DSSS - Recurrent innovation of germline genome regulation

Gene expression relies on core protein machineries that function at almost all protein-coding genes, including basal transcription factors and co-transcriptional processing factors. Animal germ cells, however, express alternative, paralog-based core machineries that enable gametogenesis. The molecular mechanism and gene regulatory impact of such paralog-based genome regulation, however, remains underexplored. We have identified a testis-specific Polymerase Associated Factor 1 Complex (tPAF) composed of paralogs of canonical Polymerase Associated Factor 1 Complex (Paf1C) proteins. Defective transcription termination in tPAF mutants causes aberrant expression of hundreds of downstream genes due to read-in transcription, compromising cell type-specific gene expression in spermatocytes leading to male infertility. Unlike most essential genes, tPAF, however, evolves unexpectedly fast. In fact, we find rapid evolution to be a shared feature of paralog-based germline gene expression pathways and we uncover functional molecular innovation underlying such evolutionary signatures. We propose that such paralog-based complexes form functional pathways and represent valuable model systems for mechanistic and evolutionary investigation of animal germline genome regulation.