Genetic Factors Linking Nucleolar Stress with R2 Retrotransposon Expression in Drosophila melanogaster

<i>R2</i> retrotransposons reside exclusively within the <i>28S</i> regions of 10-20% of all rDNA genes comprising the nucleolar organizer loci on the X and Y chromosomes of <i>Drosophila melanogaster</i>. These <i>R2</i>-inserted genes are normally silent and heterochromatic. When expressed, however, the <i>R2</i> transcript is co-transcribed with the <i>28S</i> rRNA. Self-cleavage releases a 3.6 kb mature <i>R2</i> transcript that encodes a single protein with endonuclease and reverse transcriptase activities that facilitate <i>R2</i> element transposition by target-primed reverse transcription. While we know the molecular details of <i>R2</i> transposition, we know little about the genetic mechanisms that initiate <i>R2</i> transcription. Here, we examine <i>R2</i> expression in wild type versus mutant backgrounds. <i>R2</i> expression in stage 1-4 wild type egg chambers was variable depending on the stock. <i>R2</i> expression was silent in wild type stages 5-10 but was consistently active during nurse cell nuclear breakdown in stages 12-13 regardless of the genetic background. Massive <i>R2</i> expression occurred in stages 5-10 upon loss of Udd, an RNA Pol I transcription factor. Similarly, loss of Nopp140, an early ribosome assembly factor, induced <i>R2</i> expression more so in somatic tissues. Interestingly, over-expression of the Nopp140-RGG isoform but not the Nopp140-True isoform induced <i>R2</i> expression in larval somatic tissues, suggesting Nopp140-RGG could potentially affect rDNA chromatin structure. Conversely, <i>Minute</i> mutations in genes encoding ribosomal proteins had minor positive effects on <i>R2</i> expression. We conclude that <i>R2</i> expression is largely controlled by factors regulating RNA Pol I transcription and early ribosome assembly.