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The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years

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Combining several different approaches, we have examined the structure, variability, and distribution of Tvv1 retrotransposons. Tvv1 is an unusual example of a low-copy retrotransposon metapopulation dispersed unevenly among very distant species and is promising for the development of molecular markers.

Abstract

Retrotransposons are ubiquitous throughout the genomes of the vascular plants, but individual retrotransposon families tend to be confined to the level of plant genus or at most family. This restricts the general applicability of a family as molecular markers. Here, we characterize a new plant retrotransposon named Tvv1_Sdem, a member of the Copia superfamily of LTR retrotransposons, from the genome of the wild potato Solanum demissum. Comparative analyses based on structure and sequence showed a high level of similarity of Tvv1_Sdem with Tvv1-VB, a retrotransposon previously described in the grapevine genome Vitis vinifera. Extending the analysis to other species by in silico and in vitro approaches revealed the presence of Tvv1 family members in potato, tomato, and poplar genomes, and led to the identification of full-length copies of Tvv1 in these species. We were also able to identify polymorphism in UTL sequences between Tvv1_Sdem copies from wild and cultivated potatoes that are useful as molecular markers. Combining different approaches, our results suggest that the Tvv1 family of retrotransposons has a monophyletic origin and has been maintained in both the rosids and the asterids, the major clades of dicotyledonous plants, since their divergence about 100 MYA. To our knowledge, Tvv1 represents an unusual plant retrotransposon metapopulation comprising highly similar members disjointedly dispersed among very distant species. The twin features of Tvv1 presence in evolutionarily distant genomes and the diversity of its UTL region in each species make it useful as a source of robust molecular markers for diversity studies and breeding.

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References

  • Abram M, Ferris A, Shao W, Alvord W, Hughes S (2010) Nature, position, and frequency of mutations made in a single cycle of HIV-1 replication. J Virol 84:9864–9878

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Baucom RS, Estill JC, Leebens-Mack J, Bennetzen JL (2009) Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Res 19:243–254

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boutabout M, Wilhelm M, Wilhelm FX (2001) DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Ty1. Nucleic Acids Res 29:2217–2222

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bowen NJ, Mcdonald JF (1999) Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. Genome Res 9:924–935

    Article  PubMed  CAS  Google Scholar 

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

    PubMed Central  PubMed  CAS  Google Scholar 

  • Cenci A, Combes M-C, Lashermes P (2010) Comparative sequence analyses indicate that Coffea (Asterids) and Vitis (Rosids) derive from the same paleo-hexaploid ancestral genome. Mol Gen Genet 283:493–501

    Article  CAS  Google Scholar 

  • The Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Google Scholar 

  • Cheng X, Zhang D, Cheng Z, Keller B, Ling H-Q (2009) A new family of Ty1-copia-Like retrotransposons originated in the tomato genome by a recent horizontal transfer event. Genetics 181:1183–1193

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dixit A, Ma K-H, Yu J-W, Cho E-G, Park Y-J (2006) Reverse transcriptase domain sequences from Mungbean (Vigna radiata) LTR retrotransposons: sequence characterization and phylogenetic analysis. Plant Cell Rep 25:100–111

    Article  PubMed  CAS  Google Scholar 

  • Domingo E (2002) Quasispecies theory in virology. J Virol 76:463–465

    Article  PubMed Central  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113. doi:10.1186/1471-2105-5-113

    Article  CAS  Google Scholar 

  • Eickbush TH, Jamburuthugoda VK (2008) The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res 134:221–234

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fortune PM, Roulin A, Panaud O (2008) Horizontal transfer of transposable elements in plants. Commun Integr Biol 1:74–77

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gabriel A, Willems M, Mules EH, Boeke JD (1996) Replication infidelity during a single cycle of Ty1 retrotransposition. Proc Natl Acad Sci USA 93:7767–7771

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gómez E, Schulman AH, Martínez-Izquierdo JA, Vicient CM (2006) Integrase diversity and transcription of the maize retrotransposon Grande. Genome 49:558–562

    Article  PubMed  CAS  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Jansen RK, Kaittanis C, Saski C, Lee S-B, Tomkins J, Alverson AJ, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32

    Article  PubMed Central  PubMed  CAS  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 divergence. Proc Natl Acad Sci USA 97:6603–6607

