Limits...
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.

Show MeSH

Related in: MedlinePlus

Positions of scaffolds containing orthologs of human X chromosome genes in Xenopus tropicalis chromosomes.  Of 454 amphibian orthologs of human X-borne genes identified in this study, 442 (97%) localized to X. tropicalis  chromosomes 2 and 8. Mosaic distribution of X orthologs (blue = XAR; green = XCR) suggests internal rearrangements after chromosomal fusions. cM – centimorgans, rdc - relative distance from centromere, cen – centromere.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3472169&req=5

Figure 1: Positions of scaffolds containing orthologs of human X chromosome genes in Xenopus tropicalis chromosomes. Of 454 amphibian orthologs of human X-borne genes identified in this study, 442 (97%) localized to X. tropicalis chromosomes 2 and 8. Mosaic distribution of X orthologs (blue = XAR; green = XCR) suggests internal rearrangements after chromosomal fusions. cM – centimorgans, rdc - relative distance from centromere, cen – centromere.

Mentions: We identified putative orthologs of human X chromosome genes in the X. tropicalis genome assembly, and obtained the chromosomal locations of 454 of these in two ways. Many X ortholog-containing sequence scaffolds could be directly assigned to linkage groups/chromosomes using the meiotic map. Cytogenetic locations of a subset of these genes, as well as X orthologs from scaffolds not represented on the meiotic map, were also determined by fluorescence in situ hybridization (FISH). In total, 442 (97%) of these X orthologs were found on chromosomes 2 and 8 (Additional file 1); the remaining 12 orthologs are scattered throughout other X. tropicalis chromosomes. Intriguingly, many of the scaffolds that had not been localized by genetic mapping were placed by FISH on the short arm of chromosome 2, which is known to be missing from the published meiotic linkage map (Additional file 2) [15]. The known positions of scaffolds containing human X orthologs are displayed in Figure 1.


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)

Positions of scaffolds containing orthologs of human X chromosome genes in Xenopus tropicalis chromosomes.  Of 454 amphibian orthologs of human X-borne genes identified in this study, 442 (97%) localized to X. tropicalis  chromosomes 2 and 8. Mosaic distribution of X orthologs (blue = XAR; green = XCR) suggests internal rearrangements after chromosomal fusions. cM – centimorgans, rdc - relative distance from centromere, cen – centromere.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Positions of scaffolds containing orthologs of human X chromosome genes in Xenopus tropicalis chromosomes. Of 454 amphibian orthologs of human X-borne genes identified in this study, 442 (97%) localized to X. tropicalis chromosomes 2 and 8. Mosaic distribution of X orthologs (blue = XAR; green = XCR) suggests internal rearrangements after chromosomal fusions. cM – centimorgans, rdc - relative distance from centromere, cen – centromere.
Mentions: We identified putative orthologs of human X chromosome genes in the X. tropicalis genome assembly, and obtained the chromosomal locations of 454 of these in two ways. Many X ortholog-containing sequence scaffolds could be directly assigned to linkage groups/chromosomes using the meiotic map. Cytogenetic locations of a subset of these genes, as well as X orthologs from scaffolds not represented on the meiotic map, were also determined by fluorescence in situ hybridization (FISH). In total, 442 (97%) of these X orthologs were found on chromosomes 2 and 8 (Additional file 1); the remaining 12 orthologs are scattered throughout other X. tropicalis chromosomes. Intriguingly, many of the scaffolds that had not been localized by genetic mapping were placed by FISH on the short arm of chromosome 2, which is known to be missing from the published meiotic linkage map (Additional file 2) [15]. The known positions of scaffolds containing human X orthologs are displayed in Figure 1.

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