Advertisement

Molecular Genetics and Genomics

, Volume 270, Issue 2, pp 173–180 | Cite as

Molecular evolutionary analysis of the widespread piggyBac transposon family and related "domesticated" sequences

  • A. Sarkar
  • C. Sim
  • Y. S. Hong
  • J. R. Hogan
  • M. J. Fraser
  • H. M. Robertson
  • F. H. Collins
Original Paper

Abstract

piggyBac is a short inverted-repeat-type DNA transposable element originally isolated from the genome of the moth Trichoplusia ni. It is currently the gene vector of choice for the transformation of various insect species. A few sequences with similarity to piggyBac have previously been identified from organisms such as humans ( Looper), the pufferfish Takifugu rubripes (Pigibaku), Xenopus (Tx), Daphnia (Pokey), and the Oriental fruit fly Bactrocera dorsalis. We have now identified 50 piggyBac-like sequences from publicly available genome sequences and expressed sequence tags (ESTs). This survey allows the first comparative examination of the distinctive piggyBac transposase, suggesting that it might contain a highly divergent DDD domain, comparable to the widespread DDE domain found in many DNA transposases and retroviral integrases which consists of two absolutely conserved aspartic acids separated by about 70 amino acids with a highly conserved glutamic acid about 35 amino acids further away. Many piggyBac-like sequences were found in the genomes of a phylogenetically diverse range of organisms including fungi, plants, insects, crustaceans, urochordates, amphibians, fishes and mammals. Also, several instances of "domestication" of the piggyBac transposase sequence by the host genome for cellular functions were identified. Novel members of the piggyBac family may be useful in genetic engineering of many organisms.

Keywords

piggyBac Transposable element Transposase TTAA-specific DDE domain 

Notes

Acknowledgements

The work described here was supported by NIH grants GM58826 (HMR) and P01AI45123 (P.I. Frank Collins), NIH cooperative agreement U01AI48846 (P.I. Frank Collins) and NIH cooperative agreement U01AI50687-01 (Large scale sequencing and assembly of the An. gambiae genome; P.I. Robert A. Holt, Celera Genomics)

