1887

Abstract

A laboratory culture of was examined to assess covert (latent or persistent) baculovirus infections and spontaneous disease outbreaks. Two nucleopolyhedrovirus (NPV) species were found to be reactivated from a covert state in a laboratory culture of to fully lethal forms. These were identified as multinucleopolyhedrovirus (SeMNPV) and NPV (MbNPV) using restriction enzyme analysis of purified viral DNA. Sequence data derived from both overtly and covertly virus-infected insects revealed highly conserved sequences for , and gene sequence (98–100 % nucleotide identity to SeMNPV published sequence). By monitoring spontaneous overt infections and quantifying viral DNA (by quantitative-PCR) in asymptomatic individuals over two generations we identified fluctuating trends in viral DNA levels from covert SeMNPV and MbNPV within an host population. Virus levels per insect life stage ranged from 3.51±0.101×10 to 0.29±0.036 pg (detection limit at 0.06 pg). Bioassays performed with this culture of larvae showed a differential susceptibility to SeMNPV-like or MbNPV-like viruses, with SeMNPV superinfections being extremely virulent. The data presented has broad implications relating to our understanding of transmission patterns of baculovirus in the environment and the role of covert infections in host–pathogen interaction dynamics.

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2011-05-01
2019-10-20
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References

  1. Abul-Nasr S. E. , Ammar E. D. , Abul-Ela S. M. . ( 1979; ). Effects of nuclear polyhedrosis virus on various developmental stages of the cotton leafworm Spodoptera littoralis. . J Appl Entomol 88:, 181–187.
    [Google Scholar]
  2. Anderson R. M. , May R. M. . ( 1981; ). The population dynamics of microparasites and their invertebrate hosts. . Philos Trans R Soc Lond B Biol Sci 291:, 451–524. [CrossRef]
    [Google Scholar]
  3. Andrealis T. G. . ( 1987; ). Transmission. . In Epizootiology of Insect Disease, pp. 159–176. Edited by Fuxa J. R. , Tanada Y. . . New York:: Wiley;.
    [Google Scholar]
  4. Brun G. , Plus N. . ( 1980; ). The viruses of Drosophila . . In The Genetics and Biology of Drosophila, pp. 625–702. Edited by Ashburner M. , Wright T. R. F. . . New York:: Academic Press;.
    [Google Scholar]
  5. Burden J. P. , Griffiths C. M. , Cory J. S. , Smith P. , Sait S. M. . ( 2002; ). Vertical transmission of sublethal granulovirus infection in the Indian meal moth, Plodia interpunctella. . Mol Ecol 11:, 547–555. [CrossRef] [PubMed]
    [Google Scholar]
  6. Burden J. P. , Nixon C. P. , Hodgkinson A. E. , Possee R. D. , Sait S. M. , King L. A. , Hails R. S. . ( 2003; ). Covert infections as a mechanism for long-term persistence of baculoviruses. . Ecol Lett 6:, 524–531. [CrossRef]
    [Google Scholar]
  7. Burden J. P. , Possee R. D. , Sait S. M. , King L. A. , Hails R. S. . ( 2006; ). Phenotypic and genotypic characterisation of persistent baculovirus infections in populations of the cabbage moth (Mamestra brassicae) within the British Isles. . Arch Virol 151:, 635–649. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cooper D. , Cory J. S. , Theilmann D. A. , Myers J. H. . ( 2003; ). Nucleopolyhedroviruses of forest and western tent caterpillars: cross-infectivity and evidence for activation of latent virus in high-density field populations. . Ecol Entomol 28:, 41–50. [CrossRef]
    [Google Scholar]
  9. Cory J. S. , Myers J. H. . ( 2003; ). The ecology and evolution of insect baculoviruses. . Annu Rev Ecol Evol Syst 34:, 239–272. [CrossRef]
    [Google Scholar]
  10. Farrar R. R. , Ridgway R. L. . ( 1998; ). Quantifying time-mortality relationship for nuclear polyhedrosis viruses when survivors are present. . Environ Entomol 27:, 1289–1296.[CrossRef]
    [Google Scholar]
  11. Fuxa J. R. , Richter A. R. . ( 1991; ). Selection for an increased rate of vertical transmission of Spodoptera frugiperda (Lepidoptera: Noctuidae) nuclear polyhedrosis virus. . Environ Entomol 20:, 603–609.[CrossRef]
    [Google Scholar]
  12. Fuxa J. R. , Richter A. R. . ( 1999; ). Classical biological control in an ephemeral habitat with Anticarsia gemmatalis nucleopolyhedrovirus. . BioControl 44:, 405–419. [CrossRef]
    [Google Scholar]
  13. Fuxa J. R. , Weidner E. H. , Richter A. R. . ( 1992; ). Polyhedra without virions in a vertically transmitted nuclear polyhedrosis virus. . J Invertebr Pathol 60:, 53–58. [CrossRef]
    [Google Scholar]
  14. Fuxa J. R. , Sun J. Z. , Weidner E. H. , LaMotte L. R. . ( 1999; ). Stressors and rearing diseases of Trichoplusia ni: evidence of vertical transmission of NPV and CPV. . J Invertebr Pathol 74:, 149–155. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hitchman, R. B. (2002). Pathogen dynamics and variation in insect populations. PhD thesis, Oxford Brookes University, Oxford, UK.
