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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.

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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 human chromosomes homologous to frog, chicken and opossum chromosomes. Opossum chromosomes 4 (orange) and 7 (purple) both show regions of homology on single human chromosomes 2,3, and 13, supporting their origin from a single ancestral chromosome. Amphibian (blue) and bird (grey). Figure summarizes data from Additional file 3. cen – centromere.
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Figure 3: Regions of human chromosomes homologous to frog, chicken and opossum chromosomes. Opossum chromosomes 4 (orange) and 7 (purple) both show regions of homology on single human chromosomes 2,3, and 13, supporting their origin from a single ancestral chromosome. Amphibian (blue) and bird (grey). Figure summarizes data from Additional file 3. cen – centromere.

Mentions: The history of the XAR is more complex. In all non-eutherian vertebrates studied, the regions corresponding to the XAR do not exist as separate cytological entities, but are present within chromosomes, surrounded by other conserved gene blocks that are autosomal in eutherians [8,14,23]. In order to trace the broader chromosomal context of XAR evolution, we examined homology of these nearby gene blocks in non-eutherian vertebrate genomes. Regions surrounding the identified XAR homology on opossum chromosomes 4 and 7, chicken chromosome 1, and frog chromosome 2 were compared to the human genome; incomplete genomic data for wallaby, platypus and the anole lizard preclude synteny analysis. Strikingly, these XAR-neighbouring regions of opossum chromosomes 4 and 7 showed coherent and complementary stretches of homology to parts of human chromosomes 2, 3, and 13 (Figure 3 and Additional file 3) previously hypothesized to derive from fission of a single predecessor [8,23]. The homology of these three human autosomes to both opossum 4 and 7 allows us to trace the genesis of the XAR in mammals. Localized human genome homology to both marsupial autosomes strongly supports a single pre-XAR chromosome, whose gene content was nearly identical to opossum chromosomes 4 and 7, which underwent a simple fission event to give these two autosomes in the marsupial lineage (Figure 4, second row). Human chromosomes 2, 3, and 13 show homology to both opossum chromosomes 4 and 7, and thus identify breakpoints in chromosomal rearrangement events following the divergence of marsupials from Eutheria. Human chromosomes with homology to either opossum chromosome 4 or 7, but not both (human chromosomes 11, 13, 15, and 21, Figure 3) are less informative since they do not evince breakpoints. The most parsimonious way to obtain the observed arrangement of homologies (including three breakpoints) in the eutherian lineage is a single internal translocation or inversion event in the pre-XAR, followed by fragmentation of the pre-XAR and fusion with XAR to form the eutherian X and autosomes (Figure 4, top row).


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 human chromosomes homologous to frog, chicken and opossum chromosomes. Opossum chromosomes 4 (orange) and 7 (purple) both show regions of homology on single human chromosomes 2,3, and 13, supporting their origin from a single ancestral chromosome. Amphibian (blue) and bird (grey). Figure summarizes data from Additional file 3. cen – centromere.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Regions of human chromosomes homologous to frog, chicken and opossum chromosomes. Opossum chromosomes 4 (orange) and 7 (purple) both show regions of homology on single human chromosomes 2,3, and 13, supporting their origin from a single ancestral chromosome. Amphibian (blue) and bird (grey). Figure summarizes data from Additional file 3. cen – centromere.
Mentions: The history of the XAR is more complex. In all non-eutherian vertebrates studied, the regions corresponding to the XAR do not exist as separate cytological entities, but are present within chromosomes, surrounded by other conserved gene blocks that are autosomal in eutherians [8,14,23]. In order to trace the broader chromosomal context of XAR evolution, we examined homology of these nearby gene blocks in non-eutherian vertebrate genomes. Regions surrounding the identified XAR homology on opossum chromosomes 4 and 7, chicken chromosome 1, and frog chromosome 2 were compared to the human genome; incomplete genomic data for wallaby, platypus and the anole lizard preclude synteny analysis. Strikingly, these XAR-neighbouring regions of opossum chromosomes 4 and 7 showed coherent and complementary stretches of homology to parts of human chromosomes 2, 3, and 13 (Figure 3 and Additional file 3) previously hypothesized to derive from fission of a single predecessor [8,23]. The homology of these three human autosomes to both opossum 4 and 7 allows us to trace the genesis of the XAR in mammals. Localized human genome homology to both marsupial autosomes strongly supports a single pre-XAR chromosome, whose gene content was nearly identical to opossum chromosomes 4 and 7, which underwent a simple fission event to give these two autosomes in the marsupial lineage (Figure 4, second row). Human chromosomes 2, 3, and 13 show homology to both opossum chromosomes 4 and 7, and thus identify breakpoints in chromosomal rearrangement events following the divergence of marsupials from Eutheria. Human chromosomes with homology to either opossum chromosome 4 or 7, but not both (human chromosomes 11, 13, 15, and 21, Figure 3) are less informative since they do not evince breakpoints. The most parsimonious way to obtain the observed arrangement of homologies (including three breakpoints) in the eutherian lineage is a single internal translocation or inversion event in the pre-XAR, followed by fragmentation of the pre-XAR and fusion with XAR to form the eutherian X and autosomes (Figure 4, top row).

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