Yixuan Guo ◽  
...  
Keyword(s):  
De Novo ◽  
Zebrafish Embryos ◽  
Dna Hypomethylation ◽  
Developmental Gene ◽  
Developmental Genes ◽  
Vertebrate Embryos ◽  
Polycomb Repressive Complex 1 ◽  
Genome Activation ◽  
Polycomb Complex ◽  
Zygotic Genome

Vertebrate embryos achieve developmental competency during zygotic genome activation (ZGA) by establishing chromatin states that silence yet poise developmental genes for subsequent lineage-specific activation. Here, we reveal how developmental gene poising is established de novo in preZGA zebrafish embryos. Poising is established at promoters and enhancers that initially contain open/permissive chromatin with 'Placeholder' nucleosomes (bearing H2A.Z, H3K4me1, and H3K27ac), and DNA hypomethylation. Silencing is initiated by the recruitment of Polycomb Repressive Complex 1 (PRC1), and H2Aub1 deposition by catalytic Rnf2 during preZGA and ZGA stages. During postZGA, H2Aub1 enables Aebp2-containing PRC2 recruitment and H3K27me3 deposition. Notably, preventing H2Aub1 (via Rnf2 inhibition) eliminates recruitment of Aebp2-PRC2 and H3K27me3, and elicits transcriptional upregulation of certain developmental genes during ZGA. However, upregulation is independent of H3K27me3 - establishing H2Aub1 as the critical silencing modification at ZGA. Taken together, we reveal the logic and mechanism for establishing poised/silent developmental genes in early vertebrate embryos.

scholarly journals Pluripotency factors select gene expression repertoire at Zygotic Genome Activation

2020 ◽  
Author(s):  
Meijiang Gao ◽  
Marina Veil ◽  
Marcus Rosenblatt ◽  
Anna Gebhard ◽  
Helge Hass ◽  
...  
Keyword(s):  
Gene Expression ◽  
Transcription Factors ◽  
Early Gene ◽  
Zebrafish Embryos ◽  
Fate Specification ◽  
Pluripotency Factors ◽  
Zygotic Transcription ◽  
Simultaneous Loss ◽  
Genome Activation ◽  
Zygotic Genome

AbstractAwakening of zygotic transcription in animal embryos relies on maternal pioneer transcription factors. The interplay of global and specific functions of these proteins remains poorly understood. Here, we analyzed nucleosome positioning, H3K27 acetylation, transcription, and gastrulation rates in zebrafish embryos lacking pluripotency factors Pou5f3 and Sox19b. We show that the bulk transcriptional onset does not require Sox19b and Pou5f3, but is sensitive to their balance. Pou5f3 docks H3K27ac on the enhancers of genes involved in gastrulation and ventral fate specification. Sox19b facilitates Pou5f3 access to one-third of these enhancers. The genes regulating mesendodermal and dorsal fates are primed for activation independently on Pou5f3 and Sox19b. Strikingly, the loss of either factor results in activation of silent enhancers; simultaneous loss of both leads to premature expression of differentiation genes. Our results uncover how independent activities of maternal Pou5f3 and Sox19b add up or antagonize to determine the early gene expression repertoire.

scholarly journals Prepatterning of Developmental Gene Expression by Modified Histones before Zygotic Genome Activation

2011 ◽  
Vol 21 (6) ◽  
pp. 993-1004 ◽  
Author(s):  
Leif C. Lindeman ◽  
Ingrid S. Andersen ◽  
Andrew H. Reiner ◽  
Nan Li ◽  
Håvard Aanes ◽  
...  
Keyword(s):  
Gene Expression ◽  
Zygotic Genome Activation ◽  
Developmental Gene ◽  
Developmental Gene Expression ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals Chiffon triggers global histone H3 acetylation and expression of developmental genes in Drosophila embryos

2021 ◽  
Author(s):  
Eliana F. Torres-Zelada ◽  
Smitha George ◽  
Hannah R. Blum ◽  
Vikki M. Weake
Keyword(s):  
Gene Expression ◽  
Histone Acetylation ◽  
Potential Role ◽  
Developmental Genes ◽  
Histone Acetyltransferase Gcn5 ◽  
Genome Activation ◽  
H3 Acetylation ◽  
Drosophila Embryos ◽  
Cell Cycle Kinase ◽  
Zygotic Genome

The histone acetyltransferase Gcn5 is critical for gene expression and development. In Drosophila, Gcn5 is part of four complexes (SAGA, ATAC, CHAT, and ADA) that are essential for fly viability and have key roles in regulating gene expression. Here, we show that while the SAGA, ADA, and CHAT complexes play redundant roles in embryonic gene expression, the insect-specific CHAT complex uniquely regulates expression of a subset of developmental genes. We also identify a substantial decrease in histone acetylation in chiffon mutant embryos that exceeds that observed in ada2b, suggesting broader roles for Chiffon in regulating histone acetylation outside of the Gcn5 complexes. The chiffon gene encodes two independent polypeptides that nucleate formation of either the CHAT or Dbf4-dependent kinase (DDK) complexes. DDK includes the cell cycle kinase Cdc7, which is necessary for maternally-driven DNA replication in the embryo. We identify a temporal switch between the expression of these chiffon gene products during a short window during the early nuclear cycles in embryos that correlates with the onset of zygotic genome activation, suggesting a potential role for CHAT in this process.

scholarly journals Pervasive non-CpG methylation at zebrafish mosaic satellite repeats

2020 ◽  
Author(s):  
Samuel E Ross ◽  
Allegra Angeloni ◽  
Alex de Mendoza ◽  
Ozren Bogdanovic
Keyword(s):  
Dna Methylation ◽  
Dna Methyltransferases ◽  
Cpg Methylation ◽  
Zebrafish Embryos ◽  
Neural Cells ◽  
Satellite Repeats ◽  
Cg Dinucleotides ◽  
Genome Activation ◽  
Insight Into ◽  
Zygotic Genome

AbstractIn vertebrates, DNA methylation predominantly occurs at CG dinucleotides even though widespread non-CG methylation (mCH) has been reported in mammalian embryonic and neural cells. Unlike in mammals, where mCH is found enriched at CAC/G trinucleotides and is tissue-restricted, we find that zebrafish embryos as well as adult somatic and germline tissues display robust methylation enrichment at TGCT positions associated with mosaic satellite repeats. These repeats reside in H3K9me3-marked heterochromatin and display mCH reprogramming coincident with zygotic genome activation. Altogether, this work provides insight into a novel form of vertebrate mCH and highlights the substrate diversity of vertebrate DNA methyltransferases.

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