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The role of constrained self-organization in genome structural evolution

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Abstract

A hypothesis of genome structural evolution is explored. Rapid and cohesive alterations in genome organization are viewed as resulting from the dynamic and constrained interactions of chromosomal subsystem components. A combination of macromolecular boundary conditions and DNA element involvement in far-from-equilibrium reactions is proposed to increase the complexity of genomic subsystems via the channelling of genome turnover; interactions between subsystems create higher-order subsystems expanding the phase space for further genetic evolution. The operation of generic constraints on structuration in genome evolution is suggested by i) universal, homoplasic features of chromosome organization and ii) the metastable nature of genome structures where lower-level flux is constrained by higher-order structures. Phenomena such as ‘genomic shock’, bursts of transposable element activity, concerted evolution, etc., are hypothesized to result from constrained systemic responses to endogenous/exogenous, micro/macro perturbations. The constraints operating on genome turnover are expected to increase with chromosomal structural complexity, the number of interacting subsystems, and the degree to which interactions between genomic components are tightly ordered.

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References

  • Agur, Z. and M. Kerzberg (1987). The emergence of phenotypic novelties through progressive genetic change. Amer. Nat. 129: 862–875.

    Google Scholar 

  • Beitel, L.K., J.G. McArthur and C.P. Stanners (1991). Sequence requirements for the stimulation of gene amplification by a mammalian genomic element. Gene 102: 149–156.

    Google Scholar 

  • Benfante, R., N. Landsberger, D. Maiorano and G. Badaracco (1990). A binding (p82) protein recognizes specifically the curved heterochromatic DNA in Artemia franciscana. Gene 94: 217–222.

    Google Scholar 

  • Bernardi, G. (1993a). The vertebrate genome: isochores and evolution. Mol. Biol. Evol. 10: 186–204.

    Google Scholar 

  • Bernardi, G. (1993b). Genome organization and species formation in vertebrates. J. Mol. Evol. 37: 331–337.

    Google Scholar 

  • Bernardi, G. (1995). The human genome: organization and evolutionary history. Ann. Rev. Genetics 29: 445–476.

    Google Scholar 

  • Beanúes, J., R. Beltrán and F. Azorín (1991). SV40 recombinants carrying a d(CT-GA)22 sequence show increased genomic instability. Gene 108: 269–274.

    Google Scholar 

  • Biémont, C., C. Arnault, A. Heizmann and A. Ronserray (1990). Massive changes in genomic locations of P elements in an inbred line of Drosophila melanogaster. Naturwissenschaften 77: 485–488.

    Google Scholar 

  • Bouffler, S., A. Silver and R. Fox (1993). The role of DNA repeats and associated secondary structures in genomic instability and neoplasia. Bioessays 15: 409–412.

    Google Scholar 

  • Boulikas, T. (1992). Evolutionary consequences of nonrandom damage and repair of chromatin domains. J. Mol. Evol. 35: 156–180.

    Google Scholar 

  • Britten, R.J., W.F. Baron, D.B. Stout and E.H. Davidson (1988). Sources and evolution of humanAlu repeated sequences. Proc. Nati. Acad. Sci. U.S.A. 85: 4770–4774.

    Google Scholar 

  • Brooks, D.R. and E.O. Wiley (1988). Evolution as Entropy. Chicago, University of Chicago Press.

    Google Scholar 

  • Campbell, J.H. (1985). An organizational interpretation of evolution. In: D.J. Depew and B.H. Weber, eds., Evolution at a Crossroads: The New Biology and the New Philosophy of Science, 133–167. Cambridge, MIT Press.

    Google Scholar 

  • Charlesworth, B., P. Sniegowski and W. Stephen (1994). The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215–220.

    Google Scholar 

  • Clark, S.P., C.D. Lewis and G. Felsenfeld (1990). Properties of BGP1, a poly (dG)-binding protein from chicken erythrocytes. Nucl. Acids Res. 18: 5119–5126.

