Conserved host genes act as anchors for fast-evolving piRNA clusters via promoter hijacking

PiRNA clusters evolve rapidly but are strictly regulated at the same time. Previous reports have suggested a co-transcription mechanism using tight regulation of coding genes. To test whether the "Promoter Hijacking" hypothesis is a plausible mechanism, we developed a new method to identify gene orthologs in poorly annotated genomes of placental mammals and investigated co-transcription of stochastic piRNA clusters. Our method uses context aware Hidden Markov Models analysis allowing the resolution of ambiguities between paralogs using the nearby genes. We demonstrate that the identified genes are preferentially expressed in the testes, where the piRNA pathway is most active. Our findings suggest the existence of dual-function loci, where the host gene retains its primary biological function, i.e. the production of an essential transcript or protein, subjecting the locus to strong purifying selection and ensuring its genomic stability. Concurrently, the locus acquires a secondary immune function by the generation of a long, target-laden precursor transcript that feeds the piRNA biogenesis pathway. This secondary region remains free from protein-coding constraints, allowing it to rapidly accumulate and retain new target insertions. Thus, "Promoter Hijacking" mechanism effectively updates genomic immune memory without compromising the stability or function of the host locus.