Reconstructing the genomic architecture of mammalian ancestors using multispecies comparative maps
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Review
Reconstructing the genomic architecture of mammalian ancestors using multispecies comparative maps William J. Murphy,1* Guillaume Bourque,2 Glenn Tesler,3 Pavel Pevzner3 and Stephen J. O’Brien1 1
Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD 21702, USA Centre de Recherches Mathe´matiques, Universite´ of Montre´al, Montre´al, H3C 3J7, Canada 3 Department of Computer Science and Engineering, University of California, San Diego, La Jolla, CA 92093-114, USA *Correspondence to: Tel: þ1 301 846 7478; Fax: þ 1 301 846 6327; E-mail: [email protected] 2
Date received (in revised form): 19th August 2003
Abstract Rapidly developing comparative gene maps in selected mammal species are providing an opportunity to reconstruct the genomic architecture of mammalian ancestors and study rearrangements that transformed this ancestral genome into existing mammalian genomes. Here, the recently developed Multiple Genome Rearrangement (MGR) algorithm is applied to human, mouse, cat and cattle comparative maps (with 311– 470 shared markers) to impute the ancestral mammalian genome. Reconstructed ancestors consist of 70 – 100 conserved segments shared across the genomes that have been exchanged by rearrangement events along the ordinal lineages leading to modern species genomes. Genomic distances between species, dominated by inversions (reversals) and translocations, are presented in a first multispecies attempt using ordered mapping data to reconstruct the evolutionary exchanges that preceded modern placental mammal genomes. Keywords: genome evolution, synteny, mammals, ancestral genome
Introduction Great strides in understanding the evolutionary history of whole vertebrate genomes have been made over the past decade with the explosion of comparative mapping and sequencing data from diverse organisms.1 – 7 Comparative maps from birds and mammals, coupled with recent human and mouse genomic sequences, have already provided many interesting insights into the evolutionary patterns and potential forces behind chromosomal rearrangements in vertebrates.5 – 9 Previous vertebrate gene order comparisons have been limited to single chromosome comparisons of multiple genomes5,6,10 – 12 or defining conserved segments between two whole genomes, however, rather than between multiple whole genomes.3 – 6,11,13 – 16 Comparative studies to identify and quantify the extent of conserved segments between two genomes are often based on the breakpoint analysis approach pioneered by Nadeau and Taylor.17 These early studies of rearrangements between human and mouse genomes considered breakpoints independently, without revealing combinatorial dependencies between related breakpoints. Kececioglu and Sankoff 18 were the first to explore the importance of dependencies between breakpoints, and developed an approximation algorithm for the reversal
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distance problem (eg studies of rearrangements in unichromosomal genomes). Hannenhalli and Pevzner19,20 developed a polynomial-time algorithm for the reversal distance pro
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