Skip to main content
SpringerLink
Log in

The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

The Oryctes rhinoceros nudivirus (OrNV) is a dsDNA virus with enveloped, rod-shaped virions. Its genome is 127,615 bp in size and contains 139 predicted protein-coding open reading frames (ORFs). In-depth genome sequence comparisons revealed a varying number of shared gene homologues, not only with other nudiviruses (NVs) and baculoviruses, but also with other arthropod-specific large dsDNA viruses, including the so-called Monodon baculovirus (MBV), the salivary gland hypertrophy viruses (SGHVs) and white spot syndrome virus (WSSV). Nudivirus genomes contain 20 baculovirus core gene homologues associated with transcription (p47, lef-8, lef-9, lef-4, vlf-1, and lef-5), replication (dnapol and helicase), virus structure (p74, pif-1, pif-2, pif-3, 19kda/pif-4, odv-e56/pif-5, vp91, vp39, and 38K), and unknown functions (ac68, ac81, and p33). Most strikingly, a set of homologous genes involved in peroral infection (p74, pif-1, pif-2, and pif-3) are common to baculoviruses, nudiviruses, SGHVs, and WSSV indicating an ancestral mode of infection in these highly diverged viruses. A gene similar to polyhedrin/granulin encoding the baculovirus occlusion body protein was identified in non-occluded NVs and in Musca domestica SGHV evoking the question of the evolutionary origin of the baculovirus polyhedrin/granulin gene. Based on gene homologies, we further propose that the shrimp MBV is an occluded member of the nudiviruses. We conclude that baculoviruses, NVs and the shrimp MBV, the SGHVs and WSSV share the significant number of conserved genetic functions, which may point to a common ancestry of these viruses.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. M.M. van Oers, J.M. Vlak, Curr. Drug Targets 8, 1051–1068 (2007)

    Article  PubMed  Google Scholar 

  2. E.A. Herniou, T. Luque, X. Chen, J.M. Vlak, D. Winstanley, J.S. Cory, D.R. O’Reilly, J. Virol. 75, 8117–8126 (2001)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. C.B. McCarthy, D.A. Theilmann, Virology 375, 277–291 (2008)

    Article  CAS  PubMed  Google Scholar 

  4. Y. Wang, J.P. Burand, J.A. Jehle, Virol. Sinica 22, 128–136 (2007)

    Article  Google Scholar 

  5. Y. Wang, R.G. Kleespies, A.M. Huger, J.A. Jehle, J. Virol. 81, 5395–5406 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Y. Wang, M.M. van Oers, A.M. Crawford, J.M. Vlak, J.A. Jehle, Arch. Virol. 152, 519–531 (2007)

    Article  CAS  PubMed  Google Scholar 

  7. Y. Wang, J.A. Jehle, J. Invertebr. Pathol. 101, 187–193 (2009)

    Article  CAS  PubMed  Google Scholar 

  8. D.V. Lightner, R.M. Redman, J. Invertebr. Pathol. 38, 299–302 (1981)

    Article  Google Scholar 

  9. J. Mari, J.-R. Bonami, B. Poulos, D. Lightner, Dis. Aquat. Organ. 16, 207–215 (1993)

    Article  CAS  Google Scholar 

  10. J.H. Leu, F. Yang, X. Zhang, X. Xu, G.H. Kou, C.F. Lo, Curr. Top. Microbiol. Immunol. 328, 197–227 (2009)

    CAS  PubMed  Google Scholar 

  11. J.M. Vlak, J.R. Bonami, T.W. Flegel, G.H. Kou, D.V. Lightner, C.F. Lo, P.C. Loh, P.W. Walker, in Virus Taxonomy: The Eighth Report of the International Committee on Taxonomy of Viruses, ed. by C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Elsevier Academic Press, New York, 2005), pp. 187–192

  12. A.M. Abd-Alla, F. Cousserans, A.G. Parker, J.A. Jehle, N.J. Parker, J.M. Vlak, A.S. Robinson, M. Bergoin, J. Virol. 82, 4595–4611 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. A. Garcia-Maruniak, J.E. Maruniak, W. Farmerie, D.G. Boucias, Virology 377, 184–196 (2008)

    Article  CAS  PubMed  Google Scholar 

  14. A.M. Abd-Alla, J.M. Vlak, M. Bergoin, J.E. Maruniak, A.G. Parker, J.P. Burand, J.A. Jehle, D.G. Boucias, Arch. Virol. 154, 909–918 (2009)

    Article  CAS  PubMed  Google Scholar 

  15. G.A. Wu, J.R. Jun, G.E. Sims, S.H. Kim, Proc. Natl. Acad. Sci. USA 106, 12826–12831 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Y. Wang, R.G. Kleespies, M.B. Ramle, J.A. Jehle, J. Virol. Methods 152, 106–108 (2008)

