Sex chromosome evolution: platypus gene mapping suggests that part of the human X chromosome was originally autosomal.

Watson, J. A. L.; Spencer, James; Riggs, Arthur D.; Graves, Jennifer A. Marshall

doi:10.1073/pnas.88.24.11256

Cited by 58 publications

(30 citation statements)

References 25 publications

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“…These BACs were mapped by FISH to chromosomes 15q and 18p (Fig. 1e,f) in contradiction to previous assignments to chromosomes 1 and 2 by radioactive in situ hybridization (RISH) (Watson et al 1991).…”

Section: Localization Of Platypus Ultracontigs Containing Orthologs Omentioning

confidence: 38%

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

Veyrunes¹,

Waters²,

Miethke³

et al. 2008

Genome Res.

281

258

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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.

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Section: Localization Of Platypus Ultracontigs Containing Orthologs Omentioning

confidence: 38%

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

Veyrunes¹,

Waters²,

Miethke³

et al. 2008

Genome Res.

281

258

View full text Add to dashboard Cite

show abstract

“…The q arm of the eutherian X is also conserved in marsupials (dasyurids and kangaroos) and monotremes (platypus and echidna), and comparative gene-mapping data suggest that the marsupial X chromosome represents that of an early mammalian ancestor, which in the monotreme and eutherian lineages subsequently gained different chromosomal segments through translocations with autosomes (44)(45)(46)(47). Hence, large parts of the mammalian sex chromosomes have an ancient origin (monotremes diverged from other mammals approximately 150 million years ago).…”

Section: Discussionmentioning

confidence: 99%

“…The conclusion from this would be that the avian sex chromosomes evolved at approximately the CretaceousTertiary boundary, approximately 60-100 million years ago. Chromosomal sex determination would in such a case have a more recent origin among birds than among mammals (46)(47).…”

Section: Discussionmentioning

confidence: 99%

Evolution of the avian sex chromosomes from an ancestral pair of autosomes

Fridolfsson

Cheng

Copeland

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

232

136

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Among the mechanisms whereby sex is determined in animals, chromosomal sex determination is found in a wide variety of distant taxa. The widespread but not ubiquitous occurrence, not even within lineages, of chromosomal sex determination suggests that sex chromosomes have evolved independently several times during animal radiation, but firm evidence for this is lacking. The most favored model for this process is gradual differentiation of ancestral pairs of autosomes. As known for mammals, sex chromosomes may have a very ancient origin, and it has even been speculated that the sex chromosomes of mammals and birds would share a common chromosomal ancestry. In this study we showed that the two genes, ATP5A1 and CHD1, so far assigned to the female-specific W chromosome of birds both exist in a very closely related copy on the Z chromosome but are not pseudoautosomal. This indicates a common ancestry of the two sex chromosomes, consistent with the evolution from a pair of autosomes. Comparative mapping demonstrates, however, that ATP5A1 and CHD1 are not sex-linked among eutherian mammals; this is also not the case for the majority of other genes so far assigned to the avian Z chromosome. Our results suggest that the evolution of sex chromosomes has occurred independently in mammals and birds.

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“…The largest of the unpaired chromosomes was presumed to be the X as it was present in two copies in the female. Subsequently, the X was shown to carry several genes that are X-linked in mammals (10)(11)(12), although human Xp genes were mapped to platypus autosomes 1 and 2 (13), and the mammalian SRY testis-determining gene could not be found (14). The X chromosome clearly lay at one end of the chain (7,8) and a tiny ''parachute-like'' element was at the other end (9).…”

mentioning

confidence: 99%

Resolution and evolution of the duck-billed platypus karyotype with an X ₁ Y ₁ X ₂ Y ₂ X ₃ Y ₃ X ₄ Y ₄ X ₅ Y ₅ male sex chromosome constitution

Rens

Grützner

O’Brien

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

137

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The platypus (2n ‫؍‬ 52) has a complex karyotype that has been controversial over the last three decades. The presence of unpaired chromosomes and an unknown sex-determining system especially has defied attempts at conventional analysis. This article reports on the preparation of chromosome-specific probes from flow-sorted chromosomes and their application in the identification and classification of all platypus chromosomes. This work reveals that the male karyotype has 21 pairs of chromosomes and 10 unpaired chromosomes (E1-E10), which are linked by short regions of homology to form a multivalent chain in meiosis. The female karyotype differs in that five of these unpaired elements (E1, E3, E5, E7, and E9) are each present in duplicate, whereas the remaining five unpaired elements (E2, E4, E6, E8, and E10) are absent. This finding indicates that sex is determined by the alternate segregation of the chain of 10 during spermatogenesis so that equal numbers of sperm bear either one of the two groups of five elements, i.e., five X and five Y chromosomes. Chromosome painting reveals that these X and Y chromosomes contain pairing (XY shared) and differential (X-or Y-specific) segments. Y differential regions must contain male-determining genes, and X differential regions should be dosage-compensated in the female. Two models for the evolution of the sex-determining system are presented. The resolution of the longstanding debate over the platypus karyotype is an important step toward the understanding of mechanisms of sex determination, dosage compensation, and karyotype evolution.monotremes ͉ multivalent chain ͉ X-inactivation ͉ sex determination

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Sex chromosome evolution: platypus gene mapping suggests that part of the human X chromosome was originally autosomal.

Cited by 58 publications

References 25 publications

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

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

Evolution of the avian sex chromosomes from an ancestral pair of autosomes

Resolution and evolution of the duck-billed platypus karyotype with an X ₁ Y ₁ X ₂ Y ₂ X ₃ Y ₃ X ₄ Y ₄ X ₅ Y ₅ male sex chromosome constitution

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Sex chromosome evolution: platypus gene mapping suggests that part of the human X chromosome was originally autosomal.

Cited by 58 publications

References 25 publications

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

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

Evolution of the avian sex chromosomes from an ancestral pair of autosomes

Resolution and evolution of the duck-billed platypus karyotype with an X 1 Y 1 X 2 Y 2 X 3 Y 3 X 4 Y 4 X 5 Y 5 male sex chromosome constitution

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Resolution and evolution of the duck-billed platypus karyotype with an X ₁ Y ₁ X ₂ Y ₂ X ₃ Y ₃ X ₄ Y ₄ X ₅ Y ₅ male sex chromosome constitution