Skip to main content
Log in

Nonautonomous transposable elements in prokaryotes and eukaryotes

  • Published:
Genetica Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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.

    Google Scholar 

  • Ashburner, M. 1989. Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • 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.

    Google Scholar 

  • Berg, D. E. & M. M. Howe (editors), 1989 Mobile DNA. American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Chandler, M., M. Clerget & L. Caro, 1980. IS1-promoted events associated with drug resistance plasmids. Cold Spring Harb Symp. Quant. Biol. 45: 157–165.

    Google Scholar 

  • 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.

    Google Scholar 

  • Charlesworth, B. & C. H. Langley, 1989. The population genetics of Drosophila transposable elements. Ann. Rev. Genet. 23: 251–287.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Doring, H.-P., E. Tillmann & P. Starlinger, 1984. DNA sequence of the maize transposable element Dissociation. Nature 207: 127–130.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hartl, D. L. & S. A. Sawyer, 1988. Why do unrelated insertion sequences occur together in the genome of Escherichia coli? Genetics 118: 537–541.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lawrence, J. G. & D. L. Hartl, 1991. Unusual codon usage bias occurring within insertion sequences in Escherichia coli. Genetica 84: 23–29.

    Google Scholar 

  • Lawrence, J. G., H. Ochman & D. L. Hartl, 1992. The evolution of insertion sequences in enteric bacteria. Genetics 131: 9–20.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Maruyama, K. & D. L. Hartl, 1991a. Evolution of the transposable element mariner in Drosophila species. Genetics 128: 319–329.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • McClintock, B., 1950. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36: 344–355.

    Google Scholar 

  • McClintock, B., 1951. Chromosome organization and genic expression. Cold Spring Harbor Symp. Quant. Biol. 16: 13–47.

    Google Scholar 

  • McClintock, B., 1955. Controlled mutation in maize. Carnegie Inst. Wash. Yearbook 54: 245–255.

    Google Scholar 

  • McClintock, B., 1956a. Controlling elements and the gene. Cold Spring Harbor Symp. Quant. Biol. 21: 197–216.

    Google Scholar 

  • McClintock, B., 1956b. Intranuclear systems controlling gene action and mutation. Brookhaven Symp. Biol. 8: 58–74.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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..

    Google Scholar 

  • Pfeifer, F., G. Wiedinger & W. Goebel, 1981. Genetic variability in Halobacterium halobium. J. Bacteriol. 145: 375–381.

    Google Scholar 

  • Pohlman, R. F., N. V. Fedoroff & J. Messing, 1984. The nucleotide sequence of the maize controlling element Activator. Cell 37: 635–643.

    Google Scholar 

  • 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.

    Google Scholar 

  • Rio, D. C., 1991. Regulation of Drosophila P element transposition. Trends Genet. 7: 282–287.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Spradling, A. C. & G. M. Rubin, 1982. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341–347.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Weidinger, G., G. Klotz & W. Goebel, 1979. A large plasmid from Halobacterium halobium carrying genetic information for gas vacuole information. Plasmid 2: 377–386.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00133710

Keywords

Navigation