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

Maria Francesca Cardone, Alicia Alonso, Michele Pazienza, Mario Ventura, Gabriella Montemurro, Lucia Carbone, Pieter J. de Jong, Roscoe Stanyon, Pietro D'Addabbo, Nicoletta Archidiacono, Xinwei She, Evan E. Eichler, Peter E. Warburton, Mariano Rocchi

Research output: Contribution to journalArticle

36 Citations (Scopus)

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.

Original languageEnglish (US)
Article numberR91
JournalGenome Biology
Volume7
Issue number10
DOIs
StatePublished - Oct 13 2006
Externally publishedYes

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Cercopithecidae
Centromere
centromeres
pig
chromosome
Swine
Chromosomes, Human, Pair 13
Chromosomes
chromosomes
swine
gene
Genes
genes
Perissodactyla
Carnivora
Genomic Segmental Duplications
Platyrrhini
Cebidae
Chromatin Immunoprecipitation
Hominidae

ASJC Scopus subject areas

  • Genetics
  • Cell Biology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. / Cardone, Maria Francesca; Alonso, Alicia; Pazienza, Michele; Ventura, Mario; Montemurro, Gabriella; Carbone, Lucia; de Jong, Pieter J.; Stanyon, Roscoe; D'Addabbo, Pietro; Archidiacono, Nicoletta; She, Xinwei; Eichler, Evan E.; Warburton, Peter E.; Rocchi, Mariano.

In: Genome Biology, Vol. 7, No. 10, R91, 13.10.2006.

Research output: Contribution to journalArticle

Cardone, MF, Alonso, A, Pazienza, M, Ventura, M, Montemurro, G, Carbone, L, de Jong, PJ, Stanyon, R, D'Addabbo, P, Archidiacono, N, She, X, Eichler, EE, Warburton, PE & Rocchi, M 2006, 'Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs', Genome Biology, vol. 7, no. 10, R91. https://doi.org/10.1186/gb-2006-7-10-r91
Cardone, Maria Francesca ; Alonso, Alicia ; Pazienza, Michele ; Ventura, Mario ; Montemurro, Gabriella ; Carbone, Lucia ; de Jong, Pieter J. ; Stanyon, Roscoe ; D'Addabbo, Pietro ; Archidiacono, Nicoletta ; She, Xinwei ; Eichler, Evan E. ; Warburton, Peter E. ; Rocchi, Mariano. / Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. In: Genome Biology. 2006 ; Vol. 7, No. 10.
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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.",
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AU - Cardone, Maria Francesca

AU - Alonso, Alicia

AU - Pazienza, Michele

AU - Ventura, Mario

AU - Montemurro, Gabriella

AU - Carbone, Lucia

AU - de Jong, Pieter J.

AU - Stanyon, Roscoe

AU - D'Addabbo, Pietro

AU - Archidiacono, Nicoletta

AU - She, Xinwei

AU - Eichler, Evan E.

AU - Warburton, Peter E.

AU - Rocchi, Mariano

PY - 2006/10/13

Y1 - 2006/10/13

N2 - 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.

AB - 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.

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