Novel Gene Acquisition on Carnivore Y Chromosomes

Abstract

Despite its importance in harboring genes critical for spermatogenesis and male-specific functions, the Y chromosome has been largely excluded as a priority in recent mammalian genome sequencing projects. Only the human and chimpanzee Y chromosomes have been well characterized at the sequence level. This is primarily due to the presumed low overall gene content and highly repetitive nature of the Y chromosome and the ensuing difficulties using a shotgun sequence approach for assembly. Here we used direct cDNA selection to isolate and evaluate the extent of novel Y chromosome gene acquisition in the genome of the domestic cat, a species from a different mammalian superorder than human, chimpanzee, and mouse (currently being sequenced). We discovered four novel Y chromosome genes that do not have functional copies in the finished human male-specific region of the Y or on other mammalian Y chromosomes explored thus far. Two genes are derived from putative autosomal progenitors, and the other two have X chromosome homologs from different evolutionary strata. All four genes were shown to be multicopy and expressed predominantly or exclusively in testes, suggesting that their duplication and specialization for testis function were selected for because they enhance spermatogenesis. Two of these genes have testis-expressed, Y-borne copies in the dog genome as well. The absence of the four newly described genes on other characterized mammalian Y chromosomes demonstrates the gene novelty on this chromosome between mammalian orders, suggesting it harbors many lineage-specific genes that may go undetected by traditional comparative genomic approaches. Specific plans to identify the male-specific genes encoded in the Y chromosome of mammals should be a priority.

Gene Duplication, Gene Conversion and the Evolution of the Y Chromosome

“…It is less clear whether similar patterns characterize other animal species. Current (albeit incomplete) data suggest that gene family amplification and retention might be common Y chromosome attributes (Rozen et al 2003;Verkaar et al 2004;Murphy et al 2006;Alfö ldi 2008;Wilkerson et al 2008;Krsticevic et al 2009), although the prevalence of Y-linked gene conversion outside the human and chimp lineages is less clear (but see Geraldes et al 2010). Future sequencing efforts, including evidence for gene conversion among Y-linked genes in nonhuman species, will help to determine the general relevance of the duplication and gene conversion model presented here.…”

“…In contrast to many of the single-copy genes with X-linked homologs, members of Y-linked gene families are apparently not degenerating, but rather have become fixed and maintained over many millions of years Yu et al 2008). Although Y chromosomes are not well characterized in other taxa, currently available data suggest that duplication is a common feature of Y chromosomes in other mammal species as well as Drosophila (Rozen et al 2003;Verkaar et al 2004;Murphy et al 2006;Alföldi 2008;Wilkerson et al 2008;Krsticevic et al 2009;Geraldes et al 2010). Thus, patterns of gene duplication and retention, for at least a subset of Y-linked genes, may be a general rule of Y chromosome evolution.…”

The sex-specific region of sex chromosomes in animals and plants

“…Of course, chimpanzee is lacking the two X-transposed genes acquired by the human MSY 3-4 Mya after their split. Although the human MSY appears to have limited gene loss, if any, in 6 Ma in comparison with the chimpanzee MSY, four new genes were found in the cat MSY; two are X-degenerated and the other two are originated from autosomes (Murphy et al 2006). Since cat and human diverged about 95 Mya, the two X-degenerated genes are likely lost in the human lineage, but the two genes acquired from autosomes could be lost in the human or gained after their divergence (Springer et al 2003).…”

Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution

“…We did not attempt to sequence the cat ampliconic region because previous and unpublished cytogenetic and sequence data indicate this >30-Mb region covering the long arm and pericentromeric region of the Y is comprised of a limited set of highly repetitive gene families which are difficult to assemble with next-generation sequence data, thus requiring further mapping and sequencing efforts (Supplemental Fig. 1; Supplemental Table 1; Murphy et al 2006). cDNA capture and de novo assembly of testis RNA-seq data allowed us to thoroughly characterize the cat and dog single and multicopy/ampliconic transcribed gene repertoire, which facilitated comparisons with other Y chromosomes.…”