Canonical nucleosome organization at promoters forms during genome activation

Zhang, Yong; Vastenhouw, Nadine L.; Feng, Jianxing; Fu, Kai; Wang, Chenfei; Ge, Ying; Pauli, Andrea; Hummelen, Paul Van; Schier, Alexander F.; Liu, X. Shirley

doi:10.1101/gr.157750.113

Cited by 94 publications

(111 citation statements)

References 43 publications

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“…The stereotypical nucleosome array that has been previously observed near transcription start sites in aggregate plots remains somewhat of a mystery. This organization has been observed in diverse eukaryotes (Yuan et al 2005;Mavrich et al 2008b;Lantermann et al 2010;Ponts et al 2010;Chen et al 2013b;Zhang et al 2014), suggesting that it is established by a widely conserved mechanism. However, the functional relationship between the stereotypical nucleosome array and gene transcription is unclear, since even highly expressed genes exhibit this nucleosome organization (Shivaswamy et al 2008;Lantermann et al 2010).…”

Section: Wwwgenomeorgmentioning

confidence: 98%

“…Genome-wide nucleosome maps in major model organisms have revealed strikingly similar nucleosome patterns near gene starts, where a nucleosome-depleted region upstream of the TSS is followed by a stereotypical array of nucleosomes inside the gene (Yuan et al 2005;Lee et al 2007;Mavrich et al 2008b;Lantermann et al 2010;Chang et al 2012;Chen et al 2013b;Zhang et al 2014). Recent studies have used Saccharomyces cerevisiae as a model to understand nucleosome positioning mechanisms underlying the stereotypical nucleosome pattern near eukaryotic TSSs.…”

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confidence: 99%

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DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome

et al. 2015

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A conserved hallmark of eukaryotic chromatin architecture is the distinctive array of well-positioned nucleosomes downstream from transcription start sites (TSS). Recent studies indicate that trans-acting factors establish this stereotypical array. Here, we present the first genome-wide in vitro and in vivo nucleosome maps for the ciliate Tetrahymena thermophila. In contrast with previous studies in yeast, we find that the stereotypical nucleosome array is preserved in the in vitro reconstituted map, which is governed only by the DNA sequence preferences of nucleosomes. Remarkably, this average in vitro pattern arises from the presence of subsets of nucleosomes, rather than the whole array, in individual Tetrahymena genes. Variation in GC content contributes to the positioning of these sequence-directed nucleosomes and affects codon usage and amino acid composition in genes. Given that the AT-rich Tetrahymena genome is intrinsically unfavorable for nucleosome formation, we propose that these “seed” nucleosomes—together with trans-acting factors—may facilitate the establishment of nucleosome arrays within genes in vivo, while minimizing changes to the underlying coding sequences.

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Section: Wwwgenomeorgmentioning

confidence: 98%

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confidence: 99%

DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome

et al. 2015

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“…In Xenopus , histone modifications at specific promoters exist before the MBT (Blythe et al, 2010), but the majority appear to arise during the MBT and the first major zygotic transcription phase (Akkers et al, 2009). In fish, a transcriptionally permissive chromatin state (H3K4me3) and well-positioned nucleosomes appear to be established both prior to and during gene activation, and can even be found in the absence of RNAPII, the elongation mark H3K36me3, or detectable gene expression (Lindeman et al, 2011; Pálfy et al, 2017; Vastenhouw et al, 2010; Zhang et al, 2014). These experiments suggest that some active loci can be marked by histone modifications prior to transcription, consistent with influencing initiation, although the mechanisms by which these marks are targeted to specific embryonic loci remain unknown.…”

Section: Chromatin Dynamics and Transcriptional Timingmentioning

confidence: 99%

Zygotic Genome Activation in Vertebrates

2017

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The first major developmental transition in vertebrate embryos is the maternal-to-zygotic transition (MZT) when maternal mRNAs are degraded and zygotic transcription begins. During the MZT, the embryo takes charge of gene expression to control cell differentiation and further development. This spectacular organismal transition requires nuclear reprogramming and the initiation of RNAPII at thousands of promoters. Zygotic genome activation (ZGA) is mechanistically coordinated with other embryonic events including changes in the cell cycle, chromatin state, and nuclear-to-cytoplasmic component ratios. Here, we review progress in understanding vertebrate ZGA dynamics in frogs, fish, mice, and humans to explore differences and emphasize common features.

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“…Promoters, especially of transcriptionally active genes, are known to be relatively nucleosome free in a wide variety of species (Lee et al 2007;Schones et al 2008;Weiner et al 2010;Thomas et al 2011;Valouev et al 2011). In zebrafish, wellpositioned nucleosome arrays appear at promoters during zygotic genome activation in a transcription-independent fashion, suggesting that active mechanisms may shape nucleosome occupancy at promoters during early development (Zhang et al 2014). When we searched for motifs enriched among these constitutively open peaks, all k-mers identified were highly AT rich (Supplemental Table 1).…”

Section: A Large Number Of Promoters Do Not Require Zld For Accessibimentioning

confidence: 99%

Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo

et al. 2015

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The transition from a specified germ cell to a population of pluripotent cells occurs rapidly following fertilization. During this developmental transition, the zygotic genome is largely transcriptionally quiescent and undergoes significant chromatin remodeling. In Drosophila, the DNA-binding protein Zelda (also known as Vielfaltig) is required for this transition and for transcriptional activation of the zygotic genome. Open chromatin is associated with Zelda-bound loci, as well as more generally with regions of active transcription. Nonetheless, the extent to which Zelda influences chromatin accessibility across the genome is largely unknown. Here we used formaldehyde-assisted isolation of regulatory elements to determine the role of Zelda in regulating regions of open chromatin in the early embryo. We demonstrate that Zelda is essential for hundreds of regions of open chromatin. This Zelda-mediated chromatin accessibility facilitates transcription-factor recruitment and early gene expression. Thus, Zelda possesses some key characteristics of a pioneer factor. Unexpectedly, chromatin at a large subset of Zelda-bound regions remains open even in the absence of Zelda. The GAGA factor-binding motif and embryonic GAGA factor binding are specifically enriched in these regions. We propose that both Zelda and GAGA factor function to specify sites of open chromatin and together facilitate the remodeling of the early embryonic genome.

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Canonical nucleosome organization at promoters forms during genome activation

Cited by 94 publications

References 43 publications

DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome

DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome

Zygotic Genome Activation in Vertebrates

Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo

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