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Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos.

ABSTRACT: Pioneer factors such as Zelda (Zld) help initiate zygotic transcription in Drosophila early embryos, but whether other factors support this dynamic process is unclear. Odd-paired (Opa), a zinc-finger transcription factor expressed at cellularization, controls the transition of genes from pair-rule to segmental patterns along the anterior-posterior axis. Finding that Opa also regulates expression through enhancer sog_Distal along the dorso-ventral axis, we hypothesized Opa's role is more general. Chromatin-immunoprecipitation (ChIP-seq) confirmed its in vivo binding to sog_Distal but also identified widespread binding throughout the genome, comparable to Zld. Furthermore, chromatin assays (ATAC-seq) demonstrate that Opa, like Zld, influences chromatin accessibility genome-wide at cellularization, suggesting both are pioneer factors with common as well as distinct targets. Lastly, embryos lacking opa exhibit widespread, late patterning defects spanning both axes. Collectively, these data suggest Opa is a general timing factor and likely late-acting pioneer factor that drives a secondary wave of zygotic gene expression.

SUBMITTER: Koromila T

PROVIDER: S-EPMC7417190 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Temporal control of gene expression by the pioneer factor Zelda through transient interactions in hubs.

Project description:Pioneer transcription factors can engage nucleosomal DNA, which leads to local chromatin remodeling and to the establishment of transcriptional competence. However, the impact of enhancer priming by pioneer factors on the temporal control of gene expression and on mitotic memory remains unclear. Here we employ quantitative live imaging methods and mathematical modeling to test the effect of the pioneer factor Zelda on transcriptional dynamics and memory in Drosophila embryos. We demonstrate that increasing the number of Zelda binding sites accelerates the kinetics of nuclei transcriptional activation regardless of their transcriptional past. Despite its known pioneering activities, we show that Zelda does not remain detectably associated with mitotic chromosomes and is neither necessary nor sufficient to foster memory. We further reveal that Zelda forms sub-nuclear dynamic hubs where Zelda binding events are transient. We propose that Zelda facilitates transcriptional activation by accumulating in microenvironments where it could accelerate the duration of multiple pre-initiation steps.

| S-EPMC6281682 | biostudies-literature

Opa is a late-acting, pioneer factor that coordinates with Zelda to broadly regulate gene expression in early embryos

Project description:This SuperSeries is composed of the SubSeries listed below.

2020-08-02 | GSE153329 | GEO

Zygotic pioneer factor activity of Odd-paired/Zic is necessary for late function of the Drosophila segmentation network.

Project description:Because chromatin determines whether information encoded in DNA is accessible to transcription factors, dynamic chromatin states in development may constrain how gene regulatory networks impart embryonic pattern. To determine the interplay between chromatin states and regulatory network function, we performed ATAC-seq on Drosophila embryos during the establishment of the segmentation network, comparing wild-type and mutant embryos in which all graded maternal patterning inputs are eliminated. While during the period between zygotic genome activation and gastrulation many regions maintain stable accessibility, cis-regulatory modules (CRMs) within the network undergo extensive patterning-dependent changes in accessibility. A component of the network, Odd-paired (opa), is necessary for pioneering accessibility of late segmentation network CRMs. opa-driven changes in accessibility are accompanied by equivalent changes in gene expression. Interfering with the timing of opa activity impacts the proper patterning of expression. These results indicate that dynamic systems for chromatin regulation directly impact the reading of embryonic patterning information.

| S-EPMC7190358 | biostudies-literature

Opa is a late-acting, pioneer factor that coordinates with Zelda to broadly regulate gene expression in early embryos (ATAC-seq, RNA-seq)

Project description:Pioneer factors such as Zelda (Zld) help initiate zygotic transcription in Drosophila early embryos, but whether other factors support this dynamic process is unclear. Odd-paired (Opa), a zinc-finger transcription factor expressed at cellularization, controls the transition of genes from pair-rule to segmental patterns along the anterior-posterior axis. Finding that Opa also regulates expression through enhancer sog_Distal along the dorso-ventral axis, we hypothesized Opa’s role is more general. Chromatin-immunoprecipitation (ChIP-seq) confirmed its in vivo binding to sog_Distal but also identified widespread binding throughout the genome, comparable to Zld. Furthermore, chromatin assays (ATAC-seq) demonstrate that Opa, like Zld, influences chromatin accessibility genome-wide at cellularization, suggesting both are pioneer factors with common as well as distinct targets. Lastly, embryos lacking opa exhibit widespread, late patterning defects spanning both axes. Collectively, these data suggest Opa is a general timing factor and likely late-acting pioneer factor that drives a secondary wave of zygotic gene expression contributor: Theodora Koromila (ATAC-seq-RNA-seq) contributor: Fan Gao (Bioinformatic analysis) contributor: Angelike Stathopoulos (PI) contributor: Peng He (Bioinformatic analysis)

2020-08-02 | GSE153328 | GEO

Opa is a late-acting, pioneer factor that coordinates with Zelda to broadly regulate gene expression in early embryos (ChIP-seq, ATAC-seq)

