Skip to main content

Advertisement

SpringerLink
Log in

Patterns of Hermes transposition in Drosophila melanogaster

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Transposable elements are being developed as tools for genomics and for the manipulation of insect genotypes for the purposes of biological control. An understanding of their transposition behavior will facilitate the use of these elements. The behavior of an autonomous Hermes transposable element from Musca domestica in the soma and germ-line of Drosophila melanogaster was investigated using the method of transposon display. In the germ-line, Hermes transposed at a rate of approximately 0.03 jumps per element per generation. Within the soma Hermes exhibited markedly non-random patterns of integration. Certain regions of the genome were distinctly preferred over others as integration targets, while other regions were underrepresented among the integration sites used. One particular site accounted for 4.4% of the transpositions recovered in this experiment, all of which were located within a 2.5-kb region of the actin5C promoter. This region was also present within the Hermes element itself, suggesting that this clustering is an example of transposable element "homing". Clusters of integration sites were also observed near the original donor sites; these represent examples of local hopping. The information content (sequence specificity) of the 8-bp target site was low, and the consensus target site resembles that determined from plasmid-based integration assays.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3A, B.
Fig. 4A–E.
Fig. 5.
Fig. 6
Fig. 7.

Similar content being viewed by others

References

  • Altschul SF, Gish WF, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Atkinson PW, O'Brochta DA (1992) In vivo expression of two highly conserved Drosophila genes in the Australian sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol 22:423–431

    CAS  Google Scholar 

  • Atkinson PW, O'Brochta DA (1999) Genetic transformation of non-drosophilid insects by transposable elements. Ann Entomol Soc Amer 92:930–936

    Google Scholar 

  • Atkinson PW, Pinkerton AC, O'Brochta DA (2001) Genetic transformation systems in insects. Annu Rev Entomol 46:317–346

    Article  CAS  PubMed  Google Scholar 

  • Bancroft I, Dean C (1993) Transposition pattern of the maize element Ds in Arabidopsis thaliana. Genetics 134:1221–1229

    PubMed  Google Scholar 

  • Belzile F, Yoder JI (1992) Pattern of somatic transposition in a high copy Ac tomato line. Plant J 2:173–179

    CAS  PubMed  Google Scholar 

  • Bender W, Hudson A (2000) P element homing in the Drosophila bithorax complex. Development 127:3981–3992

    CAS  PubMed  Google Scholar 

  • Bessereau JL, Wright A, Williams DC, Schuske K, Davis MW, Jorgensen EM (2001) Mobilization of a Drosophila transposon in the Caenorhabditis elegans germ line. Nature 413:70–74

    Article  CAS  PubMed  Google Scholar 

  • Bushman FD (1994) Tethering human immunodeficiency virus 1 integrase to a DNA site directs integration to nearby sequences. Proc Natl Acad Sci 91:9233–9237

    CAS  PubMed  Google Scholar 

  • Carareto CM, Kim W, Wojciechowski MF, O'Grady P, Prokchorova AV, Silva JC, Kidwell MG (1997) Testing transposable elements as genetic drive mechanisms using Drosophila P element constructs as a model system. Genetica 101:13–33

    CAS  PubMed  Google Scholar 

  • Casa AM, Brouwer C, Nagel A, Wang L, Zhang Q, Kresovich S, Wessler SR (2000) The MITE family Heartbreaker ( Hbr): molecular markers in maize. Proc Natl Acad Sci USA 97:10083–10089

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Greenblatt IM, Dellaporta SL (1992) Molecular analysis of Ac transposition and DNA replication. Genetics 130:665–676

    CAS  PubMed  Google Scholar 

  • Chin HG, Choe MS, Lee SH, Park SH, Koo JC, Kim NY, Lee JJ, Oh BG, Yi GH, Kim SC, Choi HC, Cho MJ, Han CD (1999) Molecular analysis of rice plants harboring an Ac/Ds transposable element-mediated gene trapping system. Plant J 19:615–623

    CAS  PubMed  Google Scholar 

  • Collins FC, Besansky NJ (1994) Vector biology and the control of malaria in Africa. Science 264:1874–1875

    CAS  PubMed  Google Scholar 

  • Collins FH (1994) Prospects for malaria control through the genetic manipulation of its vectors. Parasitology Today 10:370–371

    Google Scholar 

  • Curtis CF (1994) The case for malaria control by genetic manipulation of its vectors. Parasitology Today 10:371–374

    Google Scholar 

  • Curtis CF, Graves PM (1988) Methods for replacement of malaria vector populations. J Trop Med Hyg 91:43–48

    CAS  PubMed  Google Scholar 

  • Dowe MF Jr, Roman GW, Klein AS (1990) Excision and transposition of two Ds transposons from the bronze mutable 4 derivative 6856 allele of Zea mays L. Mol Gen Genet 221:475–485

    CAS  PubMed  Google Scholar 

  • Engstrom Y, Schneuwly S, Gehring W (1992) Spatial and temporal expression of an Antennapedia LacZ gene construct integrated into the endogenous Antennapedia gene of Drosophila melanogaster. Roux's Arch Dev Biol 201:65–80

