1887

Abstract

Integration of non-retroviral sequences in the genome of different organisms has been observed and, in some cases, a relationship of these integrations with immunity has been established. The genome of the green peach aphid, (clone G006), was screened for densovirus-like sequence (DLS) integrations. A total of 21 DLSs localized on 10 scaffolds were retrieved that mostly shared sequence identity with two aphid-infecting viruses, Myzus persicae densovirus (MpDNV) and Dysaphis plantaginea densovirus (DplDNV). In some cases, uninterrupted potential ORFs corresponding to non-structural viral proteins or capsid proteins were found within DLSs identified in the aphid genome. In particular, one scaffold harboured a complete virus-like genome, while another scaffold contained two virus-like genomes in reverse orientation. Remarkably, transcription of some of these ORFs was observed in , suggesting a biological effect of these viral integrations. In contrast to most of the other densoviruses identified so far that induce acute host infection, it has been reported previously that MpDNV has only a minor effect on fitness, while DplDNV can even have a beneficial effect on its aphid host. This suggests that DLS integration in the genome may be responsible for the latency of MpDNV infection in the aphid host.

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2016-04-01
2024-03-28
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References

  1. Barreau C., Jousset F. X., Bergoin M. 1996; Pathogenicity of the Aedes albopictus parvovirus (AaPV), a denso-like virus, for Aedes aegypti mosquitoes. J Invertebr Pathol 68:299–309 [View Article][PubMed]
    [Google Scholar]
  2. Belyi V. A., Levine A. J., Skalka A. M. 2010; Unexpected inheritance: multiple integrations of ancient Bornavirus and Ebolavirus/Marburgvirus sequences in vertebrate genomes. PLoS Pathog 6:e1001030 [View Article][PubMed]
    [Google Scholar]
  3. Bergoin M., Tijssen P. 2010; Densoviruses: a highly diverse group of arthropod Parvoviruses. In Insect Virology pp 59–82Edited by Asgari S., Johnson K. Norfolk, UK: Academic Press;
    [Google Scholar]
  4. Berns K. I. 1990; Parvovirus replication. Microbiol Rev 54:316–329[PubMed]
    [Google Scholar]
  5. Bertsch C., Beuve M., Dolja V. V., Wirth M., Pelsy F., Herrbach E., Lemaire O. 2009; Retention of the virus-derived sequences in the nuclear genome of grapevine as a potential pathway to virus resistance. Biol Direct 4:21 [View Article][PubMed]
    [Google Scholar]
  6. Bézier A., Annaheim M., Herbinière J., Wetterwald C., Gyapay G., Bernard-Samain S., Wincker P., Roditi I., Heller M., other authors. 2009; Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323:926–930 [View Article][PubMed]
    [Google Scholar]
  7. Buchatskii˘ L. P., Kuznetsova M. A., Lebedinets N. N., Kononko A. G. 1987; [Development and basic properties of the viral preparation viroden]. Vopr Virusol 32:729–733 (in Russian)
    [Google Scholar]
  8. Carlson J., Suchman E., Buchatsky L. 2006; Densoviruses for control and genetic manipulation of mosquitoes. Adv Virus Res 68:361–392 [View Article][PubMed]
    [Google Scholar]
  9. Cheng R. L., Xi Y., Lou Y. H., Wang Z., Xu J. Y., Xu H. J., Zhang C. X. 2014; Brown planthopper nudivirus DNA integrated in its host genome. J Virol 88:5310–5318 [View Article][PubMed]
    [Google Scholar]
  10. Chevenet F., Brun C., Bañuls A. L., Jacq B., Christen R. 2006; TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439 [View Article][PubMed]
    [Google Scholar]
  11. Chilana P., Sharma A., Rai A. 2012; Insect genomic resources: status, availability and future. Curr Sci 102:571–580
    [Google Scholar]
