Abstract
The recent availability of a number of fully sequenced genomes (including marine organisms) allowed to map very precisely the isochores, based on DNA sequences, confirming the results obtained before genome sequencing by the ultracentrifugation in CsCl. In fact, the analytical profile of human DNA showed that the vertebrate genome is a mosaic of isochores, typically megabase-size DNA segments that belong to a small number of families characterized by different GC levels. In this review, we will concentrate on some general genome features regarding the compositional organization from different organisms and their evolution, ranging from vertebrates to invertebrates until unicellular organisms. Since isochores are tightly linked to biological properties such as gene density, replication timing, and recombination, the new level of detail provided by the isochore map helped the understanding of genome structure, function, and evolution. All the findings reported here confirm the idea that the isochores can be considered as a “fundamental level of genome structure and organization.” We stress that we do not discuss in this review the origin of isochores, which is still a matter of controversy, but we focus on well established structural and physiological aspects.
Similar content being viewed by others
References
Andreozzi L, Federico C, Motta S, Saccone S, Sazanova AL, Sazanov AA, Smirnov AF, Galkina SA, Lukina NA, Rodionov AV, Carels N, Bernardi G (2001) Compositional mapping of chicken chromosomes and identification of gene-richest regions. Chromosome Res 9:521–532
Bernardi G (1965) Chromatography of nucleic acids on hydroxyapatite. Nature 206:779–783
Bernardi G (2004) Structural and evolutionary genomics. Natural selection in genome evolution. Elsevier, Amsterdam
Bernardi G (2007) The neo-selectionist theory of genome evolution. Proc Natl Acad Sci USA 104(20):8385–8390
Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11
Bernardi G, Bernardi G (1990) Compositional patterns in the nuclear genomes of cold-blooded vertebrates. J Mol Evol 31:265–281
Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244
Britten RJ, Kohne DE (1968) Repeated sequences in DNA. Science 161:529–540
Cammarano R, Costantini M, Bernardi G (2009) The isochore patterns of invertebrate genomes. BMC Genomics 10:538
Cohen NT, Dagan L, Graur D (2005) GC composition of the human genome: In search of isochores. Mol Biol Evol 22:1260–1272
Corneo G, Ginelli E, Soave C, Bernardi G (1968) Isolation and characterization of mouse and guinea pig satellite deoxyribonucleic acids. Biochemistry 7(12):4373–4379
Costantini M, Bernardi G (2008a) Replication timing, chromosomal bands and isochores. Proc Natl Acad Sci USA 105(9):3433–3437
Costantini M, Bernardi G (2008b) The short-sequence design of isochores from the human genome. Proc Natl Acad Sci USA 105(37):13971–13976
Costantini M, Clay O, Auletta F, Bernardi G (2006) An isochore map of human chromosomes. Genome Res 16(4):536–541
Costantini M, Di Filippo M, Auletta F, Bernardi G (2007a) Isochore pattern and gene distribution in the chicken genome. Gene 400:9–15
Costantini M, Auletta F, Bernardi G (2007b) Isochore patterns and gene distributions in fish genomes. Genomics 90(3):364–371
Costantini M, Clay O, Federico C, Saccone S, Auletta F, Bernardi G (2007c) Human chromosomal bands: nested structure, high-definition map and molecular basis. Chromosoma 116(1):29–40
Costantini M, Cammarano R, Bernardi G (2009) The evolution of isochore patterns in vertebrate genomes. BMC Genomics 10:146
Costantini M, Alvarez-Valin F, Costantini S, Cammarano R, Bernardi G (2013) Compositional patterns in the genomes of unicellular eukaryotes. BMC Genomics 14:755
Costantini M, Greif G, Alvarez-Valin F, Bernardi G (2016) The Anolis lizard genome: a genome without isochores? Genome Biol Evol 8:1048–1055
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
de Luca di Roseto G, Bucciarelli G, Bernardi G (2002) An analysis of the genome of Ciona intestinalis. Gene 295:311–316
Dekker J (2007) GC- and AT-rich chromatin domains differ in conformation and histone modification status and are differentially modulated by Rpd3p. Genome Biol 8:R11615
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968
Derelle E, Ferraz C, Rombauts S et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652
Di Filippo M, Bernardi G (2008) Mapping Dnase I-hypersensitive sites on human isochores. Gene 419:62–65
Dickerson RE (1992) DNA structure from A to Z. Methods Enzymol 211:67–111
Dujon B (1996) The yeast genome project: what did we learn? Trends Genet 12:263–270
Duret L, Eyre-Walker A, Galtier N (2006) A new perspective on isochore evolution. Gene 385:71–74
Eyre-Walker A, Hurst LD (2001) The evolution of isochores. Nat Rev Genet 2:549–555
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
Häring D, Kypr J (2001) No isochores in the human chromosomes 21 and 22? Biochem Biophys Res Commun 280:567–573
International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945
Isacchi A, Bernardi G, Bernardi G (1993) Compositional compartmentalization of the nuclear genomes of Trypanosoma brucei and Trypanosoma equiperdum. FEBS Lett 335:181–183
Jabbari K, Bernardi G (2000) The distribution of genes in the Drosophila genome. Gene 247:287–292
Jabbari K, Bernardi G (2004) Comparative genomics of Anopheles gambiae and Drosophila melanogaster. Gene 333:183–186
Jabbari K, Bernardi G (2017) An isochore framework underlies chromatin architecture. PLoS One 12(1):e0168023
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
Karlin S, Blaisdell BE, Sapolsky RJ, Cardon L, Burge C (1993) Assessment of DNA in homogeneities in yeast chromosome III. Nucleic Acid Res 21:703–711
Katz LA, Grant JR, Parfey LW, Burleigh JG (2012) Turning the crown upside down: gene tree parsimony roots the eukaryotic tree of life. Syst Biol 61:653–660.
