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RNA-mediated nucleosome depletion is required for elimination of transposon-derived DNA

View ORCID ProfileAditi Singh, Xyrus X. Maurer-Alcalá, Therese Solberg, Silvan Gisler, Michael Ignarski, View ORCID ProfileEstienne C. Swart, View ORCID ProfileMariusz Nowacki
doi: https://doi.org/10.1101/2022.01.04.474918
Aditi Singh
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
2Graduate School for Cellular and Biomedical Sciences, University of Bern, Freiestrasse 1, 3012 Bern, Switzerland
3Max Planck Institute for Biology, Max Planck Ring 5, 72076, Tubingen, Germany
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Xyrus X. Maurer-Alcalá
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
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Therese Solberg
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
2Graduate School for Cellular and Biomedical Sciences, University of Bern, Freiestrasse 1, 3012 Bern, Switzerland
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Silvan Gisler
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
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Michael Ignarski
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
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Estienne C. Swart
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
3Max Planck Institute for Biology, Max Planck Ring 5, 72076, Tubingen, Germany
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Mariusz Nowacki
1Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
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  • For correspondence: mariusz.nowacki@izb.unibe.ch
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Abstract

Small RNAs are known to mediate silencing of transposable elements and other genomic loci, increasing nucleosome density and preventing undesirable gene expression. Post-zygotic development of the Paramecium somatic genome requires elimination of thousands of transposon remnants (IESs) and transposable elements that are scattered throughout the germline genome (Garnier et al. 2004). The elimination process is guided by Piwi-associated small RNAs and leads to precise cleavage at IES boundaries (Bouhouche et al. 2011; Furrer et al. 2017). Previous research suggests that small RNAs induce heterochromatin formation within IESs, which, in turn, is required for DNA elimination (Liu et al. 2007). Here we show that IES recognition and precise excision is facilitated by recruitment of a homolog of a chromatin remodeler ISWI, which depletes target genomic regions of nucleosomes, making the chromatin accessible for DNA cleavage. ISWI knockdown in Paramecium leads to pronounced inhibition of DNA elimination. Furthermore, nucleosome profiling indicates that ISWI is required for IES elimination in nucleosome-dense genomic regions, while other IESs do not require small RNAs or ISWI for excision. ISWI silencing notably also reduces DNA elimination precision, resulting in aberrant excision at alternative IES boundaries. In summary, we demonstrate that chromatin remodeling that increases DNA accessibility together with small RNAs are necessary for efficient and precise DNA elimination in Paramecium.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 05, 2022.
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RNA-mediated nucleosome depletion is required for elimination of transposon-derived DNA
Aditi Singh, Xyrus X. Maurer-Alcalá, Therese Solberg, Silvan Gisler, Michael Ignarski, Estienne C. Swart, Mariusz Nowacki
bioRxiv 2022.01.04.474918; doi: https://doi.org/10.1101/2022.01.04.474918
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RNA-mediated nucleosome depletion is required for elimination of transposon-derived DNA
Aditi Singh, Xyrus X. Maurer-Alcalá, Therese Solberg, Silvan Gisler, Michael Ignarski, Estienne C. Swart, Mariusz Nowacki
bioRxiv 2022.01.04.474918; doi: https://doi.org/10.1101/2022.01.04.474918

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