Evolution of Integrated Plant Viruses

  • Thomas Hohn
  • Katja R. Richert-Pöggeler
  • Christina Staginnus
  • Glyn Harper
  • Trude Schwarzacher
  • Chee How Teo
  • Pierre-Yves Teycheney
  • Marie-Line Iskra-Caruana
  • Roger Hull

Plant pararetroviruses replicate their genome via a transcription–reverse transcription cycle like retroviruses, but unlike them their genomes do not obligatorily integrate into the host chromatin. Nevertheless, one can find complete or fragmented pararetrovirus genomes, as well as those from geminiviruses and even RNA viruses incorporated into the genomes of nearly all plants analysed. Integration events are thought to be rare and even rarer are those that find their way into the germ line. Normally, these integrated viral sequences are incomplete, rearranged and mutated and cannot easily escape as active viruses. However, in some cases apparently more recently acquired and therefore less initiated integrates can escape by direct transcription from tandem insertions or by recombination. This can lead to severe outbreaks in crop and ornamental plants. In anticipation of such events, methods have been developed for the detection and characterization of integrated virus sequences in plant genomes.


Long Terminal Repeat Rice Tungro Bacilliform Virus Tomato Golden Mosaic Virus Banana Streak Virus Musa Balbisiana 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberter B, Ali RM, Jeske H (2005) Replicative intermediates of Tomato leaf curl virus and its satellite DNAs. Virology 331:441–448PubMedCrossRefGoogle Scholar
  2. Almeida R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 15:251–258PubMedCrossRefGoogle Scholar
  3. Ando T, Kokubun H, Watanabe H, Tanaka N, Yukawa T, Hashimoto G, Marchesi E, Suarez E, Basualdo IL (2005) Phylogenetic analysis of Petunia sensu Jussieu (Solanaceae) using chloroplast DNA RFLP. Ann Bot (Lond) 96:289–297CrossRefGoogle Scholar
  4. Ashby MK, Warry A, Bejarano ER, Khashoggi A, Burrell M, Lichtenstein CP (1997) Analysis of multiple copies of geminiviral DNA in the genome of four closely related Nicotiana species suggest a unique integration event. Plant Mol Biol 35:313–321PubMedCrossRefGoogle Scholar
  5. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363PubMedCrossRefGoogle Scholar
  6. Bejarano ER, Khashoggi A, Witty M, Lichtenstein C (1996) Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc Natl Acad Sci USA 93:759–764PubMedCrossRefGoogle Scholar
  7. Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:621–627PubMedCrossRefGoogle Scholar
  8. Berry C, Hannenhalli S, Leipzig J, Bushman FD (2006) Selection of target sites for mobile DNA integration in the human genome. PLoS Comput Biol 2:1450–1462CrossRefGoogle Scholar
  9. Bill CA, Summers J (2004) Genomic DNA double-strand breaks are targets for hepadnaviral DNA integration. Proc Natl Acad Sci USA 101:11135–11140PubMedCrossRefGoogle Scholar
  10. Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park HS, Vazquez F, Robertson D, Meins F Jr, Hohn T, Pooggin MM (2006) Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246PubMedCrossRefGoogle Scholar
  11. Botstein D (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354:484–491PubMedCrossRefGoogle Scholar
  12. Coffin JM, Hughes SH, Varmus HE (1997) Retroviruses. Cold Spring Harbor Press, Cold Spring HarborGoogle Scholar
