A syntenic region conserved from fish to Mammalian x chromosome

Abstract

Sex chromosomes bearing the sex-determining gene initiate development along the male or female pathway, no matter which sex is determined by XY male or ZW female heterogamety. Sex chromosomes originate from ancient autosomes but evolved rapidly after the acquisition of sex-determining factors which are highly divergent between species. In the heterogametic male system (XY system), the X chromosome is relatively evolutionary silent and maintains most of its ancestral genes, in contrast to its Y counterpart that has evolved rapidly and degenerated. Sex in a teleost fish, the Nile tilapia (Oreochromis niloticus), is determined genetically via an XY system, in which an unpaired region is present in the largest chromosome pair. We defined the differences in DNA contents present in this chromosome with a two-color comparative genomic hybridization (CGH) and the random amplified polymorphic DNA (RAPD) approach in XY males. We further identified a syntenic segment within this region that is well conserved in several teleosts. Through comparative genome analysis, this syntenic segment was also shown to be present in mammalian X chromosomes, suggesting a common ancestral origin of vertebrate sex chromosomes.

Figure 1

Chromosomal heterogeneity in two pairs of Nile tilapia. (a) Schematic illustration of chromosome heterogeneity detected by two-color CGH analysis. (b) XX metaphase from a female tilapia. (c) XY metaphase from a male tilapia. Signals for XX-derived probe (green) and YY-derived probe (red) are seen on the largest pair of chr 1 (arrows) and a pair of small chromosomes (asterisks).

Figure 2

Strategy of RAPD sex-linked marker selection. (a) DNA pools are derived from XX, XY, and YY individuals. (b) RAPD PCR was performed with random primer sets. Fragments derived from X-linked or Y-linked are in dashed box.

Figure 3

Characterization of RAPD markers. (a) Southern analysis revealed two X-linked fragments present in XX females and XY males but absent in YY males. (b) Results of STS PCR with primers derived from R17, R52, and R102 are listed in Table 1. An X-linked 1.3 kb band was only amplified with R52 primer1 and 2 with DNA from XX female and XY males, in contrast to a maternal 1.1 kb and a paternal 1.8 kb fragment in R102 and a 2.2 kb fragment of R17 from all XY, XX, and YY autosome. NC: negative control with H₂O instead of DNA as a PCR template.

Figure 4

Processes of syntenic segment addition or transmission during sex chromosome evolution. (blue) ▬, (green) ▬ Relic of protosex chromosomes; (red) ▬ male specific regions on the Y (MSY). Divergence times were from the literature [58, 59].