Retrotransposon sequences are positioned throughout the genome of almost every eukaryote that has been sequenced. As mobilization of these elements can have detrimental effects on the transcriptional regulation and stability of an organism's genome, most organisms have evolved mechanisms to repress their movement. Here, we identify a novel role for the Drosophila melanogaster
Condensin II subunit, dCAP-D3 in preventing the mobilization of
retrotransposons located in somatic cell
euchromatin. dCAP-D3 regulates transcription of euchromatic gene clusters which contain or are proximal to
retrotransposon sequence. ChIP experiments demonstrate that dCAP-D3 binds to these loci and is important for maintaining a repressed
chromatin structure within the boundaries of the
retrotransposon and for repressing
retrotransposon transcription. We show that dCAP-D3 prevents accumulation of double stranded DNA breaks within
retrotransposon sequence, and decreased dCAP-D3 levels leads to a precise loss of
retrotransposon sequence at some dCAP-D3 regulated gene clusters and a gain of sequence elsewhere in the genome. Homologous chromosomes exhibit high levels of pairing in Drosophila somatic cells, and our FISH analyses demonstrate that
retrotransposon-containing euchromatic loci are regions which are actually less paired than euchromatic regions devoid of
retrotransposon sequences. Decreased dCAP-D3 expression increases pairing of homologous
retrotransposon-containing loci in tissue culture cells. We propose that the combined effects of dCAP-D3 deficiency on double strand break levels,
chromatin structure, transcription and pairing at
retrotransposon-containing loci may lead to 1) higher levels of homologous recombination between repeats flanking
retrotransposons in
dCAP-D3 deficient cells and 2) increased retrotransposition. These findings identify a novel role for the anti-pairing activities of
dCAP-D3/
Condensin II and uncover a new way in which
dCAP-D3/
Condensin II influences local
chromatin structure to help maintain
genome stability.