Petunia pp 343-363 | Cite as

Impact of Retroelements in Shaping the Petunia Genome

  • Katja R. Richert-Pöggeler
  • Trude Schwarzacher


Retroelements, defined by their dependence on reverse transcription for replication, are found in the genomes of bacteria, fungi, animals and plants. This chapter summarizes current knowledge about the structure, function and evolution of representatives from two retroelement groups identified in Petunia. The presence of both a viral retroelement – an inducible endogenous plant pararetrovirus, EPRV- and non-viral retroelements in the form of LTR-retrotransposons makes Petunia an ideal model system to study possible retroelement interactions. Phylogenetic relationships have been determined and chromosomal co-localization of EPRV and Metaviridae, one group of LTR-retrotransposons, has been demonstrated. The impact of partly overlapping replication pathways on element interference is discussed. While studies in Petunia and related species have led to tremendous progress in our understanding of these elements we are just beginning to comprehend the consequences of their presence and activities in their hosts.


Long Terminal Repeat Host Genome Solanaceous Plant Template Switch Reverse Transcriptase Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Arabidopsis Genome Initiative (AGI 2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.CrossRefGoogle Scholar
  2. Beguiristain, T., Grandbastien, M.-A., Puigdomenech, P. and Casacuberta, J.M. (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.CrossRefPubMedGoogle Scholar
  3. Blume, B., Barry, C.S., Hamilton, A.J., Bouzayen, M. and Grierson, D. (1997) Identification of transposon-like elements in non-coding regions of tomato ACC oxidase genes. Mol. Gen. Genet. 254, 297–303.CrossRefPubMedGoogle Scholar
  4. Camirand, A. and Brisson, N. (1990) The complete nucleotide sequence of the Tst1 retrotransposon of potato. Nucl. Acids Res. 18, 4929.CrossRefPubMedGoogle Scholar
  5. Casacuberta, J.M., Vernhettes, S., Audeon, C. and Grandbastien, M.-A. (1997) Quasispecies in retrotransposons: A role for sequence variability in Tnt1 evolution. Genetica 100, 109–117.CrossRefPubMedGoogle Scholar
  6. Eickbush, T.H. and Malik, H.S. (2002) Origins and evolution of retrotransposons. In: N.L. Craig, R. Craigie, M. Gellert, and A.M. Lambowitz (Eds.), Mobile DNA II. ASM Press, Washington, DC, pp. 1111–1146.Google Scholar
  7. Eickbush, T.H., Boeke, J.D., Sandmeyer, S.B. and Voytas, D.F. (2005) Metaviridae. In: C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Dessleberg and L.A. Ball (Eds.), Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp. 409–420.Google Scholar
  8. Ellis, T.H.N., Poyser, S.J., Knox, M.R., Vershinin, A.V. and Ambrose, M.J. (1998) Ty1-copia class retrotransposon insertion site polymorphism for linkage and diversity analysis in pea. Mol. Gen. Genet. 260, 9–19.PubMedGoogle Scholar
  9. Fauquet, C.M., Mayo, M.A., Maniloff, J., Desselberger, U. and Ball, L.A. (2005) Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego.Google Scholar
  10. Feschotte, C., Jiang, N. and Wessler, S.R. (2002) Plant transposable elements: Where genetics meets genomics. Nature Rev. 3, 329–341.Google Scholar
  11. Flavell, A.J., Smith, D.B. and Kumar, A. (1992) Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol. Gene Genet. 231, 233–242.Google Scholar
  12. Flavell, A.J., Knox, M., Pearce, S.R. and Ellis, T.H.N. (1998) Retrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis. Plant J. 16, 643–650.CrossRefPubMedGoogle Scholar
  13. Friesen, N., Brandes, A. and Heslop-Harrison, J.S. (2001) Diversity, origin and distribution of retrotransposons (gypsy and copia) in conifers. Mol. Biol. Evol. 18, 1176–1188.PubMedGoogle Scholar
