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, 8 (11), R243

The Multiple Sex Chromosomes of Platypus and Echidna Are Not Completely Identical and Several Share Homology With the Avian Z

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The Multiple Sex Chromosomes of Platypus and Echidna Are Not Completely Identical and Several Share Homology With the Avian Z

Willem Rens et al. Genome Biol.

Abstract

Background: Sex-determining systems have evolved independently in vertebrates. Placental mammals and marsupials have an XY system, birds have a ZW system. Reptiles and amphibians have different systems, including temperature-dependent sex determination, and XY and ZW systems that differ in origin from birds and placental mammals. Monotremes diverged early in mammalian evolution, just after the mammalian clade diverged from the sauropsid clade. Our previous studies showed that male platypus has five X and five Y chromosomes, no SRY, and DMRT1 on an X chromosome. In order to investigate monotreme sex chromosome evolution, we performed a comparative study of platypus and echidna by chromosome painting and comparative gene mapping.

Results: Chromosome painting reveals a meiotic chain of nine sex chromosomes in the male echidna and establishes their order in the chain. Two of those differ from those in the platypus, three of the platypus sex chromosomes differ from those of the echidna and the order of several chromosomes is rearranged. Comparative gene mapping shows that, in addition to bird autosome regions, regions of bird Z chromosomes are homologous to regions in four platypus X chromosomes, that is, X1, X2, X3, X5, and in chromosome Y1.

Conclusion: Monotreme sex chromosomes are easiest to explain on the hypothesis that autosomes were added sequentially to the translocation chain, with the final additions after platypus and echidna divergence. Genome sequencing and contig anchoring show no homology yet between platypus and therian Xs; thus, monotremes have a unique XY sex chromosome system that shares some homology with the avian Z.

