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

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 species 1,2 . According to kinship theory, imprinting is the inevitable consequence of conflictive selective forces acting on differentially expressed parental alleles 3,4 . Yet, how these epigenetic differences evolve in the first place is poorly understood 3,5,6 . 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 individuals 7–9 . 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.