Interphase-arrested<i>Drosophila</i>embryos initiate Mid-Blastula Transition at a low nuclear-cytoplasmic ratio

Strong, I; Yuan, Kai; O’Farrell, Patrick H.

doi:10.1101/143719

Cited by 4 publications

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“…Zygotic transcription then drives morphogenetic events such as cellularization and gastrulation. The slowing of the cell cycle is critical for the developmental events that follow it because short cell cycles inhibit productive transcription (Shermoen and O'Farrell 1991;Strong et al 2017). Additionally, rapid cell cycles could impair the installation of chromatin modifications that regulate gene expression, but, to our knowledge, no direct examination of the enzymes installing these modifications at the MBT exists.…”

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Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila

2019

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Acquisition of chromatin modifications during embryogenesis distinguishes different regions of an initially naïve genome. In many organisms, repetitive DNA is packaged into constitutive heterochromatin that is marked by di/ trimethylation of histone H3K9 and the associated protein HP1a. These modifications enforce the unique epigenetic properties of heterochromatin. However, in the early Drosophila melanogaster embryo, the heterochromatin lacks these modifications, which appear only later, when rapid embryonic cell cycles slow down at the midblastula transition (MBT). Here we focus on the initial steps restoring heterochromatic modifications in the embryo. We describe the JabbaTrap, a technique for inactivating maternally provided proteins in embryos. Using the JabbaTrap, we reveal a major requirement for the methyltransferase Eggless/SetDB1 in the establishment of heterochromatin. In contrast, other methyltransferases contribute minimally. Live imaging reveals that endogenous Eggless gradually accumulates on chromatin in interphase but then dissociates in mitosis, and its accumulation must restart in the next cell cycle. Cell cycle slowing as the embryo approaches the MBT permits increasing accumulation and action of Eggless at its targets. Experimental manipulation of interphase duration shows that cell cycle speed regulates Eggless. We propose that developmental slowing of the cell cycle times embryonic heterochromatin formation.

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Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila

2019

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Developmental Biology: Embryos Need to Control Their Nucleotides Just Right

Ferree

Talia

2019

Current Biology

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clearly-definable behaviours that could be subject to a mutational screen had immense heuristic value and influenced generations of neurobiologists. The pioneer British behaviour geneticists whose Drosophila work immediately preceded that of Benzer, in particular Bastock and Manning, are sometimes forgotten, partly because the complex, naturalistic behaviours they studied, and the theoretical frameworks they employed, seem to have been less amenable to the kind of explanations sought by Benzer and his followers. It could even be argued that, although Bastock was the first to identify how a gene could alter a behaviour [17,20], their work led to a dead end. This latest paper [1] shows this was not the case. The beautifully detailed research by McKellar et al. [1] indicates that one of the most complex and integrated behaviours shown by Drosophila, courtship, is slowly beginning to reveal its cellular substrates. This paper, and the model it presents of how sequential actions may be encoded, suggests a general framework for investigating stereotypical behaviour in Drosophila species and indeed in other animals. As well as developing this model in males, the next challenge will be to employ it to investigate something that is far less well understood, and which Bastock and Manning repeatedly emphasised all those years agocourtship involves female behaviour, too.

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Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 inDrosophila

Seller

Cho

O’Farrell

2018

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5 6 7Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila.Acquisition of chromatin modifications during embryogenesis distinguishes different regions of an initially 11 naïve genome. In many organisms, repetitive DNA is packaged into constitutive heterochromatin that is 12 marked by di/tri methylation of histone H3K9 and the associated protein HP1a. These modifications enforce 13 the unique epigenetic properties of heterochromatin. However, in the early Drosophila melanogaster embryo 14 the heterochromatin lacks these modifications which only appear later when rapid embryonic cell cycles slow 15 down at the Mid-Blastula Transition or MBT. Here we focus on the initial steps restoring heterochromatic 16 modifications in the embryo. We describe the JabbaTrap, a technique for inactivating maternally provided 17 proteins in embryos. Using the JabbaTrap we reveal a major requirement for the methyltransferase 18Eggless/SetDB1 in the establishment of heterochromatin. In contrast, other methyltransferases contribute 19 minimally. Live-imaging reveals that endogenous Eggless gradually accumulates on chromatin in interphase, 20 but then dissociates in mitosis and its accumulation must restart in the next cell cycle. Cell cycle slowing as the 21 embryo approaches the MBT permits increasing accumulation and action of Eggless at its targets. 22 (Janssen et al. 2018). Constitutive heterochromatin displays conserved genetic and molecular properties that are 32 stably transmitted throughout development and across generations (Allshire and Madhani 2018). However, 33 embryogenesis interrupts this stability, and the early embryos of many animals lack true heterochromatin. Thus, 34 embryogenesis involves the restoration of heterochromatin, and this restoration can serve as a paradigm for 35 how epigenetic control of the genome arises during development. 36In general, constitutive heterochromatin is transcriptionally silent, late replicating, and low in 37 recombination. The chromosomes of many species contain large megabase sized arrays of simple repeated 38 sequences, known as satellite DNA, surrounding their centromeres, and it is this pericentric repetitive DNA that 39 composes the bulk of the constitutive heterochromatin. Although heterochromatin was originally defined 40 cytologically -it remains condensed throughout the cell cycle -modern studies often emphasize the set of 41 conserved modifications to its chromatin. Heterochromatic nucleosomes are hypoacetylated and di/tri-42 methylated at lysine 9 on the N-terminal tail of Histone H3 (hereafter H3K9me2/3). The deposition of 43 H3K9me2/3 creates a binding site for HP1 proteins (Eissenberg and Elgin 2014) and HP1 can oligomerize and 44 recruit additional heterochromatin factors which could then generate a distinct compartment in the nucleus. 45Studies in Drosophila have historically made major contributions to our understanding of 46 heterochromatin (Elgin and Reuter 2013). Many key regulators of heterochromatin were discovered ...

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Interphase-arrestedDrosophilaembryos initiate Mid-Blastula Transition at a low nuclear-cytoplasmic ratio

Cited by 4 publications

References 50 publications

Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila

Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila

Developmental Biology: Embryos Need to Control Their Nucleotides Just Right

Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 inDrosophila

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