Abstract
This paper examines a model in which transposable elements provide a modular architecture for the cellular genome, complemented by cellular recombinational transformations, arising in turn as a dynamical consequence of this modular structure. It is proposed that the ecology of transposable elements in a given organism is a function of recombinational protocols of the evolving cellular genome. In mammals this is proposed to involve coordinated meiosis-phased activation of LINEs, SINEs and retrogenes complemented by endogenous retroviral transfer between cells.
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Anderson, G. R., D. L. Stoler, J. P. Scott & B. K. Farkas, 1988. Induction of VL30 element expression as a response to anoxic stress, pp. 265–74 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Ashworth, A., B. Skene, S. Swift & R. Lovell-Badge, 1990. Zfa is an expressed retroposon derived from an alternative transcript of the Zfx gene. EMBO J. 9: 1529–34.
Bains, W. J., 1986. The multiple origins of human Alu sequences. J. Mol. Evol. 23: 189–99.
Bernstein, L., S. Mount & A. Weiner, 1983. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed transcripts of the RNA into new chromosomal sites, Cell 32: 461–72.
Bingham, P. M. & Z. Zachar, 1989. Retrotransposons and the FB transposon from Drosophila melanogaster, pp. 485–502 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Blakemore, C., 1991. Images in the Brain, Sir Douglas Robb Lectures, University of Auckland.
Boeke, J. D., 1989. Transposable Elements in Saccharomyces cerevisae, pp. 335–74 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D. C.
Boeke, J., D. Eichinger & G. Fink, 1988. Regulation of yeast Ty element transposition, pp. 169–82 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Brosius, J., 1991. Retroposons-seeds of evolution, Science 251: 753.
Callan, H. G., 1963. The nature of lampbrush chromosomes. Int. Rev. Cyt. 15: 1–34.
Callan, H. G., 1969. Biochanmical activities of chromosomes during the prophase of meiosis, pp. 540–552 in A. Handbook of Molecular Cytology, edited by Lima de Faria North Holland Amsterdam.
Callahan, R., 1988. Two families of human endogenous retroviral genomes, pp. 91–100 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Carlson, D., J. Ross, 1983. Human β-globin promoter and coding sequences transribed by RNA polymerase III. Cell 34: 857–64.
Carrol, D., D. Knutzon & J. Garrett, 1989. Transposable Elements in Xenopus species, pp. 567–74 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Chao, L., C. Vargas, B. Spear & E. Cox, 1983. Transposable Elements as Mutator Genes in Evolution. Nature 303: 633–5.
Chen, I., G. McLauglin & D. Golde, 1984. Long terminal repeats of human T-cell leukemia virus II genome determine target specificity. Nature 309: 276–9.
Copeland, N., K. Hutchinson & N. Jenkins, 1983a. Excision of the DBA ecotropic provirus in dilute coat-color revertants of mice occurs by homologous recombination involving the viral LTRs. Cell 33: 379–87.
Copeland, N., N. Jenkins & B. Lee, 1983b. Association of the lethal yellow (Ay) coat color mutation with an ecotropic murine leukemia virus genome. Proc. Nat. Acad. Sci. 80: 247–9.
Davidson, E., R. Britten, 1979. Regulation of gene expression: possible role of repetitive sequences. Science 204: 1052–9.
Davidson, E. & J. Posakony, 1982. Repetitive sequence transcripts in development. Nature 297: 633.
Deinhardt, F., 1980. Biology of Primate Retroviruses, pp. 357–97 in G. Klein, Viral Oncology, Raven Press, New York.
Deininger, P. L., 1989. SINEs: Short interspersed repeated DNA elements in higher eukaryotes, pp. 619–36 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Doolittle, W., C. Sapienza, 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–3.
Dover, G., 1982. Molecular drive: A cohesive mode of species evolution. Nature 299: 111–7.
Edelman, G. M., J. A. Gally, 1970. Arrangement and Evolution of Eukaryotic genes in The neurosciences edited by F. O. Schmit, Rockefeller University Press, N.Y.
Engels, W., 1989. P elements in Drosophila melanogaster, pp. 437–84 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Federoff, N. V., 1989. Maize transposable Elements in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D. C.
Fink, G. R., 1987. Pseudogenes in yeast? Cell 49: 5–6.
Finnegan, D. J., 1983. Retroviruses and transposable elements-which came first? Nature 302: 105–6.