  13. Dallot S, Acuna P, Rivera C, Ramirez P, Cote F, Lockhart BEL, Caruana ML (2001) Evidence that the proliferation stage of micropropagation procedure is determinant in the expression of Banana streak virus integrated into the genome of the FHIA 21 hybrid (Musa AAAB). Arch Virol 146:2179–2190PubMedCrossRefGoogle Scholar
  14. Day AC, Bergerano ER, Buck KW, Burrel M, Lichtenstein CP (1991) Expression of an antisense viral gene in tobacco confers resistance to the DNA virus Tomato golden mosaic virus. Proc Natl Acad Sci USA 88:6721–6727PubMedCrossRefGoogle Scholar
  15. Eickbush TH (1997) Telomerase and retrotransposons: Which came first? Science 277(5328):911–912PubMedCrossRefGoogle Scholar
  16. Fargette D, Konate G, Fauquet C, Muller E, Peterschmitt M, Tresh JM (2006) Molecular ecology and emergence of tropical plant viruses. Annu Rev Phytopathol 442:35–260Google Scholar
  17. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus Taxonomy. VIIIth report of the International Committee on Taxonomy of Viruses. Elsevier, San DiegoGoogle Scholar
  18. Ferber MJ, Montoya DP, Yu C, Aderca I, McGee A, Thorland EC, Nagorney DM, Gostout BS, Burgart LJ, Boix L, Bruix J, McMahon BJ, Cheung TH, Chung TK, Wong YF, Smith DI, Roberts LR (2003) Integrations of the hepatitis B virus (HBV) and human papillomavirus (HPV) into the human telomerase reverse transcriptase (hTERT) gene in liver and cervical cancers. Oncogene 22:3813–3820PubMedCrossRefGoogle Scholar
  19. Fischer A, Hofmann I, Naumann K, Reuter G (2006) Heterochromatin proteins and the control of heterochromatic gene silencing in Arabidopsis. J Plant Physiol 163:358–368PubMedCrossRefGoogle Scholar
  20. Foster TM, Lough TJ, Emerson SJ, Lee RH, Bowman JL, Forster RL, Lucas WJ (2002) A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508PubMedCrossRefGoogle Scholar
  21. Froissart R, Roze D, Uzest M, Galibert L, Blanc S, Michalakis Y (2005) Recombination every day: Abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3:e89PubMedCrossRefGoogle Scholar
  22. Geering ADW, Olszewski NE, Dahal G, Thomas JE, Lockhart BEL (2001) Analysis of the distribution and structure of integrated banana streak virus DNA in a range of Musa cultivars. Mol Plant Pathol 2:207–213CrossRefGoogle Scholar
  23. Geering AD, Pooggin MM, Olszewski NE, Lockhart BE, Thomas JE (2005a) Characterisation of Banana streak Mysore virus and evidence that its DNA is integrated in the B genome of cultivated Musa. Arch Virol 150:787–796PubMedCrossRefGoogle Scholar
  24. Geering AD, Olszewski NE, Harper G, Lockhart BE, Hull R, Thomas JE (2005b) Banana contains a diverse array of endogenous badnaviruses. J Gen Virol 86:511–520PubMedCrossRefGoogle Scholar
  25. Geijskes RJ, Braithwaite KS, Smith GR, Dale JL, Harding RM (2004) Sugarcane bacilliform virus encapsidates genome concatamers and does not appear to integrate into the Saccharum officinarum genome. Arch Virol 149:791–798PubMedCrossRefGoogle Scholar
  26. Gifford R, Tristem M. (2003) The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291–315PubMedCrossRefGoogle Scholar
  27. Goodspeed TH (1947) On the evolution of the genus Nicotiana. Proc Natl Acad Sci USA 33:158–171PubMedCrossRefGoogle Scholar
  28. Gregor W, Mette MF, Staginnus C, Matzke MA, Matzke AJ (2004) A distinct endogenous Pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol 134:1191–1199PubMedCrossRefGoogle Scholar
  29. Gundersen-Rindal DE, Lynn DE (2003) Polydnavirus integration in lepidopteran host cells in vitro. J Insect Physiol 49:453–462PubMedCrossRefGoogle Scholar
