Molecular Genetics and Genomics

, Volume 278, Issue 1, pp 1–15 | Cite as

Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum)

  • Maud Petit
  • K. Yoong Lim
  • Emilie Julio
  • Charles Poncet
  • François Dorlhac de Borne
  • Ales Kovarik
  • Andrew R. Leitch
  • Marie-Angèle Grandbastien
  • Corinne Mhiri
Original Paper

Abstract

LTR-retrotransposons contribute substantially to the structural diversity of plant genomes. Recent models of genome evolution suggest that retrotransposon amplification is offset by removal of retrotransposon sequences, leading to a turnover of retrotransposon populations. While bursts of amplification have been documented, it is not known whether removal of retrotransposon sequences occurs continuously, or is triggered by specific stimuli over short evolutionary periods. In this work, we have characterized the evolutionary dynamics of four populations of copia-type retrotransposons in allotetraploid tobacco (Nicotiana tabacum) and its two diploid progenitors Nicotiana sylvestris and Nicotiana tomentosiformis. We have used SSAP (Sequence-Specific Amplification Polymorphism) to evaluate the contribution retrotransposons have made to the diversity of tobacco and its diploid progenitor species, to quantify the contribution each diploid progenitor has made to tobacco's retrotransposon populations, and to estimate losses or amplifications of retrotransposon sequences subsequent to tobacco's formation. Our results show that the tobacco genome derives from a turnover of retrotransposon sequences with removals concomitant with new insertions. We have detected unique behaviour specific to each retrotransposon population, with differences likely reflecting distinct evolutionary histories and activities of particular elements. Our results indicate that the retrotransposon content of a given plant species is strongly influenced by the host evolutionary history, with periods of rapid turnover of retrotransposon sequences stimulated by allopolyploidy.

Keywords

Allopolyploidy Retrotransposon Genome evolution Nicotiana tabacum Nicotiana tomentosiformis Nicotiana sylvestris 

