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TALE-light Imaging Reveals Maternally Guided, H3K9me2/3-independent Emergence of Functional Heterochromatin in Drosophila Embryos

Overview
Journal Genes Dev
Specialty Molecular Biology
Date 2016 Feb 27
PMID 26915820
Citations 44
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Abstract

Metazoans start embryogenesis with a relatively naïve genome. The transcriptionally inert, late-replicating heterochromatic regions, including the constitutive heterochromatin on repetitive sequences near centromeres and telomeres, need to be re-established during development. To explore the events initiating heterochromatin formation and examine their temporal control, sequence specificity, and immediate regulatory consequence, we established a live imaging approach that enabled visualization of steps in heterochromatin emergence on specific satellite sequences during the mid-blastula transition (MBT) in Drosophila. Unexpectedly, only a subset of satellite sequences, including the 359-base-pair (bp) repeat sequence, recruited HP1a at the MBT. The recruitment of HP1a to the 359-bp repeat was dependent on HP1a's chromoshadow domain but not its chromodomain and was guided by maternally provided signals. HP1a recruitment to the 359-bp repeat was required for its programmed shift to later replication, and ectopic recruitment of HP1a was sufficient to delay replication timing of a different repeat. Our results reveal that emergence of constitutive heterochromatin follows a stereotyped developmental program in which different repetitive sequences use distinct interactions and independent pathways to arrive at a heterochromatic state. This differential emergence of heterochromatin on various repetitive sequences changes their replication order and remodels the DNA replication schedule during embryonic development.

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References
1.
Duxin J, Dewar J, Yardimci H, Walter J . Repair of a DNA-protein crosslink by replication-coupled proteolysis. Cell. 2014; 159(2):346-57. PMC: 4229047. DOI: 10.1016/j.cell.2014.09.024. View

2.
Li X, Harrison M, Villalta J, Kaplan T, Eisen M . Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. Elife. 2014; 3. PMC: 4358338. DOI: 10.7554/eLife.03737. View

3.
Farrell J, OFarrell P . From egg to gastrula: how the cell cycle is remodeled during the Drosophila mid-blastula transition. Annu Rev Genet. 2014; 48:269-94. PMC: 4484755. DOI: 10.1146/annurev-genet-111212-133531. View

4.
Stasevich T, Hayashi-Takanaka Y, Sato Y, Maehara K, Ohkawa Y, Sakata-Sogawa K . Regulation of RNA polymerase II activation by histone acetylation in single living cells. Nature. 2014; 516(7530):272-5. DOI: 10.1038/nature13714. View

5.
Wei K, Grenier J, Barbash D, Clark A . Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster. Proc Natl Acad Sci U S A. 2014; 111(52):18793-8. PMC: 4284603. DOI: 10.1073/pnas.1421951112. View