  30. Gutierrez C (2000) Geminiviruses and the plant cell cycle. Plant Mol Biol 43:763–772PubMedCrossRefGoogle Scholar
  31. Hanin M, Paszkowski J (2003) Plant genome modification by homologous recombination. Curr Opin Plant Biol 6:157–162PubMedCrossRefGoogle Scholar
  32. Hansen CN (2003) Pararetrovirus-like sequences in the genomes of plants. PhD thesis, University of LeicesterGoogle Scholar
  33. Hansen CN, Heslop-Harrison JS (2004) Sequences and phylogenies of plant pararetroviruses, viruses and transposable elements. Adv Bot Res 41:165–193CrossRefGoogle Scholar
  34. Hansen CN, Harper G, Heslop-Harrison JS (2005) Characterisation of pararetrovirus-like sequences in the genome of potato (Solanum tuberosum). Cytogenet Genome Res 110:559–565PubMedCrossRefGoogle Scholar
  35. Harper G, Osuji JO, Heslop-Harrison JS, Hull R (1999) Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255:207–213PubMedCrossRefGoogle Scholar
  36. Harper G, Hull R, Lockhart B, Olszewski N (2002) Viral sequences integrated into plant genomes. Annu Rev Phytopathol 40:119–136PubMedCrossRefGoogle Scholar
  37. Harper G, Richert-Pöggeler KR, Hohn T, Hull R (2003) Detection of petunia vein-clearing virus: model for the detection of DNA viruses in plants with homologous endogenous pararetrovirus sequences. J Virol Methods 107:177–184PubMedCrossRefGoogle Scholar
  38. Harper G, Hart D, Moult S, Hull R, Geering A, Thomas J (2005) The diversity of Banana streak virus isolates in Uganda. Arch Virol 150:2407–2420PubMedCrossRefGoogle Scholar
  39. Hegedüs K, Dallmann G, Balazs E (2004) The DNA form of a retroviroid-like element is involved in recombination events with itself and with the plant genome. Virology 325:277–286PubMedCrossRefGoogle Scholar
  40. Hohn T (1994) Recombination of plant pararetroviruses. In: J Paszkowski (ed) Homologous recombination and gene silencing in plants. Kluwer, Dordrecht, pp 25–38Google Scholar
  41. Hohn T, Richert-Pöggeler KR (2006) Recent advances in DNA virus replication. In: Hetherton KR (ed) Recent advances in DNA virus replication. Research Signpost Transworld, KeralaGoogle Scholar
  42. Hull R (1992) Genome organization of retroviruses and retroelements: evolutionary considerations and implications. Semin Virol 3:373–382Google Scholar
  43. Hull R (2001) Matthews plant virology. Academic, San DiegoGoogle Scholar
  44. Hull R, Covey SN (1996) Retroelements: propagation and adaptation. Virus Genes 11:105–118CrossRefGoogle Scholar
  45. Hull R, Harper G, Lockhart B (2000) Viral sequences integrated into plant genomes. Trends Plant Sci 5:362–365PubMedCrossRefGoogle Scholar
  46. Jakowitsch J, Mette MF, van der WJ, Matzke MA, Matzke AJ (1999) Integrated pararetroviral sequences define a unique class of dispersed repetitive DNA in plants. Proc Natl Acad Sci USA 96:13241–13246PubMedCrossRefGoogle Scholar
  47. Jones DR (1999) Introduction to banana, abacá and enset. In: Jones DR (ed) Diseases of banana, abacá and enset. CABI, Wallingford, pp 1–36Google Scholar
  48. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. CABIOS 8:275–282PubMedGoogle Scholar
  49. 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
  50. Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719PubMedCrossRefGoogle Scholar
  51. Kato M, Takashima K, Kakutani T (2004) Epigenetic control of CACTA transposon mobility in Arabidopsis thaliana. Genetics 168:961–969PubMedCrossRefGoogle Scholar
  52. Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification of Nicotiana (Solanaceae). Taxon 53:73–82CrossRefGoogle Scholar