    Google Scholar 

  • Coggins, L.W., M. O'Prey and S. Akhter (1992). Intrahelical pseudoknots and interhelical associations mediated by mispaired human minisatellite DNA sequence in vitro. Gene 121: 279–285.

    Google Scholar 

  • Collick, A., M.G. Dunn and A.J. Jeffreys (1990). Detection of a novel minisatellite-specific DNAbinding protein. Nucl. Acids Res. 18: 625–629.

    Google Scholar 

  • Collick, A., M.G. Dunn and A.J. Jeffreys (1991). Minisatellite binding protein Msbp-1 is a sequence-specific single-stranded DNA-binding protein. Nucl. Acids Res. 19: 6399–6404.

    Google Scholar 

  • Cook, K.R. and G.H. Karpen (1994). A rosy future for heterochromatin. Proc. Natl. Acad. Sci. U.S.A. 91: 5219–5221.

    Google Scholar 

  • Corces, V. (1995). Keeping enhancers under control. Nature 376: 462–463.

    Google Scholar 

  • Cullis, C.A. (1985). Plant DNA variation and stress. In: J.P. Gustafson, G.L. Stebbins and F.J. Ayala, eds., Genetics, Development and Evolution, 143–155. New York, Plenum Press.

    Google Scholar 

  • Deininger, P.L. and V.K. Slagel (1988). Recently amplified Alu family members share a common parental Alu sequence. Mol. Cell. Biol. 8: 4566–4569.

    Google Scholar 

  • Dillon, N. and F. Grosveld (1994). Chromatin domains as potential units of eukaryotic gene function. Curr. Opin. Genetics Dev. 4: 260–264.

    Google Scholar 

  • Dijan, P. and H. Green (1992). The involucrin gene of Old-World monkeys and other higher primates: synapomorphies and parallelisms resulting from the same gene-altering mechanism. Mol. Biol. Evol. 9: 417–432.

    Google Scholar 

  • Doolittle, W.F. (1989). Hierarchical approaches to genome evolution. Can. J. Phil. Suppl. 14: 104–108.

    Google Scholar 

  • Doshi, P., S. Kaushal, C. Benyajati and C.A. Wu (1991). Molecular analysis of responder satellite DNA in Drosophila melanogaster: DNA bending, nucleosome structure, and Rsp-binding proteins. Mol. Biol. Evol. 8: 721–741.

    Google Scholar 

  • Dover, G.A. (1982). Molecular drive: a cohesive mode of species evolution. Nature 299: 111–117.

    Google Scholar 

  • Dover, G.A. and D. Tautz (1986). Conservation and divergence in multigene families: alternatives to selection and drift. Phil. Trans. Royal Soc. Lond. B 312: 275–289.

    Google Scholar 

  • Dujon, B. (1993). Mapping and sequencing the nuclear genome of the yeast Saccharomyces cerevisiae: strategies and results of the European enterprise. Cold Spring Harbor Symp. Quant. Biol. 58: 357–366.

    Google Scholar 

  • Elder, J.F., and B.J. Turner (1994). Concerted evolution at the population level: pupfish HindIII satellite DNA sequences. Proc. Natl. Acad. Sci. U.S.A. 91: 994–998.

    Google Scholar 

  • Elder, J.F., and B.J. Turner (1995). Concerted evolution of repetitive DNA sequences in eukaryotes. Quart. Rev. Biol. 70: 297–320.

    Google Scholar 

  • Engels, W.R. (1989). P elements in Drosophila melanogaster. In: D.E. Berg and M.M. Howe, eds., Mobile DNA, 437–484. Washington DC, American Society for Microbiology.

    Google Scholar 

  • Englander, E.W., A.P. Wolffe and B.H. Howard (1993). Nucleosome interactions with a human Alu element. J. Biol. Chem. 268: 19565–19573.

    Google Scholar 

  • Filipski, J. (1990). Evolution of DNA sequence contributions of mutational bias and selection to the origin of chromosomal compartments. Adv. Mutagenesis 2: 1–54.

