Developmental conversion of the nucleolus into an RNA Polymerase II transcriptional platform in Drosophila spermatocytes

The nucleolus is widely regarded as a specialized compartment for RNA polymerase I (Pol I)-driven ribosomal RNA transcription and ribosome biogenesis. Yet the presence of "atypical nucleoli", or nucleolus-like bodies (NLBs), which lack rRNA transcription despite containing canonical nucleolar components, has long been recognized, most notably during mammalian oogenesis and spermatogenesis. NLBs have been shown to have an essential function independent of rRNA transcription, but the nature of that function remained unclear. Here, we demonstrate that the nucleolus becomes an NLB during spermatocyte development in Drosophila melanogaster and, surprisingly, that this NLB serves as a platform for RNA polymerase II (Pol II)-mediated transcription. We find that the Y chromosome-linked fertility genes, which are heterochromatic in most cell types but highly expressed in spermatocytes, are transcribed at the spermatocyte NLB. We further show that the recruitment of active Pol II to the NLB requires known spermatocyte-specific transcriptional regulators. In their absence, the Y-linked fertility genes embedded within heterochromatin are not properly transcribed. Our findings reveal an active role for an NLB as a Pol II platform, and we propose that other NLBs may have similar functionality.