Figures

Figure 1
Figure 1
Flow karyotype of T. aculeatus. The left panel shows the upper part and the right panel the lower enlarged part of the flow karyotype. The following chromosomes sort together: 13,14; 18,19; 20,21; and 25,26. Chromosomes 1, 6, and 27 each are polymorphic and are represented by two peaks.
Figure 2
Figure 2
G-banded karyotype of T. aculeatus. Top: the male has 27 chromosome pairs and 9 unpaired chromosomes. Three kinds of information are given next to the chromosomes. Chromosomes 3, 6, and X5 contain the NOR regions. Certain chromosomes have specific regions represented by colored bars on the left of the chromosomes, 'w' means that the region is relatively under-represented (see text). The numbers on the right refer to platypus chromosome paints that hybridized to the indicated regions. Middle: the pairing regions of the nine sex chromosomes determined by chromosome painting on mitotic preparations. Those of Y3 with X3 could not be determined in mitotic metaphases. Bottom: G-banded female karyotype of T. aculeatus. The female has 32 chromosome pairs and no unpaired chromosomes.
Figure 3
Figure 3
The NOR regions of T. aculeatus. FISH with a 28S specific probe was used for identification.
Figure 4
Figure 4
Male Tac chromosome identification. (a) Tac 27 is a pair. (b) Paint X1 identifies X1 and Y1q. (c) Paint Y1 covers chromosome Y1 and X1p. (d) Paint X2 identifies X2 and the region of homology on Y1 and Y2. (e) Paint Y2 identifies Y2 and the region of homology on X2 and X3. (f) Paint X3 covers X3 and the pairing region on Y2. (g) Paint Y3 identifies chromosome Y3; no homologous regions were observed. (h) Paint X4 covers X4, Y3 and a heterochromatic centromeric region on Oan 22 or 23. (i) Paint Y4 identifies Y4 and the region of homology on X5. (j) Paint X5 covers X5 plus the pairing region on Y4. The arrow head points to a heterochromatic centromeric region on an autosome.
Figure 5
Figure 5
Female Tac chromosome identification. (a) Paint Y1 covers two copies of X1p, chromosome Y1 is not present. (b) Paint Y2 covers the homology regions on two copies of X2 and X3; Y2 is not present. (c) Paint X3 hybridizes to the chromosome pair X3. (d) Paint X5 hybridized to the chromosome pair X5. (e) Tac meiotic chain configuration. Hybridization with telomeric probe confirms a chain of nine elements. (f) Paint Y4 identifies the last but one chromosome in the chain. (g) Paint X4 covers X4 and Y3, the seventh and sixth element of the chain, the chain configuration is at the right.
Figure 6
Figure 6
G-banded karyotype of O. anatinus. The numbers on the right refer to echidna chromosome paints that hybridized to the indicated regions; compare with Figure 2 top.
Figure 7
Figure 7
Examples of cross-species chromosome painting to autosomes. (a) Paint Oan 7 and (b) paint Oan 16 hybridized to Tac 6q and 9p, and Tac 19, respectively. (c) Paint Tac 7 and (d) paint Tac 6 hybridized to Oan 2p and Oan 7q (reverse of 6a), respectively. Note that Tac 6 is a NOR-bearing chromosome but Oan 7 is not.
Figure 8
Figure 8
Oan chromosome paints hybridized to male Tac metaphases. (a) Paint Oan Y1 covers Tac Y1 and Tac X1p. (b) Paint Oan X2 hybridizes to Tac X2 and the pairing region on Tac Y2. (c) Paint Oan Y2 covers Tac Y2 and hybridizes to the pairing regions on Tac X2 and Tac X3. (d) Paint Oan X3 is mixed with paint for 11 and 13 (see text). As well as to other chromosomes as indicated, Tac X3 and the pairing region on Tac Y2 are painted. (e) Paint Oan Y3 hybridizes to a region of Tac 27 (see inset). (f) Paint Oan X4 hybridizes to Tac 27. (g) Paint Oan Y4 hybridizes to the top of Tac X4 and a region on Tac Y4. (h) Paint Oan X5 covers Tac X4. (i) Paint Oan Y5 hybridized to Tac Y3.
Figure 9
Figure 9
Tac chromosome paints hybridized to male Oan metaphases. (a) Paint Tac X1 (red) hybridized to Oan X1 and Oan Y1q. Paint Tac X2 (green) hybridized to Oan X2 and the pairing region on Oan Y2 and Y1p (arrow head). (b) Paint Tac Y2 covers Oan Y2 and hybridized to Oan X2 and Oan X3. (c) Paint Tac X3 hybridized to Oan X3 and the pairing region on Oan Y2, the two additional signals are centromeric heterochromatin. (d) Tac paint X5 hybridized to Oan 12p. (e) Paint Tac Y4 (red) hybridizes to Oan 12p, and to Oan X5p and Oan Y4p. Paint Tac 27 identified Oan Y3, Oan X4, and Oan Y4q. (f) Paint Tac X4 covers Oan X5.
Figure 10
Figure 10
Gene mapping. (a) BAC-clone FISH of DMRT1 on echidna X4. (b) Localization of PDE6A by PCR. (c) BAC-clone FISH mapping PDE6A to the pairing regions of X1 and Y1.
Figure 11
Figure 11
Location of mapped human 5 and human 9 genes in human, chicken and platypus. Gene names in italic are mapped in platypus by PCR, gene names in bold are mapped by both PCR and BAC-clone FISH. EPB41L4B is in contig 29 (Additional data file 1, P15RS).
Figure 12
Figure 12
Idiogram showing location of genes in platypus. Gene names in pink are human X-linked genes, gene names in green are homologues of genes imprinted in mouse, gene names in blue are homologues of genes in the mammalian sex determining pathway, gene names in black are Sox gene orthologues, and genes in grey are other previously mapped genes. Gene names in red under a chromosome are mapped in this report by PCR only. Gene names in red next to a chromosome are mapped in this report by PCR and BAC-clone FISH (DMRT1 mapped previously [6,8]). The numbers on the left refer to the gene location in human. The location in chicken is indicated as well, for example, FST located on platypus 1p is on human 5q, chicken Z.

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