Skip to main content
Log in

Novel Transposable Elements in Solanaceae: Evolutionary Relationships among Tnt1-related Sequences in Wild Petunia Species

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Transposable elements (TEs) are widespread in eukaryotic genomes. The diversity and abundance of TEs are highly variable among species and may correspond to particular relationships between a species and the elements in its genome. There are often many TE families within a single genome; thus, the amplification of one TE family may influence the amplification of other families. LTR retrotransposons (LTR-RTs) are extremely abundant in flowering plants, and Tnt1 is one of the most well known. First characterized in tobacco, Tnt1-related sequences have since been reported in other genera of Solanaceae. In this study, we investigated the profile of Tnt1-related sequences among the species of three Solanaceae genera through genomic amplification and the cloning of partial sequences. The analysis of these sequences revealed high levels of diversity and showed that the sequences are not as closely related to Tnt1 as had been previously hypothesized. The classification of the sequences yielded ten possible families of LTR-RTs, which are, in addition to Tnt1, all members of the Tork clade within the Copia superfamily. However, the sequences did not follow the phylogeny of the species and were not homogeneously distributed. One family includes only sequences of taxa that inhabit dry areas. These findings were consistent with previous suggestions of an early association of Tnt1-related elements with the evolution of several Solanaceae species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Araújo PG, Casacuberta JM, Costa AP, Hashimoto RY, Grandbastien MA, Van Sluys MA (2001) Retrolyc1 subfamilies defined by different U3 LTR regulatory regions in the Lycopersicon genus. Mol Genet Genomics 266:35–41

    Article  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Beguiristain T, Grandbastien MA, Puigdomenech P, Casacuberta JM (2001) Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol 127:212–221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr. Opin Genet Dev 15:621–627

    Article  CAS  Google Scholar 

  • Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434

    Article  CAS  PubMed  Google Scholar 

  • Casacuberta JM, Grandbastien MA (1993) Characterization of LTR sequences involved in the protoplast specific expression of the tobacco Tnt1 retrotransposon. Nucleic Acid Res 21:2087–2093

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chen S, Matsubara K, Kokubun H, Kodama H, Watanabe H, Marchesi E, Ando T (2007) Phylogenetic analysis of the genus Petunia (Solanaceae) based on the sequence of the Hf1 gene. J Plant Res 120:385–397

    Article  CAS  PubMed  Google Scholar 

  • Cordaux R, Hedges DJ, Batzer MA (2004) Retrotransposition of Alu elements: how many sources? Trends Genet 20:464–467

    Article  CAS  PubMed  Google Scholar 

  • Costa APP, Scortecci KC, Hashimoto RY, Araujo PG, Grandbastien MA, Van Sluys MA (1999) Retrolyc1-1, a member of the Tnt1 l retrotransposon super-family in the Lycopersicon peruvianum genome. Genetica 107:65–72

    Article  CAS  Google Scholar 

  • Dunn IS, Blattner FR (1987) Sharons 36 to 40: multi-enzyme, high capacity, recombination deficient replacement vectors with polylinkers and polystuffers. Nucleic Acids Res 15:2677–2698

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gerats T, Vandenbusshe M (2005) A model system for comparative research: Petunia. Trends Plant Sci 10:251–256

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Grandbastien MA, Lucas H, Morel J-B, Mhiri C, Vernhettes S, Casacuberta JM (1997) The expression of tobacco Tnt1 retrotransposon is linked to plant defense responses. Genetica 100:241–252

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Pinzón I, Jesús E, Santiago N, Casacuberta JM (2009) The frequent transcriptional read-through of the tobacco Tnt1 retrotransposon and its possible implications for the control of resistance genes. J Mol Evol 6:269–278

    Article  Google Scholar 

  • Hirochika H (1993) Activation of tobacco retrotransposon during tissue culture. EMBO J 12:2521–2528

    CAS  PubMed  Google Scholar 

  • Hua-Van A, Le Rouzic A, Boutin T, Filée J, Capy P (2011) The struggle for life of the genome’s selfish architects. Biol Direct 6:19–48

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 diversity. Proc Natl Acad Sci USA 97:6603–6607

    Article  CAS  PubMed  Google Scholar 

  • Kalendar R, Flavell AJ, Ellis TH, Sjakste T, Moisy C, Schulman AH (2011) Analysis of plant diversity with retrotransposon-based molecular markers. Heredity 106:520–530

    Article  CAS  PubMed  Google Scholar 

  • Kalmykova AI, Gvozdev VA (2004) Selective expansion of the newly evolved genomic variants of retrotransposon 1731 in the Drosophila genomes. Mol Biol Evol 21:2281–2289

    Article  CAS  PubMed  Google Scholar 

  • Kawakami T, Strakosh SC, Zhen Y, Ungerer MC (2010) Different scales of Ty1/Copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species. Heredity 104:341–350