Finnegan, D. J., 1985. Transposable Elements in euckaryotes. Int. Rev. Cyt. 93: 281–325.
Finnegan, D. J., 1989a. F and related elements in Drosophila melanogaster, pp. 519–21 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Finnegan, D. J., 1989b. The I factor and I-R hybrid dysgenesis in Drosophila melanogaster, pp. 503–18 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Firtel, R. A., 1989. Mobile elements in the cellular slime mold Dictyostellium discoidium, pp. 557–66 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Geyer, P., M. Green & V. Corces, 1988. Molecular basis of transposable element-induced mutation in Drosophila melanogaster, pp. 123–30 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Graur, D., Y. Shuali & W. Li, 1989. Deletions in processed pseudogenes accumulate faster in rodents than in humans. J. Mol. Evol. 28: 279–85.
Green, M. M., 1988. Mobile DNA elements and spontaneous gene mutation, pp. 41–50 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Gorczynski, R. & E. Steele, 1980. Inheritance of acquired immunological tolerance to foreign histocompatibility antigens in mice. Proc. Nat. Acad. Sci. 77: 2871–5.
Hawley, R., M. Shulman, H. Murialdo, D. Gibson & N. Hozumi, 1982. Mutant immunoglobulin genes have repetitive DNA elements inserted into their intervening sequences. Proc. Nat. Acad. Sci. 79: 7425–7429.
Hollis, G.F., P. A. Hieter, O. McBride, D. Swam & P. Leder, 1982. Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing. Nature 296: 321–3.
Hutchinson, C., S. Hardies, D. Loeb, W. Shehee & M. Edgell. LINEs and related retrotransposons: Long interspersed repeated sequences in the eucaryotic genome, pp. 593–618 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Inouye, M. & S. Inouye, 1991. Retroelements in bacteria. TIBS Jan: 18–21.
Jeffreys, A., V. Wilson & S. Thein, 1985. Hypervariable ‘minisatellite’ regions in human DNA. Nature 314: 67.
Jenkins, N., N. Copeland, B. Taylor & B. Lee, 1981. Dilute (d) coat colour mutation of DBA/2J mice is associated with the site of integration of an ecotropic MuLV genome. Nature 293: 370–4.
Johns, M., J. Mottinger & M. Freeling, 1985. A low copy number Copia-like transposon in maize. EMBO J. 4: 1093–102.
Kenter, A. & B. Birshtein, 1981. Chi, a promoter of generalized recombination in λ phage is present in immunoglobulin genes. Nature 293: 402–4.
King, C., 1978. Unified field theories and the origins of life Univ. Auckland. Math. Dept. Rep. Series. 134.
King, C., 1985. A model for transposon-based eucaryote regulatory evolution. J. Theor. Biol. 114: 447–462.
King, C., 1989. Dual-Time Supercausality Physics Essays 2/2: 128–151.
King, C., 1991. Fractal and Chaotic Dynamics in Nervous Systems Progress in Neurobiology 36: 279–308.
Koishi, R. & N. Okada, 1991. Distribution of the salmonid Hpal family demonstrated by in vitro runoff transcription assay of total DNA. J. Mol. Evol. 32: 43–52.
Kuff, E. L., 1988. Factors affecting retrotransposition of intracisternal A-particle proviral element, pp. 79–90 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Lassar, A., M. Martin & R. Roeder, 1983. Transcription of class III genes: formation of preinitiation complexes. Science 222: 740–8.
Lemischka, I. & P. Sharp, 1982. The sequences of an expressed rat α-tubulin gene and a pseudogene with an inserted repetitive element. Nature 300: 330–5.
Limbach, K. & R. Wu, 1985. Characterization of a mouse somatic cytochrome c gene and three cytochrome c pseudogenes. Nucleic Acid Res. 13: 617–30.
Limborska, S., S. Korneev, N. Maleeva, A. Slominsky Jinsharadze, P. Ivanov & A. Ryskov, 1987. Cloning of Alu-containing cDNAs from human fibroblasts and identification of smal Alu polyA RNAs in a variety of human normal and tumor cells. FEBS Lett. 212: 208–12.
Lueders, K. & E. Kuff, 1977. Sequences associated with intracisternal A particles are reiterated in the mouse genome. Cell 12: 963–972.
