Abstract
The compositional distributions of high molecular weight DNA fragments from 20 species belonging to 9 out of the 17 eutherian orders were investigated by analytical CsCl density gradient centrifugation and by preparative fractionation in Cs2SO4/BAMD density gradients followed by analysis of the fractions in CsCl. These compositional distributions reflect those of the isochores making up the corresponding genomes.
A “general distribution” was found in species belonging to eight mammalian orders. A “myomorph distribution” was found in Myomorpha, but not in the other rodent infraorders Sciuromorpha and Histricomorpha, which share the general distribution. Two other distributions were found in a megachiropteran (but not in microchiropteran, which, again, shares the general distribution) and in pangolin (a species from the only genus of the order Pholidota), respectively.
The main difference between the general distribution and all other distributions is that the former contains sizable amounts (6–10%) of GC-rich isochores (detected as DNA fragments equal to, or higher than, 1.710 g/cm3 in modal buoyant density), which are scarce, or absent, in the other distributions. This difference is remarkable because gene concentrations in mammalian genomes are paralleled by GC levels, the highest gene concentrations being present in the GC-richest isochores.
The compositional distributions of mammalian genomes reported here shed light on mammalian phylogeny. Indeed, all orders investigated, with the exception of Pholidota, seem to share a common ancestor. The compositional patterns of the megachiropteran and of Myomorpha may be derived from the general pattern or have independent origins.
Similar content being viewed by others
References
Aïssani B, D'Onofrio G, Mouchiroud D, Gardiner K, Gautier C, Bernardi G (1991) The compositional properties of human genes. J Mol Evol 32:497–503
Allard MW, Myamoto MM (1991) Tests for rodent polyphyly. Nature 353:610–611
Ansari HA, Takagi N, Sasaki M (1988) Morphological differentiation of sex chromosomes in three species of ratite birds. Cytogenet. Cell Genet 47:185–188
Arrighi FE, Mandel M, Bergendahl J, Hsu TC (1970) Buoyant densities of DNA of mammals. Biochem Genet 4:367–376
Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958
Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11
Bernardi G, Mouchiroud D, Gautier C, Bernardi G (1988) Compositional patterns in vertebrate genomes: conservation and change in evolution. J Mol Evol 28:7–18
Bernardi G (1989) The isochore organization of the human genome. Ann Rev Genet 23:637–661
Bernardi G, Bernardi G (1990a) Compositional patterns in the nuclear genomes of cold-blooded vertebrates. J Mol Evol 31:265–281
Bernardi G, Bernardi G (1990b) Compositional transitions in the nuclear genomes of cold-blooded vertebrates. J Mol Evol 31:282–293
Bernardi G, Bernardi G (1991) Compositional properties of nuclear genes from cold-blooded vertebrates. J Mol Evol 33:57–67
Bernardi G (1993a) The vertebrate genome: isochores and evolution. Mol Biol Evol 10:186–204
Bernardi G (1993b) Genome organization and species formation in vertebrates. J Mol Evol (in press)
Bettecken T, Aïssani B, Müller CR, Bernardi G (1992) Compositional mapping of the human dystrophin gene. Gene 122:329–35
Bulmer M, Wolfe KH, Sharp PM (1991) Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci USA 88:5974–5978
Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York, NY, USA
Catzeflis FM, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Trends Ecol Evol 7:122–126
Colbert EH, Morales M (1991) Evolution of the vertebrates, 4th ed. Wiley-Liss, New York
Corneo G, Ginelli E, Soave C, Bernardi G (1968) Isolation and characterization of mouse and guinea pig satellite DNA's. Biochemistry 7:4373–4379
Cortadas J, Macaya G, Bernardi G (1977) An analysis of the bovine genome by density gradient centrifugation: fractionation in Cs2SO4/3,6 bis (acetato-mercurimethyl) dioxane density gradient. Eur J Biochem 76:13–19
Cortadas J, Olofsson B, Meunier-Rotival M, Macaya G, Bernardi G (1979) The DNA components of the chicken genome. Eur J Biochem 99:179–186
Cuny G, Soriano P, Macaya G, Bernardi G (1981) The major components of the mouse and human genomes: preparation, basic properties and compositional heterogeneity. Eur J Biochem 111:227–233
D'Onofrio G, Mouchiroud D, Aïssani B, Gautier C, Bernardi G (1991) Correlations between the compositional properties of human genes, codon usage and aminoacid composition of proteins. J Mol Evol 32:504–510