  12. Croizier L., Jousset F. X., Veyrunes J. C., López-Ferber M., Bergoin M., Croizier G. 2000; Protein requirements for assembly of virus-like particles of Junonia coenia densovirus in insect cells. J Gen Virol 81:1605–1613 [View Article][PubMed]
    [Google Scholar]
  13. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J. F., Guindon S., Lefort V., other authors. 2008; Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:(Web Server)W465–W469 [View Article][PubMed]
    [Google Scholar]
  14. Ding C., Urabe M., Bergoin M., Kotin R. M. 2002; Biochemical characterization of Junonia coenia densovirus nonstructural protein NS-1. J Virol 76:338–345 [View Article][PubMed]
    [Google Scholar]
  15. Dupont F. 2003; Risk assessment of the use of autonomous parvovirus-based vectors. Curr Gene Ther 3:567–582 [View Article][PubMed]
    [Google Scholar]
  16. Edgar R. C. 2004; muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  17. El-Far M., Li Y., Fédière G., Abol-Ela S., Tijssen P. 2004; Lack of infection of vertebrate cells by the densovirus from the maize worm Mythimna loreyi (MlDNV). Virus Res 99:17–24 [View Article][PubMed]
    [Google Scholar]
  18. Finnegan D. J. 1989; Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107 [View Article][PubMed]
    [Google Scholar]
  19. Flegel T. W. 2009; Hypothesis for heritable, anti-viral immunity in crustaceans and insects. Biol Direct 4:32 [View Article][PubMed]
    [Google Scholar]
  20. Goic B., Vodovar N., Mondotte J. A., Monot C., Frangeul L., Blanc H., Gausson V., Vera-Otarola J., Cristofari G., Saleh M. C. 2013; RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila . Nat Immunol 14:396–403 [View Article][PubMed]
    [Google Scholar]
  21. Hu Y. Y., Zhang J. M., Yin Y. N., Wu K. L., He M. 2000; Pathogenicity island: a novel pesticide enhanced by insect hormone for controlling cockroaches. Chin J Hyg Insectic Equipm 6:29–32
    [Google Scholar]
  22. International Aphid Genomics Consortium 2010; Genome sequence of the pea aphid Acyrthosiphon pisum . PLoS Biol 8:e1000313 [View Article][PubMed]
    [Google Scholar]
  23. Jiang H., Zhang J. M., Wang J. P., Yang B., Liu C. F., Lu J., Hu Y. Y. 2007; Genetic engineering of Periplaneta fuliginosa densovirus as an improved biopesticide. Arch Virol 152:383–394 [View Article][PubMed]
    [Google Scholar]
  24. Jones D. T., Taylor W. R., Thornton J. M. 1992; The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282[PubMed]
    [Google Scholar]
  25. Katzourakis A., Gifford R. J. 2010; Endogenous viral elements in animal genomes. PLoS Genet 6:e1001191 [View Article][PubMed]
    [Google Scholar]
  26. Kohany O., Gentles A. J., Hankus L., Jurka J. 2006; Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7:474 [View Article][PubMed]
    [Google Scholar]
  27. Krupovic M., Forterre P. 2015; Single-stranded DNA viruses employ a variety of mechanisms for integration into host genomes. Ann N Y Acad Sci 1341:41–53 [View Article][PubMed]
    [Google Scholar]
  28. Legendre D., Rommelaere J. 1992; Terminal regions of the NS-1 protein of the parvovirus minute virus of mice are involved in cytotoxicity and promoter trans inhibition. J Virol 66:5705–5713[PubMed]
    [Google Scholar]
  29. Liu H., Fu Y., Li B., Yu X., Xie J., Cheng J., Ghabrial S. A., Li G., Yi X., Jiang D. 2011a; Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 11:276 [View Article][PubMed]
    [Google Scholar]
  30. Liu H., Fu Y., Xie J., Cheng J., Ghabrial S. A., Li G., Peng Y., Yi X., Jiang D. 2011b; Widespread endogenization of densoviruses and parvoviruses in animal and human genomes. J Virol 85:9863–9876 [View Article][PubMed]
    [Google Scholar]
  31. Liu K., Li Y., Jousset F. X., Zadori Z., Szelei J., Yu Q., Pham H. T., Lépine F., Bergoin M., Tijssen P. 2011c; The Acheta domesticus densovirus, isolated from the European house cricket, has evolved an expression strategy unique among parvoviruses. J Virol 85:10069–10078 [View Article][PubMed]