  14. Geijskes, R.J., Braithwaite, K.S., Smith, G.R., Dale, J.L. and Harding, R.M. (2004) Sugarcane bacilliform virus encapsidates genome concatamers and does not appear to integrate into the Saccharum officinarum genome. Arch. Virol. 149, 791–798.CrossRefPubMedGoogle Scholar
  15. Grandbastien, M.-A., Spielmann, A. and Caboche, M. (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337, 376–380.CrossRefPubMedGoogle Scholar
  16. Grandbastien, M.-A., Spielmann, A., Pouteau, S., Huttner, E., Longuet, M., Kunert, K., Meyer, C., Rouze, P. and Caboche, M. (1991) Characterization of mobile endogenous copia-like transposable elements in the genome of Solanaceae. In: R.G. Hermann and B. Larkins (Eds.), Plant Molecular Biology 2. Plenum Press, NY, pp. 333–343.Google Scholar
  17. Grandbastien, M.-A., Lucas, H., Mhiri, C., Morel, J.-B., Vernhettes, S. and Casacuberta, J.M. (1997) The expression of the tobacco Tnt1 retrotransposon is linked to plant defense response. Genetica 100, 241–252.CrossRefPubMedGoogle Scholar
  18. Grandbastien, M.-A. (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3, 181–187.CrossRefGoogle Scholar
  19. Grandbastien, M.-A., Audeon, C., Bonnivard, E., Casacuberta, J.M., Chalhoub, B., Costa, A.P.P., Le, Q.H., Melayah, D., Petit, M., Poncet, C., Tam, S.M., Van Sluys, M.A. and Mhiri, C. (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet. Genome Res. 110, 229–241.Google Scholar
  20. Gregor, W., Mette, M.F., Staginnus, C., Matzke, M.A. and Matzke, A.J. (2004) A distinct endogenous pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol. 134, 1191–1199.CrossRefPubMedGoogle Scholar
  21. Guyot, R., Cheng, X., Su, Y., Cheng, Z., Schlagenhauf, E., Keller, B. and Ling, H.-Q. (2005) Complex organization and evolution of the tomato pericentromeric region at the FER gene locus. Plant Physiol. 138, 1205–1215.CrossRefPubMedGoogle Scholar
  22. Hanin, M. and Paszkowski, J. (2003) Plant genome modification by homologous recombination. Curr. Opin. Plant Biol. 6, 157–162.CrossRefPubMedGoogle Scholar
  23. Hansen, C.N. and Heslop-Harrison, J.S. (2004) Sequences and phylogenies of plant pararetroviruses, viruses and transposable elements. Adv. Bot. Res. 41, 165–193.CrossRefGoogle Scholar
  24. Hansen, C.N., Harper, G. and Heslop-Harrison, J.S. (2005) Characterization of pararetrovirus-like sequences in the genome of potato (Solanum tuberosum). Cytogenet. Genome Res. 110, 559–565.CrossRefPubMedGoogle Scholar
  25. Harper, G., Hull, R., Lockhart, B. and Olszewski, N. (2002) Viral sequences integrated into plant genomes. Annu. Rev Phytopathol 40, 119–136.CrossRefPubMedGoogle Scholar
  26. Havecker, E.R., Gao, X. and Voytas, D.F. (2004) The diversity of LTR retrotransposons. Genome Biol. 5, 1–6.CrossRefGoogle Scholar
  27. Havecker, E.R., Gao, X. and Voytas, D.F. (2005) The sireviruses, a plant-specific lineage of the Ty1/copia retrotransposons, interact with a family of proteins related to Dynein light chain 8. Plant Physiol. 139, 857–868.CrossRefPubMedGoogle Scholar
  28. Heslop-Harrison, J.S., Brandes, A., Taketa, S., Schmidt, T., Vershinin, A.V., Alkhimova, E.G., Kamm, A., Doudrick, R.L., Schwarzacher, T., Katsiotis, A., Kubis, S., Kumar, A., Pearce, S.R., Flavell, A.J. and Harrison, G.E. (1997) The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100, 197–204.CrossRefPubMedGoogle Scholar
  29. Heslop-Harrison, J.S. (2000) Comparative genome organization in plants: From sequence and markers to chromatin and chromosomes. Plant Cell 12, 617–635.CrossRefPubMedGoogle Scholar
  30. Hirochika, H. (1993) Activation of tobacco retrotransposon during tissue culture. EMBO J. 12, 2521–2528.PubMedGoogle Scholar
