The origin and loss of the ubiquitin activating enzyme gene on the mammalian Y chromosome

Abstract

Mammalian sex chromosomes are thought to be descended from a homologous pair of autosomes: a testis-determining allele which defined the Y chromosome arose, recombination between the nascent X and Y chromosomes became restricted and the Y chromosome gradually lost its non-essential genetic functions. This model was originally inferred from the occurrence of few Y-linked genetic traits, pairing of the X and Y chromosomes during male meiosis and, more recently, the existence of X-Y homologous genes. The comparative analysis of such genes is a means by which the validity of this model can be evaluated. One well-studied example of an X-Y homologous gene is the ubiquitin activating enzyme gene ( UBE1 ), which is X-linked with a distinct Y-linked gene in many eutherian ('placental') and metatherian (marsupial) mammals. Nonetheless, no UBE1 homologue has yet been detected on the human Y chromosome. Here we describe a more extensive study of UBE1 homologues in primates and a prototherian mammal, the platypus. Our findings indicate that UBE1 lies within the X-Y pairing segment of the platypus but is absent from the human Y chromosome, having been lost from the Y chromosome during evolution of the primate lineage. Thus UBE1 illustrates the key steps of 'autosomal to X-specific' evolution of genes on the sex chromosomes.

Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes

“…3). These localizations are inconsistent with early mapping using radioactive in situ hybridization with human cDNA probes (Watson et al 1990;Wilcox et al 1996;Mitchell et al 1998) but consistent with later studies using FISH mapping of homologous lambda phage clones (Waters et al 2005). These contradictions can be attributed to previous misidentification of Giemsa-stained pair 6 and X 1 , and to the unreliability of radioactive in situ hybridization of small heterologous human clones onto divergent platypus chromosomes.…”

“…Early comparative mapping using radioactive in situ hybridization with heterologous probes suggested that X 1 , located at one end of the chain, shared homology with the ancient part of the mammalian X (Watson et al 1990;Wilcox et al 1996;Mitchell et al 1998; but see also Waters et al 2005). At the other end of the chain, fluorescent in situ hybridization (FISH) of a large insert BAC-clone showed that X 5 contained the Z-borne putative bird sex-determination gene DMRT1 El-Mogharbel et al 2007).…”

Gene dosage in the evolution and function of mammalian sex chromosomes

“…Independent attrition also explains why a gene may show different stages of loss or specialization in different lineages. For instance, UBE1Y maps to the large PAR in monotremes, recognizes differentiated but active copies on the X and Y in marsupials, mouse and other eutherians, is degraded in some primates and completely lost in hominids (Mitchell et al, 1998).…”

Sex chromosomes and sex determination in weird mammals

“…Rather than discrete classes of genes with different evolutionary origins, the differences in copy number, activity and functions that distinguish "Class I and II" genes seem to be stages through which once autosomal genes pass on their way to either male-specific glory or inactivity and evolutionary oblivion (Graves, 2002). This scenario is supported by studies of UBE1Y, which displays all these stages in different mammalian lineages (Mitchell et al, 1998).…”