    Google Scholar 

  • Fischer SE, Wienholds E, Plasterk RHA (2001) Regulated transposition of a fish transposon in the mouse germ line. Proc Natl Acad Sci USA 98:6759–6764

    Article  CAS  PubMed  Google Scholar 

  • Galindo MI, Ladeveze V, Lemeunier F, Kalmes R, Periquet G, Pascual L (1995) Spread of the autonomous transposable element hobo in the genome of Drosophila melanogaster. Mol Biol Evol 12:723–734

    CAS  PubMed  Google Scholar 

  • Golic KG (1994) Local transposition of P elements in Drosophila melanogaster and recombination between duplicated elements using a site-specific recombinase. Genetics 137:551–563

    CAS  PubMed  Google Scholar 

  • Good AG, Meister GA, Brock HW, Grigliatti TA, Hickey DA (1989) Rapid spread of transposable P elements in experimental populations of Drosophila melanogaster.Genetics 122:387–396

    CAS  Google Scholar 

  • Goryshin IY, Jendrisak J, Hoffman LM, Meis R, Reznikoff WS (2000) Insertional transposon mutagenesis by electroporation of released Tn5 transposition complexes. Nat Biotechnol 18:97–100

    Google Scholar 

  • Greenblatt IM (1984) A chromosomal replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, Modulator, in maize. Genetics 108:471–485

    Google Scholar 

  • Grotewold E, Athma P, Paterson T (1991) A possible hot spot for Ac insertion in the maize P gene. Mol Gen Genet 230:329–331

    CAS  PubMed  Google Scholar 

  • Hama C, Ali Z, Kornberg TB (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4:1079–1093

    CAS  PubMed  Google Scholar 

  • Horie K, Kuroiwa A, Ikawa M, Okabe M, Kondoh G, Matsuda Y, Takeda J (2001) Efficient chromosomal transposition of the Tc1/mariner -like transposon Sleeping Beauty in mice. Proc Natl Acad Sci USA 98:9191–9196

    Article  CAS  PubMed  Google Scholar 

  • Hudson A, O'Connor M, McCall K, Bender W (1995) P-element homing within the Bithorax complex. 36th Annual Drosophila Research Conference, Abstract 240

  • Kassis JA, Noll E, VanSickle EP, Odenwald WF, Perrimon N (1992) Altering the insertional specificity of a Drosophila transposable element. Proc Natl Acad Sci USA 89:1919–1923

    CAS  PubMed  Google Scholar 

  • Keller J, Lim E, Dooner HK (1993) Preferential transposition of Ac to linked sites in Arabidopsis. Theor Appl Genet 86:585–588

    CAS  Google Scholar 

  • Kidwell MG (1992) Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86:275–286

    CAS  PubMed  Google Scholar 

  • Kimura K, Kidwell MG (1994) Differences in P element population dynamics between the sibling species Drosophila melanogaster and Drosophila simulans. Genet Res Camb 63:27–38

    CAS  Google Scholar 

  • Ladeveze V, Galindo MI, Pascual L, Periquet G, Lemeunier F (1994) Invasion of the hobo transposable element studied by in situ hybridization on polytene chromosomes of Drosophila melanogaster. Genetica 93:91–100

    CAS  PubMed  Google Scholar 

  • Ladeveze V, Galindo I, Chaminade N, Pascual L, Periquet G, Lemeunier F (1998) Transmission pattern of hobo transposable element in transgenic lines of Drosophila melanogaster. Genet Res Camb 71:97–107

    Article  CAS  Google Scholar 

  • Liao G, Rehm EJ, Rubin GM (2000) Insertion site preferences of the P transposable element in Drosophila melanogaster.Proc Natl Acad Sci USA 97:3347–3351

    Article  CAS  PubMed  Google Scholar 

  • Long D, Goodrich J, Wilson K, Sundberg E, Martin M, Puangsomlee P, Coupland G (1997) Ds elements on all five Arabidopsis chromosomes and assessment of their utility for transposon tagging. Plant J 11:145–148

    Google Scholar 

  • Meister GA, Grigliatti TA (1993) Rapid spread of a P element/ Adh gene construct through experimental populations of Drosophila melanogaster. Genome 36:1169–1175

    CAS  PubMed  Google Scholar 

  • Newfeld SJ, Takaesu NT (1999) Local transposition of a hobo element within the decapentaplegic locus of Drosophila. Genetics 151:177–187

    CAS  PubMed  Google Scholar 

  • O'Brochta DA, Warren WD, Saville KJ, Atkinson PW (1996) Hermes, a functional non-drosophilid insect gene vector from Musca domestica. Genetics 142:907–914

    CAS  PubMed  Google Scholar 

  • Osborne BI, Corr CA, Prince JP, Hehl R, Tanksley SD, McCormick S, Baker B (1991) Ac transposition from a T-DNA can generate linked and unlinked clusters of insertions in the tomato genome. Genetics 129:833–844

    CAS  PubMed  Google Scholar 

  • Peterson T (1990) Intragenic transposition of Ac generates a new allele of the maize P gene. Genetics 126:469–476

