Abstract
Defective (nonautonomous) copies of transposable elements are relatively common in the genomes of eukaryotes but less common in the genomes of prokaryotes. With regard to transposable elements that exist exclusively in the form of DNA (nonretroviral transposable elements), nonautonomous elements may play a role in the regulation of transposition. In prokaryotes, plasmid-mediated horizontal transmission probably imposes a selection against nonautonomous elements, since nonautonomous elements are incapable of mobilizing themselves. The lower relative frequency of nonautonomous elements in prokaryotes may also retlect the coupling of transcription and translation, which may bias toward the cis activation of transposition. The cis bias we suggest need not be absolute in order to militate against the long-term maintenance of prokaryotic elements unable to transpose on their own. Furthermore, any cis bias in transposition would also decrease the opportunity for trans repression of transposition by nonautonomous elements.
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References
Ajioka, J. W. & D. L. Hartl, 1989. Populations dynamics of transposable elements, pp. 939–958 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Ashburner, M. 1989. Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
Berg, D. E., 1989. Transposon Tn5, pp. 185–210 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Berg, D. E. & M. M. Howe (editors), 1989 Mobile DNA. American Society for Microbiology, Washington, D.C.
Bingham, P. M. & M. G. Kidwell & G. M. Rubin, 1982. The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain specific transposon family. Cell 29: 995–1004.
Black, D. M., M. S. Jackson, M. G. Kidwell & G. A. Dover, 1987. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster using a novel and general method. Cell 25: 693–704.
Capy, P., J. R. David & D. L. Hartl, 1992. Evolution of the transposable element mariner in the Drosophila melanogaster species subgroup. Genetica 86: 37–46.
Capy, P., K. Maruyama, J. R. David & D. L. Hartl, 1991. Insertion sites of the transposable element mariner are fixed in the genome of Drosophila sechellia. J. Mol. Evol. 33: 450–456.
Chandler, M., M. Clerget & L. Caro, 1980. IS1-promoted events associated with drug resistance plasmids. Cold Spring Harb Symp. Quant. Biol. 45: 157–165.
Charlebois, R. L. & W. F. Doolittle, 1989. Transposable elements and genome structure in Halobacteria, pp. 297–307 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Charlesworth, B. & C. H. Langley, 1989. The population genetics of Drosophila transposable elements. Ann. Rev. Genet. 23: 251–287.
Daniels, S. B., K. R. Peterson, L. D. Strausbaugh, M. G. Kidwell & A. Chovnick, 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124: 339–355.
Derbyshire, K. M., L. Hwang & N. D. F. Grindley, 1987. Genetic analysis of the interaction of the insertion sequence IS903 transposase with its terminal inverted repeats. Proc. Natl. Acad. Sci., USA 84: 8049–8053.
Doring, H.-P., E. Tillmann & P. Starlinger, 1984. DNA sequence of the maize transposable element Dissociation. Nature 207: 127–130.
Ebert, K., C. Hanke, H. Delius, W. Goebel & F. Pfeifer, 1987. A new insertion element, ISH26, from Halobacterium halobium. Mol. Gen. Genet. 206: 81–87.
Engels, W. R., 1989. P elements in Drosophila melanogaster, pp. 437–484 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Fedoroff, N. V., 1989. Maize transposable elements, pp. 375–411 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Galas, D. J. & M. Chandler, 1989. Bacterial insertion sequences, pp. 109–162 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Grindley, N. D. & C. M. Joyce, 1980. Genetic and DNA sequence analysis of kanamycin resistance transposon Tn903. Proc. Natl. Acad. Sci. USA 77: 7176–7180.
Hartl, D. L. & S. A. Sawyer, 1988. Why do unrelated insertion sequences occur together in the genome of Escherichia coli? Genetics 118: 537–541.
Hirsch, H. J., H. Saedler & P. Starlinger, 1972. Insertion mutation in the control region of the galactose operon of E. coli. II. Physical characterization of the mutations. Mol. Gen. Genet. 115: 266–276.
Isberg, R. R., A. L. Lazaar & M. Syvanen, 1982. Regulation of Tn5 by the right repeat proteins: control at the level of the transposition reactions? Cell 30: 883–892.
Johnson, R. C., J. C. P. Yin & W. S. Reznikoff, 1982. Control of Tn5 transposition in Escherichia coli is mediated by protein from the right repeat. Cell 30: 873–883.
Jordan, E., H. Saedler & P. Starlinger, 1968. 0-zero and strong polar mutations in the gal operon are insertions. Mol. Gen. Genet. 102: 353–363.
Lawrence, J. G. & D. L. Hartl, 1991. Unusual codon usage bias occurring within insertion sequences in Escherichia coli. Genetica 84: 23–29.
Lawrence, J. G., H. Ochman & D. L. Hartl, 1992. The evolution of insertion sequences in enteric bacteria. Genetics 131: 9–20.
Leung, P. C., D. B. Teplow & R. M. Harshey, 1989. Interaction of distinct domains in Mu transposase with Mu DNA ends and an internal transpositional enhancer, Nature 338: 656–658.
Machida, Y., C. Machida, H. Ohtsubo & E. Ohtsubo, 1982. Factors determining frequency of plasmid cointegration mediated by insertion sequence IS1. Proc. Natl. Acad. Sci. USA 79: 277–281.
Maruyama, K. & D. L. Hartl, 1991a. Evolution of the transposable element mariner in Drosophila species. Genetics 128: 319–329.
