Evolutionary insights enabled by assembly and annotation of dog's Y chromosome

Mammalian sex chromosomes, the oldest XX\XY system, are thought to have evolved from a pair of autosomes around 180 million years ago. During evolution, X and Y chromosomes differentiated along their lengths progressively. On the Y chromosome, this manifested as inhibition of recombination, genetic decay, and inversions. The mammalian Y chromosome, which is widely known for its diverse and complex repetitive sequences, differs from other chromosomes in terms of its size, genomic structure, gene content, and evolutionary trajectory. It is well known that the Y chromosome is crucial for testis development and gametogenesis. Morbidities are also related to Y chromosome dysfunction: deletions located on the Y chromosome can cause defective spermatogenesis and male sterility, while tumour susceptibility is also linked to Y chromosome genes. The Y chromosome is also a unique tracer of ancestry; its paternal genetic information enables the investigation of male demography and the application of forensic medicine. Humans, mice, rhesus macaques, chimpanzees, and cattle are just a few of the model species for which whole or almost complete Y chromosome sequences have been obtained. In this effort, a dog Y chromosome was assembled to high contiguity and used to shed light on genome structure, the course of Y chromosome evolution, and gene features. Dog Y chromosome sequences are based on reads from a Labrador retriever dog produced with various sequencing platforms. Long reads of PacBio sequencing were assembled using Falcon and Flye, followed by scaffolding steps with Bionano and Dovetail Hi-C technologies. Two generated superscaffolds were then oriented and connected resulting in dog male-specific Y chromosome sequences of 6.78 Mb in length. Constituents of the assembled Y chromosome include a single-copy region, multiple-copy region, X-transposed regions, and autosomal homologous sequences. Other unique features of the chromosome include the detection of massive repetitive sequences, such as the enrichment of LINE transposable elements at the distal end of MSY and 0.86 Mb of LINE1_CF that occur as tandem repeats. MSY genes were annotated and characterised to determine their copy number, transcriptional expression, phylogeny, divergence rate, and polymorphisms. It is inferred that dog MSY genes arose from three evolutionary strata, and five genes -- TSPY, CUL4BY, BCORY, SRY, and UBE1Y – occur as multiple copies. Based on their expression, MSY genes were grouped into three categories: ubiquitous, low-expression, and testis-specific. These categories displayed significantly different evolutionary rates, potentially as a consequence, or in response, to their presumed different functional roles. Phylogenetic analysis identified evidence of conversion events in seven MSY genes, revealing a dynamic evolution of dog Y chromosomes. The pseudoautosomal boundary (PAB) of dog sex chromosomes was also defined. The dog PAB descended from the common ancestor of the Canidae. The PAB contains CLDN34 and TETY2 in the X-linked and Y-linked PAB, respectively. CLDN34 and TETY2 appear to share the same promoter in the PAB and they are co-expressed in the testes. The PAB’s SINE content accumulated near the PAB, suggesting that these small mobile elements may have catalysed or reinforced inhibition of recombination in this region. Finally, the dog's Y chromosome was found to have a novel gene called PRSSLY. This unusual gene appears to be the first gene to arise from the paired ancestral gene that was lost from mammalian X chromosomes, but maintained on Y chromosomes. Single-cell transcriptomics and in situ hybridisation analyses revealed that PRSSLY expression occurs within the semineferours tubules of the testes, suggesting that its encoded protein facilitates spermatogenesis. Taken together, this project elucidated lineage-specific characteristics of the dog Y chromosome and underlined its dynamic nature through gene activity, structural features, and boundary sequences. These discoveries add to the understanding of mammalian Y chromosome evolution and provide the scientific community with a valuable resource to improve whole genome sequence analysis.

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