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Distribution dynamics of the Tnt1 retrotransposon in tobacco

Abstract

Retrotransposons contribute significantly to the size, organization and genetic diversity of plant genomes. Although many retrotransposon families have been reported in plants, to this day, the tobacco Tnt1 retrotransposon remains one of the few elements for which active transposition has been shown. Demonstration that Tnt1 activation can be induced by stress has lent support to the hypothesis that, under adverse conditions, transposition can be an important source of genetic variability. Here, we compared the insertion site preference of a collection of newly transposed and pre-existing Tnt1 copies identified in plants regenerated from protoplasts or tissue culture. We find that newly transposed Tnt1 copies are targeted within or close to host gene coding sequences and that the distribution of pre-existing insertions does not vary significantly from this trend. Therefore, in spite of their potential to disrupt neighboring genes, insertions within or near CDS are not preferentially removed with age. Elimination of Tnt1 insertions within or near coding sequences may be relaxed due to the polyploid nature of the tobacco genome. Tnt1 insertions within or near CDS are thus better tolerated and can putatively contribute to the diversification of tobacco gene function.

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

  3. Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7:732–736

  4. Casacuberta JM, Grandbastien M-A (1993) Characterisation of LTR sequences involved in the protoplast specific expression of the tobacco Tnt1 retrotransposon. Nucleic Acids Res 21:2087–2093

  5. Casacuberta JM, Vernhettes S, Grandbastien M-A (1995) Sequence variability within the tobacco retrotransposon Tnt1 population. EMBO J 14:2670–2678

  6. Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311:1–11

  7. Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allotetraploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252

  8. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA mini-preparation: version II. Plant Mol Biol Rep 1:19–21

  9. Delon R, Poisson C, Bardon J-C, Taillurat P (1999) Les Nicotianées en collection à l’Institut du Tabac, 3ème Edition, Annales du Tabac

  10. Gao L, McCarthy EM, Ganko EW, McDonald JF (2004) Evolutionary history of Oryza sativa LTR retrotransposons: a preliminary survey of the rice genome sequences. BMC Genomics 5:18

  11. Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

  12. Grandbastien M-A, Audéon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa A-PP, Le QH, Melayah D, Petit M, Poncet C, Tam S-M, Van Sluys M-A, Mhiri C (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res 110:229–241

  13. Kashkush K, Feldman M, Levy A (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33: 102–106

  14. Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution Int J Org Evolution 55:1–24

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

  16. Medstrand P, van de Lagemaat LN, Mager DL (2002) Retroelement distribution in the human genome: variations associated with age and proximity to genes. Genome Res 12:1483–1495

  17. Melayah D, Bonnivard E, Chalhoub B, Audeon C, Grandbastien M-A (2001) The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors. Plant J 28:159–168

  18. Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

  19. Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780

  20. Okamuro JK, Goldberg RB (1985) Tobacco single-copy DNA is highly homologous to sequences present in the genomes of its diploid progenitors. Mol Gen Genet 198:290–298

  21. Pouteau S, Huttner E, Grandbastien M-A, Caboche M (1991) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J 10:1911–1918

  22. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

  23. Schröder ARW, Shinn P, Chen H, Berry C, Ecker JR, Bushman F (2002) HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110:521–529

  24. The Arabidopsis Genome Initiative (2002) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

  25. Vitte C, Bennetzen JL (2006) Eukaryotic transposable elements and genome evolution special feature: analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643

  26. Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253:687–694

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Acknowledgments

We thank Dr. C. Mhiri and Dr. S.-M. Tam for critical comments on our manuscript, and Dr A. Leitch for kindly providing us with N. tomentosiformis (NIC 479/84) and N. sylvestris (TW137) accessions. This work was funded by an EEC BIOTECH program BIO4-CT96-0508 (TEBIODIV) and a Fonds Nature et Technologies du Québec fellowship to Q. H. L.

Author information

Correspondence to Marie-Angèle Grandbastien.

Additional information

Communicated by R. Hagemann.

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Le, Q.H., Melayah, D., Bonnivard, E. et al. Distribution dynamics of the Tnt1 retrotransposon in tobacco. Mol Genet Genomics 278, 639–651 (2007). https://doi.org/10.1007/s00438-007-0281-6

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Keywords

  • LTR-retrotransposon
  • Nicotiana tabacum
  • Target site
  • Stress
  • Evolution