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.
Similar content being viewed by others
References
B Aissaini G D’Onofrio D Mouchiroud K Gardiner C Gautier G Bernardi (1991) ArticleTitleThe compositional properties of human genes J Mol Evol 32 493–503 Occurrence Handle1908020
PF Arndt CB Burge T Hwa (2003a) ArticleTitleModelling of neighbor-dependent mutation in DNA sequence evolution J Comput Biol 10 313–322 Occurrence Handle10.1089/10665270360688039 Occurrence Handle1:CAS:528:DC%2BD3sXms1ajt7s%3D
PF Arndt DA Petrov T Hwa (2003b) ArticleTitleDistinct changes of genomic biases in nucleotide substitution at the time of mammalian radiation Mol Biol Evol 20 1887–1896 Occurrence Handle10.1093/molbev/msg204 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Kgtrs%3D
EMS Belle N Smith A Eyre-Walker (2002) ArticleTitleAnalysis of the phylogenetic distribution of isochores in vertebrates and a test of the thermal stability hypothesis J Mol Evol 55 356–363 Occurrence Handle10.1007/s00239-002-2333-1 Occurrence Handle1:CAS:528:DC%2BD38XmtlGhsbs%3D Occurrence Handle12187388
G Bernardi (2000) ArticleTitleIsochores and the evolutionary genomics of vertebrates Gene 241 3–17 Occurrence Handle10.1016/S0378-1119(99)00485-0 Occurrence Handle1:CAS:528:DyaK1MXotVGksrw%3D Occurrence Handle10607893
G Bernardi B Olofsson J Filipski M Zerial J Salinas (1985) ArticleTitleThe mosaic genome of warm-blooded vertebrates Science 228 953–958 Occurrence Handle1:CAS:528:DyaL2MXksVyquro%3D Occurrence Handle4001930
DJ Colgan (1999) ArticleTitlePhylogenetic studies of marsupials based on phosphoglycerate kinase DNA sequences Mol Phylogenet Evol 11 13–26 Occurrence Handle10.1006/mpev.1998.0553 Occurrence Handle1:CAS:528:DyaK1MXhvVGgsrs%3D Occurrence Handle10082607
L Duret D Mouchiroud M Gouy (1994) ArticleTitleHovergen: A database of homologous vertebrate genes Nucleic Acids Res 22 2360–2365 Occurrence Handle1:CAS:528:DyaK2cXlt1Kltrg%3D Occurrence Handle8036164
L Duret M Semon G Piganeau D Mouchiroud N Galtier (2002) ArticleTitleVanishing GC-rich isochores in mammalian genomes Genetics 162 1837–1847 Occurrence Handle1:CAS:528:DC%2BD3sXht1ajs7s%3D Occurrence Handle12524353
A Eyre-Walker (1993) ArticleTitleRecombination and mammalian genome evolution Proc R Soc Lond B Biol Sci 252 237–243 Occurrence Handle1:CAS:528:DyaK2cXht1Khs7w%3D
A Eyre-Walker (1998) ArticleTitleProblems with parsimony in sequences of biase base composition J Mol Evol 47 686–690 Occurrence Handle1:CAS:528:DyaK1cXotVGjt7g%3D Occurrence Handle9847410
A Eyre-Walker LD Hurst (2001) ArticleTitleThe evolution of isochores Nat Rev Genet 2 549–555 Occurrence Handle10.1038/35080577 Occurrence Handle1:CAS:528:DC%2BD3MXltVCksb8%3D Occurrence Handle11433361
J Festenstein (1981) ArticleTitleEvolutionary trees from DNA sequences: A maximum likelihood approach J Mol Evol 17 368–376 Occurrence Handle1:CAS:528:DyaL3MXls1Cisr8%3D Occurrence Handle7288891
N Galtier D Mouchiroud (1998) ArticleTitleIsochore evolution in mammals: A human-like ancestral structure Genetics 150 1577–1584 Occurrence Handle1:CAS:528:DyaK1MXitVelug%3D%3D Occurrence Handle9832533
N Galtier M Gouy (1998) ArticleTitleInferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis Mol Biol Evol 15 871–879 Occurrence Handle1:CAS:528:DyaK1cXksFCisbY%3D Occurrence Handle9656487
N Galtier M Gouy C Gautier (1996) ArticleTitleSeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny Comput Applic Biosci 12 543–548 Occurrence Handle1:CAS:528:DyaK2sXhtlWktLw%3D