  53. Kononov ME, Bassuner B, Gelvin SB (1997) Integration of T-DNA binary vector ‘backbone’ sequences into the tobacco genome: evidence for multiple complex patterns of integration. Plant J 11:945–957PubMedCrossRefGoogle Scholar
  54. Kroemer JA, Webb BA (2004) Polydnaviruses genes and genomes: emerging gene families and new insights into Polydnavirus replication. Annu Rev Entomol 49:431–456PubMedCrossRefGoogle Scholar
  55. Kulcheski FR, Muschner VC, Lorenz-Lemke AP, Stehmann JR, Bonatto SL, Salzano FM, Freitas LB (2006) Molecular phylogenetic analysis of Petunia juss. (Solanaceae). Genetica 126:3–14PubMedCrossRefGoogle Scholar
  56. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532PubMedCrossRefGoogle Scholar
  57. Kunii M, Kanda M, Nagano H, Uyeda I, Kishima Y, Sano Y (2004) Reconstruction of putative DNA virus from endogenous rice tungro bacilliform virus-like sequences in the rice genome: implications for integration and evolution. BMC Genomics 5:80PubMedCrossRefGoogle Scholar
  58. Lafleur DA, Lockhart BEL, Olszweski NE (1996) Portions of Banana streak badnavirus genome are integrated in the genome of its host Musa sp. Phytopathology 86:100Google Scholar
  59. Laten HM, Majumdar A., Gaucher EA (1998) SIRE-1, a copia/Ty1-like retroelement fromp soybean, encodes a retrovirial envelope-like protein. Proc Natl Acad Sci USA 95:6897–6902PubMedCrossRefGoogle Scholar
  60. Lescot M, Ciampi AY, Ruis M, Blanc G, Leebens-Mack J, Grasmeur O, D’Hunt A, da Silva FR, Ronning CM, Cheung F, Hans BJ, Alhoff R, Arbogast T, Hine E, Pappas G, Souza MT, Miller R, Glaszmann JC, Town CD, Piffanelli P (2005) Fresh insights into the Musa genome and its comparison with rice.
  61. Lheureux F, Carreel F, Jenny C, Lockhart BE, Iskra-Caruana ML (2003) Identification of genetic markers linked to banana streak disease expression in inter-specific Musa hybrids. Theor Appl Genet 106:594–598PubMedGoogle Scholar
  62. Lheureux F, Laboureau N, Muller E, Lockhart BEL, Iskra-Caruana ML (2007) Molecular characterization of Banana streak virus acuminata vietnam isolated from Musa acuminata siamea (banana cultivar). Arch Virol (in press)Google Scholar
  63. Lockhart BE, Menke J, Dahal G, Olszewski NE (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 81:1579–1585PubMedGoogle Scholar
  64. Lovisolo O, Hull R, Rösler O (2003) Coevolution of viruses with hosts and vectors and possible paleontology. Adv Virus Res 62:325–379PubMedCrossRefGoogle Scholar
  65. Malik HS, Eickbush TH (1999) Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons J Virol 73:5186–5190PubMedGoogle Scholar
  66. Maori E, Tanne E, Sela I (2007) Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362:342–349PubMedCrossRefGoogle Scholar
  67. Matzke MA, Mette MF, Aufsatz W, Jakowitsch J, Matzke AJ (2000) Integrated pararetroviral sequences. Nat Biotechnol 18:579PubMedCrossRefGoogle Scholar
  68. Matzke M, Gregor W, Mette MF, Aufsatz W, Kanno T, Jakowitsch J, Matzke AJM (2004) Endogenous pararetroviruses of allotetraploid Nicotiana tabacum and its diploid progenitors, N.sylvestris and N.tomentosiformis. Biol J Linn Soc 82:627–638CrossRefGoogle Scholar
  69. Mayo MA, Jolly CA (1991) The 5′ nucleotide sequence of the genome of potato leaf roll virus RNA: evidence of recombination between virus and host RNA. J Gen Virol 72:2591–2595PubMedCrossRefGoogle Scholar
  70. Meins F, Si-Ammour A, Blevins T (2005) RNA silencing systems and their relevance to plant development. Annu Rev Cell Dev Biol 21:297–318PubMedCrossRefGoogle Scholar
