Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs

Maria Francesca Cardone¹ , Alicia Alonso² , Michele Pazienza¹ , Mario Ventura¹ , Gabriella Montemurro¹ , Lucia Carbone¹ , Pieter J de Jong³ , Roscoe Stanyon⁴ , Pietro D'Addabbo¹ , Nicoletta Archidiacono¹ , Xinwei She⁵ , Evan E Eichler⁵ , Peter E Warburton² and Mariano Rocchi¹

¹Department of Genetics and Microbiology, University of Bari, Bari, Italy

²Department of Human Genetics, Mount Sinai School of Medicine, New York, New York 10029, USA

³Children's Hospital Oakland Research Institute, Oakland, California 94609, USA

⁴Department of Animal Biology and Genetics 'Leo Pardi', University of Florence, Florence, Italy

⁵Howard Hughes Medical Institute, Department of Genome Sciences, University of Washington School of Medicine, Seattle, Washington 98195, USA

author email corresponding author email

Genome Biology 2006, 7:R91doi:10.1186/gb-2006-7-10-r91


Published:	13 October 2006

Subject areas: Evolution, Genetics

Abstract

Background

Evolutionary centromere repositioning and human analphoid neocentromeres occurring in clinical cases are, very likely, two stages of the same phenomenon whose properties still remain substantially obscure. Chromosome 13 is the chromosome with the highest number of neocentromeres. We reconstructed the mammalian evolutionary history of this chromosome and characterized two human neocentromeres at 13q21, in search of information that could improve our understanding of the relationship between evolutionarily new centromeres, inactivated centromeres, and clinical neocentromeres.

Results

Chromosome 13 evolution was studied, using FISH experiments, across several diverse superordinal phylogenetic clades spanning >100 million years of evolution. The analysis revealed exceptional conservation among primates (hominoids, Old World monkeys, and New World monkeys), Carnivora (cat), Perissodactyla (horse), and Cetartiodactyla (pig). In contrast, the centromeres in both Old World monkeys and pig have apparently repositioned independently to a central location (13q21). We compared these results to the positions of two human 13q21 neocentromeres using chromatin immunoprecipitation and genomic microarrays.

Conclusion

We show that a gene-desert region at 13q21 of approximately 3.9 Mb in size possesses an inherent potential to form evolutionarily new centromeres over, at least, approximately 95 million years of mammalian evolution. The striking absence of genes may represent an important property, making the region tolerant to the extensive pericentromeric reshuffling during subsequent evolution. Comparison of the pericentromeric organization of chromosome 13 in four Old World monkey species revealed many differences in sequence organization. The region contains clusters of duplicons showing peculiar features.