  31. Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H. and Kanda, M. (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci., USA 93, 7783–7788.CrossRefGoogle Scholar
  32. Hohn, T. and Richert-Pöggeler, K.R. (2006) Recent advances in DNA virus replication. In: K.L. Hefferon (Ed.), Recent Advances in DNA Virus Replication. Research Signpost 37/661. Kerala, India, pp. 289–319Google Scholar
  33. Hohn, T., Richert-Pöggeler, K.R., Staginnus, C., Harper, G., Schwarzacher, T., Teo, C.H., Teycheney, P.-Y., Iskra-Caruana, M.L. and Hull, R. (2008) Evolution of integrated plant viruses. In: M. Rossinck (Ed.), Plant Virus Evolution. Springer-Verlag, Berlin, pp. 53–82.CrossRefGoogle Scholar
  34. Hull, R., Harper, G. and Lockhart, B. (2000) Viral sequences integrated into plant genomes. Trends Plant Sci. 5, 362–365.CrossRefPubMedGoogle Scholar
  35. Hull, R. (2002) Plant Virology. Academic Press, London.Google Scholar
  36. Jääskeläinen, M., Mykkanen, A.H., Arna, T., Vicient, C.M., Suoniemi, A., Kalendar, R., Savilahti, H. and Schulman, A.H. (1999) Retrotransposon BARE-1: Expression of encoded proteins and formation of virus-like particles in barley cells. Plant J. 20, 413–422.CrossRefPubMedGoogle Scholar
  37. Jakowitsch, J., Mette, M.F., van der Winden, W.J., Matzke, M.A. and Matzke, A.J. (1999) Integrated pararetroviral sequences define a unique class of dispersed repetitive DNA in plants. Proc. Natl. Acad. Sci., USA 96, 13241–13246.CrossRefPubMedGoogle Scholar
  38. Kalendar, R., Tanskanen, J., Immonen, S., Nevo, E. and Schulman, A.H. (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.CrossRefPubMedGoogle Scholar
  39. Kamm, A., Doudrick, R.L., Heslop-Harrison, J.S. and Schmidt, T. (1996) The genomic and physical organization of Ty1-copia–like sequences as a component of large genomes in Pinus elliottii var. elliottii and other gymnosperms. Proc. Natl. Acad. Sci., USA 93, 2708–2713.CrossRefPubMedGoogle Scholar
  40. Katsiotis, A., Schmidt, T. and Heslop-Harrison, J.S. (1996) Chromosomal and genomic organization of Ty1-copia-like retrotransposon sequences in the genus Avena. Genome 39, 410–417.CrossRefPubMedGoogle Scholar
  41. Kubis, S.E., Heslop-Harrison, J.S., Desel, C. and Schmidt, T. (1998) The genomic organization of non-LTR retrotransposons (LINEs) from three Beta species and five other angiosperms. Plant Mol. Biol. 36, 821–831.Google Scholar
  42. Kulcheski, F.R., Muschner, V.C., Lorenz-Lemke, A.P., Stehmann, J.R., Bonatto, S.L., Salzano, F.M. and Freitas, L.B. (2006) Molecular phylogenetic analysis of Petunia juss. (Solanaceae). Genetica 126, 3–14.CrossRefPubMedGoogle Scholar
  43. Kumar, A. and Bennetzen, J.L. (1999) Plant retrotransposons. Annu. Rev. Genet. 33, 479–532.CrossRefPubMedGoogle Scholar
  44. Laten, H.M., Majumdar, A. and Gaucher, E.A. (1998) SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc. Natl. Acad. Sci, USA 95, 6897–6902.CrossRefPubMedGoogle Scholar
  45. Leitch, I.J., Soltis, D.E., Soltis, P.S. and Bennett, M.D. (2005) Evolution of DNA amounts across land plants (Embryophyta). Ann. Bot. 95, 207–217.CrossRefPubMedGoogle Scholar
  46. Lockhart, B.E., Menke, J., Dahal, G. and Olszewski, N.E. (2000) Characterization and genomic analysis of tobacco vein clearing virus, a plant pararetrovirus that is transmitted vertically and related to sequences integrated in the host genome. J. Gen.Virol. 81, 1579–1585.PubMedGoogle Scholar
  47. Manetti, M.E., Rossi, M., Costa, A.P.P., Clausen, A.M. and Van Sluys, M.-A. (2007) Radiation of the Tnt1 retrotransposon superfamily in three Solanaceae genera. BMC Evol. Biol. 7, 34.CrossRefPubMedGoogle Scholar
  48. Mao, L., Begum, D., Goff, S.A. and Wing, R.A. (2001) Sequence and analysis of the tomato JOINTLESS locus. Plant Physiol. 126, 1331–1340.CrossRefPubMedGoogle Scholar
