Selfish conflict underlies RNA-mediated parent-of-origin effects

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 and Alejandro Burga ()
Additional contact information
Pinelopi Pliota: Vienna BioCenter (VBC)
Hana Marvanova: Vienna BioCenter (VBC)
Alevtina Koreshova: Vienna BioCenter (VBC)
Yotam Kaufman: The Hebrew University of Jerusalem
Polina Tikanova: Vienna BioCenter (VBC)
Daniel Krogull: Vienna BioCenter (VBC)
Andreas Hagmüller: Vienna BioCenter (VBC)
Sonya A. Widen: Vienna BioCenter (VBC)
Dominik Handler: Vienna BioCenter (VBC)
Joseph Gokcezade: Vienna BioCenter (VBC)
Peter Duchek: Vienna BioCenter (VBC)
Julius Brennecke: Vienna BioCenter (VBC)
Eyal Ben-David: The Hebrew University of Jerusalem
Alejandro Burga: Vienna BioCenter (VBC)

Nature, 2024, vol. 628, issue 8006, 122-129

Abstract: Abstract Genomic imprinting—the non-equivalence of maternal and paternal genomes—is a critical process that has evolved independently in many plant and mammalian species1,2. According to kinship theory, imprinting is the inevitable consequence of conflictive selective forces acting on differentially expressed parental alleles3,4. Yet, how these epigenetic differences evolve in the first place is poorly understood3,5,6. Here we report the identification and molecular dissection of a parent-of-origin effect on gene expression that might help to clarify this fundamental question. Toxin-antidote elements (TAs) are selfish elements that spread in populations by poisoning non-carrier individuals7–9. In reciprocal crosses between two Caenorhabditis tropicalis wild isolates, we found that the slow-1/grow-1 TA is specifically inactive when paternally inherited. This parent-of-origin effect stems from transcriptional repression of the slow-1 toxin by the PIWI-interacting RNA (piRNA) host defence pathway. The repression requires PIWI Argonaute and SET-32 histone methyltransferase activities and is transgenerationally inherited via small RNAs. Remarkably, when slow-1/grow-1 is maternally inherited, slow-1 repression is halted by a translation-independent role of its maternal mRNA. That is, slow-1 transcripts loaded into eggs—but not SLOW-1 protein—are necessary and sufficient to counteract piRNA-mediated repression. Our findings show that parent-of-origin effects can evolve by co-option of the piRNA pathway and hinder the spread of selfish genes that require sex for their propagation.

Date: 2024
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DOI: 10.1038/s41586-024-07155-z

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