Lueders, K., A. Leder, P. Leder & E. Kuff, 1982. Association between a transposed α-globin pseudogene and retroviruslike elements in the BALB/c mouse genome. Nature 295: 426–8.
MacLeod, A. & K. Talbot, 1983. A processed gene defining a gene family encoding a human non-muscle tropomyosin. J. Mol. Biol. 167: 523–37.
Manley, J. & M. Colozzo, 1982. Synthesis in vitro of an exceptionally long RNA transcript promoted by an Alu sequence. Nature 300: 376–9.
McClintock, B., 1978. Mechanisms that rapidly reorganize the genome Stadler Genet. Symp. 10: 25–48.
McClintock, B., 1984. The significance of the responses of the genome to challenge. Science 226: 792–801.
McDonald, J. F., 1990. Macroevolution and retroviral elements. BioScience 40: 183–91.
McDonald, J. F., D. Strand, M. Brown, S. Paskewitz, A. Csink & S. Voss, 1988. Evidence of host-mediated regulation of retroviral element expression at the post-transcriptional level, pp. 219–34 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Meuth, M., 1989. Illegitimate recombination in mammalian cells, pp. 833–60 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Moreau, J., L. Marcaud, F. Maschat, J. Kejzlarova-Lepesant, J. Lepesant & K. Scherrer, 1982. A + T-rich linkers define functional domains in eukaryotic DNA. Nature 295: 260–2.
Moroni, C., G. Schuman, 1977. Are endogenous C-type viruses involved in the immune system? Nature 269: 600–1.
Okada, N., 1990. Transfer RNA-like structure of the human Alu family: Implications of its generation mechanism and possible functions. J. Mol. Evol. 31: 500–510.
Orgel, L. & F. Crick, 1980. Selfish DNA: the ultimate parasite. Nature 284: 604–7.
Phillips, S., E. Birkenmeier, R. Callahan & E. Eicher, 1982. Male and female mouse DNAs can be discriminated using retroviral probes. Nature 297: 241–243.
Pollard, J. W., 1987. The moveable genome Rivista di Biologia-Biol. Forum 80: 11–54.
Quentin, Y., 1988. The Alu family developed through successive waves of fixation closely connected with primate lineage history. J. Mol. Evol. 27: 194–202.
Reanney, D. C., 1974. Viruses and evolution. Int. Rev. Cytol. 37: 21–55.
Reanny, D. C., 1975. A regulatory role for viral RNA in eukaryotes. J. Theor. Biol. 49: 461–92.
Reanny, D. C., 1976. Extrachromosomal elements as possible agents of adaption and development. Bact. Rev. 40: 552–90.
Ridley, M., 1985. Selfish DNA comes of age New Scientist 16 May: 34–7.
Rogers, J., 1985. The origin and evolution of Retroposons Int. Rev. Cytol. 93: 281–326.
Rosen, E., A. Siversten & H. Firtel, 1983. An unusual transposon encoding heat shock inducible and developmentally regulated transcripts in dictyostellium. Cell. 35: 243–51.
Saffer, J. & S. Thurston S, 1989. A negative regulatory element with properties similar to those of enhancers is contained within an Alu sequence. Mol. Cell. Biol. 9: 355–364.
Samuelson Wiebauer, K., C. Snow & M. Meisler, 1990. Retroviral & pseudogene insertion sites reveal lineage of human salivary & pancreatic amylase genes from a single gene during primate evolution. Mol. Cell. Biol.: 2513–20.
Sawyer, M., N. Nachlas & S. Panem, 1978. C-type viral antigen expression in human placenta. Nature 275: 62–4.
Sharp, P., 1983. Conversion of RNA into DNA in mammals: Alu-like elements and pseudogenes. Nature 301: 471–2.
Schwartz-Sommer, Z., 1987. The significance of plant transposable elements in biological processes in Structure and Function of Eukaryotic Chromosomes. Hennig H. Springer-Verlag Berlin Heidelberg 213–21.
Speck, N. & D. Baltimore, 1987. Six distinct nuclear factors interact with the 75-base pair repeat of the Moloney murine leukemia virus enhancer. Mol. Cell. Biol. 7: 1101–10.
Srikantha, T., D. Landsman & M. Bustin, 1987. Retropseudogenes for human chromosomal protein HMG-17. J. Mol. Biol. 197: 405–13.
Staber, F. G. & E. Schläfli, 1978. Expression of endogenous C-type virtal antigen on mormal mouse haemopoietic stem cells. Nature 275: 669–71.
Stavenhagen, J. & D. Robins, 1988. An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene. Cell 55: 247–54.
Steele, E., 1984. Somatic Selection and Adaptive Evolution: On the Inhertiance of Acquired Characters 2nd ed. Univ. Chicago Press, Chicago.
Stoye, J. P. & J. M. Coffin, 1987. The four classes of endogenous murine leukemia virus: Structural relationships and potential for recombination. J. Virol. 61: 2659–69.
Stoye, J. P. & J. M. Coffin, 1988. Polymorphism of murine endogenous proviruses revealed by using virus class specific oligonucleotide probes. J. Virol. 62: 168–75.
Sutcliffe, J., R. Milner, J. Gottesfeld & R. Lerner, 1984a. Identifier sequences are transcribed specifically in brain. Nature 308: 237–241.
Sutcliffe, J., R. Milner, J. Gottesfeld & W. Reynolds, 1984b. Control of neuronal gene expression. Science 225: 1308–15.
Tchurikov, N., T. Gerasimova, S. Georgieva, L. Mizrokhi, P. Georgiev & Y. Ilyn, 1988. Concerted transposition in Drosophila melanogaster, pp. 103–11 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Banbury Report 30, Cold Spring Harbor Laboratory.
Temin, H. M., 1980. Origin of retroviruses from cellular moveable genetic elements. Cell 21: 599–600.
Temin, H. M., 1989. Retrons in bacteria. Nature 339: 254–5.
Ueda, S., S. Hakai, Y. Nishida, H. Hisajima & T. Honjo, 1982. Long terminal repeat-lke elements flank a human immunoglobulin epsilon pseudogene that lacks introns. EMBO J. 1: 1539–44.
Ullu, E. & C. Tschudi, 1984. Alu sequences are processed 7sL RNA genes. Nature 312: 171–172.
Vanin, E. F., 1984. Processed pseudogenes: Characteristics and evolution. Biochem. Biophys. Acta 782: 231–241.
Varmus, H., 1982. Form and function of retroviral proviruses. Science 216: 812–20.
Varmus, H. & P. Brown, 1989. Retroviruses, pp. 53–108 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society for Microbiology, Washington D.C.
Voliva, C., S. Martin, C. Hutchinson & M. Edgell, 1984. Dispersal processes associated with the L1 family of interspersed repetitive DNA sequences. J. Mol. Biol. 178: 795–813.
Waddington, C. H., 1957. The Strategy of the Genes Allen & Unwin, London.
Watson, J. & J. Sutcliffe, 1987. Primate brain-specific cytoplasmic transcript of the Alu repeat family. Mol. Cell. Biol. 7: 3324–7.
Watson, J. D., N. H. Hopkins, J. W. Roberts, J. A. Stietz & A. M. Weiner, 1987. Molecular Biology of the Gene, Benjamin-Cummings, Menlo Park California.
Weiner, A., P. Deininger & A. Efstratiadis, 1986. Nonviral retroposons: genes, pseudogenes and transposable elements generated by the reverse flow of genetic information. Ann. Rev. Biochem. 55: 631–61.
Willard, C., H. Nguyen & C. Schmid, 1987. Existence of three distince Alu subfamilies. J. Mol. Evol. 26: 180–86.
Wolfe, S. L., 1972. pp. 418–9 Biology of the Cell, Wadsworth Belmont CA.
Yamamoto, T., C. Davis, M. Brown, W. Schneider, M. Casey, J. Goldstein & D. Russel, 1984. The human LDL receptor: A cysteine-rich protein with multiple Alu sequences in its mRNA Cell 39: 27–38.
Xiong, Y. & T. H. Eickbush, 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9/10: 3353–62.
Zuckerkandl, E., G. Latter & J. Jurka, 1989. Maintenance of function without selection. Alu sequences as ‘cheap genes’. J. Mol. Evol. 29: 504–12.
Zuker, C., J. Cappello, R. Chisholm & H. Lodish, 1983. A repetitive gene family that is induced during differentiation and by heat shock. Cell. 34: 997–1005.
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King, C.C. Modular transposition and the dynamical structure of eukaryote regulatory evolution. Genetica 86, 127–142 (1992). https://doi.org/10.1007/BF00133716
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DOI: https://doi.org/10.1007/BF00133716