References

  1. Adams KL, Wendel JF (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21:539–543PubMedCrossRefGoogle Scholar
  2. Alix K, Ryder CD, Moore J, King GJ, Pat Heslop-Harrison JS (2005) The genomic organization of retrotransposons in Brassica oleracea. Plant Mol Biol 59:839–851PubMedCrossRefGoogle Scholar
  3. Araujo PG, Casacuberta JM, Costa APP, Hashimoto RY, Grandbastien M-A, Van Sluys M-A (2001) Retrolyc1 subfamilies defined by different U3 regulatory regions in the Lycopersicon genus. Mol Gen Genom 266:35–41CrossRefGoogle Scholar
  4. Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132PubMedCrossRefGoogle Scholar
  5. Casacuberta JM, Vernhettes S, Audeon C, Grandbastien M-A (1997) Quasispecies in retrotransposons: a role for sequence variability in Tnt1 evolution. Genetica 100:109–117PubMedCrossRefGoogle Scholar
  6. Chantret N, Salse J, Sabot F, Rahman S, Bellec A, Laubin B, Dubois I, Dossat C, Sourdille P, Joudrier P, Gautier MF, Cattolico L, Beckert M, Aubourg S, Weissenbach J, Caboche M, Bernard M, Leroy P, Chalhoub B (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045PubMedCrossRefGoogle Scholar
  7. Chen ZJ, Ni Z (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28:240–252PubMedCrossRefGoogle Scholar
  8. Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Mol Phylogenet Evol 33:75–90PubMedCrossRefGoogle Scholar
  9. Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252PubMedCrossRefGoogle Scholar
  10. Comai L (2000) Genetic and epigenetic interactions in allopolyploid plants. Plant Mol Biol 43:387–399PubMedCrossRefGoogle Scholar
  11. Costa PP, Scortecci KC, Hashimoto RY, Araujo PG, Grandbastien M-A, Van Sluys M-A (1999) Retrolyc1-1, a member of the Tnt1 retrotransposon super-family in the Lycopersicon peruvianum genome. Genetica 107:65–72CrossRefGoogle Scholar
  12. Dellaporta SL, Wood L, Hicks J (1983) Molecular biology of plants: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  13. Delon R, Poisson C, Bardon J-C, Taillurat P (1999) Les Nicotianées en collection à l’Institut du Tabac, 3ème Edition, Annales du TabacGoogle Scholar
  14. Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079PubMedCrossRefGoogle Scholar
  15. Ellis THN, Poyser SJ, Knox MR, Vershinin AV, Ambrose MJ (1998) Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity in pea. Mol Gen Genet 260:9–19PubMedGoogle Scholar
  16. Goodspeed TH (1954) The genus Nicotiana. Chronica Botanica Company, MAGoogle Scholar
  17. Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–187CrossRefGoogle Scholar
  18. Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated via plant cell genetics. Nature 337:376–380PubMedCrossRefGoogle Scholar
  19. Grandbastien M-A, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa APP, Le QH, Melayah D, Petit M, Poncet C, Tam SM, Van Sluys M-A, Mhiri C (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res, Special Issue on “Retrotransposable Elements and Genome Evolution” 110:229–241Google Scholar
  20. Gregor W, Mette MF, Staginnus C, Matzke MA, Matzke AJM (2004) A distinct endogenous pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol 134:1191–1199PubMedCrossRefGoogle Scholar
  21. Han FP, Fedak G, Ouellet T, Liu B (2003) Rapid genomic changes in interspecific and intergeneric hybrids and allopolyploids of Triticeae. Genome 46:716–723PubMedCrossRefGoogle Scholar
  22. Hanson RE, Zhao XP, Islam-Faridi MN, Paterson AH, Zwick MS, Crane CF, McKnight TD, Stelly DM, Price HJ (1998) Evolution of interspersed repetitive elements in Gossypium (Malvaceae). Am J Bot 85:1364–1368CrossRefGoogle Scholar
  23. Hasegawa K, Yukawa Y, Sugita M, Sugiura M (2002) Organization and transcription of the gene family encoding chlorophyll a/b-binding proteins in Nicotiana sylvestris. Gene 289:161–168PubMedCrossRefGoogle Scholar
  24. Heslop-Harrison JS, Brandes A, Taketa S, Schmidt T, Vershinin AV, Alkhimova EG, Kamm A, Doudrick RL, Schwarzacher T, Katsiotis A, Kubis S, Kumar A, Pearce SR, Flavell AJ, Harrison GE (1997) The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100:97–204CrossRefGoogle Scholar
  25. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 6:2521–2528Google Scholar
  26. Julio E, Verrier JL, Dorlhac de Borne F (2006) Development of SCAR markers linked to three disease resistances based on AFLP within Nicotiana tabacum L. Theor Appl Genet 2:335–346Google Scholar
  27. Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci USA 97:6603–6607PubMedCrossRefGoogle Scholar
  28. Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659PubMedGoogle Scholar
  29. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106PubMedCrossRefGoogle Scholar
  30. Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73–82CrossRefGoogle Scholar
  31. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532PubMedCrossRefGoogle Scholar
  32. Leitch AR, Lim KY, Webb DR, McFadden GI (2001) In situ hybridisation. In: Hawes C, Satiat-Jeunemaitre B (eds) Plant cell biology, a practical approach. Oxford University Press, OxfordGoogle Scholar
  33. Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663. Reports of the international polyploidy conference, 27–30 April 2003, London, UKGoogle Scholar
  34. Leprince A-S, Grandbastien M-A, Meyer C (2001) Retrotransposons of the Tnt1B family are mobile in Nicotiana plumbaginifolia and can induce alternative splicing of the host gene upon insertion. Plant Mol Biol 47:533–541CrossRefGoogle Scholar
  35. Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR (2000a) Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109:161–172CrossRefGoogle Scholar
  36. Lim KY, Matyasek R, Lichtenstein CP, Leitch AR (2000b) Molecular cytogenetic analyses and phylogeny of the Nicotiana section Tomentosae. Chromosoma 109:245–258CrossRefGoogle Scholar
  37. Lim KY, Matyasek M, Kovarik A, Leitch AR (2004a) Genome evolution in allotetraploid Nicotiana. Biol J Linn Soc 82: 599–606. Reports of the international polyploidy conference, 27–30 April 2003, London, UKGoogle Scholar
  38. Lim KY, Skalicka K, Koukalova B, Volkov RA, Matyasek R, Hemleben V, Leitch AR, Kovarik A. (2004b) Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana. Genetics 166:1935–1946CrossRefGoogle Scholar
  39. Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43:874–880PubMedCrossRefGoogle Scholar
