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

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 toxins 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.