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Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis.

Mácha J, Teichmanová R, Sater AK, Wells DE, Tlapáková T, Zimmerman LB, Krylov V - BMC Genomics (2012)

Bottom Line: Chromosomal regions orthologous to Therian X chromosomes have been located in the genome of the frog X. tropicalis.These X chromosome ancestral components experienced a series of fusion and breakage events to give rise to avian autosomes and mammalian sex chromosomes.The early branching tetrapod X. tropicalis' simple diploid genome and robust synteny to amniotes greatly enhances studies of vertebrate chromosome evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Division of Developmental Biology, MRC-National Institute for Medical Research, Mill Hill, London, UK.

ABSTRACT

Background: The X and Y sex chromosomes are conspicuous features of placental mammal genomes. Mammalian sex chromosomes arose from an ordinary pair of autosomes after the proto-Y acquired a male-determining gene and degenerated due to suppression of X-Y recombination. Analysis of earlier steps in X chromosome evolution has been hampered by the long interval between the origins of teleost and amniote lineages as well as scarcity of X chromosome orthologs in incomplete avian genome assemblies.

Results: This study clarifies the genesis and remodelling of the Eutherian X chromosome by using a combination of sequence analysis, meiotic map information, and cytogenetic localization to compare amniote genome organization with that of the amphibian Xenopus tropicalis. Nearly all orthologs of human X genes localize to X. tropicalis chromosomes 2 and 8, consistent with an ancestral X-conserved region and a single X-added region precursor. This finding contradicts a previous hypothesis of three evolutionary strata in this region. Homologies between human, opossum, chicken and frog chromosomes suggest a single X-added region predecessor in therian mammals, corresponding to opossum chromosomes 4 and 7. A more ancient X-added ancestral region, currently extant as a major part of chicken chromosome 1, is likely to have been present in the progenitor of synapsids and sauropsids. Analysis of X chromosome gene content emphasizes conservation of single protein coding genes and the role of tandem arrays in formation of novel genes.

Conclusions: Chromosomal regions orthologous to Therian X chromosomes have been located in the genome of the frog X. tropicalis. These X chromosome ancestral components experienced a series of fusion and breakage events to give rise to avian autosomes and mammalian sex chromosomes. The early branching tetrapod X. tropicalis' simple diploid genome and robust synteny to amniotes greatly enhances studies of vertebrate chromosome evolution.

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Regions of homology between human X and Xenopus tropicalis, Gallus gallus and Monodelphis domestica chromosomes.  Only gene blocks larger than 0.7 Mbp are shown. Data are from Additional file 1 and the Comparative Genomic display of the Ensembl database [18]. cen – centromere, chr. - chromosome.
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Figure 2: Regions of homology between human X and Xenopus tropicalis, Gallus gallus and Monodelphis domestica chromosomes. Only gene blocks larger than 0.7 Mbp are shown. Data are from Additional file 1 and the Comparative Genomic display of the Ensembl database [18]. cen – centromere, chr. - chromosome.

Mentions: On X. tropicalis chromosomes 2 and 8, scaffolds containing large blocks of human X orthologs are interrupted by gene clusters corresponding to other human chromosomes (Additional file 1). Chromosome 2 contains nearly all the XAR genes (134), with 306 XCR orthologs found on chromosome 8 (Figure 2, Additional file 1). These results confirm the remarkable evolutionary conservation of chromosomal content noted in the genome assembly analysis [14], despite some bias due to easier identification of frog orthologs in synteny blocks where neighbouring gene identities are also conserved. The exceptions to the XCR and XAR conservation are two XCR genes found on chromosome 2 (scaffold 422). This is likely to result from a translocation in Amphibia, since chicken and opossum orthologs of these two genes reside as expected in chromosome 4 and X, respectively. The XAR–XCR boundary is located between the RGN and PCTK1 genes, an interval containing the NDUFB11RBM10 border previously suggested by human-marsupial comparisons [16]. The X. tropicalis sex determining locus has been mapped [17] to the neighbourhood of scaffolds 494, 605 and 735 on chromosome 7, and does not appear to be linked to amphibian X-borne genes.


Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis.

