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Open Access Research article

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

Jaroslav Mácha1, Radka Teichmanová1, Amy K Sater2, Dan E Wells2, Tereza Tlapáková1, Lyle B Zimmerman3* and Vladimír Krylov1

Author Affiliations

1 Department of Cell Biology, Faculty of Science, Charles University in Prague, Vinicna 7, Prague 2, Czech Republic

2 Department of Biology and Biochemistry, University of Houston, Houston, TX, 77204-5001, USA

3 Division of Developmental Biology, MRC-National Institute for Medical Research, Mill Hill, London, NW7 1AA, UK

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BMC Genomics 2012, 13:315  doi:10.1186/1471-2164-13-315

Published: 16 July 2012

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.

Keywords:
X chromosome; Evolution; Xenopus; Synteny; Genome; TAG