Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka

Abstract

Sequencing of the human Y chromosome has uncovered the peculiarities of the genomic organization of a heterogametic sex chromosome of old evolutionary age, and has led to many insights into the evolutionary changes that occurred during its long history. We have studied the genomic organization of the medaka fish Y chromosome, which is one of the youngest heterogametic sex chromosomes on which molecular data are available. The Y specific and adjacent regions were sequenced and compared to the X. The male sex-determining gene, dmrt1bY, appears to be the only functional gene in the Y-specific region. The Y-specific region itself is derived from the duplication of a 43-kb fragment from linkage group 9. All other coduplicated genes except dmrt1bY degenerated. The Y-specific region has accumulated large stretches of repetitive sequences and duplicated pieces of DNA from elsewhere in the genome, thereby growing to 258 kb. Interestingly the non-recombining part of the Y did not spread out considerably from the original duplicated fragment, possibly because of a large sequence duplication bordering the Y-specific fragment. This may have conserved the more ancestral structure of the medaka Y and provides insights into some of the initial processes of Y chromosome evolution.

Linkage Analysis Reveals the Independent Origin of Poeciliid Sex Chromosomes and a Case of Atypical Sex Inheritance in the Guppy (Poecilia reticulata)

“…At least four different chromosomes gave rise to the SDL in different species of Oryzias, suggesting that several master sexdetermining genes may have evolved even in closely related species (Takehana et al 2007a,b;Tanaka et al 2007). The O. latipes Dmrt1bY containing the Y-specific segment is only 250 kb in length, while the rest of the Y is completely homologous with the X chromosome (Kondo et al 2006), suggesting that a small segment of DNA, having at least one important functional gene for male sex determination, is sufficient to serve as a focal point for sex chromosome divergence.…”

Heritable artificial sex chromosomes in the medaka, Oryzias latipes

“…The Yspecific region proved to be 258 kb long and DMY appeared to be the only functional gene in this region (Kondo et al, 2006). In addition, we found a wild medaka population in which Y chromosomes bearing a loss-offunction DMY mutation were present in one-third of females (Otake et al, 2008).…”

“…Here, we show that the introduction of DMY is sufficient to produce an artificial sex chromosome in this species. Furthermore, unlike Sry, DMY appears to have arisen from duplication of the autosomal DMRT1 gene and its insertion into LG 1 (Kondo et al, 2006). This event suggests that any chromosome could have become the sex chromosome in the ancestor of medaka.…”

“…One of these DM-domain genes, DMRT1 (DM-related transcription factor 1), has been implicated in male sexual development in vertebrates (Zarkower, 2001). The cDNA sequences of medaka DMY and DMRT1 show a high similarity (about 80%), and comparative analysis of X and Y chromosomes indicated that DMY arose through a duplication event of the autosomal DMRT1 gene (Kondo et al, 2006). This DMRT1 duplication event is estimated to have occurred about 10 million years ago, suggesting that the medaka Y chromosome is one of the youngest male sex-determining systems in vertebrates.…”

Inherited XX sex reversal originating from wild medaka populations

“…In the medaka, the sex chromosomes are homomorphic (Matsuda et al, 1998) and sex-reversed XY females and XX males are fully fertile (Yamamoto 1953(Yamamoto , 1958. The Y chromosome-specific region in the medaka is no more than 258 kb in length and DMY is regarded as the only functional gene in the Y-specific region (Kondo et al, 2006). Thus, the medaka Y chromosome is regarded as equal to the X chromosome except for its sexdetermining function.…”