    Article  CAS  PubMed  Google Scholar 

  17. T.A. Jackson, A.M. Crawford, T.R. Glare, J. Invertebr. Pathol. 89, 91–94 (2005)

    Article  PubMed  Google Scholar 

  18. R.L. Tatusov, N.D. Fedorova, J.D. Jackson, A.R. Jacobs, B. Kiryutin, E.V. Koonin, D.M. Krylov, R. Mazumder, S.L. Mekhedov, A.N. Nikolskaya, B.S. Rao, S. Smirnov, A.V. Sverdlov, S. Vasudevan, Y.I. Wolf, J.J. Yin, D.A. Natale, BMC Bioinformatics 4, 41 (2003)

    Article  PubMed Central  PubMed  Google Scholar 

  19. A. Marchler-Bauer, J.B. Anderson, M.K. Derbyshire, C. DeWeese-Scott, N.R. Gonzales, M. Gwadz, L. Hao, S. He, D.I. Hurwitz, J.D. Jackson, Z. Ke, D. Krylov, C.J. Lanczycki, C.A. Liebert, C. Liu, F. Lu, S. Lu, G.H. Marchler, M. Mullokandov, J.S. Song, N. Thanki, R.A. Yamashita, J.J. Yin, D. Zhang, S.H. Bryant, Nucleic Acids Res. 35, D237–D240 (2007)

    Article  CAS  PubMed  Google Scholar 

  20. L.Y. Geer, M. Domrachev, D.J. Lipman, S.H. Bryant, Genome Res. 12, 1619–1623 (2002)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. L.J. McGuffin, D.T. Jones, Bioinformatics 19, 874–881 (2003)

    Article  CAS  PubMed  Google Scholar 

  22. C. Notredame, D.G. Higgins, J. Heringa, J. Mol. Biol. 302, 205–217 (2000)

    Article  CAS  PubMed  Google Scholar 

  23. R.C. Edgar, BMC Bioinformatics 5, 113 (2004)

    Article  PubMed Central  PubMed  Google Scholar 

  24. R. Chenna, H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins, J.D. Thompson, Nucleic Acids Res. 31, 3497–3500 (2003)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. K. Katoh, K. Misawa, K. Kuma, T. Miyata, Nucleic Acids Res. 30, 3059–3066 (2002)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. T. Lassmann, E.E. Sonnhammer, Nucleic Acids Res. 33, 7120–7128 (2005)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. D.A. Theilmann, G.W. Blissard, B. Bonning, J.A. Jehle, D.R. O’Reilly, G.F. Rohrmann, S. Thiem, J.M. Vlak, in Virus Taxonomy: The Eighth Report of the International Committee on Taxonomy of Viruses, ed. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Elsevier Academic Press, New York 2005), pp. 177–185

  28. L.A. Guarino, M.D. Summers, J. Virol. 57, 563–571 (1986)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. C.H. Cheng, S.M. Liu, T.Y. Chow, Y.Y. Hsiao, D.P. Wang, J.J. Huang, H.H. Chen, J. Virol. 76, 9024–9034 (2002)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. L.M. Iyer, S. Balaji, E.V. Koonin, L. Aravind, Virus Res. 117, 156–184 (2006)

    Article  CAS  PubMed  Google Scholar 

  31. M. Fang, Y. Nie, S. Harris, M.A. Erlandson, D.A. Theilmann, J. Virol. 83, 12569–12578 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. T. Ohkawa, J.O. Washburn, R. Sitapara, E. Sid, L.E. Volkman, J. Virol. 79, 15258–15264 (2005)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. W.O. Sparks, R.L. Harrison, B.C. Bonning, Virology 409, 69–76 (2011)

    Article  CAS  PubMed  Google Scholar 

  34. K. Peng, M.M. van Oers, Z. Hu, J.W. van Lent, J.M. Vlak, J. Virol. 84, 9497–9504 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. F. Yang, J. He, X. Lin, Q. Li, D. Pan, X. Zhang, X. Xu, J. Virol. 75, 11811–11820 (2001)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. P. Faulkner, J. Kuzio, G.V. Williams, J.A. Wilson, J. Gen. Virol. 78, 3091–3100 (1997)

    Article  CAS  PubMed  Google Scholar 

  37. S. Gutiérrez, I. Kikhno, M. López Ferber, J. Gen. Virol. 85, 331–341 (2004)

    Article  PubMed  Google Scholar 

  38. S.C. Braunagel, W.K. Russell, G. Rosas-Acosta, D.H. Russell, M.D. Summers, Proc. Natl. Acad. Sci. USA 100, 9797–9802 (2003)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. F. Deng, R. Wang, M. Fang, Y. Jiang, X. Xu, H. Wang, X. Chen, B.M. Arif, L. Guo, Z. Hu, J. Virol. 81, 9377–9385 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. H. Kariithi, I.A. Ince, S. Boeren, J. Vervoort, M. Bergoin, M.M. van Oers, A.M. Abd-Alla, J.M. Vlak, J. Gen. Virol. 91, 3065–3074 (2010)

    Article  CAS  PubMed  Google Scholar 

  41. O.P. Perera, T.B. Green, S.M. Stevens Jr, S. White, J.J. Becnel, J. Virol. 81, 4585–4590 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Z. Li, Q. Lin, J. Chen, J.L. Wu, T.K. Lim, S.S. Loh, X. Tang, C.L. Hew, Mol. Cell Proteomics 6, 1609–1620 (2007)