Lamolle G, Protasio A, Iriarte A, Jara E, Simón D, Musto H (2016) An sochore-like structure in the genome of the flatworm Schistosoma mansoni. Genome Biol Evol 8:2312–2318
Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh WES et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Macaya G, Thiery JP, Bernardi G (1976) An approach to the organization of eukaryotic genomes at a macromolecular level. J Mol Biol 108:237–254
McCutchan TF, Dame JB, Miller LH, Barnwell J (1984) Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science 225:808–811
Meselson M, Stahl FW, Vinograd J (1957) Equilibrium sedimentation of macromolecules in density gradients. Proc Natl Acad Sci USA 43:581–588.
Montero LM, Salinas J, Matassi G, Bernardi G (1990) Gene distribution and isochore organization in the nuclear genome of plants. Nucleic Acids Res 18(7):1859–1867
Musto H, Rodríguez-Maseda H, Bernardi G (1994) The nuclear genomes of African and American trypanosomes are strikingly different. Gene 141:63–69
Musto H, Naya H, Zavala A, Romero H, Alvarez-Valín F, Bernardi G (2006) Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 18:347(1):1–3.
Naya H, Romero H, Zavala A, Alvarez B, Musto H (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55(3):260–264
Nekrutenko A, Li WH (2001) Assessment of compositional heterogeneity within and between eukaryotic genomes. Genome Res 10:1986–1995
Niimura Y, Gojobori T (2002) In silico chromosome staining: reconstruction of Giemsa bands from the whole human genome sequence. Proc Natl Acad Sci USA 99(2):797–802
Palenik B, Grimwood J, Aerts A et al (2007) The tin eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104:7705–7710
Pollak Y, Katzen A, Spira D, Golenser J (1982) The genome of Plasmodium falciparum I: DNA composition. Nucleic Acid Res 10:539–546
Rodríguez-Maseda H, Musto H (1994) The compositional compartments of the nuclear genomes of Trypanosoma brucei and T. cruzi. Gene 151:221–224
Romero H, Pereira E, Naya H, Musto H (2009) Oxygen and guanine-cytosine profiles in marine environments. J Mol Evol 69(2):203–206
Saccone S, Federico C, Andreozzi L, D’Antoni S, Bernardi G (2002) Localization of the gene-richest and the gene-poorest isochores in the interphase nuclei of mammals and birds. Gene 300:169–178
Segal E, Fondufe-Mittendorf Y, Chen L, Thåström AC, Field Y, Moore YK, Wang JZ, Widom J (2006) A genomic code for nucleosome positioning. Nature 442:772–778
Sharp PM, Lloyd AT (1993) Regional base composition variation along yeast chromosome III: evolution of chromosome primary structure. Nucleic Acid Res 21:179–183
Thiery JP, Macaya G, Bernardi G (1976) An analysis of eukaryotic genomes by density gradient centrifugation. J Mol Biol 108:219–235
van Rheede T, Bastiaans T, Boone DN, Hedges SB, de Jong WW, Madsen O (2006) The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and Therians. Mol Biol Evol 23:587–597
Zerial M, Salinas J, Filipski J, Bernardi G (1986) Gene distribution and nucleotide sequence organization in the human genome. Eur J Biochem 160:479–485
Zhang R, Zhang CT (2004) Isochore structures in the genome of the plant Arabidopsis thaliana. J Mol Evol 59(2):227–238
Acknowledgements
We thank Prof. Giorgio Bernardi for his strong support in all the work cited in this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Costantini, M., Musto, H. The Isochores as a Fundamental Level of Genome Structure and Organization: A General Overview. J Mol Evol 84, 93–103 (2017). https://doi.org/10.1007/s00239-017-9785-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-017-9785-9