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PIGY, a new plant envelope-class LTR retrotransposon

Abstract

Plant LTR retrotransposons of the envelope class define a new branch in the Metaviridae family. They differ from other LTR retrotransposons mainly by the presence of an additional ORF downstream of the gag-pol region which has been hypothesized to be equivalent to the envelope gene of retroviruses. Here we present a newly identified element from pea (Pisum sativum), named PIGY, that has all the features characteristic of this group of LTR retrotransposons. In addition to the potential coding sequence downstream of the gag-pol region, PIGY has a primer binding site complementary to tRNAasp and a polypurine tract with a TGGGG motif and is of large size (13,645 bp). The relationship between PIGY and other retrotransposons of the env-class was confirmed by a phylogenetic analysis of their reverse transcriptase domains. One distinctive feature of PIGY is that its env-like region is actually composed of two similar ORFs, each of which encodes a protein with similarity to the Athila envelope-like protein. PIGY is present in the pea genome in 1–5×103 copies and is transcriptionally active, suggesting that some of these elements may still be capable of active transposition. Another new env-class retrotransposon similar to PIGY was also identified among genomic sequences of Medicago truncatula.

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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 25:3389–3402

  2. Arkhipova IR (2001) Transposable element in the animal kingdom. Mol Biol 35:157–167

  3. Baranyi M, Greilhuber J (1996) Flow cytometric and Feulgen analysis of genome size variation in Pisum. Theor Appl Genet 92:297–307

  4. Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 274:227–274

  5. Bhattacharya S, Bakre A, Bhattacharya A (2002) Mobile genetic elements in protozoan parasites. J Genet 81:73–86

  6. Boeke JD, Stoye JP (1997) Retrotransposons, endogenous retroviruses, and the evolution of retroelements. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 343–436

  7. Chavanne F, Zhang DX, Liaud MF, 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

  8. Deininger PL, Batzer MA (2002) Mammalian retroelements. Genome Res 12:1455–1465

  9. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1:19–21

  10. Gualberti G, Doležel J, Macas J, Lucretti S (1996) Preparation of pea (Pisum sativum L.) chromosome and nucleus suspensions from single root tips. Theor Appl Genet 92:744–751

  11. Havecker ER, Voytas DF (2003) The soybean retroelement SIRE1 uses stop-codon suppression to express its envelope-like protein. EMBO Rep 4:274–277

  12. Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouzé P, Brunak S (1996) Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res 24:3439–3452

  13. Hirochika H, Hirochika R (1993) Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn J Genet 68:35–46

  14. Hofmann K, Stoffel W (1993) TMBASE—a database of membrane spanning protein segments. Biol Chem Hoppe-Seyler 374:166

  15. Hull R (2001) Classifying reverse transcribing elements: a proposal and a challenge to the ICTV. Arch Virol 146:2255–2261

  16. Kim A, Terzian C, Santamaria P, Pélisson A, Prud’homme N, Bucheton A (1994) Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci USA 95:1285–1289

  17. Krogh A, Larrson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

  18. Kumekawa N, Ohtsubo E, Ohtsubo H (1999) Identification and phylogenetic analysis of gypsy-type retrotransposons in the plant kingdom. Genes Genet Syst 74:299–307

  19. Laten HM (1999) Phylogenetic evidence for Ty1-copia-like endogenous retroviruses in plant genomes. Genetica 107:87–93

  20. Laten HM, Majumdar A, Gaucher EA (1998) SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope like protein. Proc Natl Acad Sci USA 95:6897–6902

  21. Leitch AR, Schwarzacher T, Jackson D, Leitch IJ (1994) In situ hybridization. BIOS Scientific Publishers Ltd, Oxford

  22. Lerat E, Capy E (1999) Retrotransposons and retroviruses: analysis of the envelope gene. Mol Biol Evol 16:1198–1207

  23. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

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

  25. Malik HS, Eickbush TH (2001) Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11:1187–1197

  26. Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318

  27. Marchler-Bauer A et al (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387

  28. Neumann P, Nouzová M, Macas J (2001) Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L). Genome 44:716–728

  29. Neumann P, Požárková D, Macas J (2003) Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol 53:399–410

  30. Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448

  31. Peterson-Burch BD, Voytas DF (2002) Genes of the Pseudoviridae (Ty1/copia retrotransposons). Mol Biol Evol 19:1832–1845

  32. Peterson-Burch BD, Wright DA, Laten HM, Voytas DF (2000) Retroviruses in plants? Trends Genet 16:151–152

  33. Rabson AB, Graves BJ (1997) Synthesis, assembly, and processing of viral proteins. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 263–334

  34. Schmidt T (1999) LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol Biol 40:903–910

  35. Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG (1994) An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8:2046–2057

  36. Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10

  37. Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241

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

  39. Swanstrom R, Wills JW (1997) Synthesis, assembly, and processing of viral proteins. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 263–334

  40. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

  41. Vicient CM, Kalendar R, Schulman AH (2001) Envelope class retrovirus-like elements are widespread, transcribed and spliced, and insertionally polymorphic in plants. Genome Res 11:2041–2049

  42. Vogt VM (1997) Retroviral virions and genomes. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 27–70

  43. Wilhelm M, Wilhelm F-X (2001) Reverse transcription of retroviruses and LTR retrotransposons. Cell Mol Life Sci 58:1246–1262

  44. Wöstemeyer J, Kreibich A (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41:189–198

  45. Wright DA, Voytas DF (2001) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131

  46. Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

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Acknowledgements

We thank Ms. H. Štěpančíková for excellent technical assistance, Dr. M. Nouzová for help with DNA sequencing, and Ms. S. M. Rafelski for assistance in preparation of the manuscript. This work was supported by grants (Nos. 521/00/0655 and 521/02/P007) from the Grant Agency of the Czech Republic

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Correspondence to Pavel Neumann.

Additional information

Communicated by M.-A. Grandbastien

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Neumann, P., Požárková, D., Koblížková, A. et al. PIGY, a new plant envelope-class LTR retrotransposon. Mol Genet Genomics 273, 43–53 (2005). https://doi.org/10.1007/s00438-004-1092-7

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Keywords

  • LTR retrotransposon
  • Envelope
  • Pisum sativum
  • Medicago truncatula