Mitochondrial and repetitive DNA defining the sheep genome landscape

Repetitive DNA sequences (tandemly repeated and dispersed elements) vary in abundance, composition and organization between individuals, breeds, and related species. Here, we aimed to define the repetitive DNA landscape in sheep (Ovis aries). Whole genome sequence reads (38Gbp; 10x genome coverage) from five Kurdistani sheep individuals were investigated by graph-based read clustering (RepeatExplorer), frequency analysis of short motifs (k-mers), alignment to reference genome assemblies, de novo assembly and fluorescent in situ hybridization. To show genes in the sequences, the scrapie locus was identified and found to be associated with intermediate susceptibility. Mitochondrial genomes of breeds Hamdani and Karadi were assembled and grouped with known sheep haplogroups. Notably, abundant nuclear mitochondrial DNA segments (numts) were found at centromeres of chromosomes, and included mitochondrial sequences from ancestral species. The tandemly repeated DNA satellite I sequence represented 6% of the genome and satellite II was 2%. Meiotic analysis showed a loose chromatin loop organization of satellite I, while satellite II sequences were tightly organized and attached to the synaptonemal complex along with telomere repeats. Novel species-specific tandem sequences (1% of the genome) were also found. Non-LTR retrotransposons including LINEs and derived SINEs represented more than 20% of the genome, while DNA transposons comprise a lower proportion (<0.05%). Complete genomes of endogenous beta-retroviruses (enJSRV) plus three classes of endogenous retroviruses (ERVs) were identified. In total, repetitive sequences covered 30% of the genome, with tandemly repeated sequences at centromeres, and non-LTR retroelements families showing a centromeric to dispersed distribution with some being amplified on sex or submetacentric chromosomes. ERVs showed centromeric to dispersed distribution. Our results provide informative DNA markers within Bovidae lineages. Rapidly evolving repetitive sequences allow us to study processes of chromosome or genome evolution, homogenization or diversification in sheep, and more broadly across the Bovidae.