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

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...

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Autores principales: Mácha, Jaroslav, Teichmanová, Radka, Sater, Amy K, Wells, Dan E, Tlapáková, Tereza, Zimmerman, Lyle B, Krylov, Vladimír
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3472169/
https://www.ncbi.nlm.nih.gov/pubmed/22800176
http://dx.doi.org/10.1186/1471-2164-13-315
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author Mácha, Jaroslav
Teichmanová, Radka
Sater, Amy K
Wells, Dan E
Tlapáková, Tereza
Zimmerman, Lyle B
Krylov, Vladimír
author_facet Mácha, Jaroslav
Teichmanová, Radka
Sater, Amy K
Wells, Dan E
Tlapáková, Tereza
Zimmerman, Lyle B
Krylov, Vladimír
author_sort Mácha, Jaroslav
collection PubMed
description 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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spelling pubmed-34721692012-10-17 Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis Mácha, Jaroslav Teichmanová, Radka Sater, Amy K Wells, Dan E Tlapáková, Tereza Zimmerman, Lyle B Krylov, Vladimír BMC Genomics Research Article 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. BioMed Central 2012-07-16 /pmc/articles/PMC3472169/ /pubmed/22800176 http://dx.doi.org/10.1186/1471-2164-13-315 Text en Copyright ©2012 Mácha et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Mácha, Jaroslav
Teichmanová, Radka
Sater, Amy K
Wells, Dan E
Tlapáková, Tereza
Zimmerman, Lyle B
Krylov, Vladimír
Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title_full Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title_fullStr Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title_full_unstemmed Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title_short Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis
title_sort deep ancestry of mammalian x chromosome revealed by comparison with the basal tetrapod xenopus tropicalis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3472169/
https://www.ncbi.nlm.nih.gov/pubmed/22800176
http://dx.doi.org/10.1186/1471-2164-13-315
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