    Google Scholar 

  • Filipski, J., J. Salinas and F. Rodier (1989). Chromosome localization-dependent compositional bias of point mutations in Alu repetitive sequences. J. Mol. Biol. 206: 563–566.

    Google Scholar 

  • Fogle, T. (1990). Are genes units of inheritance? Biol. Phil. 5: 349–371.

    Google Scholar 

  • Fontana, W. and L. Buss (1994). What would be conserved if “the tape were played twice”? Proc. Natl. Acad. Sci. U.S.A. 91: 757–761.

    Google Scholar 

  • Fontdevila, A. (1992). Genetic instability and rapid speciation: are they coupled? In: J.F. McDonald, ed., Transposable Elements and Evolution, 242–253. Dordrecht, Kluwer Acad. Publ.

    Google Scholar 

  • Gaillard, C. and F. Strauss (1994). Association of poly (CA)-poly (TG) DNA fragments into fourstranded complexes bound by HMG1 and 2. Science 264: 433–436.

    Google Scholar 

  • Gerstel, D.U. and L.A. Burns (1976). Enlarged euchromatic chromosomes (“megachromosomes”) in hybrids between Nicotiana tabacum and N. plumbaginiflora. Genetics 46: 139–153.

    Google Scholar 

  • Green, H. and P. Dijan (1992). Consecutive actions of different gene-altering mechanisms in the evolution of involucrin. Mol. Biol. Evol. 9: 977–1017.

    Google Scholar 

  • Haaf, T. and M. Schmid (1991). Chromosome topology in mammalian interphase nuclei. Exp. Cell Res. 192: 325–332.

    Google Scholar 

  • Hardison, R. and W. Miller (1993). Use of long sequence alignments to study the evolution and regulation of mammalian globin gene clusters. Mol. Biol. Evol. 10: 73–102.

    Google Scholar 

  • Heslop-Harrison, J.S. (1990). Gene expression and parental dominance in hybrid plants. Development Suppl. 21–28.

  • Hillis, D.M., C. Moritz, C.A. Porter and R.J. Baker (1991). Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251: 308–310.

    Google Scholar 

  • Holmquist, G.P. (1989). Evolution of chromosome bands: molecular ecology of noncoding DNA. J. Mol. Evol. 28: 469–486.

    Google Scholar 

  • Holmquist, G.P. (1992). Chromosome bands, their chromatin flavors, and their functional features. Amer. J. Hum. Genetics 51: 17–37.

    Google Scholar 

  • Holmquist, G.P. (1994). Chromatin self-organization by mutation bias. J. Mol. Evol. 39: 436–438.

    Google Scholar 

  • Holmquist, G.P. and J. Filipski (1994). Organization of mutations along the genome: a prime determinant of genome evolution. Trends Ecol. Evol. 9: 65–69.

    Google Scholar 

  • Hopmann, R., D. Duncan and I. Duncan (1995). Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans. Genetics 139: 815–833.

    Google Scholar 

  • Jabs, E.W., C.A. Goble and G.R. Cutting (1989). Macromolecular organization of human centromeric regions reveals high-frequency, polymorphic macro DNA repeats. Proc. Natl. Acad. Sci. U.S.A. 86: 202–206.

    Google Scholar 

  • Jansson, S., G. Meyer-Gauen, R. Cerff and W. Martin (1994). Nucleotide distribution in Gymnosperm nuclear sequences suggests a models for GC-content change in land-plant nuclear genomes. J. Mol. Evol. 39: 34–46.

    Google Scholar 

  • Jeffreys, A.J., V. Wilson and S.L. Thein (1985). Hypervariable “minisatellite” regions in human DNA. Nature 314: 67–73.

    Google Scholar 

  • Jensen, S., L. Cavarec, M.-P. Gassama and T. Heidmann (1995). Defective I elements introduced into Drosophila as transgenes can regulate reactivity and prevent I-R hybrid dysgenesis. Mol. Gen. Genetics 248: 381–390.

    Google Scholar 

  • Junakovic, N., C. DiFranco, M. Best-Belpomme and G. Echalier (1988). On the transposition of copialike elements in cultured Drosophila cells. Chromosoma 97: 212–218.