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH (2008) Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci USA 105:5833–5838

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalendar R, Lee D, Schulman AH (2011) Java web tools for PCR, in silico PCR, and oligonucleotide assembly and analysis. Genomics 98:137–144

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9:411–412

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Le Rouzic A, Boutin TS, Capy P (2007) Long-term evolution of transposable elements. Proc Natl Acad Sci USA 104:19375–19380

    Article  PubMed Central  PubMed  Google Scholar 

  • Llorens C, Muñoz-Pomer A, Bernad L, Botella H, Moya A (2009) Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Biol Direct 4:41

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lohe AR, Moriyama EN, Lidholm DA, Hartl DL (1995) Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol Biol Evol 12:62–72

    Article  PubMed  CAS  Google Scholar 

  • Macas J, Koblízková A, Navrátilová A, Neumann P (2009) Hypervariable 3′ UTR region of plant LTR-retrotransposons as a source of novel satellite repeats. Gene 448:198–206

    Article  PubMed  CAS  Google Scholar 

  • Manetti ME, Rossi M, Nakabashi M, Grandbastien MA, Van Sluys MA (2009) The Tnt1 family member Retrosol copy number and structure disclose retrotransposon diversification in different Solanum species. Mol Gen Genet 281:261–271

    Article  CAS  Google Scholar 

  • Moisy C, Blanc S, Merdinoglu D, Pelsy F (2008a) Structural variability of Tvv1 grapevine retrotransposons can be caused by illegitimate recombination. Theor Appl Genet 116:671–682

    Article  PubMed  CAS  Google Scholar 

  • Moisy C, Garrison KE, Meredith CP, Pelsy F (2008b) Characterization of ten novel Ty1/copia-like retrotransposon families of the grapevine. BMC Genomics 9:1–14

    Article  CAS  Google Scholar 

  • Nielen S, Campos-Fonseca F, Leal-Bertioli S, Guimarães P, Seijo G, Town C, Arrial R et al (2010) FIDEL-a retrovirus-like retrotransposon and its distinct evolutionary histories in the A- and B-genome components of cultivated peanut. Chromosome Res 18(2):227–246

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ojosnegros S, Perales C, Mas A, Domingo E (2011) Quasispecies as a matter of fact: viruses and beyond. Virus Res 162(1–2):203–215

    Article  PubMed  CAS  Google Scholar 

  • Otto TD, Gomes LH, Alves-Ferreira M, De Miranda AB, Degrave WM (2008) ReRep: computational detection of repetitive sequences in genome survey sequences (GSS). BMC Bioinforma 9:366

    Article  CAS  Google Scholar 

  • Pelsy F (2007) Untranslated leader region polymorphism of Tvv1, a retrotransposon family, is a novel marker useful for analyzing genetic diversity and relatedness in the genus Vitis. Theor Appl Genet 116:15–27

    Article  PubMed  CAS  Google Scholar 

  • Pelsy F, Merdinoglu D (2002) Complete sequence of Tvv1, a family of Ty 1 copia-like retrotransposons of Vitis vinifera L., reconstituted by chromosome walking. Theor Appl Genet 105:614–621

    Article  PubMed  CAS  Google Scholar 

  • Preston BD (1996) Error-prone retrotransposition: rime of the ancient mutators. Proc Natl Acad Sci USA 93:7427–7431

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Piegu B, Wing R, Panaud O (2008) Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza. Plant J 53:950–959

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Piegu B, Fortune PM, Sabot F, D’Hont A, Manicacci D, Panaud O (2009) Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae. BMC Evol Biol 9:58

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Sabot F, Schulman AH (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity 97:381–388

    Article  PubMed  CAS  Google Scholar 

  • Sabot F, Schulman AH (2007) Template switching can create complex LTR retrotransposon insertions in Triticeae genomes. BMC Genomics 8:247

    Article  PubMed Central  PubMed  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 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Schulman AH (2013) Retrotransposon replication in plants. Curr Opin Virol 3(6):604–614

    Google Scholar 

  • Schulman AH, Wicker T (2013) A field guide to transposable elements. In: Fedoroff NV (ed) Plant transposons and genome dynamics in evolution. Wiley, Hoboken, pp 15–40