N Galtier G Piganeau D Mouchiroud L Duret (2001) ArticleTitleGC-content evolution in mammalian genomes: The biased gene conversion hypothesis Genetics 159 907–911 Occurrence Handle1:CAS:528:DC%2BD3MXot1Srsbg%3D Occurrence Handle11693127
GP Holmquist (1992) ArticleTitleChromosome bands, their chromatine flavours and their functional features Am J Hum Genet 51 17–37 Occurrence Handle1:CAS:528:DyaK38Xls1Crtb0%3D Occurrence Handle1609794
S Hughes D Zelus D Mouchiroud (1999) ArticleTitleWarm-blooded isochore structure in Nile crocodile and turtle Mol Biol Evol 16 1521–1527 Occurrence Handle1:CAS:528:DyaK1MXntlKjsrg%3D Occurrence Handle10555283
InstitutionalAuthorNameInternational Human Genome Sequencing Consortium (2001) ArticleTitleInitial sequencing and analysis of the human genome Nature 409 860–921
F Kadi D Mouchiroud G Sabeur G Bernardi (1993) ArticleTitleThe compositional patterns of the avian genomes and their evolutionary implications J Mol Evol 37 544–551 Occurrence Handle10.1007/BF00160434 Occurrence Handle1:CAS:528:DyaK2cXislyhsQ%3D%3D
M Kimura (1983) The neutral theory of molecular evolution Cambridge University Press Cambridge
A Kong DF Gudbjartsson J Sainz GM Jonsdottir SA Gudjonsson B Richardsson S Sigurdardottir J Barnard B Hallbeck G Masson A Shlien ST Palsson ML Frigge TE Thorgeirsson JR Gulcher K Stefansson (2002) ArticleTitleA high-resolution recombination map of the human genome Nat Gene 31 241–247 Occurrence Handle1:CAS:528:DC%2BD38XkvVGmtLc%3D
MJ Lercher NG Smith A Eyre-Walker LD Hurst (2002) ArticleTitleThe evolution of isochores. Evidence from SNP frequency distributions Genetics 162 1805–1810 Occurrence Handle1:CAS:528:DC%2BD3sXht1ajs70%3D Occurrence Handle12524350
F-GR Liu MM Miyamoto NP Freire PQ Ong MR Tennant TS Young KF Gugel (2001) ArticleTitleMolecular and morphological supertress for eutherian (placental) mammals Science 291 1786–1789 Occurrence Handle10.1126/science.1056346 Occurrence Handle1:CAS:528:DC%2BD3MXhslSku7k%3D Occurrence Handle11230694
JA Marshall M Westerman (2002) ArticleTitleMarsupial genetics and genomics Trends Genet 18 517–521 Occurrence Handle12350341
WJ Murphy E Eizirik WE Johnson YP Zhang OA Ryder SJ O’Brien (2001) ArticleTitleMolecular phylogenetics and the origins of placental mammals Nature 409 614–618 Occurrence Handle10.1038/35054550 Occurrence Handle1:CAS:528:DC%2BD3MXhtVylt7Y%3D Occurrence Handle11214319
RA Ream GC Johns GN Somero (2003) ArticleTitleBase 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 Occurrence Handle1:CAS:528:DC%2BD3sXktlOrug%3D%3D Occurrence Handle12519912
K Tamura (1992) ArticleTitleEstimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases Mol Biol Evol 9 678–687 Occurrence Handle1:CAS:528:DyaK38Xks1eqsbY%3D Occurrence Handle1630306
JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleClustal 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 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417
MT Webster NG Smith H Ellegren (2003) ArticleTitleCompositional evolution of noncoding DNA in the human and chimpanzee genomes Mol Biol Evol 20 278–286 Occurrence Handle1:CAS:528:DC%2BD3sXhsVOiurg%3D Occurrence Handle12598695
Author information
Authors and Affiliations
Corresponding author
Appendix
Rights and permissions
About this article
Cite this article
Belle, E.M.S., Duret, L., Galtier, N. et al. The Decline of Isochores in Mammals: An Assessment of the GC ContentVariation Along the Mammalian Phylogeny. J Mol Evol 58, 653–660 (2004). https://doi.org/10.1007/s00239-004-2587-x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00239-004-2587-x