Supplementary material

Supplementary Data Files

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–402PubMedGoogle Scholar
  2. Aparicio S, et al (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310CrossRefPubMedGoogle Scholar
  3. Beall EL, Mahoney MB, Rio DC (2002) Identification and analysis of a hyperactive mutant form of Drosophila P -element transposase. Genetics 162:217–227Google Scholar
  4. Carroll D, Knutson DS, Garrett JE (1989) Transposable elements in Xenopus species. In: Berg DE, Howe MM (eds) Mobile DNA. ASM Press, Washington, D.C, pp 567–574Google Scholar
  5. Cary LC, Goebel M, Corsaro BG, Wang HG, Rosen E, Fraser MJ (1989) Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172:156–169PubMedGoogle Scholar
  6. Craig NL, Craigie RC, Gellert M, Lambowitz AM (2002) Mobile DNA II. ASM Press, Washington D.C.Google Scholar
  7. Davies DR, Braam LM, Reznikoff WS, Rayment I (1999) The three-dimensional structure of a Tn5 transposase-related protein determined to 2.9-Å resolution. J Biol Chem 274:11904–11913Google Scholar
  8. Dehal P, et al (2002) The draft genome sequence of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167CrossRefPubMedGoogle Scholar
  9. Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif. Proc Natl Acad Sci USA 91:942–946Google Scholar
  10. Fraser MJ (2000) The TTAA-specific family of transposable elements: identification, functional characterization, and utility for transformation of insects. In: Handler AH, James AA (eds) Insect transgenesis. CRC Press, Boca Raton, pp 249–270Google Scholar
  11. Fraser MJ, Cary L, Boonvisudhi K, Wang HG (1995) Assay for movement of lepidopteran transposon IFP2 in insect cells using a baculovirus genome as a target DNA. Virology 211:397–407Google Scholar
  12. Fraser MJ, Ciszczon T, Elick T, Bauser C (1996) Precise excision of TTAA-specific lepidopteran transposons piggyBac ( IFP2) and tagalong ( TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol Biol 5:141–151Google Scholar
  13. Gardner MJ, (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511CrossRefPubMedGoogle Scholar
  14. Grossman GL, Rafferty CS, Clayton JR, Stevens TK, Mukabayire O, Benedict MQ (2001) Germline transformation of the malaria vector, Anopheles gambiae , with the piggyBac transposable element. Insect Mol Biol 10:597–604Google Scholar
  15. Handler AM (2002) Use of the piggyBac transposon for germ-line transformation of insects. Insect Biochem Mol Biol 32:1211–1220Google Scholar
  16. Handler AM, Harrell RA 2nd (1999) Germline transformation of Drosophila melanogaster with the piggyBac transposon vector. Insect Mol Biol 8:449–457Google Scholar
  17. Handler AM, McCombs SD (2000) The piggyBac transposon mediates germ-line transformation in the Oriental fruit fly and closely related elements exist in its genome. Insect Mol Biol 9:605–612Google Scholar
  18. Holt RA, et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149CrossRefPubMedGoogle Scholar
  19. Horn C, Wimmer EA (2000) A versatile vector set for animal transgenesis. Dev Genes Evol 210:630–637PubMedGoogle Scholar
  20. Horn C, Offen N, Nystedt S, Hacker U, Wimmer EA (2003) piggyBac -based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 163:647–661Google Scholar
  21. International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedGoogle Scholar
  22. Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 16:418–420Google Scholar
  23. Kipling D, Warburton PE (1997) Centromeres, CENP-B and Tigger too. Trends Genet 13:141–145PubMedGoogle Scholar
  24. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920PubMedGoogle Scholar
  25. Lobo NF, Hua-Van A, Li X, Nolen BM, Fraser MJ (2002) Germ line transformation of the yellow fever mosquito, Aedes aegypti , mediated by transpositional insertion of a piggyBac vector. Insect Mol Biol 11:133–139Google Scholar
  26. Mouse Genome Sequencing Consortium (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562CrossRefPubMedGoogle Scholar
  27. Nolan T, Bower TM, Brown AE, Crisanti A, Catteruccia F (2002) piggyBac -mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker. J Biol Chem 277:8759–8762Google Scholar
  28. Peloquin JJ, Thibault ST, Staten R, Miller TA (2000) Germ-line transformation of pink bollworm (Lepidoptera: Gelechiidae) mediated by the piggyBac transposable element. Insect Mol Biol 9:323–333CrossRefPubMedGoogle Scholar
  29. Penton EH, Sullender BW, Crease TJ (2002) Pokey, a new DNA transposon in Daphnia (Cladocera: Crustacea). J Mol Evol 55:664–673Google Scholar
  30. Robertson HM (2002) Evolution of DNA transposons in eukaryotes. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington, D.C., pp 1093–1110Google Scholar
  31. Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862PubMedGoogle Scholar
  32. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504CrossRefPubMedGoogle Scholar
  33. Smit AF (1999) Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev 9:657–663PubMedGoogle Scholar
  34. Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony and Other Methods. Sinauer Press, New YorkGoogle Scholar
  35. Tamura T, et al (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18:81–84PubMedGoogle Scholar
  36. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  37. Unsal K, Morgan GT (1995) A novel group of families of short interspersed repetitive elements (SINEs) in Xenopus: evidence of a specific target site for DNA-mediated transposition of inverted-repeat SINEs. J Mol Biol 248:812–823Google Scholar
  38. Wang HG, Fraser MJ (1993) TTAA serves as the target site for TFP3 lepidopteran transposon insertions in both nuclear polyhedrosis virus and Trichoplusia ni genomes. Insect Mol Biol 1:109–116Google Scholar
  39. Zieler H, Huynh CQ (2002) Intron-dependent stimulation of marker gene expression in cultured insect cells. Insect Mol Biol 11:87–95Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • A. Sarkar
    • 1
  • C. Sim
    • 1
  • Y. S. Hong
    • 1
  • J. R. Hogan
    • 1
  • M. J. Fraser
    • 1
  • H. M. Robertson
    • 2
  • F. H. Collins
    • 1
  1. 1.Center for Tropical Disease Research and Training, Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Department of EntomologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations