The Decline of Isochores in Mammals: An Assessment of the GC ContentVariation Along the Mammalian Phylogeny
Article Received: 19 August 2003 Accepted: 10 December 2003 Abstract
Whether isochores, the large-scale variation of the GC content in mammalian genomes, are being maintained has recently been questioned. It has been suggested that GC-rich isochores originated in the ancestral amniote genome but that whatever force gave rise to them is no longer effective and that isochores are now disappearing from mammalian genomes. Here we investigated the evolution of the GC content of 41 coding genes in 6 to 66 species of mammals by estimating the ancestral GC content using a method which allows for different rates of substitution between sites. We found a highly significant decrease in the GC content during early mammalian evolution, as well as a weaker but still significant decrease in the GC content of GC-rich genes later in at least three groups of mammals: primates, rodents, and carnivores. These results are of interest because they confirm the recently suggested disappearance of GC-rich isochores in some mammalian genomes, and more importantly, they suggest that this disappearance started very early in mammalian evolution.
Keywords Isochore Genome GC content Noncoding DNA Mammal Primate
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References Aissaini, B, D’Onofrio, G, Mouchiroud, D, Gardiner, K, Gautier, C, Bernardi, G 1991 The compositional properties of human genes J Mol Evol 32 493 503 PubMed Google Scholar Arndt, PF, Burge, CB, Hwa, T 2003a Modelling of neighbor-dependent mutation in DNA sequence evolution J Comput Biol 10 313 322 CrossRef Google Scholar Arndt, PF, Petrov, DA, Hwa, T 2003b Distinct changes of genomic biases in nucleotide substitution at the time of mammalian radiation Mol Biol Evol 20 1887 1896 CrossRef Google Scholar Belle, EMS, Smith, N, Eyre-Walker, A 2002 Analysis of the phylogenetic distribution of isochores in vertebrates and a test of the thermal stability hypothesis J Mol Evol 55 356 363 CrossRef PubMed Google Scholar Bernardi, G 2000 Isochores and the evolutionary genomics of vertebrates Gene 241 3 17 CrossRef PubMed Google Scholar Bernardi, G, Olofsson, B, Filipski, J, Zerial, M, Salinas, J 1985 The mosaic genome of warm-blooded vertebrates Science 228 953 958 PubMed Google Scholar Colgan, DJ 1999 Phylogenetic studies of marsupials based on phosphoglycerate kinase DNA sequences Mol Phylogenet Evol 11 13 26 CrossRef PubMed Google Scholar Duret, L, Mouchiroud, D, Gouy, M 1994 Hovergen: A database of homologous vertebrate genes Nucleic Acids Res 22 2360 2365 PubMed Google Scholar Duret, L, Semon, M, Piganeau, G, Mouchiroud, D, Galtier, N 2002 Vanishing GC-rich isochores in mammalian genomes Genetics 162 1837 1847 PubMed Google Scholar Eyre-Walker, A 1993 Recombination and mammalian genome evolution Proc R Soc Lond B Biol Sci 252 237 243 Google Scholar Eyre-Walker, A 1998 Problems with parsimony in sequences of biase base composition J Mol Evol 47 686 690 PubMed Google Scholar Eyre-Walker, A, Hurst, LD 2001 The evolution of isochores Nat Rev Genet 2 549 555 CrossRef PubMed Google Scholar Festenstein, J 1981 Evolutionary trees from DNA sequences: A maximum likelihood approach J Mol Evol 17 368 376 PubMed Google Scholar Galtier, N, Mouchiroud, D 1998 Isochore evolution in mammals: A human-like ancestral structure Genetics 150 1577 1584 PubMed Google Scholar Galtier, N, Gouy, M 1998 Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis Mol Biol Evol 15 871 879 PubMed Google Scholar Galtier, N, Gouy, M, Gautier, C 1996 SeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny Comput Applic Biosci 12 543 548 Google Scholar Galtier, N, Piganeau, G, Mouchiroud, D, Duret, L 2001 GC-content evolution in mammalian genomes: The biased gene conversion hypothesis Genetics 159 907 911 PubMed Google Scholar Holmquist, GP 1992 Chromosome bands, their chromatine flavours and their functional features Am J Hum Genet 51 17 37 PubMed Google Scholar Hughes, S, Zelus, D, Mouchiroud, D 1999 Warm-blooded isochore structure in Nile crocodile and turtle Mol Biol Evol 16 1521 1527 PubMed Google Scholar International Human Genome Sequencing Consortium 2001 Initial sequencing and analysis of the human genome Nature 409 860 921 Google Scholar Kadi, F, Mouchiroud, D, Sabeur, G, Bernardi, G 1993 The compositional patterns of the avian genomes and their evolutionary implications J Mol Evol 37 544 551 CrossRef Google Scholar Kimura, M 1983The neutral theory of molecular evolution Cambridge University Press Cambridge Google Scholar Kong, A, Gudbjartsson, DF, Sainz, J, Jonsdottir, GM, Gudjonsson, SA, Richardsson, B, Sigurdardottir, S, Barnard, J, Hallbeck, B, Masson, G, Shlien, A, Palsson, ST, Frigge, ML, Thorgeirsson, TE, Gulcher, JR, Stefansson, K 2002 A high-resolution recombination map of the human genome Nat Gene 31 241 247 Google Scholar Lercher, MJ, Smith, NG, Eyre-Walker, A, Hurst, LD 2002 The evolution of isochores. Evidence from SNP frequency distributions Genetics 162 1805 1810 PubMed Google Scholar Liu, F-GR, Miyamoto, MM, Freire, NP, Ong, PQ, Tennant, MR, Young, TS, Gugel, KF 2001 Molecular and morphological supertress for eutherian (placental) mammals Science 291 1786 1789 CrossRef PubMed Google Scholar Marshall, JA, Westerman, M 2002 Marsupial genetics and genomics Trends Genet 18 517 521 PubMed Google Scholar Murphy, WJ, Eizirik, E, Johnson, WE, Zhang, YP, Ryder, OA, O’Brien, SJ 2001 Molecular phylogenetics and the origins of placental mammals Nature 409 614 618 CrossRef PubMed Google Scholar Ream, RA, Johns, GC, Somero, GN 2003 Base compositions of genes encoding α-actine and lactate deshydrogenase-A from differently adapted vertebrates show no temperature-adaptive variation in G+C content Mol Biol Evol 20 105 110 PubMed Google Scholar Tamura, K 1992 Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases Mol Biol Evol 9 678 687 PubMed Google Scholar Thompson, JD, Higgins, DG, Gibson, TJ 1994 Clustal W: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673 4680 PubMed Google Scholar Webster, MT, Smith, NG, Ellegren, H 2003 Compositional evolution of noncoding DNA in the human and chimpanzee genomes Mol Biol Evol 20 278 286 PubMed Google Scholar