    Chapter  Google Scholar 

  • Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smith RA, Anderson DJ, Preston BD (2004) Purifying selection masks the mutational flexibility of HIV-1 reverse transcriptase. J Biol Chem 279:26726–26734

    Article  PubMed  CAS  Google Scholar 

  • Stuart-Rogers C, Flavell AJ (2001) The evolution of Ty1-copia group retrotransposons in gymnosperms. Mol Biol Evol 18:155–163

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Tanskanen J, Pentikäinen O, Johnson MS, Schulman AH (1998) The core domain of retrotransposon integrase in Hordeum: predicted structure and evolution. Mol Biol Evol 15:1135–1144

    Article  PubMed  CAS  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(10):2731–2739

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tanskanen J, Sabot F, Vicient CM, Schulman AH (2007) Life without GAG: the BARE-2 retrotransposon as a parasite’s parasite. Gene 390:166–174

    Article  PubMed  CAS  Google Scholar 

  • Vershinin AV, Ellis TH (1999) Heterogeneity of the internal structure of PDR1, a family of Ty1/copia-like retrotransposons in pea. Mol Gen Genet 262:703–713

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Vitte C, Chaparro C, Quesneville H, Panaud O (2007a) Spip and Squiq, two novel rice non-autonomous LTR retro-element families related to RIRE3 and RIRE8. Plant Sci 172:8–19

    Article  CAS  Google Scholar 

  • Vitte C, Panaud O, Quesneville H (2007b) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8:218

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106:3853–3858

    Article  PubMed Central  PubMed  Google Scholar 

  • Wawrzynski A, Ashfield T, Chen NWG, Mammadov J, Nguyen A, Podicheti R, Cannon SB, Thareau V, Ameline-Torregrosa C, Cannon E et al (2008) Replication of nonautonomous retroelements in soybean appears to be both recent and common. Plant Physiol 148:1760–1771

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wicker T, Keller B (2007) Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17(7):1072–1081

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wicker T, Schlagenhauf E, Graner A, Close TJ, Keller B, Stein N (2006) 454 sequencing put to the test using the complex genome of barley. BMC Genomics 7:275

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Taudien S, Houben A, Keller B, Graner A, Platzer M, Stein N (2009) A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. Plant J 59:712–722

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13778

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by funding from Région Alsace, INRA, and the Academy of Finland (Project 123074). We thank Emilie Haegy and Romain Guyot (IRD, Montpellier) for technical assistance, and the members of the experimental unit of INRA-Colmar for the production of plants in the greenhouse. We also thank Véronique Lefebvre (INRA, Avignon), Gilles Pilate (INRA, Orléans), Veronique Brault (INRA-Colmar), Florence Lahogue-Esnault, Michel Renard and Jean-Paul Dantec (INRA, Rennes) who kindly provided us DNA and plant samples.

Conflict of interest

The authors declare that they have no conflict of interest.

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The experiments comply with the current laws of the countries in which they were performed.

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Authors and Affiliations

  1. MTT/BI Plant Genomics Lab, Institute of Biotechnology, University of Helsinki, P.O. Box 65, Biocenter 3, Viikinkaari 1, 00014, Helsinki, Finland

    Cédric Moisy, Alan H. Schulman, Ruslan Kalendar & Jan P. Buchmann

  2. Biotechnology and Food Research, MTT Agrifood Research Finland, Myllytie 1, 31600, Jokioinen, Finland

    Cédric Moisy & Alan H. Schulman

  3. INRA, UMR1131, 68000, Colmar, France

    Frédérique Pelsy

  4. Université de Strasbourg, UMR1131, 67000, Strasbourg, France

    Frédérique Pelsy

  5. INRA, UMR AGAP 1334, DAVEM, 2 place Pierre Viala, 34060, Montpellier Cedex 1, France

    Cédric Moisy

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  1. Cédric Moisy
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  2. Alan H. Schulman
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  3. Ruslan Kalendar
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  5. Frédérique Pelsy
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Correspondence to Cédric Moisy.

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Communicated by P. Heslop-Harrison.

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Moisy, C., Schulman, A.H., Kalendar, R. et al. The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years. Theor Appl Genet 127, 1223–1235 (2014). https://doi.org/10.1007/s00122-014-2293-z

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  • DOI: https://doi.org/10.1007/s00122-014-2293-z

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