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

2019 ◽  
Author(s):  
Máté Pálfy ◽  
Gunnar Schulze ◽  
Eivind Valen ◽  
Nadine L. Vastenhouw
Keyword(s):  
Transcription Factors ◽  
Rna Polymerase ◽  
Rna Polymerase Ii ◽  
Regulatory Elements ◽  
Chromatin Accessibility ◽  
Zebrafish Genome ◽  
Zygotic Genome Activation ◽  
Lineage Specification ◽  
Genome Activation ◽  
Zygotic Genome

ABSTRACTIn 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.

scholarly journals CLAMP and Zelda function together as pioneer transcription factors to promote Drosophila zygotic genome activation

2020 ◽  
Author(s):  
Jingyue Ellie Duan ◽  
Leila E. Rieder ◽  
Annie Huang ◽  
William T. Jordan ◽  
Mary McKenney ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Chromatin Accessibility ◽  
Open Chromatin ◽  
Zygotic Genome Activation ◽  
Early Embryos ◽  
Male Specific Lethal ◽  
Genome Transcription ◽  
Male Specific ◽  
Genome Activation ◽  
Zygotic Genome

ABSTRACTBecause zygotic genome activation (ZGA) is an essential process across metazoans, it is key to evolve multiple pioneer transcription factors (TFs) to protect organisms from loss of a single factor. Pioneer TF Zelda (ZLD) is the only known factor which increases accessibility of chromatin to promote ZGA in the early Drosophila embryo. However, many genomic loci remain accessible without ZLD and have GA-rich motifs. Therefore, we hypothesized that other pioneer TFs that function with ZLD have not yet been identified in early embryos, especially those that bind to GA-rich motifs, such as CLAMP (Chromatin-linked adaptor for Male-specific lethal MSL proteins). Here, we determine that CLAMP is a novel pioneer TF which interacts directly with nucleosomes, regulates zygotic genome transcription, promotes chromatin accessibility, and facilitates the binding of ZLD to promoters. Thus, the maternal factor CLAMP functions with ZLD as a pioneer TF to open chromatin and drive zygotic genome activation.

scholarly journals Endodermal Maternal Transcription Factors Establish Super-Enhancers during Zygotic Genome Activation

Cell Reports ◽  
2019 ◽  
Vol 27 (10) ◽  
pp. 2962-2977.e5 ◽  
Author(s):  
Kitt D. Paraiso ◽  
Ira L. Blitz ◽  
Masani Coley ◽  
Jessica Cheung ◽  
Norihiro Sudou ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Zygotic Genome Activation ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals The miR-430 locus with extreme promoter density is a transcription body organizer, which facilitates long range regulation in zygotic genome activation

2021 ◽  
Author(s):  
Yavor Hadzhiev ◽  
Lucy Wheatley ◽  
Ledean Cooper ◽  
Federico Ansaloni ◽  
Celina Whalley ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
Gene Cluster ◽  
Core Promoter ◽  
Single Copy ◽  
Early Embryo ◽  
Zygotic Genome Activation ◽  
Pol Ii ◽  
A Minor ◽  
Genome Activation ◽  
Zygotic Genome

In anamniote embryos the major wave of zygotic genome activation (ZGA) starts during the mid-blastula transition. This major wave of ZGA is facilitated by several mechanisms, including dilution of repressive maternal factors and accumulation of activating transcription factors during the fast cell division cycles preceding the mid-blastula transition. However, a set of genes escape global genome repression and are activated substantially earlier, during what is called, the minor wave of genome activation. While the mechanisms underlying the major wave of genome activation have been studied extensively, the minor wave of genome activation is little understood. In zebrafish the earliest expressed RNA polymerase II (Pol II) transcribed genes are activated in a pair of large transcription bodies depleted of chromatin, abundant in elongating Pol II and nascent RNAs (Hadzhiev et al., 2019; Hilbert et al., 2021). This transcription body includes the miR-430 gene cluster required for maternal mRNA clearance. Here we explored the genomic, chromatin organisation and cis-regulatory mechanisms of the minor wave of genome activation occurring in the transcription body. By long read genome sequencing we identified a remarkable cluster of miR-430 genes with over 300 promoters and spanning 0.6 Mb, which represent the highest promoter density of the genome. We demonstrate that the miR-430 gene cluster is required for the formation of the transcription body and acts as a transcription organiser for minor wave activation of a set of zinc finger genes scattered on the same chromosome arm, which share promoter features with the miR-430 cluster. These promoter features are shared among minor wave genes overall and include the TATA-box and sharp transcription start site profile. Single copy miR-430 promoter transgene reporter experiments indicate the importance of promoter-autonomous mechanisms regulating escape from global repression of the early embryo. These results together suggest that formation of the transcription body in the early embryo is the result of high promoter density coupled to a minor wave-specific core promoter code for transcribing key minor wave ZGA genes, which are required for the overhaul of the transcriptome during early embryonic development.

Exchanges of histone methylation and variants during mouse zygotic genome activation

Zygote ◽  
2019 ◽  
Vol 28 (1) ◽  
pp. 51-58 ◽  
Author(s):  
Mingtian Deng ◽  
Baobao Chen ◽  
Zifei Liu ◽  
Yu Cai ◽  
Yongjie Wan ◽  
...  
Keyword(s):  
Histone Methylation ◽  
Histone Variants ◽  
Chromatin Accessibility ◽  
Mouse Embryos ◽  
Zygotic Genome Activation ◽  
Male And Female ◽  
Histone 3 ◽  
Female Pronucleus ◽  
Genome Activation ◽  
Zygotic Genome

SummaryMinor and major zygotic genome activation (ZGA) are crucial for preimplantation development. During this process, histone variants and methylation influence chromatin accessibility and consequently regulated the expression of zygotic genes. However, the detailed exchanges of these modifications during ZGA remain to be determined. In the present study, the epigenetic modifications of histone 3 on lysine 9 (H3K9), 27 (H3K27) and 36 (H3K36), as well as four histone variants were determined during minor and major ZGA and in post-ZGA stages of mouse embryos. Firstly, microH2A1, H3K27me3 and H3K36me3 were asymmetrically stained in the female pronucleus during minor ZGA but lost staining in major ZGA. Secondly, H3K9me2 and H3K9me3 were strongly stained in the female pronucleus, but weakly stained in the male pronucleus and disappeared after ZGA. Thirdly, H2A.Z and H3.3 were symmetrically stained in male and female pronuclei during minor ZGA. Moreover, H3K27me2 was not statistically changed during mouse early development, while H3K36me2 was only detected in 2- and 4-cell embryos. In conclusion, our data revealed dynamics of histone methylation and variants during mice ZGA and provided details of their exchange in mice embryogenesis. Moreover, we further inferred that macroH2A1, H2A.Z, H3K9me2/3 and H3K27me2/3 may play crucial roles during mouse ZGA.

scholarly journals Histone variant H2A.Z regulates zygotic genome activation

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Dafne Ibarra-Morales ◽  
Michael Rauer ◽  
Piergiuseppe Quarato ◽  
Leily Rabbani ◽  
Fides Zenk ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
De Novo ◽  
Housekeeping Genes ◽  
Histone Variant ◽  
Small Subset ◽  
Zygotic Genome Activation ◽  
Transcription Start Sites ◽  
Genome Activation ◽  
Zygotic Genome

AbstractDuring embryogenesis, the genome shifts from transcriptionally quiescent to extensively active in a process known as Zygotic Genome Activation (ZGA). In Drosophila, the pioneer factor Zelda is known to be essential for the progression of development; still, it regulates the activation of only a small subset of genes at ZGA. However, thousands of genes do not require Zelda, suggesting that other mechanisms exist. By conducting GRO-seq, HiC and ChIP-seq in Drosophila embryos, we demonstrate that up to 65% of zygotically activated genes are enriched for the histone variant H2A.Z. H2A.Z enrichment precedes ZGA and RNA Polymerase II loading onto chromatin. In vivo knockdown of maternally contributed Domino, a histone chaperone and ATPase, reduces H2A.Z deposition at transcription start sites, causes global downregulation of housekeeping genes at ZGA, and compromises the establishment of the 3D chromatin structure. We infer that H2A.Z is essential for the de novo establishment of transcriptional programs during ZGA via chromatin reorganization.

scholarly journals CLAMP and Zelda function together to promote Drosophila zygotic genome activation

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jingyue Duan ◽  
Leila Rieder ◽  
Megan M Colonnetta ◽  
Annie Huang ◽  
Mary Mckenney ◽  
...  
Keyword(s):  
Transcription Factor ◽  
Embryonic Development ◽  
Essential Role ◽  
Chromatin Accessibility ◽  
Zygotic Genome Activation ◽  
Zygotic Transcription ◽  
Pioneer Factor ◽  
Pioneer Transcription Factor ◽  
Genome Activation ◽  
Zygotic Genome

During the essential and conserved process of zygotic genome activation (ZGA), chromatin accessibility must increase to promote transcription. Drosophila is a well-established model for defining mechanisms that drive ZGA. Zelda (ZLD) is a key pioneer transcription factor (TF) that promotes ZGA in the Drosophila embryo. However, many genomic loci that contain GA-rich motifs become accessible during ZGA independent of ZLD. Therefore, we hypothesized that other early TFs that function with ZLD have not yet been identified, especially those that are capable of binding to GA-rich motifs such as CLAMP. Here, we demonstrate that Drosophila embryonic development requires maternal CLAMP to: 1) activate zygotic transcription; 2) increase chromatin accessibility at promoters of specific genes that often encode other essential TFs; 3) enhance chromatin accessibility and facilitate ZLD occupancy at a subset of key embryonic promoters. Thus, CLAMP functions as a pioneer factor which plays a targeted yet essential role in ZGA.

scholarly journals Zygotic pioneer factor activity of Odd-paired/Zic is necessary for establishing the Drosophila Segmentation Network

2019 ◽  
Author(s):  
Isabella V. Soluri ◽  
Lauren M. Zumerling ◽  
Omar A. Payan Parra ◽  
Eleanor G. Clark ◽  
Shelby A. Blythe
Keyword(s):  
Regulatory Networks ◽  
Significant Proportion ◽  
Regulatory Elements ◽  
Chromatin Accessibility ◽  
Embryonic Patterning ◽  
Network Function ◽  
Pioneer Factor ◽  
Genome Activation ◽  
Pair Rule ◽  
Zygotic Genome

AbstractBecause regulatory networks of transcription factors drive embryonic patterning, it is possible that chromatin accessibility states impact how networks interact with information encoded in DNA. To determine the interplay between chromatin states and regulatory network function, we performed ATAC seq on Drosophila embryos over the period spanning the establishment of the segmentation network, from zygotic genome activation to gastrulation. Chromatin accessibility states are dynamic over this period, and establishment of the segmentation network requires maturation of the ground chromatin state. Elimination of all maternal patterning information allows identification of patterning-dependent and -independent dynamic chromatin regions. A significant proportion of patterning-dependent accessibility stems from pioneer activity of the pair-rule factor Odd-paired (opa). While opa is necessary to drive late opening of segmentation network cis-regulatory elements, competence for opa to pioneer is regulated over time. These results indicate that dynamic systems for chromatin regulation directly impact the interpretation of embryonic patterning information.

scholarly journals The Spatio-Temporal Control of Zygotic Genome Activation

2018 ◽  
Author(s):  
George E. Gentsch ◽  
Nick D. L. Owens ◽  
James C. Smith
Keyword(s):  
Cell Cycle ◽  
Rna Polymerase Ii ◽  
Temporal Dynamics ◽  
Bmp Signaling ◽  
Cycle Duration ◽  
Zygotic Genome Activation ◽  
Significant Events ◽  
Spatio Temporal ◽  
Genome Activation ◽  
Zygotic Genome

SUMMARYOne of the earliest and most significant events in embryonic development is zygotic genome activation (ZGA). In several species, bulk transcription begins at the mid-blastula transition (MBT) when, after a certain number of cleavages, the embryo attains a particular nuclear-to-cytoplasmic (N/C) ratio, maternal repressors become sufficiently diluted, and the cell cycle slows down. Here we resolve the frog ZGA in time and space by profiling RNA polymerase II (RNAPII) engagement and its transcriptional readout. We detect a gradual increase in both the quantity and the length of RNAPII elongation before the MBT, revealing that >1,000 zygotic genes disregard the N/C timer for their activation, and that the sizes of newly transcribed genes are not necessarily constrained by cell cycle duration. We also find that Wnt, Nodal and BMP signaling together generate most of the spatio-temporal dynamics of regional ZGA, directing the formation of orthogonal body axes and proportionate germ layers.

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