Noncanonical Compensation of Zygotic X Transcription in Early Drosophila melanogaster Development Revealed through Single-Embryo RNA-Seq

Lott, Susan E.; Villalta, Jacqueline E.; Schroth, Gary P.; Luo, Shujun; Tonkin, Leath A.; Eisen, Michael B.

doi:10.1371/journal.pbio.1000590

Cited by 212 publications

(425 citation statements)

References 57 publications

(57 reference statements)

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“…While Vielfaltig's mechanism of action is unknown, we and others previously noted an enrichment for TAGteam motifs in regions bound by six anterior-posterior transcription factors (Li et al 2008;Bradley et al 2010). Hypothesizing that this relationship between TAGteam motifs and transcription factor binding might be causative, we reanalyzed the ChIP (MacArthur et al 2009), DNase I , and RNA-seq (Lott et al 2011) data sets described above and found that the presence of TAGteam motifs is associated with high levels of binding of all assayed factors. Levels of binding are globally proportional to RNA polymerase II occupancy of promoters and gene expression levels during the onset of zygotic transcription.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 92%

“…DNase I digestion data, measuring chromatin accessibility, is available as well for identically staged embryos Thomas et al 2011). Furthermore, a recent study measured levels of both maternally contributed and zygotically transcribed mRNAs from mitotic cycles 10-14 (Lott et al 2011) when widespread transcription of the zygotic genome commences, allowing us to connect transcription factor binding to gene expression.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

“…However, this explanation is predicated upon the assumption that regions bound by many transcription factors generally possess enhancer activity. We assessed whether overlapping binding of many factors is globally associated with gene expression using a published RNA-seq time course of single D. melanogaster embryos from mitotic cycles 10-14 (Lott et al 2011), when widespread zygotic transcription begins. Consistent with previous reports that TAGteam motifs are important for early expression (ten Bosch et al 2006), we found that TAGteam motifs in gene promoters, defined as 1.5 kb centered on the TSS, were associated with strong increases in the expression level of zygotically transcribed genes from cycles 10-14 (Fig.…”

Section: Binding Of Multiple Transcription Factors Is Associated Withmentioning

confidence: 99%

“…A list of genes, their coordinates (including transcription start sites), and their expression levels from mitotic cycles 10-14 was obtained from published data (Data set S1) (Lott et al 2011). We used this publication's classification of genes as zygotically or maternally transcribed.…”

Section: Gene Expression Analysesmentioning

confidence: 99%

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The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo

Satija¹,

Bradley²

2012

Genome Res.

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Highly overlapping patterns of genome-wide binding of many distinct transcription factors have been observed in worms, insects, and mammals, but the origins and consequences of this overlapping binding remain unclear. While analyzing chromatin immunoprecipitation data sets from 21 sequence-specific transcription factors active in the Drosophila embryo, we found that binding of all factors exhibits a dose-dependent relationship with ''TAGteam'' sequence motifs bound by the zinc finger protein Vielfaltig, also known as Zelda, a recently discovered activator of the zygotic genome. TAGteam motifs are present and well conserved in highly bound regions, and are associated with transcription factor binding even in the absence of canonical recognition motifs for these factors. Furthermore, levels of binding in promoters and enhancers of zygotically transcribed genes are correlated with RNA polymerase II occupancy and gene expression levels. Our results suggest that Vielfaltig acts as a master regulator of early development by facilitating the genome-wide establishment of overlapping patterns of binding of diverse transcription factors that drive global gene expression.[Supplemental material is available for this article.]Genome-wide chromatin immunoprecipitation (ChIP) experiments in diverse metazoans have shown that many transcription factors bind thousands of highly overlapping loci in undifferentiated cells (Boyer et al.

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Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 92%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Section: Binding Of Multiple Transcription Factors Is Associated Withmentioning

confidence: 99%

Section: Gene Expression Analysesmentioning

confidence: 99%

See 2 more Smart Citations

The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo

Satija¹,

Bradley²

2012

Genome Res.

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“…It is clear, therefore, that each syncytial nuclear cycle can be treated as a single, or even multiple developmental time points. A few recent RNA-sequencing (RNA-seq)-based studies have in fact divided embryonic development into time points based on syncytial nuclear divisions for this very reason (Lott et al 2011;Ali-Murthy et al 2013). In previous studies, however, the syncytial nuclear stage, especially nuclear cycles [10][11][12][13][14], have been grouped together in a small number of developmental stages or time points (Bownes 1975;Bate and Martinez Arias 1993;Graveley et al 2011).…”

mentioning

confidence: 99%

Quantitative Single-Embryo Profile ofDrosophilaGenome Activation and the Dorsal–Ventral Patterning Network

Sandler¹,

Stathopoulos

2016

Genetics

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During embryonic development of Drosophila melanogaster, the maternal-to-zygotic transition (MZT) marks a significant and rapid turning point when zygotic transcription begins and control of development is transferred from maternally deposited transcripts. Characterizing the sequential activation of the genome during the MZT requires precise timing and a sensitive assay to measure changes in expression. We utilized the NanoString nCounter instrument, which directly counts messenger RNA transcripts without reverse transcription or amplification, to study .70 genes expressed along the dorsal-ventral (DV) axis of early Drosophila embryos, dividing the MZT into 10 time points. Transcripts were quantified for every gene studied at all time points, providing the first dataset of absolute numbers of transcripts during Drosophila development. We found that gene expression changes quickly during the MZT, with early nuclear cycle 14 (NC14) the most dynamic time for the embryo. twist is one of the most abundant genes in the entire embryo and we use mutants to quantitatively demonstrate how it cooperates with Dorsal to activate transcription and is responsible for some of the rapid changes in transcription observed during early NC14. We also uncovered elements within the gene regulatory network that maintain precise transcript levels for sets of genes that are spatiotemporally cotranscribed within the presumptive mesoderm or dorsal ectoderm. Using these new data, we show that a fine-scale, quantitative analysis of temporal gene expression can provide new insights into developmental biology by uncovering trends in gene networks, including coregulation of target genes and specific temporal input by transcription factors.

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How gene expression in fast‐proliferating cells keeps pace

2015

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The development of living organisms requires a precise coordination of all basic cellular processes, in space and time. Early embryogenesis of most species with externally deposited eggs starts with a series of extremely fast cleavage cycles. These divisions have a strong influence on gene expression as mitosis represses transcription and pre-mRNA processing. In this review, we will describe the distinct adaptations for efficient gene expression and discuss the emerging role of the multifunctional NineTeen Complex (NTC) in gene expression and genomic stability during fast proliferation.

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Noncanonical Compensation of Zygotic X Transcription in Early Drosophila melanogaster Development Revealed through Single-Embryo RNA-Seq

Abstract: Mmany genes from the X chromosome are expressed at the same level in female and male embryos during early Drosophila development, prior to the establishment of MSL-mediated dosage compensation, suggesting the existence of a novel mechanism.

Cited by 212 publications

References 57 publications

The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo

The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo

Quantitative Single-Embryo Profile ofDrosophilaGenome Activation and the Dorsal–Ventral Patterning Network

How gene expression in fast‐proliferating cells keeps pace

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