    Google Scholar 

  • Karlin, S., I. Ladunga and B.E. Blaisdell (1994). Heterogeneity of genomes: measures and values. Proc. Natl. Acad. Sci. U.S.A. 91: 12837–12841.

    Google Scholar 

  • Kauffman, S.A. (1993). The Origins of Order: Self-Organization and Selection in Evolution. New York, Oxford University Press.

    Google Scholar 

  • Kaukinen, J. and S.L. Varvio (1992). Artiodactyl retroposons: association with microsatallites and use in SINEmorph detection by PCR. Nucl. Acids Res. 20: 2955–2958.

    Google Scholar 

  • Kelly, R., G. Bulfield, A. Collick, M. Gibbs and A.J. Jeffreys (1989). Characterization of a highly unstable mouse minisatellite locus: evidence for somatic mutation during early development. Genomics 5: 844–856.

    Google Scholar 

  • Kelly, R., M. Gibbs, A. Collick, M. Gibbs and A.J. Jeffreys (1991). Spontaneous mutation at the hypervariable mouse minisatellite locus Ms6-hm: flanking DNA sequence and analysis of germline and early somatic mutation events. Phil. Proc. Royal Soc. Lond. B 245: 235–245.

    Google Scholar 

  • Kennison, J.A. (1995). The polycomb and trithorax group protein of Drosophila: trans-regulators of homeotic gene function. Ann. Rev. Genetics 29: 289–303.

    Google Scholar 

  • King, M. (1982). A case for simultaneous multiple chromosomal rearrangements. Genetica 59: 53–60.

    Google Scholar 

  • King, M. (1993). Species Evolution. Cambridge University Press.

  • Levinson, G., J.L. Marsh, J.T. Epplen and G.A. Gutman (1985). Cross-hybridizing snake satellite, Drosophila, and mouse sequences may have arisen independently. Mol. Biol. Evol. 2: 494–504.

    Google Scholar 

  • Lima de Faria, A. (1983). Molecular Evolution and Organization of the Chromosome. New York, Elsevier Press.

    Google Scholar 

  • Manuelidis, L. (1990). A view of interphase chromosomes. Science 250: 1533–1540.

    Google Scholar 

  • Matzke, M. and A. Matzke (1993). Genome imprinting in plants: parental effects and trans-inactivation phenomena. Ann. Rev. Plant Physiol. Plant Mol. Biol. 44: 53–76.

    Google Scholar 

  • McArthur, J.G., L.K. Beitel, J.W. Chamberlain and C.P. Stanners (1991). Elements which stimulate gene amplification in mammalian cells: role of recombinogenic sequences/ structures and transcriptional activation. Nucl. Acids Res. 19: 2477–2484.

    Google Scholar 

  • McClintock, B. (1978). Mechanisms that rapidly reorganize the genome. Stadler Symp. 10: 25–47.

    Google Scholar 

  • McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226: 792–801.

    Google Scholar 

  • Mietz, J.A., J.P. Fewell and E.L. Kuff (1992). Selective amplification of a discrete family of endogenous proviral elements in normal BALB/c lymphocytes. Mol. Cell. Biol. 12: 220–228.

    Google Scholar 

  • Miklos, G.L.G. (1985). Localized highly repetitive DNA sequences in vertebrate and invertebrate genomes. In: R.J. MacIntyre, ed., Molecular Evolutionary Genetics, 241–321. New York, Plenum Press.

    Google Scholar 

  • Mitani, K., Y. Takahashi and R.A. Kominami (1990). GGCAGG motif in minisatellites affecting their germline instability. J. Biol. Chem. 265: 15203–15210.

    Google Scholar 

  • Modi, W.S. (1993). Rapid, localized amplification of a unique satellite DNA family in the rodent Microtus chrotorrhinus. Chromosoma 102: 484–490.

    Google Scholar 

  • Müller, H.-P. and H.E. Varmus (1994). DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J. 13: 4704–4714.