Easteal S (1990) The pattern of mammalian evolution and the relative rate of molecular evolution. Genetics 124:165–173
Filipski J, Thiery JP, Bernardi G (1973) An analysis of the bovine genome by Cs2SO4-Ag+ density gradient centrifugation. J Mol Biol 80:177–197
Graur D, Hide WA, Li W-H (1991) Is the guinea-pig a rodent? Nature 351:646–652
Hasegawa M, Cao Y, Adachi J, Yano T-A (1992) Rodent polyphyly? Nature 355:595
Hudson AP, Cuny G, Cortadas J, Haschemeyer AEV, Bernardi G (1980) An analysis of fish genomes by density gradient centrifugation. Eur J Biochem 112:203–210
Kadi F, Mouchiroud D, Sabeur G, Bernardi G (1993) The compositional patterns of the avian genomes and their evolutionary implications. J Mol Evol (submitted)
Kay ERM, Simmons NS, Dounce AL (1952) An improved preparation of sodium desoxyribonucleate. J Am Chem Soc 74:1724–1726
Kirk JTO (1967) Effect of methylation of cytosine residues on the buoyant density of DNA in caesium chloride solutions. J Mol Biol 28:171–712
Kopecka H, Macaya G, Cortadas J, Thiery JP, Bernardi G (1978) Restriction enzyme analysis of satellite DNA components from the bovine genome. Eur J Biochem 84:189–195
Li W-H, Gouy M, Sharp PM, D'Huigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707
Li W-H, Hide WA, Graur D (1992) Origin of rodents and guineapigs. Nature 359:277–278
Luckett WP, Hartenberger J-L (1993) Monophyly or polyphyly of the order Rodentia: possible conflict between morphological and molecular interpretations. J Mammal Evol (in press)
Macaya G, Cortadas J, Bernardi G (1978) An analysis of the bovine genome by density gradient centrifugation. Eur J Biochem 84:179–188
Meunier-Rotival M, Cortadas J, Macaya G, Bernardi G (1979) Isolation and organization of calf ribosomal DNA. Nucleic Acids Res 6:2109–2123
Mouchiroud D, Fichant G, Bernardi G (1987) Compositional compartmentalization and gene composition in the genome of vertebrates. J Mol Evol 26:198–204
Mouchiroud D, Gautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol 27:3311–320
Mouchiroud D, Gautier C (1990) Codon usage changes and sequence dissimilarity between human and rat. J Mol Evol 31:81–91
Mouchiroud D, D'Onofrio G, Aïssani B, Macaya G, Gautier C, Bernardi G (1991) The distribution of genes in the human genome. Gene 100:181–187
Mouchiroud D, Bernardi G (1993) Compositional properties of coding sequences and mammalian phylogeny. J Mol Evol (in press)
Novacek MJ (1990) Morphology, paleontology and the higher clades of mammals. In: Genoways HH (ed) Current mammalogy vol 2. Plenum, New York, pp 507–543
Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125
Nowak RM, Paradiso J (1983) Walker's mammals of the world, 4th ed. Johns Hopkins University Press, Baltimore and London.
O'Brien SJ, Seuanez HN (1988) Mammalian genome organization: an evolutionary view. Ann Rev Genet 22:323–351
Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231:1304–1306
Pettigrew JD (1991) Wings or brain? Convergent evolution in the origin of bats. Syst Zool 40:199–216
Rynditch A, Kadi F, Geryk J, Zoubak S, Svoboda J, Bernardi G (1991) The isopycnic, compartmentalized integration of Rous sarcoma virus sequences. Gene 106:165–172
Salinas J, Zerial M, Filipski J, Bernardi G (1986) Gene distribution and nucleotide sequence organization in the mouse genome. Eur J Biochem 160:469–478
Smith JD (1976) Comments on flight and evolution of bats. In: Hecht MR, Goody PC, Hecht BM (eds) Major patterns of vertebrate evolution. Plenum Press, New York, pp 427–437
Stanhope MJ, Czelusniak J, Si J-S, Nickerson J, Goodman M (1992) A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. Mol Phylogenet Evol 1:148–160
Sueoka N (1959) A statistical analysis of deoxyribonucleic acid distribution in density gradient centrifugation. Proc Natl Acad Sci USA 45:1480–1490
Thiery JP, Macaya G, Bernardi G (1976) An analysis of eukaryotic genomes by density gradient centrifugation. J Mol Biol 108:219–235
Zerial M, Salinas J, Filipski J, Bernardi G (1986) Gene distribution and nucleotide sequence organization in the human genome. Eur J Biochem 160:479–48
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sabeur, G., Macaya, G., Kadi, F. et al. The isochore patterns of mammalian genomes and their phylogenetic implications. J Mol Evol 37, 93–108 (1993). https://doi.org/10.1007/BF02407344
Issue Date:
DOI: https://doi.org/10.1007/BF02407344