Mácha J, Teichmanová R, Sater AK, Wells DE, Tlapáková T, Zimmerman LB, Krylov V - BMC Genomics (2012)

Regions of homology between human X and Xenopus tropicalis, Gallus gallus and Monodelphis domestica chromosomes.  Only gene blocks larger than 0.7 Mbp are shown. Data are from Additional file 1 and the Comparative Genomic display of the Ensembl database [18]. cen – centromere, chr. - chromosome.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472169&req=5

Figure 2: Regions of homology between human X and Xenopus tropicalis, Gallus gallus and Monodelphis domestica chromosomes. Only gene blocks larger than 0.7 Mbp are shown. Data are from Additional file 1 and the Comparative Genomic display of the Ensembl database [18]. cen – centromere, chr. - chromosome.
Mentions: On X. tropicalis chromosomes 2 and 8, scaffolds containing large blocks of human X orthologs are interrupted by gene clusters corresponding to other human chromosomes (Additional file 1). Chromosome 2 contains nearly all the XAR genes (134), with 306 XCR orthologs found on chromosome 8 (Figure 2, Additional file 1). These results confirm the remarkable evolutionary conservation of chromosomal content noted in the genome assembly analysis [14], despite some bias due to easier identification of frog orthologs in synteny blocks where neighbouring gene identities are also conserved. The exceptions to the XCR and XAR conservation are two XCR genes found on chromosome 2 (scaffold 422). This is likely to result from a translocation in Amphibia, since chicken and opossum orthologs of these two genes reside as expected in chromosome 4 and X, respectively. The XAR–XCR boundary is located between the RGN and PCTK1 genes, an interval containing the NDUFB11RBM10 border previously suggested by human-marsupial comparisons [16]. The X. tropicalis sex determining locus has been mapped [17] to the neighbourhood of scaffolds 494, 605 and 735 on chromosome 7, and does not appear to be linked to amphibian X-borne genes.

Bottom Line: Chromosomal regions orthologous to Therian X chromosomes have been located in the genome of the frog X. tropicalis.These X chromosome ancestral components experienced a series of fusion and breakage events to give rise to avian autosomes and mammalian sex chromosomes.The early branching tetrapod X. tropicalis' simple diploid genome and robust synteny to amniotes greatly enhances studies of vertebrate chromosome evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Division of Developmental Biology, MRC-National Institute for Medical Research, Mill Hill, London, UK.

ABSTRACT

Background: The X and Y sex chromosomes are conspicuous features of placental mammal genomes. Mammalian sex chromosomes arose from an ordinary pair of autosomes after the proto-Y acquired a male-determining gene and degenerated due to suppression of X-Y recombination. Analysis of earlier steps in X chromosome evolution has been hampered by the long interval between the origins of teleost and amniote lineages as well as scarcity of X chromosome orthologs in incomplete avian genome assemblies.

Results: This study clarifies the genesis and remodelling of the Eutherian X chromosome by using a combination of sequence analysis, meiotic map information, and cytogenetic localization to compare amniote genome organization with that of the amphibian Xenopus tropicalis. Nearly all orthologs of human X genes localize to X. tropicalis chromosomes 2 and 8, consistent with an ancestral X-conserved region and a single X-added region precursor. This finding contradicts a previous hypothesis of three evolutionary strata in this region. Homologies between human, opossum, chicken and frog chromosomes suggest a single X-added region predecessor in therian mammals, corresponding to opossum chromosomes 4 and 7. A more ancient X-added ancestral region, currently extant as a major part of chicken chromosome 1, is likely to have been present in the progenitor of synapsids and sauropsids. Analysis of X chromosome gene content emphasizes conservation of single protein coding genes and the role of tandem arrays in formation of novel genes.

Conclusions: Chromosomal regions orthologous to Therian X chromosomes have been located in the genome of the frog X. tropicalis. These X chromosome ancestral components experienced a series of fusion and breakage events to give rise to avian autosomes and mammalian sex chromosomes. The early branching tetrapod X. tropicalis' simple diploid genome and robust synteny to amniotes greatly enhances studies of vertebrate chromosome evolution.

Show MeSH
Related in: MedlinePlus