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The evolution of an RNA-based memory of self in the face of genomic conflict

Pinelopi Pliota, Hana Marvanova, Alevtina Koreshova, Yotam Kaufman, Polina Tikanova, Daniel Krogull, Andreas Hagmüller, Sonya A. Widen, Dominik Handler, Joseph Gokcezade, Peter Duchek, Julius Brennecke, View ORCID ProfileEyal Ben-David, View ORCID ProfileAlejandro Burga
doi: https://doi.org/10.1101/2022.06.17.496645
Pinelopi Pliota
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Hana Marvanova
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
2Vienna BioCenter PhD Program, Doctoral School of the University of Vienna and Medical University of Vienna, A-1030, Vienna, Austria
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Alevtina Koreshova
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
2Vienna BioCenter PhD Program, Doctoral School of the University of Vienna and Medical University of Vienna, A-1030, Vienna, Austria
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Yotam Kaufman
3Department of Biochemistry and Molecular Biology, Institute for Medical Research Israel-Canada, The Hebrew University of Jerusalem, Jerusalem, Israel
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Polina Tikanova
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
2Vienna BioCenter PhD Program, Doctoral School of the University of Vienna and Medical University of Vienna, A-1030, Vienna, Austria
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Daniel Krogull
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
2Vienna BioCenter PhD Program, Doctoral School of the University of Vienna and Medical University of Vienna, A-1030, Vienna, Austria
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Andreas Hagmüller
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Sonya A. Widen
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Dominik Handler
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Joseph Gokcezade
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Peter Duchek
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Julius Brennecke
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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Eyal Ben-David
3Department of Biochemistry and Molecular Biology, Institute for Medical Research Israel-Canada, The Hebrew University of Jerusalem, Jerusalem, Israel
4Illumina Artificial Intelligence Laboratory, Illumina Inc, San Diego, CA, USA
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  • ORCID record for Eyal Ben-David
Alejandro Burga
1Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
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  • ORCID record for Alejandro Burga
  • For correspondence: alejandro.burga@imba.oeaw.ac.at
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Abstract

Distinguishing endogenous genes from selfish ones is essential for germline integrity. In animals, small regulatory RNAs play a central role in this process; however, the underlying principles are largely unknown. To fill this gap, we studied how selfish toxin-antidote elements (TAs) evade silencing in the nematode Caenorhabditis tropicalis. We found that the slow-1/grow-1 TA is active only when maternally inherited. Surprisingly, this parent-of-origin effect stems from a regulatory role of the toxin’s mRNA: maternal slow-1 mRNA—but not SLOW-1 protein—licenses slow-1 expression in the zygote by counteracting piRNAs. Our results indicate that epigenetic licensing—known to play a role in C. elegans sex-determination—is likely a common mechanism that hinders the spread of selfish genes in wild populations while ensuring a lasting memory of self in the germline.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* These authors jointly supervised this work

Copyright 
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-NC-ND 4.0 International license.
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Posted June 20, 2022.
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The evolution of an RNA-based memory of self in the face of genomic conflict
Pinelopi Pliota, Hana Marvanova, Alevtina Koreshova, Yotam Kaufman, Polina Tikanova, Daniel Krogull, Andreas Hagmüller, Sonya A. Widen, Dominik Handler, Joseph Gokcezade, Peter Duchek, Julius Brennecke, Eyal Ben-David, Alejandro Burga
bioRxiv 2022.06.17.496645; doi: https://doi.org/10.1101/2022.06.17.496645
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The evolution of an RNA-based memory of self in the face of genomic conflict
Pinelopi Pliota, Hana Marvanova, Alevtina Koreshova, Yotam Kaufman, Polina Tikanova, Daniel Krogull, Andreas Hagmüller, Sonya A. Widen, Dominik Handler, Joseph Gokcezade, Peter Duchek, Julius Brennecke, Eyal Ben-David, Alejandro Burga
bioRxiv 2022.06.17.496645; doi: https://doi.org/10.1101/2022.06.17.496645

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