Telomere-to-telomere assemblies of cattle and sheep Y-chromosomes uncover divergent structure and gene content

Abstract

Reference genomes of cattle and sheep have lacked contiguous assemblies of the sex-determining Y chromosome. Here, we assemble complete and gapless telomere to telomere (T2T) Y chromosomes for these species. We find that the pseudo-autosomal regions are similar in length, but the total chromosome size is substantially different, with the cattle Y more than twice the length of the sheep Y. The length disparity is accounted for by expanded ampliconic region in cattle. The genic amplification in cattle contrasts with pseudogenization in sheep suggesting opposite evolutionary mechanisms since their divergence 19MYA. The centromeres also differ dramatically despite the close relationship between these species at the overall genome sequence level. These Y chromosomes have been added to the current reference assemblies in GenBank opening new opportunities for the study of evolution and variation while supporting efforts to improve sustainability in these important livestock species that generally use sire-driven genetic improvement strategies.

Fig. 1. Global structure of the cattle and sheep Y chromosomes.

The structure of the cattle and the sheep Y-chromosomes showing the differences and the similarities between the two species. A The self-identity dotplots highlight the mosaic of repetitive sequence on the q-arms while the tracks below it show the different sequence classes, gene annotation, LINEs and SINEs. B The repeat content annotation indicates that more than half of both Y-chromosomes is repetitive DNA. C Centromere content and organization shows that the two Y-chromosomes have tandemly arrayed repeat unit at the centromere; while the cattle centromeric repeat is organized into a higher order repeat (HOR) of a 73 bp monomer, the sheep repeat unit is a composite of a tandem LINE and SINE element with spacer DNA between the copies. Source data are provided as a Source Data file.

Fig. 2. Ampliconic genes content comparison between cattle and sheep.

A The copy distribution of the protein-coding and the pseudogene copies of the ampliconic genes families on the cattle and sheep Y-chromosomes show remarkable differences (Source data are provided as a Source Data file). B The gene density showing the number of ampliconic genes across the Y-chromosomes calculated in 100 kb bin sizes highlighting the loci of the protein-coding genes on the upper tracks and the pseudogenes on the lower tracks. There are no protein-coding copies of TSPY1 on the Sheep-Y on the lower panel a TSPY1 island (high blue clustered spike) is located on the cattle-Y harboring a tandem array of 44 copies out of the total 68 protein-coding copies on the chromosome. More pseudogenes are found on the Sheep-Y relative to the protein-coding genes suggesting that some of the ampliconic genes are being pseudogenized, losing their protein-coding capabilities.

Fig. 3. Content and organization of the Y-chromosome centromeres.

A The Cattle-Y centromere is organized as a tandem array of highly identical higher-order repeat (HOR) unit spanning 2.5 Mb. The 3.7 kb HOR contains copies of a 73 bp monomeric unit arranged into four segments where segments 1 and 3 are tandem arrays of 5 copies (5-mer) and 6 copies (6-mer) respectively in red color while segments 2 and 4 in light blue color contain copies of the monomeric unit but not in tandem arrays as in segments 1 and 3. The arrows representing the monomers have different color densities to highlight the divergence between them. B The Sheep-Y centromere spanning about 120.7 kb organized as an array of a 2.5 kb composite repeat unit comprising a BOV-A2 SINE and a BovB LINE tranposable elements embedded between two segments of DNA.