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.

CLAMP regulates Zygotic Genome Activation in Drosophila embryos

Genetics ◽  
2021 ◽  
Author(s):  
Megan M Colonnetta ◽  
Juan E Abrahante ◽  
Paul Schedl ◽  
Daryl M Gohl ◽  
Girish Deshpande
Keyword(s):  
Temporal Dynamics ◽  
Embryonic Patterning ◽  
Zygotic Genome Activation ◽  
Promoter Sequences ◽  
Genome Wide ◽  
Zygotic Transcription ◽  
Pioneer Factor ◽  
Genome Activation ◽  
Drosophila Embryos ◽  
Zygotic Genome

Abstract Embryonic patterning is critically dependent on zygotic genome activation (ZGA). In Drosophila melanogaster embryos, the pioneer factor Zelda directs ZGA, possibly in conjunction with other factors. Here we have explored novel involvement of Chromatin-Linked Adapter for MSL Proteins (CLAMP) during ZGA. CLAMP binds thousands of sites genome-wide throughout early embryogenesis. Interestingly, CLAMP relocates to target promoter sequences across the genome when ZGA is initiated. Although there is a considerable overlap between CLAMP and Zelda binding sites, the proteins display distinct temporal dynamics. To assess whether CLAMP occupancy affects gene expression, we analyzed transcriptomes of embryos zygotically compromised for either clamp or zelda and found that transcript levels of many zygotically-activated genes are similarly affected. Importantly, compromising either clamp or zelda disrupted the expression of critical segmentation and sex determination genes bound by CLAMP (and Zelda). Furthermore, clamp knockdown embryos recapitulate other phenotypes observed in Zelda-depleted embryos, including nuclear division defects, centrosome aberrations, and a disorganized actomyosin network. Based on these data, we propose that CLAMP acts in concert with Zelda to regulate early zygotic transcription.

scholarly journals Whole-Transcriptome Sequencing-Based Analysis of DAZL and Its Interacting Genes during Germ Cells Specification and Zygotic Genome Activation in Chickens

2020 ◽  
Vol 21 (21) ◽  
pp. 8170
Author(s):  
Deivendran Rengaraj ◽  
Sohyoung Won ◽  
Jong Won Han ◽  
DongAhn Yoo ◽  
Heebal Kim ◽  
...  
Keyword(s):  
Germ Cells ◽  
Transcriptome Sequencing ◽  
Germ Plasm ◽  
Prediction Method ◽  
Zygotic Genome Activation ◽  
Zygotic Transcription ◽  
Whole Transcriptome Sequencing ◽  
Genome Activation ◽  
Whole Transcriptome ◽  
Zygotic Genome

The deleted in azoospermia like (DAZL) is required for germ cells development and maintenance. In chickens, the mRNA and protein of DAZL, a representative maternally inherited germ plasm factor, are detected in the germ plasm of oocyte, zygote, and all stages of the intrauterine embryos. However, it is still insufficient to explain the origin and specification process of chicken germ cells, because the stage at which the zygotic transcription of DAZL occurs and the stage at which the maternal DAZL RNA/protein clears have not yet been fully identified. Moreover, a comprehensive understanding of the expression of DAZL interacting genes during the germ cells specification and development and zygotic genome activation (ZGA) is lacking in chickens. In this study, we identified a set of DAZL interacting genes in chickens using in silico prediction method. Then, we analyzed the whole-transcriptome sequencing (WTS)-based expression of DAZL and its interacting genes in the chicken oocyte, zygote, and Eyal-Giladi and Kochav (EGK) stage embryos (EGK.I to EGK.X). In the results, DAZL transcripts are increased in the zygote (onset of transcription), maintained the increased level until EGK.VI, and decreased from EGK.VIII (possible clearance of maternal RNAs). Among the DAZL interacting genes, most of them are increased either at 1st ZGA or 2nd ZGA, indicating their involvement in germ cells specification and development.

scholarly journals ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Mette Bentsen ◽  
Philipp Goymann ◽  
Hendrik Schultheis ◽  
Kathrin Klee ◽  
Anastasiia Petrova ◽  
...  
Keyword(s):  
Transcription Factor ◽  
Transcription Factor Binding ◽  
Zygotic Genome Activation ◽  
Factor Binding ◽  
Genome Activation ◽  
Kinetics Of ◽  
Zygotic Genome

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

eLife ◽  
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.

