Patterns of chromatin accessibility along the anterior-posterior axis in the early Drosophila embryo

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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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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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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Drosophila Embryo: Maternal Interactions in Specification of the Anterior–Posterior Axis

Encyclopedia of Life Sciences ◽

10.1002/9780470015902.a0029150 ◽

2020 ◽

pp. 50-58

Author(s):

Jan‐Michael Kugler ◽

Paul Lasko

Keyword(s):

Drosophila Embryo ◽

Anterior Posterior ◽

Anterior Posterior Axis

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Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen

Development ◽

10.1242/dev.109.4.811 ◽

1990 ◽

Vol 109 (4) ◽

pp. 811-820 ◽

Cited By ~ 16

Author(s):

W. Driever ◽

V. Siegel ◽

C. Nusslein-Volhard

Keyword(s):

Drosophila Embryo ◽

Beta Globin ◽

P Transformation ◽

Early Drosophila Embryo ◽

Maternal Effect Genes ◽

Translational Block ◽

Maternal Gene ◽

Anterior Posterior

A small number of maternal effect genes determine anterior-posterior pattern in the Drosophila embryo. Embryos from females mutant for the maternal gene bicoid lack head and thorax. bcd mRNA becomes localized to the anterior tip of the egg during oogenesis and is the source for the morphogen gradient of bcd protein. Here we show that in vitro transcribed bicoid mRNA that has its own leader sequences substituted by the Xenopus beta-globin 5′ untranslated sequences is translated more efficiently than bicoid mRNA with the natural 5′ mRNA leader when tested in vitro and in Drosophila Schneider cells. When injected into bicoid mutant embryos, only the bcd mRNA with the beta-globin leader sequence, substituted for the natural leader, is able to induce anterior development. We used P-transformation to show that sequences in the 5′ leader are neither necessary for localization of the transcript nor for the translational block of the bcd mRNA during oogenesis. For our injection experiments, we used only one of the identified splicing forms of bcd mRNA. The bcd protein species derived from this mRNA is able to induce anterior development at any position along the anterior-posterior axis. Thus bicoid protein can induce development of head and thorax independent of any other specifically localized morphogenetic factor. Our findings further support the notion that the concentration gradient of bcd protein, and not the existence of different forms of bcd protein, is responsible for specifying subregions of the embryo.

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