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.

Characterization of the bovine pseudoautosomal boundary: Documenting the evolutionary history of mammalian sex chromosomes

“…It precludes conclusions regarding their location with respect to the PAB. However, it indicates that the higher retention rate of SHROOM2 relative to X-specific sequences that was observed in male radiation hybrids (Murphy et al 2006) may not be due to its location on the PAR.…”

“…In other mammals studied, the PAR is thought to be larger as it encompasses genes that are pseudoautosomal in (Toder et al 1997), and cat (Murphy et al 2006). The PAR of Mus musculus domesticus includes Sts, but none of the genes that are pseudoautosomal in human.…”

“…This assumption applies to lemurs (Gläser et al 1999), sheep (Toder et al 1997), cattle (Moore et al 2001), dog (Toder et al 1997), and cat (Murphy et al 2006). The PAR of Mus musculus domesticus includes Sts, but none of the genes that are pseudoautosomal in human.…”

“…An autosome to proto-gonosome translocation occurring after placental mammals diverged from marsupials has increased the size of the eutherian neo-gonosome by addition of the "X added region" (XAR) (Graves 2006). Autosome to Y transposition has augmented the content of the Y chromosome in male-beneficial genes, including retrotransposition of CDY before the divergence of marsupials and eutherians (Lahn and Page 1999;Skaletsky et al 2003), transposition of DAZ during primate evolution (Saxena et al 1996), and transposition of FLJ36031 prior to carnivore radiation and TETY1 following the divergence of cat and dog lineages (Murphy et al 2006). Moreover, the human Y euchromosome has acquired an X transposed region (XTR) after its divergence from chimpanzees (Skaletsky et al 2003).…”

Evolutionary history of novel genes on the tammar wallaby Y chromosome: Implications for sex chromosome evolution

“…4), implies that they were lost from the Yearly in eutherian evolution. In contrast, just one gene with an XCR homolog (CUL4BY) appears to be Y-borne in at least one eutherian lineage (Laurasiatheria) (Murphy et al 2006), but absent from the marsupial Y.…”