Dynamic reprogramming of chromatin accessibility during Drosophila embryo development

Drastic epigenetic reprogramming occurs during human gametogenesis and early embryo development. Advances in low-input and single-cell epigenetic techniques have provided powerful tools to dissect the genome-wide dynamics of different epigenetic molecular layers in these processes. In this review, we focus mainly on the most recent progress in understanding the dynamics of DNA methylation, chromatin accessibility, and histone modifications in human gametogenesis and early embryo development. Deficiencies in remodeling of the epigenomes can cause severe developmental defects, infertility, and long-term health issues in offspring. Aspects of the external environment, including assisted reproductive technology procedures, parental diets, and unhealthy parental habits, may disturb the epigenetic reprogramming processes and lead to an aberrant epigenome in the offspring. Here, we review the current knowledge of the potential risk factors of aberrant epigenomes in humans.

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P-TEFb, the Super Elongation Complex and Mediator Regulate a Subset of Non-paused Genes during Early Drosophila Embryo Development

PLoS Genetics ◽

10.1371/journal.pgen.1004971 ◽

2015 ◽

Vol 11 (2) ◽

pp. e1004971 ◽

Cited By ~ 10

Author(s):

Olle Dahlberg ◽

Olga Shilkova ◽

Min Tang ◽

Per-Henrik Holmqvist ◽

Mattias Mannervik

Keyword(s):

Embryo Development ◽

Drosophila Embryo ◽

Elongation Complex ◽

Super Elongation Complex ◽

Early Drosophila Embryo

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Phosphorylation of Pnut in the Early Stages of Drosophila Embryo Development Affects Association of the Septin Complex with the Membrane and Is Important for Viability

G3 Genes|Genome|Genetics ◽

10.1534/g3.117.300186 ◽

2017 ◽

Vol 8 (1) ◽

pp. 27-38 ◽

Cited By ~ 1

Author(s):

Katarina Akhmetova ◽

Maxim Balasov ◽

Anton Svitin ◽

Elena Chesnokova ◽

Matthew Renfrow ◽

...

Keyword(s):

Embryo Development ◽

Drosophila Embryo ◽

Early Stages

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TFIIH trafficking and its nuclear assembly during early Drosophila embryo development

Developmental Biology ◽

10.1016/j.ydbio.2007.03.235 ◽

2007 ◽

Vol 306 (1) ◽

pp. 356-357

Author(s):

Javier Aguilar-Fuentes ◽

Viviana Valadez-Graham ◽

Enrique Reynaud ◽

Mario Zurita

Keyword(s):

Embryo Development ◽

Drosophila Embryo ◽

Nuclear Assembly ◽

Early Drosophila Embryo

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GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo

eLife ◽

10.7554/elife.66668 ◽

2021 ◽

Vol 10 ◽

Author(s):

Marissa M Gaskill ◽

Tyler J Gibson ◽

Elizabeth D Larson ◽

Melissa M Harrison

Keyword(s):

Chromatin Accessibility ◽

Drosophila Embryo ◽

Gaga Factor ◽

Zygotic Transcription ◽

Early Drosophila Embryo ◽

Zygotic Gene ◽

Pioneer Factor ◽

Pioneer Factors ◽

Genome Activation ◽

Development Proceeds

Following fertilization, the genomes of the germ cells are reprogrammed to form the totipotent embryo. Pioneer transcription factors are essential for remodeling the chromatin and driving the initial wave of zygotic gene expression. In Drosophila melanogaster, the pioneer factor Zelda is essential for development through this dramatic period of reprogramming, known as the maternal-to-zygotic transition (MZT). However, it was unknown whether additional pioneer factors were required for this transition. We identified an additional maternally encoded factor required for development through the MZT, GAGA Factor (GAF). GAF is necessary to activate widespread zygotic transcription and to remodel the chromatin accessibility landscape. We demonstrated that Zelda preferentially controls expression of the earliest transcribed genes, while genes expressed during widespread activation are predominantly dependent on GAF. Thus, progression through the MZT requires coordination of multiple pioneer-like factors, and we propose that as development proceeds control is gradually transferred from Zelda to GAF.

