The retrotransposon R2 maintains Drosophila ribosomal DNA repeats

Ribosomal DNA (rDNA) loci contain hundreds of tandemly repeated copies of ribo-somal RNA genes needed to support cellular viability. This repetitiveness makes it highly susceptible to copy number (CN) loss due to intrachromatid recombination between rDNA copies, threatening multigenerational maintenance of rDNA. How this threat is counteracted to avoid extinction of the lineage has remained unclear. Here, we show that the rDNA-specific retrotransposon R2 is essential for restorative rDNA CN expansion to maintain rDNA loci in the Drosophila male germline. The depletion of R2 led to defective rDNA CN maintenance, causing a decline in fecun-dity over generations and eventual extinction. We find that double-stranded DNA breaks created by the R2 endonuclease, a feature of R2's rDNA-specific retrotransposi-tion, initiate the process of rDNA CN recovery, which relies on homolog y-dependent repair of the DNA break at rDNA copies. This study reveals that an active retrotrans-poson provides an essential function for its host, contrary to transposable elements' reputation as entirely selfish. These findings suggest that benefiting host fitness can be an effective selective advantage for transposable elements to offset their threat to the host, which may contribute to retrotransposons' widespread success throughout taxa.

Automated summary

A specific retrotransposon called R2 is essential for maintaining the copy number of ribosomal DNA (rDNA) in Drosophila male germline. R2 induces double-stranded DNA breaks at rDNA copies, triggering their repair and preventing copy number loss. This study reveals the important role of retrotransposons in host fitness.