Skip to main content
SpringerLink
Log in

PpRT1: the first complete gypsy-like retrotransposon isolated in Pinus pinaster

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

We have isolated and characterized a complete retrotransposon sequence, named PpRT1, from the genome of Pinus pinaster. PpRT1 is 5,966 bp long and is closely related to IFG7 gypsy retrotransposon from Pinus radiata. The long terminal repeats (LTRs) have 333 bp each and show a 5.4% sequence divergence between them. In addition to the characteristic polypurine tract (PPT) and the primer binding site (PBS), PpRT1 carries internal regions with homology to retroviral genes gag and pol. The pol region contains sequence motifs related to the enzymes protease, reverse transcriptase, RNAseH and integrase in the same typical order known for Ty3/gypsy-like retrotransposons. PpRT1 was extended from an EST database sequence indicating that its transcription is occurring in pine tissues. Southern blot analyses indicate however, that PpRT1 is present in a unique or a low number of copies in the P. pinaster genome. The differences in nucleotide sequence found between PpRT1 and IFG7 may explain the strikingly different copy number in the two pine species genome. Based on the homologies observed when comparing LTR region among different gypsy elements we propose that the highly conserved LTR regions may be useful to amplify other retrotransposon sequences of the same or close retrotransposon family.

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. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CH:

Chromatin organization modifier

EST:

Expressed sequence tag

LTR:

Long terminal repeat

PBS:

Primer binding site

PCR:

Polymerase chain reaction

PPT:

Polypurine tract

RVE:

Integrase core domain

RVT:

Reverse transcriptase

References

  • Atchison ML (1988) Enhancers: mechanism of action and cell specificity. Annu Rev Cell Biol 4:127–153

    Article  PubMed  CAS  Google Scholar 

  • Baker T, Luo L (1994) Identification of residues in the Mu transposase essential for catalysis. Proc Natl Acad Sci USA 91:6654–6658

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JF (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36

    Article  PubMed  CAS  Google Scholar 

  • Bushman F (1993) Retroelement transposition—dodging the genes. Curr Biol 3:533–535

    Article  PubMed  CAS  Google Scholar 

  • Capy P, Langin T, Higuet D, Maurer P, Bazin C (1997) Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? Genetica 100:63–72

    Article  PubMed  CAS  Google Scholar 

  • Chavanne F, Zhang D-X, Liaud M-F, Cerff R (1998) Structure and evolution of Cyclops: a novel giant retrotransposon of the Ty3/Gypsy family highly amplified in pea and other legume species. Plant Mol Biol 37:363–375

    Article  PubMed  CAS  Google Scholar 

  • Colicelli J, Goff SP (1985) Mutants and pseudorevertantes of Moloney murine leukemia virus with alterations at the integration site. Cell 42:573–580

    Article  PubMed  CAS  Google Scholar 

  • Crawford S, Goff SP (1985) A deletion mutation in the 5′ part of the pol gene of Moloney murine leukemia virus blocks proteolytic processing of the gag and pol polyproteins. J Virol 58:899–907

    Google Scholar 

  • Curcio MJ, Garfinkel DJ (1999) New lines of host defense: inhibition of Ty1 retrotransposition by Fus3p and NER/TFIIH. Trends Genet 15:43–45

    Article  PubMed  CAS  Google Scholar 

  • Doolittle RF, Feng D-F, Jonhson MS, Mcclure MA (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64:1–30

    Article  PubMed  CAS  Google Scholar 

  • Eissenberg JC (2001) Molecular biology of chromo domain: an ancient chromatin module comes of age. Gene 275:19–29

    Article  PubMed  CAS  Google Scholar 

  • Esposito D, Craigie R (1998) Sequence specificity of viral end DNA binding by HIV-1 integrase reveals critical regions for protein-DNA interaction. EMBO J 17:5832–5843

    Article  PubMed  CAS  Google Scholar 

  • Favell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R (1992) Ty-1 copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res 20:3639–3644

    Article  Google Scholar 

  • Fayet O, Ramond P, Polard P, Frère MF, Chandler M (1990) Functional similarities between retroviruses and the IS3 family of bacterial insertion sequences? Mol Microbiol 4:1771–1777

    Article  PubMed  CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Genetics 3:329–341

    PubMed  CAS  Google Scholar 

  • Hansen CN, Heslop-Harrison JS (2004) Sequences and phylogenies of plant pararetroviruses, viruses and transposable elements. Adv Bot Res 41:165–193

    Article  CAS  Google Scholar 

  • Johns MA, Mottinger J, Freeling M (1985) A low copy number, copia-like transposon in maize. EMBO J 4:1093–1102

    PubMed  CAS  Google Scholar 

  • Katoh I, Yoshinaka Y, Rein A, Shibuya M, Odaka T, Oroszlan S (1985) Murine leukemia virus maturation: protease region required for conversion from ‘immature’ to ‘mature’ core form and for virus infectivity. Virology 145:280–292