Maruyama, K. & D. L. Hartl, 1991b. Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J. Mol. Evol. 33: 514–524.
Maruyama, K., K. D. Schoor & D. L. Hartl, 1991. Identification of nucleotide substitutions necessary for trans-activation of mariner transposable elements in Drosophila: Analysis of naturally occurring elements. Genetics 128: 777–784.
McClintock, B., 1950. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36: 344–355.
McClintock, B., 1951. Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16: 13–47.
McClintock, B., 1955. Controlled mutation in maize. Carnegie Inst. Wash. Yearbook 54: 245–255.
McClintock, B., 1956a. Controlling elements and the gene. Cold Spring Harbor Symp. Quant. Biol. 21: 197–216.
McClintock, B., 1956b. Intranuclear systems controlling gene action and mutation. Brookhaven Symp. Biol. 8: 58–74.
Michaelis, G., H. Saedler, P. Venkov & P. Starlinger, 1969. Two insertions in the galactose operon having different sizes but homologous DNA sequences. Mol. Gen. Genet. 104: 193–210.
Miller, W. J., S. Hagemann & W. Pinsker, 1991. Selective conservation of a tandemly amplified ‘P-element repressor gene’ in the genome of Drosophila guanche, p. 59 in Abstracts of the 12th European Drosophila Conference, Mainz Germany.
Misra, S. & C. Rio, 1990. Cytotype control of Drosophila P element transposition: The 66 kd protein is a repressor of transposase activity. Cell 40: 269–284.
Morisato, D., J. C. Way, H.-J. Kim & N. Kleckner, 1983. Tn10 transposase acts preferentially on nearby transposon ends in vivo. Cell 32: 799–807.
Nakayama, C., D. B. Teplow & R. M. Harshey, 1987. Structural domains in Mu transposase: identification of the site-specific DNA-binding domain. Proc. Natl. Acad. Sci., USA 84: 1809–1813.
New, J. H., A. K. Eggleston & M. Fennewald, 1988. Binding of the Tn3 transposase to the inverted repeats of Tn3. J. Mol. Biol. 201: 589–599.
Pato, M. L., 1989. Tn3 and related transposable elements: sitespecific recombination and transposition, pp. 23–52 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C..
Pfeifer, F., G. Wiedinger & W. Goebel, 1981. Genetic variability in Halobacterium halobium. J. Bacteriol. 145: 375–381.
Pohlman, R. F., N. V. Fedoroff & J. Messing, 1984. The nucleotide sequence of the maize controlling element Activator. Cell 37: 635–643.
Reinitz, D. M., J. A. Inverso & J. M. Mansfield, 1989. Complete nucleotide sequence of an E. coli insertion element containing an internal 88 base pair direct repeat (IS5-D). Nuclei Acids Res. 17: 3990.
Rio, D. C., 1991. Regulation of Drosophila P element transposition. Trends Genet. 7: 282–287.
Sawyer, S. A., D. E. Dykhuizen, R. F. DuBose, L. Green, T. Mutangadura-Mhlanga, D. F. Wolczyk & D. L. Hartl, 1987. Distribution and abundance of insertion sequences among natural isolates of Escherichia coli. Genetics 115: 51–63.
Shapiro, J. A., 1969. Mutations caused by the insertion of genetic material in the galactose operon of Escherichia coli. J. Mol. Biol. 40: 93–105.
Sherratt, D., 1989. Tn3 and related transposable elements: sitespecific recombination and transposition, pp. 163–184 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Simsek, M., S. DeSarma, U. L. RajBhandary & H. G. Khorana, 1982. A transposable element from Halobacterium halobium which inactivates the bacteriorhodopsin gene. Proc. Natl. Acad. Sci., USA 79: 7268–7272.
Spradling, A. C. & G. M. Rubin, 1982. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341–347.
Stadler, R., P. Caspers, F. Olasz & W. Arber, 1990. The N-terminal domain of the insertion sequence 30 transposase interacts specifically with the terminal inverted repeats of the element. J. Biol. Chem. 265: 3757–3762.
Streck, R. D., J. E. MacGaffey & S. K. Beckendorf, 1986. The structure of hobo transposable elements and their insertion sites. EMBO J. 5: 3615–3623.
Sutton, W. D., W. L. Gerlach, D. Schwartz & W. J. Peacock, 1984. Molecular analysis of Ds controlling element mutations at the Adh1 locus of maize. Science 223: 1265–1268.
Umeda, M. & E. Ohtsubo, 1991. Four types of IS1 with differences in nucleotide sequence reside in the Escherichia coli K-12 chromosome. Gene 98: 1–5.
Weidinger, G., G. Klotz & W. Goebel, 1979. A large plasmid from Halobacterium halobium carrying genetic information for gas vacuole information. Plasmid 2: 377–386.
Wiater, L. A. & N. D. F. Grindley, 1988. γδ transposase and integration host factor bind cooperatively at both ends of γδ. EMBO J. 7: 1907–1911.
Zerbib, D., M. Jakowec, P. Prentki, D. Galas & M. Chandler, 1987. Expression of proteins essential for IS1 transposition: specific binding of InsA to the ends of IS1. EMBO J. 6: 3163–3169.
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Hartl, D.L., Lozovskaya, E.R. & Lawrence, J.G. Nonautonomous transposable elements in prokaryotes and eukaryotes. Genetica 86, 47–53 (1992). https://doi.org/10.1007/BF00133710
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DOI: https://doi.org/10.1007/BF00133710