    Google Scholar 

  • Nachman, M.W. and J.B. Searle (1995). Why is the house mouse karyotype so variable? Trends Ecol. Evol. 10: 397–402.

    Google Scholar 

  • Nasir, J., M.K. Maconochie and S.D.M. Brown (1991). Coamplification of Ll LINE elements with localised low copy repeats in Giemsa dark bands: implications for genome organization. Nucl. Acids Res. 19: 3255–3260.

    Google Scholar 

  • Ohta, T. (1992). The meaning of natural selection revisited at the molecular level. Trends Ecol. Evol. 7: 311–312.

    Google Scholar 

  • Okada, N. (1991). SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol. Evol. 11: 358–361.

    Google Scholar 

  • Olmo, E. (1991). Genome variations in the transition from amphibians to reptiles. J. Mol. Evol. 33: 68–75.

    Google Scholar 

  • Peschke, V.M. and R.L. Phillips (1991). Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theor. Applied Genetics 81: 90–97.

    Google Scholar 

  • Peterson, P.A. (1985). Mobile elements in maize: a force in evolutionary and plant breeding processes. In: J.P. Gustafson, G.L. Stebbins and F.J. Ayala, eds. Genetics, Development and Evolution, 47–78. New York, Plenum Press.

    Google Scholar 

  • Pike, -M., A. Carlisle, C. Newell, S. B. Hong and P.R. Musich (1986). Sequence and evolution of Rhesus monkey alphoid DNA. J. Mol. Evol. 23: 127–137.

    Google Scholar 

  • Qumsiyeh, M.B. (1994). Evolution of number and morphology of mammalian chromosomes. J. Hered. 85: 455–465.

    Google Scholar 

  • Radic, M.Z., M. Saghbini, T.S. Elton, R. Reeves and B.A. Hamkolo (1992). Hoechst 33258, distamycin A, and high mobility group protein I (HMG-I) compete for binding to mouse satellite DNA. Chromosoma 101: 602–608.

    Google Scholar 

  • Ratner, V.A., S.A. Zabanov, O.V. Kolesnikova and L.A. Vasilyeva (1992). Induction of the mobile genetic element Dm-4l2 transpositions in the Drosophila genome by heat shock treatment. Proc. Natl. Acad. Sci. U.S.A. 89: 5650–5654.

    Google Scholar 

  • Rhoades, M.M. and Dempsey, E. (1973). Chromatin elimination induced by the B chromosome of maize. J. Hered. 64: 12–18.

    Google Scholar 

  • Richards, R.I. and G.R. Sutherland (1992). Heritable unstable DNA sequences. Nature Genetics 1: 7–9.

    Google Scholar 

  • Roseman, R.R., J.M. Swan and P.M. Geyer (1995). A Drosophila insulator protein facilitates dosage compensation of the X chromosome mini-white gene located at autosomal insertion sites, Development 121: 3573–3582.

    Google Scholar 

  • Rubin, C.M., C.A. Vande Voort, R.L. Teplitz and C.W. Schmid (1994). Alu repeated DNAs are differentially methylated in primate germ cells. Nucl. Acids Res. 22: 5121–5127.

    Google Scholar 

  • Salthe, S.N. (1985). Evolving Hierarchical Systems. New York, Columbia University Press.

    Google Scholar 

  • Salthe, S.N. (1993). Development and Evolution. Cambridge, MIT Press.

    Google Scholar 

  • Schneeberger, R.G. and C.A. Cullis (1991). Specific DNA alterations associated with the environmental induction of heritable changes in flax. Genetics 128: 619–630.

    Google Scholar 

  • Shapiro, J.A. (1991). Genomes as smart systems. Genetica 84: 3–4.

    Google Scholar 

  • Shapiro, J.A. (1992). Natural genetic engineering in evolution. Genetica 86: 99–111.

    Google Scholar 

  • Sniegowski, P.D. and R.E. Lenski (1995). Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Ann. Rev. Genetics 26: 553–578.