  71. Mette MF, Kanno T, Aufsatz W, Jakowitsch J, van der Winden J, Matzke MA, Matzke AJ (2002) Endogenous viral sequences and their potential contribution to heritable virus resistance in plants. EMBO J 21:461–469PubMedCrossRefGoogle Scholar
  72. Mumm JP, Landy A, Gelles J (2006) Viewing single lambda site-specific recombination events from start to finish. EMBO J 25:4586–4595PubMedCrossRefGoogle Scholar
  73. 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 92:352–358PubMedCrossRefGoogle Scholar
  74. Ndowora T, Dahal G, LaFleur D, Harper G, Hull R, Olszewski NE, Lockhart B (1999) Evidence that badnavirus infection in Musa can originate from integrated pararetroviral sequences. Virology 255:214–220PubMedCrossRefGoogle Scholar
  75. Noreen F, Akbergenov R, Hohn T, Richert-Pöggeler KR (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 (in press)Google Scholar
  76. Ohba T, Yoshioka Y, Machida C, Machida Y (1995) DNA rearrangement associated with the integration of T-DNA in tobacco: an example for multiple duplications of DNA around the integration target. Plant J 7:157–164PubMedCrossRefGoogle Scholar
  77. Orend G, Linkwitz A, Doerfler W (1994) Selective sites of adenovirus (foreign) DNA integration into the hamster genome: changes in integration patterns. J Virol 68:187–194PubMedGoogle Scholar
  78. Pahalawatta V, Droffel K, Pappo HR (2007) Seed transmission of Daheia mosaic virus in Daheia punata Plant Dis 91:88–91CrossRefGoogle Scholar
  79. Paszkowski J, Shillito RD, Saul M, Mandak V, Hohn T, Hohn B, Potrykus I (1984) Direct gene transfer to plants. EMBO J 3:2717–2722PubMedGoogle Scholar
  80. Piffanelli P, Noa-Carrazana J. C, Lescot M, Benabdelmouna A, Dolezel J, Matsumoto T, Silva-Rosales L, Lheureux F, Teycheney P.-Y, Geering A, D’Hont A, Glaszmann J.-C, Sasaki T, Caruana M.-L (2005) Molecular analysis of Banana streak virus (BSV) “integrants” into the nuclear genome of Musa balbisiana. In: Abstracts of the XIIIth international congress of virology, San FranciscoGoogle Scholar
  81. Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14PubMedCrossRefGoogle Scholar
  82. Richert-Pöggeler KR, Shepherd RJ (1997) Petunia vein clearing virus: a plant pararetrovirus with the core sequence for an integrase function. Virology 236:137–146PubMedCrossRefGoogle Scholar
  83. Richert-Pöggeler KR, Noreen F, Schwarzacher T, Harper G, Hohn T (2003) Induction of infectious petunia vein clearing (pararetro) virus from endogenous provirus in petunia. EMBO J 22:4836–4845PubMedCrossRefGoogle Scholar
  84. Safár J, Noa-Carrazana JC, Virana J, Bartos J, Alkhimova O, Sabou X, Samikova H, Lhereux F, Caruana ML, Dolezei J, Piffanelli P (2004) Creation of a BAC resource to study the structure and evolution of the banana (Musa balbisiana) genome. Genome 47:1182–1191PubMedCrossRefGoogle Scholar
  85. Samuelson LC, Wiebauer K, Snow CM, Meisler MH (1990) Retroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution. Mol Cell Biol. 10:2513–2520PubMedGoogle Scholar
  86. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  87. Schmidt O, Theopold U, Strand MR (2001) Innate immunity and evasion by insect parasitoids. BioEssays 23:344–351PubMedCrossRefGoogle Scholar
  88. Schwach F, Vaistij FE, Jones L, Baulcombe DC (2005) An RNA-dependent RNA polymerase prevents meristem invasion by Potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852PubMedCrossRefGoogle Scholar