    CAS  PubMed  Google Scholar 

  • Pinkerton AC, Michel K, O'Brochta DA, Atkinson PW (2000) Green fluorescent protein as a genetic marker in transgenic Aedes aegypti.Insect Mol Biol 9:1–10

    Article  CAS  PubMed  Google Scholar 

  • Preston CR, Engels WR (1989) Spread of P transposable elements in inbred lines of Drosophila melanogaster. Prog Nucleic Acids Res Mol Biol 36:71–85

    CAS  Google Scholar 

  • Robbins TP, Carpenter R, Coen ES (1989) A chromosomal rearrangement suggests that donor and recipient sites are associated during Tam3 transposition in Antirrhinum majus. EMBO J 8:5–13

    CAS  Google Scholar 

  • Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241–245

    CAS  PubMed  Google Scholar 

  • Robertson HM, Lampe DJ (1995) Distribution of transposable elements in arthropods. Annu Rev Entomol 40:333–357

    Article  CAS  PubMed  Google Scholar 

  • Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353

    CAS  PubMed  Google Scholar 

  • Saville KJ, Warren WD, Atkinson PW, O'Brochta DA (1999) Integration specificity of the hobo element of Drosophila melanogaster is dependent on sequences flanking the target site. Genetica 105:133–147

    Article  CAS  PubMed  Google Scholar 

  • Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100

    CAS  PubMed  Google Scholar 

  • Silva JC, Kidwell MG (2000) Horizontal transfer and selection in the evolution of P elements. Mol Biol Evol 17:1542–1547

    CAS  PubMed  Google Scholar 

  • Smith D, Wohlgemuth J, Calvi BR, Franklin I, Gelbart WM (1993) hobo enhancer trapping mutagenesis in Drosophila reveals an insertion specificity different from P elements. Genetics 135:1063–1076

    CAS  PubMed  Google Scholar 

  • Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347

    CAS  PubMed  Google Scholar 

  • Steller H, Pirrotta V (1986) P transposons controlled by the heat shock promoter. Molec. Cell Biol. 6:1640–1649

    Google Scholar 

  • Sundararajan P, Atkinson PW, O'Brochta DA (1999). Transposable element interactions in insects: Crossmobilization of hobo and Hermes. Insect Mol Biol 8:359–368

    Article  CAS  PubMed  Google Scholar 

  • Taillebourg E, Dura JM (1999) A novel mechanism for P element homing in Drosophila. Proc Natl Acad Sci USA 96:6856--6861

    Article  CAS  PubMed  Google Scholar 

  • Thummel CS, Boulet AM, Lipshitz HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74:445–456

    CAS  PubMed  Google Scholar 

  • Tower J, Karpen GH, Craig N, Spradling AC (1993) Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics 133:347–359

    CAS  PubMed  Google Scholar 

  • Van den Broeck D, Maes T, Sauer M, Zethof H, De Keukeleire P, D'Hauw M, Van Montagu M, Gerats T (1998) Transposon display identifies individual transposable elements in high copy number lines. Plant J 13:121–129

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    CAS  PubMed  Google Scholar 

  • Warren WD, Atkinson PW, O'Brochta DA (1994) The Hermes transposable element from the housefly, Musca domestica, is a short inverted repeat-type element of the hobo, Ac, and Tam3 ( hAT) element family. Genet Res Camb 64:87–97

    CAS  Google Scholar 

  • Weil CF, Marillonnet S, Burr B, Wessler SR (1992) Changes in state of the Wx-m5allele of maize are due to intragenic transposition of Ds. Genetics 130:175–185

    CAS  PubMed  Google Scholar 

  • Yoder JI (1990) Rapid proliferation of the maize transposable element Activator in transgenic tomato. Plant Cell 2:723–730

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Spradling AC (1993) Efficient and dispersed local P element transposition from Drosophila females. Genetics 133:361–373

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Institutes of Health (Grants GM48102 and AI45741). Drs. Won Kim, Hyeyoung Koo and Anne Grundschober-Freimoser provided helpful comments and suggestions. Mr. Jamison Orsetti provided valuable technical advice and assistance

Author information

Author notes

  1. A. C. Pinkerton

    Present address: Lion Bioscience Inc., , 9880 Campus Point Drive, San Diego, CA 92121, USA

Authors and Affiliations

  1. Center for Biosystems Research, Plant Sciences Building, Room 5115, University of Maryland Biotechnology Institute, College Park, MD 20742-4450, USA

    N. Guimond & D. A. O'Brochta

  2. Department of Entomology, University of California, Riverside, CA 92521, USA

    D. K. Bideshi, A. C. Pinkerton & P. W. Atkinson

Authors
  1. N. Guimond
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. K. Bideshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. C. Pinkerton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. W. Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. A. O'Brochta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. A. O'Brochta.

Additional information

Communicated by G. P. Georgiev

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guimond, N., Bideshi, D.K., Pinkerton, A.C. et al. Patterns of Hermes transposition in Drosophila melanogaster . Mol Gen Genomics 268, 779–790 (2003). https://doi.org/10.1007/s00438-002-0800-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-002-0800-4

Keywords

Search

Navigation