    Article  CAS  PubMed  Google Scholar 

  43. X. Xie, L. Xu, F. Yang, J. Virol. 80, 10615–10623 (2006)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. L. Li, S. Lin, F. Yang, J. Gen. Virol. 87, 1909–1915 (2006)

    Article  CAS  PubMed  Google Scholar 

  45. D.F. Li, M.C. Zhang, H.J. Yang, Y.B. Zhu, X. Xu, Virology 368, 122–132 (2007)

    Article  CAS  PubMed  Google Scholar 

  46. A. Bézier, M. Annaheim, J. Herbinière, C. Wetterwald, G. Gyapay, S. Bernard-Samain, P. Wincker, I. Roditi, M. Heller, M. Belghazi, R. Pfister-Wilhem, G. Periquet, C. Dupuy, E. Huguet, A.N. Volkoff, B. Lanzrein, J.M. Drezen, Science 323, 926–930 (2009)

    Article  PubMed  Google Scholar 

  47. S. Wyder, F. Blank, B. Lanzrein, J. Insect Physiol. 49, 491–500 (2003)

    Article  CAS  PubMed  Google Scholar 

  48. E.A. Herniou, J.A. Olszewski, J.S. Cory, D.R. O’Reilly, Annu. Rev. Entomol. 48, 211–234 (2003)

    Article  CAS  PubMed  Google Scholar 

  49. H.A. Lauzon, A. Garcia-Maruniak, P.M. Zanotto, J.C. Clemente, E.A. Herniou, C.J. Lucarotti, B.M. Arif, J.E. Maruniak, J. Gen. Virol. 87, 1477–1489 (2006)

    Article  CAS  PubMed  Google Scholar 

  50. O.P. Perera, S.M. Valles, T.B. Green, S. White, C.A. Strong, J.J. Becnel, J. Invertebr. Pathol. 91, 35–42 (2006)

    Article  CAS  PubMed  Google Scholar 

  51. A.M. Huger, A. Krieg, in Atlas of Invertebrate Viruses, ed. by J.R. Adams, J.R. Bonami (CRC Press, Inc., Boca Raton, 1991), pp. 287–319

  52. A.K. Raina, J.R. Adams, B. Lupiani, D.E. Lynn, W. Kim, J.P. Burand, E.M. Dougherty, J. Invertebr. Pathol. 76, 6–12 (2000)

    Article  CAS  PubMed  Google Scholar 

  53. P. Chaivisuthangkura, C. Tawilert, T. Tejangkura, S. Rukpratanporn, S. Longyant, W. Sithigorngul, P. Sithigorngul, Virology 381, 261–267 (2008)

    Article  CAS  PubMed  Google Scholar 

  54. C.M. Long, G.F. Rohrmann, G.F. Merrill, Virology 388, 231–235 (2009)

    Article  CAS  PubMed  Google Scholar 

  55. L.M. Iyer, L. Aravind, E.V. Koonin, J. Virol. 75, 11720–11734 (2001)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. M. Lange, J.A. Jehle, Virology 317, 220–236 (2003)

    Article  CAS  PubMed  Google Scholar 

  57. J.A. Jehle, H. Backhaus, J. Gen. Virol. 75, 1815–1820 (1994)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant of the Deutsche Forschungsgemeinschaft (Je245-7) to J.A.J. M.v.O. was supported by a MEERVOUD grant from the Research Council of Earth and Life Sciences (ALW) with financial aid from the Netherlands Organization for Scientific Research (NWO) (Project 836.05.070). Dwight Lynn is acknowledged for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Laboratory for Biotechnological Crop Protection, Department of Phytopathology, Agricultural Service Center Palatinate (DLR Rheinpfalz), 67435, Neustadt a. d. Weinstrasse, Germany

    Yongjie Wang & Johannes A. Jehle

  2. Laboratory of Marine and Food Microbiology, College of Food Science and Technology, Shanghai Ocean University, Shanghai, China

    Yongjie Wang

  3. AG Systematics and Evolutionary Biology, Faculty V, Institute for Biology and Environmental Sciences (IBU), Carl von Ossietzky University Oldenburg, 26111, Oldenburg, Germany

    Olaf R. P. Bininda-Emonds

  4. Laboratory of Virology, Wageningen University, 6708 PB, Wageningen, The Netherlands

    Monique M. van Oers & Just M. Vlak

  5. Institute for Biological Control, Julius Kuehn Institute, Heinrichstr. 243, 64287, Darmstadt, Germany

    Johannes A. Jehle

Authors
  1. Yongjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olaf R. P. Bininda-Emonds
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Monique M. van Oers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Just M. Vlak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Johannes A. Jehle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes A. Jehle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1802 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Y., Bininda-Emonds, O.R.P., van Oers, M.M. et al. The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes 42, 444–456 (2011). https://doi.org/10.1007/s11262-011-0589-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-011-0589-5

Keywords

Search

Navigation