Project description:Pioneer factors such as Zelda initiate zygotic transcription within Drosophila early embryos, but whether other factors also support this dynamic patterning process is unclear. Odd-paired (Opa) is a zinc-finger transcription factor expressed during cellularization, shown to act as timing factor to control pair-rule to segmental patterning transition along the anterior-posterior (AP) axis. We found Opa regulates expression through an enhancer active along the dorso-ventral axis (sog_Distal), specifically, to support its late embryonic expression. Opa chromatin immunoprecipitation identified occupancy at this enhancer sequence as well widespread binding throughout the genome, comparable to Zelda. Furthermore, chromatin assays (ATAC-seq) demonstrate that Opa, like Zelda, influences accessibility and has both common as well as distinct target sequences. opa mutants also exhibit DV and AP patterning changes suggesting Opa acts broadly. This study suggests Opa is a late-acting, pioneer factor whose action follows Zelda to herald in a second wave of zygotic gene expression. NIH Grants R35GM118146 and R03HD097535 to A.S.

2020-08-02 | GSE140722 | GEO

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

Project description:Because chromatin determines whether information encoded in DNA is accessible to transcription factors, dynamic chromatin states in development may constrain how gene regulatory networks impart embryonic pattern. 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, comparing wild-type and mutant embryos in which all graded maternal patterning inputs are eliminated. While during the period between zygotic genome activation and gastrulation many regions maintain stable accessibility, cis-regulatory modules (CRMs) within the segmentation network undergo extensive patterning-dependent changes in accessibility. A component of the network, Odd-paired (opa), is necessary for pioneering accessibility of segmentation network CRMs. 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.

2020-02-01 | GSE141538 | GEO

Continued Activity of the Pioneer Factor Zelda Is Required to Drive Zygotic Genome Activation.

Project description:Reprogramming cell fate during the first stages of embryogenesis requires that transcriptional activators gain access to the genome and remodel the zygotic transcriptome. Nonetheless, it is not clear whether the continued activity of these pioneering factors is required throughout zygotic genome activation or whether they are only required early to establish cis-regulatory regions. To address this question, we developed an optogenetic strategy to rapidly and reversibly inactivate the master regulator of genome activation in Drosophila, Zelda. Using this strategy, we demonstrate that continued Zelda activity is required throughout genome activation. We show that Zelda binds DNA in the context of nucleosomes and suggest that this allows Zelda to occupy the genome despite the rapid division cycles in the early embryo. These data identify a powerful strategy to inactivate transcription factor function during development and suggest that reprogramming in the embryo may require specific, continuous pioneering functions to activate the genome.

| S-EPMC6544384 | biostudies-literature

Cell-type-specific chromatin occupancy by the pioneer factor Zelda drives key developmental transitions in Drosophila.

Project description:During Drosophila embryogenesis, the essential pioneer factor Zelda defines hundreds of cis-regulatory regions and in doing so reprograms the zygotic transcriptome. While Zelda is essential later in development, it is unclear how the ability of Zelda to define cis-regulatory regions is shaped by cell-type-specific chromatin architecture. Asymmetric division of neural stem cells (neuroblasts) in the fly brain provide an excellent paradigm for investigating the cell-type-specific functions of this pioneer factor. We show that Zelda synergistically functions with Notch to maintain neuroblasts in an undifferentiated state. Zelda misexpression reprograms progenitor cells to neuroblasts, but this capacity is limited by transcriptional repressors critical for progenitor commitment. Zelda genomic occupancy in neuroblasts is reorganized as compared to the embryo, and this reorganization is correlated with differences in chromatin accessibility and cofactor availability. We propose that Zelda regulates essential transitions in the neuroblasts and embryo through a shared gene-regulatory network driven by cell-type-specific enhancers.

| S-EPMC8660810 | biostudies-literature

Opa is a late-acting, pioneer factor that coordinates with Zelda to broadly regulate gene expression in early embryos

Project description:Opa is a late-acting, pioneer factor that coordinates with Zelda to broadly regulate gene expression in early embryos

| PRJNA642120 | ENA

The Zic family homologue Odd-paired regulates Alk expression in Drosophila.

Project description:The Anaplastic Lymphoma Kinase (Alk) receptor tyrosine kinase (RTK) plays a critical role in the specification of founder cells (FCs) in the Drosophila visceral mesoderm (VM) during embryogenesis. Reporter gene and CRISPR/Cas9 deletion analysis reveals enhancer regions in and upstream of the Alk locus that influence tissue-specific expression in the amnioserosa (AS), the VM and the epidermis. By performing high throughput yeast one-hybrid screens (Y1H) with a library of Drosophila transcription factors (TFs) we identify Odd-paired (Opa), the Drosophila homologue of the vertebrate Zic family of TFs, as a novel regulator of embryonic Alk expression. Further characterization identifies evolutionarily conserved Opa-binding cis-regulatory motifs in one of the Alk associated enhancer elements. Employing Alk reporter lines as well as CRISPR/Cas9-mediated removal of regulatory elements in the Alk locus, we show modulation of Alk expression by Opa in the embryonic AS, epidermis and VM. In addition, we identify enhancer elements that integrate input from additional TFs, such as Binou (Bin) and Bagpipe (Bap), to regulate VM expression of Alk in a combinatorial manner. Taken together, our data show that the Opa zinc finger TF is a novel regulator of embryonic Alk expression.

| S-EPMC5393633 | biostudies-literature

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