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Letter

The Origin of Human Chromosome 1 and Its Homologs in Placental Mammals

¹ Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland 21702, USA ² Comparative Molecular Cytogenetics Core, Genetics Branch, National Cancer Institute, Frederick, Maryland 21702, USA

Developing ordered gene maps from multiple mammalian species coupled with chromosome-painting data provide a powerful resource for resolving the evolutionary history of chromosomes and whole genomes. In this work, we recapitulate the evolutionary history of human chromosome 1 and its homologs in placental mammals, putatively the largest physical unit in the ancestral placental genome. Precise definition of translocation exchange breakpoints in human, carnivore, cetartiodactyl, and rodent-ordered gene maps demonstrate that chromosome breakpoints, previously considered as equivalent, actually represent distinct chromosome positions and exchange events. Multidirectional chromosome painting, using probes from homologs to chromosome 1 in seven mammal species from six orders of placental mammals, confirm the gene-mapping results and indicate that the multiple human chromosome 1 homologs in these species are derived from independent fissions of a single ancestral chromosome. Chromosome painting using human chromosome 1 probes identifies a single human chromosome 1 homolog in phylogenetically distant taxa, the two-toed sloth, cetaceans, and higher primates. The diverse phylogenetic occurrence of a single Hsa1 synteny among the major clades of placental mammals suggests that human chromosome 1 represents an intact ancestral chromosome, which was variously fissioned in the majority of placental species. We find that the number of human chromosome 1 fissions in a specific lineage reflects its general rate of genomic evolution. Further, historic chromosome exchange appears to have been disproportionately clustered in two breakpoint hotspots on the long arm.

³ These authors contributed equally to this work.

⁴ Corresponding author: E-MAIL murphywi{at}mail.ncifcrf.gov; FAX (301) 846-6327.

[Supplemental material is available online at www.genome.org. Feline gene segments have been deposited in GenBank under accession numbers CC596505–CC596511. The following individuals kindly provided reagents, samples, or unpublished information as indicated in the paper: O. Ryder.]

Article published online before print in July 2003.

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