A time of change: Dynamics of chromatin and transcriptional regulation during nuclear programming in early Drosophila development

Abstract

SUMMARYIn order for a new organism to form, the genomes of the highly specialized egg and sperm need to be reprogrammed into a totipotent state that is capable of generating all of the cell types that comprise an organism. This reprogramming occurs by erasing chromatin modifications, leaving the cells in a na€ ıve state, followed by the induction of specialized programming events. Pioneer factors bind to the genome prior to zygotic genome activation, followed by acetylation of histones and further chromatin specialization by the addition of methylation marks later during differentiation. Genomewide approaches have provided insight into the genomic and epigenomic regulation of gene expression during development, providing a new perspective on the process of cell specification and differentiation. In this review, we discuss how distal DNA and core promoter elements, RNA polymerase pausing, transcription factors, and coregulators interact to shape the chromatin landscape and direct tissue-specific expression patterns during embryo development, focusing on the well-characterized Drosophila embryo.Mol. Reprod. Dev. 82: 735À746, 2015. ß

Maternal Proteins That Are Phosphoregulated upon Egg Activation Include Crucial Factors for Oogenesis, Egg Activation and Embryogenesis inDrosophila melanogaster

“…Five of these genes encode factors involved in chromatin organization, including su(var)205 (Hines et al 2009), pzg (Eggert et al 2004, Gan et al 2011), BRWD3 (Chen et al 2015), ball (Aihara et al 2004, Ivanovska et al 2005) and bre1 (Bray et al 2005, Xuan et al 2013). The activity of these factors may need to be regulated appropriately to allow the dynamic reorganization of chromatin landscape that accompanies the differentiation of the oocyte during oogenesis (Boija & Mannervik 2015, Iovino 2014), followed by conversion to totipotency during egg activation. Understanding how phosphoregulation modulates the activities of these factors and the kinases and other pathways involved in the phosphoregulation of these factors in response to the calcium signal that initiates egg activation will give valuable information about the mechanisms that facilitate the transition between differentiated and totipotent cellular states.…”

Transcriptional precision and accuracy in development: from measurements to models and mechanisms

“…During the MZT, maternal factors are degraded while the zygotic transcription of thousands of genes ensues, taking control over development. This process is associated with stepwise changes in the chromatin landscape both at enhancers and promoters ( Boija and Mannervik, 2015 ; Cantone and Fisher, 2013 ; Hontelez et al, 2015 ; Hug et al, 2017 ; Li et al, 2014 ). In Drosophila , the TF Zelda (also known as Vielfaltig) is known to reshape the chromatin landscape at this critical developmental stage, regulating the transcriptional activation and temporal coordination of a substantial subset of early embryonic genes ( Foo et al, 2014 ; Harrison et al, 2011 ; Liang et al, 2008 ; Nien et al, 2011 ; Schulz et al, 2015 ; Sun et al, 2015 ).…”

Chromatin Control of Developmental Dynamics and Plasticity

“…The onset of zygotic transcription naturally also requires TF activity. In Drosophila an important role is played by the zincfinger protein Zelda (Boija and Mannervik, 2015;Harrison and Eisen, 2015). Zelda is expressed prior to ZGA and is necessary for ZGA to proceed properly.…”

“…This repressive potential is abolished by acetylation of H3K56, which interferes with the H1-nucleosome interaction, re-establishing TF-binding site accessibility (Bernier et al, 2015). In addition, H1 mediates crosstalk with other repressive mechanisms such as Su(var)3-9-dependent H3K9 methylation in Drosophila (Boija and Mannervik, 2015). In ESCs it interferes with H3K4 methylation at imprinted promoters by SETD7 (SET7/9) and stimulates DNA methylation by DNMT1/3B (Yang et al, 2013).…”