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

2019 ◽  
Vol 74 (1) ◽  
pp. 185-195.e4 ◽  
Author(s):  
Stephen L. McDaniel ◽  
Tyler J. Gibson ◽  
Katharine N. Schulz ◽  
Meilin Fernandez Garcia ◽  
Markus Nevil ◽  
...  
Keyword(s):  
Zygotic Genome Activation ◽  
Pioneer Factor ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals Reciprocal zebrafish-medaka hybrids reveal maternal control of zygotic genome activation timing

2021 ◽  
Author(s):  
Krista R Gert ◽  
Luis Enrique Cabrera Quio ◽  
Maria Novatchkova ◽  
Yixuan Guo ◽  
Bradley R Cairns ◽  
...  
Keyword(s):  
Early Development ◽  
Hybrid System ◽  
Control Mechanisms ◽  
Zygotic Genome Activation ◽  
Zygotic Transcription ◽  
Versatile Tool ◽  
Paternal Control ◽  
Genome Activation ◽  
Zygotic Genome

After fertilization, the sperm and egg contribute unequally to the newly formed zygote. While the sperm contributes mainly paternal DNA, the egg provides both maternal DNA and the bulk of the future embryonic cytoplasm. Most embryonic processes (like the onset of zygotic transcription) depend on maternally-provided cytoplasmic components, and it is largely unclear whether paternal components besides the centrosome play a role in the regulation of early embryogenesis. Here we report a reciprocal zebrafish-medaka hybrid system as a powerful tool to investigate paternal vs. maternal influence during early development. By combining expression of zebrafish Bouncer on the medaka egg with artificial egg activation, we demonstrate the in vitro generation of paternal zebrafish x maternal medaka (reripes) hybrids. These hybrids complement the previously established paternal medaka x maternal zebrafish (latio) hybrids (Herberg et al., 2018). As proof of concept, we investigated maternal vs. paternal control of zygotic genome activation (ZGA) timing using this reciprocal hybrid system. RNA-seq analysis of the purebred fish species and hybrids revealed that the onset of ZGA is primarily governed by the egg. Overall, our study establishes the reciprocal zebrafish-medaka hybrid system as a versatile tool to dissect parental control mechanisms during early development.

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

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.

scholarly journals Perturbation of maternal PIASy abundance disrupts zygotic genome activation and embryonic development via SUMOylation pathway

Biology Open ◽  
2019 ◽  
Vol 8 (10) ◽  
pp. bio048652 ◽  
Author(s):  
Chika Higuchi ◽  
Mari Yamamoto ◽  
Seung-Wook Shin ◽  
Kei Miyamoto ◽  
Kazuya Matsumoto
Keyword(s):  
Embryonic Development ◽  
Zygotic Genome Activation ◽  
Genome Activation ◽  
Zygotic Genome

scholarly journals Arginine Regulates Zygotic Genome Activation in Porcine Embryos through Promoting Polyamine Synthesis☆

2021 ◽  
Author(s):  
Tianrui Zhang ◽  
Yingying Zheng ◽  
Tianya Kuang ◽  
Lianyu Yang ◽  
Hailong Jiang ◽  
...  
Keyword(s):  
Embryonic Development ◽  
Lipid Droplet ◽  
Immunofluorescent Staining ◽  
Block Group ◽  
Arginine Metabolism ◽  
Zygotic Genome Activation ◽  
Cell Stage ◽  
Polyamine Synthesis ◽  
Genome Activation ◽  
Zygotic Genome

Abstract Background:Arginine has a positive effect on preimplantation development in pigs. However, the exact mechanism by which arginine promotes embryonic development to the blastocyst stage is not undefined. Here, single-cell RNA-sequencing technology was applied to porcine in vivo pre-implantation embryos from zygote to morula to determine transcription patterns of arginine metabolism-related genes during preimplantation embryonic development.Results:Transcriptome sequencing showed that arginine metabolism-related genes clearly changed from the 2-cell stage to the 4-cell stage, where zygotic genome activation (ZGA) occurred in porcine embryos. Further analysis of the correlation between arginine metabolism and ZGA shows that arginine metabolism-related genes are significantly correlated with key ZGA genes such as ZSCAN4, DPPA2 and EIF1A, indicating that arginine metabolism may be an indicator of porcine ZGA. To explore the correlation between arginine metabolism and ZGA, embryos cultured in the medium that removes all the amino acids, proteins and pyruvate in the PZM3 medium were employed to generate the ZGA blocked embryo model. The 4-cell arrest rate significantly increased at 72 h after activation, indicating impeded embryonic development. Meanwhile, results of immunofluorescent staining showed that the expression of SIRT1 protein during ZGA was significantly inhibited. Results of quantitative PCR showed that the expression of zygotic genes (ZSCAN4, DPPA2 and EIF1A) was significantly decreased. The above results indicate that the ZGA blocked embryo model was successfully established. Adding of arginine recovered embryonic development, SIRT1 and zygotic genes expression levels and initiated the ZGA. In addition, ROS content significantly increased when ZGA was blocked, and the GSH, ATP and lipid droplet content significantly decreased. After the addition of arginine in the block group, the ROS content significantly decreased, and the GSH, ATP and lipid droplet content significantly increased. Moreover, the ornithine decarboxylase (ODC) inhibitor difluoromethylornithine (DFMO) and arginine were added to the block group at the same time, and the effect of arginine was found to be inhibited. Conclusions: Arginine is essential for ZGA in porcine embryos. Arginine contributes to porcine ZGA by promoting polyamine synthesis in porcine embryos.

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