    [Google Scholar]
  32. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔ C T method. Methods 25:402–408 [View Article][PubMed]
    [Google Scholar]
  33. 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 362:342–349 [View Article][PubMed]
    [Google Scholar]
  34. Monde K., Contreras-Galindo R., Kaplan M. H., Markovitz D. M., Ono A. 2012; Human endogenous retrovirus K Gag coassembles with HIV-1 Gag and reduces the release efficiency and infectivity of HIV-1. J Virol 86:11194–11208 [View Article][PubMed]
    [Google Scholar]
  35. Monsarrat P., Mariau D., Genty P. 1984; Densovirus en lutte biologique. Bull Soc Entomol Fr 89:816–821
    [Google Scholar]
  36. Mutuel D., Ravallec M., Chabi B., Multeau C., Salmon J. M., Fournier P., Ogliastro M. 2010; Pathogenesis of Junonia coenia densovirus in Spodoptera frugiperda: a route of infection that leads to hypoxia. Virology 403:137–144 [View Article][PubMed]
    [Google Scholar]
  37. Ramsey J. S., Wilson A. C., de Vos M., Sun Q., Tamborindeguy C., Winfield A., Malloch G., Smith D. M., Fenton B., other authors. 2007; Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genomics 8:423 [View Article][PubMed]
    [Google Scholar]
  38. Rhode S. L. III, Richard S. M. 1987; Characterization of the trans-activation-responsive element of the parvovirus H-1 P38 promoter. J Virol 61:2807–2815[PubMed]
    [Google Scholar]
  39. Rozen S., Skaletsky H. 2000; Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386[PubMed]
    [Google Scholar]
  40. Ryabov E. V., Keane G., Naish N., Evered C., Winstanley D. 2009; Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea . Proc Natl Acad Sci U S A 106:8465–8470 [View Article][PubMed]
    [Google Scholar]
  41. Suto C. 1979; Characterization of a virus newly isolated from the smoky-brown cockroach, Periplaneta fuliginosa (Serville). Nagoya J Med Sci 42:13–25[PubMed]
    [Google Scholar]
  42. Szelei J., Woodring J., Goettel M. S., Duke G., Jousset F. X., Liu K. Y., Zadori Z., Li Y., Styer E., other authors. 2011; Susceptibility of North-American and European crickets to Acheta domesticus densovirus (AdDNV) and associated epizootics. J Invertebr Pathol 106:394–399 [View Article][PubMed]
    [Google Scholar]
  43. Tal J., Attathom T. 1993; Insecticidal potential of insect parvovirus GmDNV. Arch Insect Biochem Physiol 22:345–356 [View Article]
    [Google Scholar]
  44. Thézé J., Bézier A., Periquet G., Drezen J. M., Herniou E. A. 2011; Paleozoic origin of insect large dsDNA viruses. Proc Natl Acad Sci U S A 108:15931–15935 [View Article][PubMed]
    [Google Scholar]
  45. van Munster M., Dullemans A. M., Verbeek M., van den Heuvel J. F., Reinbold C., Brault V., Clérivet A., van der Wilk F. 2003a; Characterization of a new densovirus infecting the green peach aphid Myzus persicae . J Invertebr Pathol 84:6–14 [View Article][PubMed]
    [Google Scholar]
  46. van Munster M., Dullemans A. M., Verbeek M., van den Heuvel J. F., Reinbold C., Brault V., Clérivet A., van der Wilk F. 2003b; A new virus infecting Myzus persicae has a genome organization similar to the species of the genus Densovirus . J Gen Virol 84:165–172 [View Article][PubMed]
    [Google Scholar]
  47. Xu P., Liu Y., Graham R. I., Wilson K., Wu K. 2014; Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLoS Pathog 10:e1004490 [View Article][PubMed]
    [Google Scholar]
  48. Yang C. C., Xiao X., Zhu X., Ansardi D. C., Epstein N. D., Frey M. R., Matera A. G., Samulski R. J. 1997; Cellular recombination pathways and viral terminal repeat hairpin structures are sufficient for adeno-associated virus integration in vivo and in vitro. J Virol 71:9231–9247[PubMed]
    [Google Scholar]
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