In animals, 21-35 nt long PIWI-interacting RNAs (piRNAs) silence transposable elements, regulate gene expression, and fight viral infection. piRNAs guide PIWI proteins to cleave target RNA, promote heterochromatin assembly, and methylate DNA. The architecture of the piRNA pathway allows it both to provide adaptive, sequence-5 based immunity to rapidly evolving viruses and transposons and to regulate conserved host genes. piRNAs silence transposons in the germline of most animals, while somatic piRNA functions have been lost, gained, and lost again across evolution. Moreover, most piRNA pathway proteins are deeply conserved, but different animals employ remarkably divergent strategies to produce piRNA precursor transcripts. Here, we 10 discuss how a common piRNA pathway allows animals to recognize diverse targets, ranging from selfish genetic elements to genes essential for gametogenesis.

GeneCore for preparation of the Methyl-seq libraries. Author contributionsA.Z. contributed to the design, execution and analysis of most experiments. T.A. helped established the IP conditions and performed the mass-spectrometry analysis under the guidance of J.R. and R.C.A. R.B. and Y.K. performed the bioinformatic analysis of the Methyl-seq data or sRNA-seq as well as RNA-seq data, respectively. T.S. prepared the sRNA-seq libraries and together with Y.K. the RNA-seq libraries of P20 testes. M.H and A.C. performed the homology alignment of the SPOC and TFIIS-M domains. L.V. performed the IF staining of HA-MIWI2 and generated the gonocytes microarray dataset. Y.R.P. performed the phylogenetic analysis under guidance of A.S. D.O'C. conceived and supervised this study. D.O'C. and A.Z wrote the final version of the manuscript.