  49. Matsubara, K., Kodama, H., Kokubun, H., Watanabe, H. and Ando, T. (2005) Two novel transposable elements in a cytochrome P450 gene govern anthocyanin biosynthesis of commercial petunias. Gene 358, 121–126.CrossRefPubMedGoogle Scholar
  50. Matzke, M., Gregor, W., Mette, M.F., Aufsatz, W., Kanno, T., Jakowitsch, J. and Matzke, A.J.M. (2004) Endogenous pararetroviruses of allotetraploid Nicotiana tabacum and its diploid progenitors, N. sylvestris and N. tomentosiformis. Biol. J. Linnean Soc. 82, 627–638.CrossRefGoogle Scholar
  51. Mette, M.F., Kanno, T., Aufsatz, W., Jakowitsch, J., van der Winden, W.J., Matzke, M.A. and Matzke, A.J. (2002) Endogenous viral sequences and their potential contribution to heritable virus resistance in plants. EMBO J. 21, 461–469.CrossRefPubMedGoogle Scholar
  52. Mishiba, K.-I., Ando, T., Mii, M., Watanabe, H., Kokubun, H., Hashimoto, G. and Marchesi, E. (2000) Nuclear DNA content as an index character discriminating taxa in the genus Petunia sensu Jussieu (Solanaceae). Ann. Bot. 85, 665–673.CrossRefGoogle Scholar
  53. Mueller, L.A., Tanksley, S.D., Giovannoni, J.J., van Eck, J., Stack, S., Choi, D., Kim, B.D., Chen, M., Cheng, Z., Li, C. et al. (2005) The tomato sequencing project: The first cornerstone of the International Solanaceae Project (SOL). Comp. Funct. Genom. 6, 153–158.Google Scholar
  54. Noreen, F., Akbergenov, R., Hohn, T. and Richert-Pöggeler, K.R. (2007) Distinct expression of endogenous Petunia vein clearing virus and the DNA transposon dTph1 in two Petunia hybrida lines is correlated with differences in histone modification and siRNA production. Plant J. 50, 219–229.CrossRefPubMedGoogle Scholar
  55. Peterson-Burch, B.D., Wright, D.A., Laten, H.M. and Voytas, D.F. (2000) Retroviruses in plants? Trends Genet. 16, 151–152.Google Scholar
  56. Peterson-Burch, B.D. and Voytas, D.F. (2002) Genes of the Pseudoviridae (Ty1/copia retrotransposons). Mol. Biol. Evol. 19, 1832–1845.PubMedGoogle Scholar
  57. Pouteau, S., Huttner, E., Grandbastien, M.A. and Caboche, M. (1991) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 10, 1911–1918.PubMedGoogle Scholar
  58. Puchta, H. (2005) The repair of double-strand breaks in plants: Mechanisms and consequences for genome evolution. J. Exp. Bot. 56, 1–14.CrossRefPubMedGoogle Scholar
  59. Richert, K.R. (1992) Untersuchungen zur Charakterisierung des Petunia Vein Clearing Virus (PVCV), ein Samenübertragbares Pararetrovirus. Ph.D. Thesis Georg-August-University, Göttingen, Germany.Google Scholar
  60. Richert-Pöggeler, K.R. and Shepherd, R.J. (1997) Petunia vein clearing virus: A plant pararetrovirus with the core sequence for an integrase function. Virol. 236, 137–146.CrossRefGoogle Scholar
  61. Richert-Pöggeler, K.R., Noreen, F., Schwarzacher, T., Harper, G. and Hohn, T. (2003) Induction of infectious petunia vein clearing (pararetro) virus from endogenous provirus in petunia. EMBO J. 22, 4836–4845.CrossRefPubMedGoogle Scholar
  62. Roda, H.R., Balakrishnan, M., Hanson, M.N., Wöhrl, B.M., Le Grice, S.F.J., Roques, B.P., Gorelick, R.J. and Bambara, R.A. (2003) Role of the reverse transcriptase, nucleocapsid protein, and template structure in the two-step transfer mechanism in retroviral recombination. J. Biol. Chem. 278, 31536–31546.CrossRefPubMedGoogle Scholar
  63. Rogers, S.A. and Pauls, K.P. (2000) Ty1-copia-like retrotransposons of tomato (Lycopersicon esculentum Mill.). Genome 43, 887–894.CrossRefPubMedGoogle Scholar
  64. SanMiguel, P., Tikhonov, A., Jin, Y.-K., Motchoulskaia, N., Zakharov, D., Melake-Berhan, A., Springer, P.S., Edwards, K.J., Lee, M., Avramova, Z. and Bennetzen, J.L. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765–768.CrossRefPubMedGoogle Scholar