    Google Scholar 

  • Soriano, P., M. Meunier-Rotival and G. Bernardi (1983). The distribution of interspersed repeats is nonuniform and conserved in the mouse and human genomes. Proc. Natl. Acad. Sci. U.S.A. 80: 1816–1820.

    Google Scholar 

  • Spector, D.L. (1993). Macromolecular domains within the cell nucleus. Ann. Rev. Cell Biol. 9: 265–315.

    Google Scholar 

  • Sternberg, R.M. von, G.E. Novick, G.-P. Gao and R.J. Herrera (1992). Genome canalization: the coevolution of transposable and interspersed repetitive elements with single copy DNA. Genetica 86: 215–246.

    Google Scholar 

  • Strand, M., T.A. Prolla, R.M. Liskay and T.D. Petes (1993). Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365: 274–276.

    Google Scholar 

  • Tautz, D. and M. Renz (1984). Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucl. Acids Res. 12: 4127–4138.

    Google Scholar 

  • Traut, W. (1987). Hypervariable Bkm DNA loci in a moth, Ephestia kuehniella: does transposition cause restriction fragment length polymorphism? Genetics 115: 493–498.

    Google Scholar 

  • Usdin, K. and A.V. Furano (1989). Insertion of L1 elements into sites that can form non-B DNA. J. Biol. chem. 264: 20736–20743.

    Google Scholar 

  • Vavilov, N. (1922). The law of homologous series in variation. J. Genetics 12: 47–89.

    Google Scholar 

  • Vershinin, A.V., E.A. Salina and S.K. Svitashev (1992). Is there a connection between genomic changes and wide hybridization? Hereditas 116: 213–217.

    Google Scholar 

  • Vogt, P. (1990). Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved “chromatin folding code”. Hum. Genetics 84: 301–336.

    Google Scholar 

  • Wahls, W.P., L.J. Wallace and P.D. Moore (1990). Hypervariable minisatellite DNA is a hotspot for homologous recombination in human cells. Cell 60: 95–103.

    Google Scholar 

  • Wang, Y.-H. and J. Griffith (1995). Expanded CTG triplet blocks from the myotonic dystrophy gene create the strongest known natural nucleosome positioning elements. Genomics 25: 570–573.

    Google Scholar 

  • Weiler, K.S. and B.T. Wakimoto (1995). Heterochromatin and gene expression in Drosophila. Ann. Rev. Genetics 29: 577–605.

    Google Scholar 

  • White, M.J.D. (1975). Chromosomal repatterning: regularities and restrictions. Genetics 79: 63–72.

    Google Scholar 

  • Willard, H.F. (1985). Chromosome-specific organization of human alpha satellite DNA. Amer. J. Hum. Genetics 37: 524–532.

    Google Scholar 

  • Wu, C.-I., T.W. Lyttle, M.-L. Wu and G.F. Lin (1988). Association between a satellite DNA sequence and the responder of segregation distorter in D. melanogaster. Cell 54: 179–189.

    Google Scholar 

  • Yamazaki, H., S. Nomoto, Y. Mishima and R. Kominami (1992). A 35-kDa protein binding to a cytosine-rich strand of hypervariable DNA. J. Biol. Chem. 267: 12311–12316.

    Google Scholar 

  • Zhang, P. and A.C. Spradling (1995). The Drosophila salivary gland chromocenter contains highly polytenized subdomains of mitotic heterochromatin. Genetics 139: 659–670.

    Google Scholar 

  • Zuckerkandl, E. (1986). Polite DNA: functional density and functional compatibility in genomes. J. Mol. Evol. 24: 12–27.

    Google Scholar 

  • Zuckerkandl, E. (1992). Revisiting junk DNA. J. Mol. Evol. 34: 259–271.

    Google Scholar 

  • Zuckerkandl, E. (1994). Molecular pathways to parallel evolution. I. Gene nexuses and their morphological correlates. J. Mol. Evol. 39: 661–678.

    Google Scholar 

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von Sternberg, R. The role of constrained self-organization in genome structural evolution. Acta Biotheor 44, 95–118 (1996). https://doi.org/10.1007/BF00048418

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