  89. Sink KC (1984) Taxonomy. In: Sink KC (ed) Petunia. Springer, New YorkGoogle Scholar
  90. Skalická 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 166:291–303PubMedCrossRefGoogle Scholar
  91. Staginnus C, Richert-Pöggeler KR (2006) Endogenous pararetroviruses: two-faced travelers in the plant genome. Trends Plant Sci 11:485–491PubMedCrossRefGoogle Scholar
  92. Staginnus C, Gregor W, Mette MF, Teo CH, Borroto-Fernandez EG, Laimer da Camara Machado M, Matzke MA, Schwarzacher T (2007) Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biol 7:24PubMedCrossRefGoogle Scholar
  93. Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  94. Tanne E, Sela I (2005) Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: evidence for recombination between viral and host RNAs. Virology 332:614–622PubMedCrossRefGoogle Scholar
  95. Tsuei DJ, Chang MH, Chen PJ, Hsu TY, Ni YH (2002) Characterization of integration patterns and flanking cellular sequences of hepatitis B virus in childhood hepatocellular carcinomas. J Med Virol 68: 513–521PubMedCrossRefGoogle Scholar
  96. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science 313(5793):1596–1604PubMedCrossRefGoogle Scholar
  97. Vera A, Daros JA, Flores R, Hernandez C (2000) The DNA of a plant retroviroid-like element is fused to different sites in the genome of a plant pararetrovirus and shows multiple forms with sequence deletions. J Virol 74:10390–10400PubMedCrossRefGoogle Scholar
  98. Wang MB, Metzlaff M (2005) RNA silencing and antiviral defense in plants. Curr Opin Plant Biol 8:216–222PubMedCrossRefGoogle Scholar
  99. Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172:2529–2540PubMedCrossRefGoogle Scholar
  100. Wassenegger M (2005) The role of the RNAi machinery in heterochromatin formation. Cell 122:13–16PubMedCrossRefGoogle Scholar
  101. Wentzensen N, Vinokurova S, von Knoebel Doeberitz M (2004) Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res 64:3878–3884PubMedCrossRefGoogle Scholar
  102. White KA, Nagy PD (2004) Advances in the molecular biology of Tombusviruses: gene expression, genome replication, and recombination. Prog Nucleic Acid Res Mol Biol 78:187–228PubMedCrossRefGoogle Scholar
  103. Wilson DM III, Thompson LH (2007) Molecular mechanisms of sister-chromatid exchange. Mutat Res 616:11–23PubMedGoogle Scholar
  104. Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362PubMedGoogle Scholar
  105. Yang W, Summers J (1999) Integration of hepadnavirus DNA in infected liver: evidence for a linear precursor. J Virol 73:9710–9717PubMedGoogle Scholar
  106. Yano ST, Panbehi B, Das A, Laten H.M (2005) Diaspora, a large family of Ty3-gypsy retrotransposons in Glycine max, is an envelope-less member of an endogenous plant retrovirus lineage. BMC Evol Biol 5:30PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Thomas Hohn
    • 1
  • Katja R. Richert-Pöggeler
    • 2
  • Christina Staginnus
    • 3
  • Glyn Harper
    • 4
  • Trude Schwarzacher
    • 5
  • Chee How Teo
    • 5
  • Pierre-Yves Teycheney
    • 6
  • Marie-Line Iskra-Caruana
    • 7
  • Roger Hull
    • 4
  1. 1.Botanical InstituteUniversity of BaselSwitzerland
  2. 2.Federal Biological Research Centre for Agriculture and ForestryGermany
  3. 3.Gregor Mendel Institute of Molecular Plant Biology GmbHAustria
  4. 4.John Innes CentreNorwich Research ParkUK
  5. 5.University of LeicesterUK
  6. 6.Station de NeufchâteauGuadeloupe
  7. 7.CIRAD/UMR BGPIFrance

Personalised recommendations