  40. Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29:365–379PubMedCrossRefGoogle Scholar
  41. Liu ZL, Wang YM, Shen Y, Guo W, Hao S, Liu B (2004) Extensive alterations in DNA methylation and transcription in rice caused by introgression from Zizania latifolia. Plant Mol Biol 54:571–582PubMedCrossRefGoogle Scholar
  42. Lönnig W-E, Saedler H (2002) Chromosome rearrangements and transposable elements. Annu Rev Genet 36:389–410PubMedCrossRefGoogle Scholar
  43. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869PubMedCrossRefGoogle Scholar
  44. Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230PubMedCrossRefGoogle Scholar
  45. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801PubMedCrossRefGoogle Scholar
  46. Melayah D, Bonnivard E, Chalhoub B, Audéon C, Grandbastien M-A (2001) The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors. Plant J 28:159–168PubMedCrossRefGoogle Scholar
  47. Melayah D, Lim KY, Bonnivard E, Chalhoub B, Dorlhac de Borne F, Mhiri C, Leitch AR, Grandbastien M-A (2004) Distribution of the Tnt1 retrotransposon family in the amphidiploid tobacco (Nicotiana tabacum) and its wild Nicotiana relatives. Biol J Linn Soc 82:639–649. Reports of the international polyploidy conference, 27–30 April 2003, London, UKGoogle Scholar
  48. Murad L, Bielawski JP, Matyasek R, Kovarik A, Nichols RA, Leitch AR, Lichtenstein CP (2004) The origin and evolution of geminivirus-related DNA sequences in Nicotiana. Heredity 92:352–8PubMedCrossRefGoogle Scholar
  49. Murad L, Lim KY, Christopodulou V, Matyasek R, Lichtenstein CP, Kovarik A, Leitch AR (2002) The origin of tobacco’s T genome is traced to a particular lineage within Nicotiana tomentosiformis (Solanaceae). Am J Bot 89:921–928Google Scholar
  50. Okamoto H, Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6:527–534PubMedCrossRefGoogle Scholar
  51. O’Neill RJ, O’Neill MJ, Marshall Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393:68–72PubMedCrossRefGoogle Scholar
  52. 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 6:711–717CrossRefGoogle Scholar
  53. Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5:R79PubMedCrossRefGoogle Scholar
  54. Peterson-Burch BD, Nettleton D, Voytas DF (2004) Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biol 5:R78PubMedCrossRefGoogle Scholar
  55. Ramsay J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639CrossRefGoogle Scholar
  56. Ren N, Timko MP (2001) AFLP analysis of genetic polymorphism and evolutionary relationships among cultivated and wild Nicotiana species. Genome 4:559–571CrossRefGoogle Scholar
  57. Shan XH, Liu ZL, Dong ZY, Wang YM, Chen Y, Lin XY, Long LK, Han FP, Dong YS, Liu B (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22:976–990PubMedCrossRefGoogle Scholar
  58. Shirasu K, Schulman AS, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915PubMedCrossRefGoogle Scholar
  59. Skalicka K, Lim KY, Matyasek R, Koukalova B, Leitch AR, Kovarik A (2003) Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. Am J Bot 90:988–996Google Scholar
  60. Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A (2005) Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166:291–303Google Scholar
  61. Sneath PH, Sokal RR (1973) Numerical taxonomy. In: Freeman WH (ed) The principles and practice of numerical classification, San Francisco, USAGoogle Scholar
  62. Swofford DL (2002) PAUP* 4.0 beta 10. Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, SunderlandGoogle Scholar
  63. Tam SM, Mhiri C, Vogelaar A, Kerkveld M, Pearce S, Grandbastien M-A (2005) Comparative analyses of genetic diversities within tomato and pepper collections detected by retrotransposon-based SSAP, AFLP and SSR. Theor Appl Genet 110:819–831PubMedCrossRefGoogle Scholar
  64. Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein NM, Bennetzen JL, Avramova Z (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414PubMedCrossRefGoogle Scholar
  65. Vernhettes S, Grandbastien M-A, Casacuberta JM (1998) The evolutionary analysis of the Tnt1 retrotransposon in Nicotiana species reveals the high plasticity of its regulatory sequences. Mol Biol Evol 15:827–836PubMedGoogle Scholar
  66. Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20:528–540PubMedCrossRefGoogle Scholar
  67. Vitte C, Panaud O (2005) LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res 110:91–107PubMedCrossRefGoogle Scholar
  68. Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16:311–320PubMedGoogle Scholar
  69. Vos P, Hogers R, Bleeker M, Reijans M, van der 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 23:4407–4414PubMedCrossRefGoogle Scholar
  70. Wang YM, Dong ZY, Zhang ZJ, Lin XY, Shen Y, Zhou D, Liu B (2005) Extensive de novo genomic variation in rice induced by introgression from wild rice (Zizania latifolia Griseb.). Genetics 170:1945–1956PubMedCrossRefGoogle Scholar
  71. Waugh R, Mclean K, Flavell AJ, Pearce SR, Kumar A, Thomas BBT, Powell W (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence specific amplification polymorphisms (SSAP). Mol Gen Genet 253:687–694PubMedCrossRefGoogle Scholar
  72. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249PubMedCrossRefGoogle Scholar
  73. Yukawa M, Tsudzuki T, Sugiura M (2006) The chloroplast genome of Nicotiana sylvestris and Nicotiana tomentosiformis: complete sequencing confirms that the Nicotiana sylvestris progenitor is the maternal genome donor of Nicotiana tabacum. Mol Gen Genomics 275:367–373CrossRefGoogle Scholar
  74. Zhao XP, Si Y, Hanson RE, Crane CF, Price HJ, Stelly DM, Wendel JF, Paterson AH (1998) Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Res 8:479–492PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Maud Petit
    • 1
  • K. Yoong Lim
    • 3
  • Emilie Julio
    • 4
  • Charles Poncet
    • 1
    • 2
  • François Dorlhac de Borne
    • 4
  • Ales Kovarik
    • 5
  • Andrew R. Leitch
    • 3
  • Marie-Angèle Grandbastien
    • 1
  • Corinne Mhiri
    • 1
  1. 1.Laboratoire de Biologie Cellulaire, UR501Institut Jean-Pierre Bourgin, INRAVersailles cedexFrance
  2. 2.INRA UMR Diversité et Génomes des Plantes CultivéesMontpellier cedex 1France
  3. 3.School of Biological and Chemical Sciences, Queen MaryUniversity of LondonLondonUK
  4. 4.Institut du TabacBergeracFrance
  5. 5.Institute of BiophysicsBrnoCzech Republic

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