    Article  CAS  PubMed  Google Scholar 

  • Kulcheski FR, Muschner VC, Lorenz-Lemke AP, Stehmann JR, Bonatto SL, Salzano FM, Freitas LB (2006) Molecular phylogenetic analysis of Petunia Juss. (Solanaceae). Genetica 126:3–14

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolle M, Fuster G, Bernet GP, Maumus F, Munoz-Pomer A, Sempere JM, Latorre A, Moya A (2011) The Gypsy Database (GyDB) of mobile genetic elements, Release 2.0. Nucleic Acids Res 39(Database issue):D70–D74

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lorenz-Lemke AP, Mäder G, Muschner VC, Stehmann JR, Bonatto SL, Salzano FM, Freitas LB (2006) Diversity and natural hybridization in a highly endemic species of Petunia (Solanaceae), A molecular and ecological analysis. Mol Ecol 15:4487–4497

    Article  CAS  PubMed  Google Scholar 

  • Manetti ME, Rossi M, Costa APP, Clausen AM, Van Sluys MA (2007) Radiation of the Tnt1 retrotransposon superfamily in three Solanaceae genera. BMC Evol Biol 7:34–46

    Article  PubMed Central  PubMed  Google Scholar 

  • Mao L, Wood TC, Yu Y, Budiman MA, Tomkins J, Woo SS, Sasinowski M, Presting G, Frisch D, Goff S, Dean RA, Wing RA (2000) Rice transposable elements: a survey of 73,000 sequence-tagged-connectors. Genome Res 10:982–990

    Article  CAS  PubMed  Google Scholar 

  • Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Roy A, Frascaria N, MacKay J, Bousquet J (1992) Segregating random amplified polymorphic DNAs (RAPDs) in Betula alleghaniensisis. Theor Appl Genet 85:173–180

    CAS  PubMed  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Stehmann JR, Lorenz-Lemke AP, Freitas LB, Semir J (2009) The genus Petunia. In: Gerats T, Strommer J (eds) Petunia evolutionary, developmental and physiological genetics. Springer, New York, pp 1–28

    Google Scholar 

  • Tam SM, Lefebvre V, Palloix A, Sage-Palloix AM, Mhiri C, Grandbastien MA (2009) LTR-retrotransposons Tnt1 and T135 markers reveal genetic diversity and evolutionary relationships of domesticated peppers. Theor Appl Genet 119:973–989

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5, Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Tenaillon M, Hollister JD, Gaut BS (2010) A triptych of the evolution of plant transposable elements. Trends Plant Sci 15:471–478

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsukamoto T, Ando T, Kokubun H, Watanabe H, Tanaka R, Hashimoto G, Marchesi E, Kao T-H (1998) Differentiation in the status of self-incompatibility among all natural taxa of Petunia (Solanaceae). Acta Phytotaxon Geobot 49:115–133

    Google Scholar 

  • Vernhettes S, Grandbastien MA, Casacuberta JM (1997) In vivo characterization of transcriptional regulatory sequences involved in the defense-associated expression of the tobacco retrotransposon Tnt1. Plant Mol Biol 35:673–679

    Article  CAS  PubMed  Google Scholar 

  • Vernhettes S, Grandbastien MA, Casacuberta JM (1998) The evolutionary analysis of the Tnt1 retrotransposon in Nicotiana species reveals the high variability of its regulatory sequences. Mol Biol Evol 15:827–836

    Article  CAS  PubMed  Google Scholar 

  • Vicient CM, Kalendar R, Schulman AH (2005) Variability, recombination, and mosaic evolution of the barley BARE-1 retrotransposon. J Mol Evol 61:275–291

    Article  CAS  PubMed  Google Scholar 

  • Wei F, Stein JC, Liang C, Zhang J, Fulton RS et al (2009) Detailed analysis of a contiguous 22-Mb region of the maize genome. PLoS Genet 5:e1000728

    Article  PubMed Central  PubMed  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm M, Wilhelm FX (2001) Reverse transcription of retroviruses and LTR retrotransposons. Cell Mol Life Sci 58:1246–1262

    Article  CAS  PubMed  Google Scholar 

  • Zedek F, Smerda J, Smarda P, Bures P (2010) Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biol 10:265–275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Associate Editor and three anonymous reviewers for their comments and suggestions, which have improved this manuscript. This project was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) and the Programa de Pós-Graduação em Genética e Biologia Molecular da Universidade Federal do Rio Grande do Sul (PPGBM-UFRGS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Loreta B. Freitas.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kriedt, R.A., Cruz, G.M.Q., Bonatto, S.L. et al. Novel Transposable Elements in Solanaceae: Evolutionary Relationships among Tnt1-related Sequences in Wild Petunia Species. Plant Mol Biol Rep 32, 142–152 (2014). https://doi.org/10.1007/s11105-013-0626-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-013-0626-8

Keywords

Navigation