  65. Schwarzacher, T. (2003) DNA, chromosomes and in situ hybridization. Genome 46, 953–962.CrossRefPubMedGoogle Scholar
  66. Staginnus, C. and Richert-Pöggeler, K.R. (2006) Endogenous pararetroviruses: Two-faced travelers in the plant genome. Trends Plant Sci. 11, 485–491.CrossRefPubMedGoogle Scholar
  67. Staginnus, C., Gregor, W., Mette, M.F., Teo, C.H., Borroto-Fernandez, E.G., Laimer da Camara Machado, M., Matzke, M. and Schwarzacher, T. (2007) Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biol. 7, 24.CrossRefPubMedGoogle Scholar
  68. Takeda, S., Sugimoto, K., Kakutani, T. and Hirochika, H. (2001) Linear DNA intermediates of the Tto1 retrotransposon in Gag particles accumulated in stressed tobacco and Arabidopsis thaliana. Plant J. 28, 307–317.CrossRefPubMedGoogle Scholar
  69. Tam, S.M., Causse, M., Garchy, C., Burck, H., Mhiri, C. and Grandbastien, M.-A. (2007) The distribution of copia-type retrotransposons and the evolutionary history of tomato and related wild species. J. Evol. Biol. 20, 1056–1072.CrossRefPubMedGoogle Scholar
  70. Tatout, C., Lavie, L. and Deragon, J.-M. (1998) Similar target site selection occurs in integration of plant and mammalian retroposons. J. Mol. Ecol. 47, 463–470.CrossRefGoogle Scholar
  71. Vershinin, A.V., Druka, A., Alkhimova, A.G., Kleinhofs, A. and Heslop-Harrison, J.S. (2002) LINEs and gypsy-like retrotransposons in Hordeum species. Plant Mol. Biol. 49, 1–14.CrossRefPubMedGoogle Scholar
  72. Vitte, C. and Panaud, O. (2005) LTR retrotransposons and flowering plant genome size: Emergence of the increase/decrease model. Cytogenet. Genome Res. 110, 91–107.Google Scholar
  73. Vitte, C. and Bennetzen, J.L. (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc. Natl. Acad. Sci, USA 103, 17638–17643.CrossRefPubMedGoogle Scholar
  74. Voytas, D.F., Cummings, M.P., Konieczny, A., Ausubel, F.M. and Rodermel, S.R. (1992) Copia-like retrotransposons are ubiquitous among plants. Proc. Natl. Acad. Sci., USA 89, 7124–7128.CrossRefPubMedGoogle Scholar
  75. Voytas, D.F. and Boeke, J.D. (2002) Ty1 and Ty5 of Saccharomyces cerevisiae. In: N.L. Craig, R. Craigie, M. Gellert and A.M. Lambowitz (Eds.), Mobile DNA II. ASM Press, Washington, DC, pp. 631–662.Google Scholar
  76. Wang, Y., Tang, X., Cheng, Z., Mueller, L., Giovannoni, J. and Tanksley, S.D. (2006) Euchromatin and pericentromeric heterochromatin: Comparative composition in the tomato genome. Genetics 172, 2529–2540.CrossRefPubMedGoogle Scholar
  77. White, S.E., Habera, L.F. and Wessler, S.R. (1994) Retrotransposons in the flanking region of normal plant genes: Role for copia-like retroelements in the evolution of gene structure and expression. Proc. Natl. Acad. Sci., USA 91, 11792–11796.CrossRefPubMedGoogle Scholar
  78. Wright, D.A. and Voytas, D.F. (1998) Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149, 703–715.PubMedGoogle Scholar
  79. Xiong, Y. and Eickbush, T.H. (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9, 3353–3362.PubMedGoogle Scholar
  80. Yang, T.J., Lee, J., Chang, S.B., Yu, Y., de Yong, H. and Wing, R.A. (2005) In-depth sequence analysis of the tomato chromosome 12 centromeric region: Identification of a large CAA block and characterization of pericentromere retrotransposons. Chromos. 114, 103–117.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Katja R. Richert-Pöggeler
    • 1
  • Trude Schwarzacher
    • 2
  1. 1.Institute for Epidemiology and Pathogen DiagnosticsJulius Kühn-Institut (JKI) – Federal Research Centre for Cultivated PlantsMesseweg 11–12Deutschland
  2. 2.Department of BiologyUniversity of Leicester, University RoadLeicester LEI 7RHUK

Personalised recommendations