    Article  PubMed  CAS  Google Scholar 

  • Kirchner J, Sandmeyer S (1993) Proteolytic processing of Ty3 protein is required for transposition. J Virol 67:19–28

    PubMed  CAS  Google Scholar 

  • Konieczny A, Voytas DF, Cummingst MP, Ausubel FM (1991) A superfamily of Arabidopsis thaliana retrotransposons. Genetics 127:801–809

    PubMed  CAS  Google Scholar 

  • Kossack DS, Kinlaw CS (1999) IFG, a gypsy-like retrotransposon in Pinus (Pinaceae), has an extensive history in pines. Plant Mol Biol 39:417–426

    Article  PubMed  CAS  Google Scholar 

  • Kulkosky J, Jones KS, Katz RA, Mack JPG, Skalka AM (1992) Residues critical for retroviral integrative recombination in a region that Is highly conserved among retroviral retrotransposon integrases and bacterial insertion-sequence transposases. Mol Cell Biol 12:2331–2338

    PubMed  CAS  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  PubMed  CAS  Google Scholar 

  • Lynch C, Tristem M (2003) A co-opted gypsy-type LTR-retrotransposon is conserved in the genomes of humans, sheep, mice and rats. Curr Biol 13:1518–1523

    Article  PubMed  CAS  Google Scholar 

  • Lyubomirskaya NV, Kim AI, Ilyin YV (2003) Retrotransposon gypsy and its role in genetic instability of a mutator strain of Drosophila melanogaster. Russ J Genet 39:112–119

    Article  CAS  Google Scholar 

  • Malik HS, Eickbush TH (1999) Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol 73:5186–5190

    PubMed  CAS  Google Scholar 

  • McDonald JF, Matyunina LV, Wilson S, Jordan IK, Bowen NJ, Miller WJ (1997) LTR retrotransposons and the evolution of eukaryotic enhancers. Genetica 100:3–13

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11

  • Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED (2002) Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416:103–107

    Article  PubMed  CAS  Google Scholar 

  • Pearce SR, Stuart-Rogers C, Knox MR, Kumar A, Ellis THN, Flavell AJ (1999) Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J 19:711–717

    Article  PubMed  CAS  Google Scholar 

  • Perlman PS, Boeke JD (2004) Ring around the retroelement. Science 303:182–184

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

  • SanMiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82(Suppl A):37–44

    Article  CAS  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  PubMed  CAS  Google Scholar 

  • Springer MS, Britten RJ (1993) Phylogenetic-relationships of reverse-transcriptase and Rnase-H sequences and aspects of genome structure in the gypsy group of retrotransposons. Mol Biol Evol 10:1370–1379

    PubMed  CAS  Google Scholar 

  • Sprinzl M, Steegborn C, Hübel F, Steinberg S (1996) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 24:68–72

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Anamthawat-Jonsson K, Arna T, Schulman A (1996) Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome. Plant Mol Biol 30:1321–1329

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Tanskanen J, Schlman AH (1998) Gypsy-like retrotransposon are widespread in the plant kingdom. Plant J 13:699–705

    Article  PubMed  CAS  Google Scholar 

  • Temin HM (1980) Origin of retroviruses from cellular movable genetic elements. Cell 21:599–600

    Article  PubMed  CAS  Google Scholar 

  • Tijan R, Maniatis T (1994) Transcriptional activation: a complex puzzle with few easy pieces. Cell 77:5–8

    Article  Google Scholar 

  • Varmus H, Brown P (1989) Retroviruses. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, pp 53–108

    Google Scholar 

Download references

Acknowledgments

Dr. Christophe Plomion (INRA, France) is gratefully acknowledged for providing the initial 183 bp sequence of PpRT1 retrotransposon. This research was supported by Fundação para a Ciência e Tecnologia (FCT) and the III Framework Program of the EC through grant SFRH/BPD/17902/2004 (CM) and through project POCTI/AGR/46283/2002.

Author information

Authors and Affiliations

  1. Forest Biotech Lab, Instituto de Biologia Experimental e Tecnológica (IBET/ITQB), Quinta do Marquês, 2784-505, Oeiras, Portugal

    Margarida Rocheta, Jorge Cordeiro, M. Oliveira & Célia Miguel

  2. Dep. Biologia Vegetal, Univ. Lisboa, Fac. Ciências, Campo Grande, 1749-016, Lisbon, Portugal

    M. Oliveira

Authors
  1. Margarida Rocheta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Cordeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Célia Miguel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margarida Rocheta.

Additional information

The PpRT1 nucleotide sequence has been deposited in NCBI database under accession number DQ394069.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rocheta, M., Cordeiro, J., Oliveira, M. et al. PpRT1: the first complete gypsy-like retrotransposon isolated in Pinus pinaster . Planta 225, 551–562 (2007). https://doi.org/10.1007/s00425-006-0370-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0370-5

Keywords

Search

Navigation