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TFIIH trafficking and its nuclear assembly during early Drosophila embryo development

Journal of Cell Science ◽

10.1242/jcs.03150 ◽

2006 ◽

Vol 119 (18) ◽

pp. 3866-3875 ◽

Cited By ~ 12

Author(s):

J. Aguilar-Fuentes

Keyword(s):

Embryo Development ◽

Drosophila Embryo ◽

Nuclear Assembly ◽

Early Drosophila Embryo

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CCAT: Combinatorial Code Analysis Tool for transcriptional regulation

Nucleic Acids Research ◽

10.1093/nar/gkt1302 ◽

2013 ◽

Vol 42 (5) ◽

pp. 2833-2847 ◽

Cited By ~ 16

Author(s):

Peng Jiang ◽

Mona Singh

Keyword(s):

Embryo Development ◽

Binding Sites ◽

Developmental Stages ◽

Chromatin Accessibility ◽

Analysis Tool ◽

Computational Framework ◽

Code Analysis ◽

Genome Wide ◽

Transcriptional Regulatory ◽

Combinatorial Code

Abstract Combinatorial interplay among transcription factors (TFs) is an important mechanism by which transcriptional regulatory specificity is achieved. However, despite the increasing number of TFs for which either binding specificities or genome-wide occupancy data are known, knowledge about cooperativity between TFs remains limited. To address this, we developed a computational framework for predicting genome-wide co-binding between TFs (CCAT, Combinatorial Code Analysis Tool), and applied it to Drosophila melanogaster to uncover cooperativity among TFs during embryo development. Using publicly available TF binding specificity data and DNaseI chromatin accessibility data, we first predicted genome-wide binding sites for 324 TFs across five stages of D. melanogaster embryo development. We then applied CCAT in each of these developmental stages, and identified from 19 to 58 pairs of TFs in each stage whose predicted binding sites are significantly co-localized. We found that nearby binding sites for pairs of TFs predicted to cooperate were enriched in regions bound in relevant ChIP experiments, and were more evolutionarily conserved than other pairs. Further, we found that TFs tend to be co-localized with other TFs in a dynamic manner across developmental stages. All generated data as well as source code for our front-to-end pipeline are available at http://cat.princeton.edu.

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Spatially uniform establishment of chromatin accessibility in the early Drosophila embryo

10.1101/195073 ◽

2017 ◽

Author(s):

Jenna E. Haines ◽

Michael B. Eisen

Keyword(s):

Chromatin Accessibility ◽

Drosophila Embryo ◽

Direct Result ◽

Open Chromatin ◽

Relative Contribution ◽

Genome Wide ◽

Zygotic Transcription ◽

Early Drosophila Embryo ◽

Nucleosome Density ◽

Anterior Posterior

AbstractAs the Drosophila embryo transitions from the use of maternal RNAs to zygotic transcription, domains of open chromatin, with relatively low nucleosome density and specific histone marks, are established at promoters and enhancers involved in patterned embryonic transcription. However, it remains unclear whether open chromatin is a product of activity - transcription at promoters and patterning transcription factor binding at enhancers - or whether it is established by independent mechanisms. Recent work has implicated the ubiquitously expressed, maternal factor Zelda in this process. To assess the relative contribution of activity in the establishment of chromatin accessibility, we have probed chromatin accessibility across the anterior-posterior axis of early Drosophila melanogaster embryos by applying a transposon based assay for chromatin accessibility (ATAC-seq) to anterior and posterior halves of hand-dissected, cellular blastoderm embryos. We find that genome-wide chromatin accessibility is remarkably similar between the two halves. Promoters and enhancers that are active in exclusively one half of the embryo have open chromatin in the other half, demonstrating that chromatin accessibility is not a direct result of activity. However, there is a small skew at enhancers that drive transcription exclusively in either the anterior or posterior half of the embryo, with greater accessibility in the region of activity. Taken together these data support a model in which regions of chromatin accessibility are defined and established by ubiquitous factors, and fine-tuned subsequently by activity.

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The pioneer factor GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo

10.1101/2020.07.15.204248 ◽

2020 ◽

Author(s):

Marissa M. Gaskill ◽

Tyler J. Gibson ◽

Elizabeth D. Larson ◽

Melissa M. Harrison

Keyword(s):

Transcriptional Control ◽

Chromatin Accessibility ◽

Drosophila Embryo ◽

Gaga Factor ◽

Zygotic Transcription ◽

Early Drosophila Embryo ◽

Zygotic Gene ◽

Pioneer Factor ◽

Pioneer Factors ◽

Genome Activation

AbstractFollowing fertilization, the genomes of the germ cells are reprogrammed to form the totipotent embryo. Pioneer transcription factors are required for remodeling the chromatin and driving the initial wave of zygotic gene expression. In Drosophila melanogaster, the pioneer factor Zelda is essential for development through this dramatic period of reprogramming, known as the maternal- to-zygotic transition (MZT). However, it was unknown whether additional pioneer factors were necessary for this transition. We identified an additional maternally encoded factor required for development through the MZT, GAGA Factor (GAF). GAF is needed to activate widespread zygotic transcription and to remodel the chromatin accessibility landscape. We demonstrated that Zelda preferentially controls expression of the earliest transcribed genes, while genes expressed during widespread activation are predominantly dependent on GAF. Thus, progression through the MZT requires coordination of multiple pioneer factors, and we propose that as development proceeds transcriptional control is gradually transferred from Zelda to GAF.

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