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, 18 (6), 965-73

Bird-like Sex Chromosomes of Platypus Imply Recent Origin of Mammal Sex Chromosomes

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Bird-like Sex Chromosomes of Platypus Imply Recent Origin of Mammal Sex Chromosomes

Frédéric Veyrunes et al. Genome Res.

Abstract

In therian mammals (placentals and marsupials), sex is determined by an XX female: XY male system, in which a gene (SRY) on the Y affects male determination. There is no equivalent in other amniotes, although some taxa (notably birds and snakes) have differentiated sex chromosomes. Birds have a ZW female: ZZ male system with no homology with mammal sex chromosomes, in which dosage of a Z-borne gene (possibly DMRT1) affects male determination. As the most basal mammal group, the egg-laying monotremes are ideal for determining how the therian XY system evolved. The platypus has an extraordinary sex chromosome complex, in which five X and five Y chromosomes pair in a translocation chain of alternating X and Y chromosomes. We used physical mapping to identify genes on the pairing regions between adjacent X and Y chromosomes. Most significantly, comparative mapping shows that, contrary to earlier reports, there is no homology between the platypus and therian X chromosomes. Orthologs of genes in the conserved region of the human X (including SOX3, the gene from which SRY evolved) all map to platypus chromosome 6, which therefore represents the ancestral autosome from which the therian X and Y pair derived. Rather, the platypus X chromosomes have substantial homology with the bird Z chromosome (including DMRT1) and to segments syntenic with this region in the human genome. Thus, platypus sex chromosomes have strong homology with bird, but not to therian sex chromosomes, implying that the therian X and Y chromosomes (and the SRY gene) evolved from an autosomal pair after the divergence of monotremes only 166 million years ago. Therefore, the therian X and Y are more than 145 million years younger than previously thought.

Figures

Figure 1.
Figure 1.
BACs mapped by FISH to (a–d) the sex chromosomes and (e–g) autosomes orthologous to the human X on male platypus metaphase spreads: (a) CH236-72 A21; (b) CH236-3 C11; (c) CH236-20 M7; (d) (green) CH236-271 I19 and (red) CH236-165 F5; (e) (green) CH236-359 L11 (representing UltraContig462) and (red) CH236-97 I3 (chromosome 15 anchor BAC); (f) (green) CH236-427 K7 (representing UltraContig222) and (red) Ch236-330 L7 (chromosome 18 anchor BAC): (g) (green) CH236-337 O23 (representing UltraContig420) and (red) CH236-30 G14 (representing UltraContig519). Scale bars, 10 μm.
Figure 2.
Figure 2.
The 10 sex chromosomes from male platypus with the location of the 32 BACs mapped in this study and four BACs/genes mapped in recent studies (colored bands). BAC numbers are indicated, and homology with chicken is represented by different colors. BACs that hybridized to both an X and a Y revealed pseudoautosomal regions and are connected by lines.
Figure 3.
Figure 3.
The human (HSA) X chromosome compared to orthologous platypus (OAN), opossum (MDO), and chicken (GGA) chromosomes. All shades of blue are orthologous to the X conserved region (XCR) of the placental mammal X chromosome. Royal blue on the human X, opossum X, and chicken 4p were anchored to platypus chromosome 6 prior to this study; navy blue regions on these chromosomes are orthologous to unanchored UltraContigs in the platypus assembly; whereas pale blue is predicted orthology with platypus chromosome 6. Red is orthologous to X added region (XAR), and pink is the predicted orthology to platypus chromosomes 15 and 18. None of the X added orthologous regions were anchored in platypus before this study. The numbers of all unanchored UltraContigs (see Table 1 for list of anchoring BACs) are listed left of the chicken and opossum chromosomes, and right of the human X. FISH locations of BACs on platypus chromosomes 6, 15, and 18 are shown, and lines indicate orthology with the human, opossum, and chicken genomes. Some of the platypus UltraContigs have been broken up in human, opossum, and/or chicken. Vertical lines next to platypus chromosome 6 indicate that FISH could not achieve resolution between BACs.
Figure 4.
Figure 4.
Phylogeny displaying the different sex chromosome systems of major vertebrate groups. Homology between genomes, and with ancestral autosomes, is indicated by the same color. Key events are marked on the tree. (Green) A chicken-like ZW system appears to be ancestral to all amniotes, which was retained in birds and caught up in the meiotic chain of monotremes. There was a switch from ZW to XY systems independently in both therian and monotreme mammals. (Red) The region added to the sex chromosomes of placental mammals was broken independently in opossum and monotremes. (Green) The autosome orthologous to the bird Z chromosome was broken in the therian ancestor and subsequently scrambled onto several autosomes in mouse; therefore only the chromosome carrying Dmrt1 is displayed in that species.

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