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Trading Genome Vulnerability for Stable Genetic Inheritance: Active Retrotransposons Help Maintain Pericentromeric Heterochromatin Required for Faithful Cell Division

By Yajing Hao, Dongpeng Wang, Shuheng Wu, Xiao Li, Changwei Shao, Peng Zhang, Jia-Yu Chen, Do-Hwan Lim, Xiang-Dong Fu, Shunmin He, Runsheng Chen

Posted 20 Aug 2019
bioRxiv DOI: 10.1101/740753

Retrotransposons are extensively populated in vertebrate genomes, which, when active, are thought to cause genome instability with potential benefit to genome evolution. Retrotransposon-derived RNAs are also known to give rise to small endo-siRNAs to help maintain heterochromatin at their sites of transcription; however, as not all heterochromatic regions are equally active in transcription, it remains unclear how heterochromatin is maintained across the genome. Here, we attack these problems by defining the origins of repeat-derived RNAs and their specific chromatin registers in Drosophila S2 cells. We demonstrate that repeat RNAs are predominantly derived from active Gypsy elements, and upon their processing by Dicer-2, these endo-siRNAs act in cis and trans to help maintain pericentromeric heterochromatin. Remarkably, we show that synthetic repeat-derived siRNAs are sufficient to rescue Dicer-2 deficiency-induced defects in heterochromatin formation in interphase and chromosome segregation during mitosis, thus demonstrating that active retrotransposons are actually required for stable genetic inheritance.

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