Nuclear Chromosome Dynamics in the Drosophila Male Germ Line Contribute to the Nonrandom Genomic Distribution of Retrogenes

The origin of RNA-based gene duplicates, that is, retrogenes, involves the reverse transcription of an mRNA derived from a parental gene to generate a cDNA copy, its insertion elsewhere in the genome, and the recruitment of regulatory sequences. Drosophila retrogenes are preferentially expressed in testis and a higher than expected number transpose to autosomal locations from the X chromosome. However, the influence of genomic context on the insertion preference of retrogenes remains poorly understood. We find that the distribution of retrogenes in the Drosophila melanogaster genome can be explained by an insertion bias toward chromosome domains containing testis-biased genes that are located at the nuclear periphery in somatic cells, but at inner positions in the male germ line. The lower fraction of these chromosome domains accessible in the male germ line on the X chromosome as compared with the autosomes also contributes to the scarcity of retrogenes on the X chromosome.