  16. Hughes P. R. , Wood H. A. . ( 1981; ). A synchronous peroral technique for the bioassay of insect viruses. . J Invertebr Pathol 37:, 154–159. [CrossRef]
    [Google Scholar]
  17. Hughes D. S. , Possee R. D. , King L. A. . ( 1993; ). Activation and detection of a latent baculovirus resembling Mamestra brassicae nuclear polyhedrosis virus in M. brassicae insects. . Virology 194:, 608–615. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hughes D. S. , Possee R. D. , King L. A. . ( 1997; ). Evidence for the presence of a low-level, persistent baculovirus infection of Mamestra brassicae insects. . J Gen Virol 78:, 1801–1805.[PubMed]
    [Google Scholar]
  19. Hunter-Fujita F. R. , Entwistle P. F. , Evans H. F. , Crook N. E. . (editors) ( 1998; ). Insect Viruses and Pest Management. Chichester, UK:: John Wiley;.
    [Google Scholar]
  20. Jehle J. A. , Lange M. , Wang H. , Hu Z. , Wang Y. , Hauschild R. . ( 2006; ). Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. . Virology 346:, 180–193. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kane M. , Golovkina T. . ( 2010; ). Common threads in persistent viral infections. . J Virol 84:, 4116–4123. [CrossRef] [PubMed]
    [Google Scholar]
  22. Karpov A. E. . ( 1979; ). Latency of baculoviruses and its practical significance. . Mol Biol 22:, 74–83.
    [Google Scholar]
  23. Khurad A. M. , Mahulikar A. , Rathod M. K. , Rai M. M. , Kanginakudru S. , Nagaraju J. . ( 2004; ). Vertical transmission of nucleopolyhedrovirus in the silkworm, Bombyx mori L. . J Invertebr Pathol 87:, 8–15. [CrossRef] [PubMed]
    [Google Scholar]
  24. King L. A. , Possee R. D. . ( 1992; ). The Baculovirus Expression System. A Laboratory Guide. London:: Chapman & Hall;.[CrossRef]
    [Google Scholar]
  25. Kouassi L. N. , Tsuda K. , Goto C. , Mukawa S. , Sakamaki Y. , Kusigemati K. , Nakamura M. . ( 2009; ). Prevalence of latent virus in Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) and its activation by a heterologous virus. . Appl Entomol Zool (Jpn) 44:, 95–102. [CrossRef]
    [Google Scholar]
  26. Kukan B. . ( 1999; ). Vertical transmission of nucleopolyhedrovirus in insects. . J Invertebr Pathol 74:, 103–111. [CrossRef] [PubMed]
    [Google Scholar]
  27. L’Heritier P. . ( 1970; ). Drosophila viruses and their role as evolutionary factors. . Evol Biol 4:, 185–209.
    [Google Scholar]
  28. Longworth J. F. , Cunningham J. C. . ( 1968; ). The activation of occult nuclear-polyhedrosis viruses by foreign nuclear polyhedra. . J Invertebr Pathol 10:, 361–367. [CrossRef]
    [Google Scholar]
  29. Murillo R. , Elvira S. , Munoz D. , Williams T. , Caballero P. . ( 2006; ). Genetic and phenotypic variability in Spodoptera exigua nucleopolyhedrovirus isolates from greenhouse soils in southern Spain. . Biol Control 38:, 157–165. [CrossRef]
    [Google Scholar]
  30. Murillo R. , Muñoz D. , Ruiz-Portero M. C. , Alcázar M. D. , Belda J. E. , Williams T. , Caballero P. . ( 2007; ). Abundance and genetic structure of nucleopolyhedrovirus populations in greenhouse substrate reservoirs. . Biol Control 42:, 216–225. [CrossRef]
    [Google Scholar]
  31. Myers J. H. , Malakar R. , Cory J. S. . ( 2000; ). Sublethal nucleoplyhedrosis infection effects on female pupal weight, egg mass size, and vertical transmission in gypsy moth (Lepidoptera: Lymantriidae). . Environ Entomol 29:, 1268–1272. [CrossRef]
    [Google Scholar]
  32. Pijlman G. P. , Dortmans J. C. , Vermeesch A. M. , Yang K. , Martens D. E. , Goldbach R. W. , Vlak J. M. . ( 2002; ). Pivotal role of the non-hr origin of DNA replication in the genesis of defective interfering baculoviruses. . J Virol 76:, 5605–5611. [CrossRef] [PubMed]
    [Google Scholar]
  33. Pijlman G. P. , van Schijndel J. E. , Vlak J. M. . ( 2003; ). Spontaneous excision of BAC vector sequences from bacmid-derived baculovirus expression vectors upon passage in insect cells. . J Gen Virol 84:, 2669–2678. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rothman L. D. , Myers J. M. . ( 1996; ). Debilitating effects of viral diseases on host Lepidoptera. . J Invertebr Pathol 67:, 1–10. [CrossRef]
    [Google Scholar]
  35. Simón O. , Williams T. , Caballero P. , Possee R. D. . ( 2008; ). Effects of Acp26 on in vitro and in vivo productivity, pathogenesis and virulence of Autographa californica multiple nucleopolyhedrovirus. . Virus Res 136:, 202–205. [CrossRef] [PubMed]
    [Google Scholar]
  36. Smits P. H. , Vlak J. M. . ( 1988; ). Biological activity of Spodoptera exigua nuclear polyhedrosis virus against S. exigua larvae. . J Invertebr Pathol 51:, 107–114. [CrossRef]
    [Google Scholar]
  37. Sorrell I. , White A. , Pedersen A. B. , Hails R. S. , Boots M. . ( 2009; ). The evolution of covert, silent infection as a parasite strategy. . Proc Biol Sci 276:, 2217–2226. [CrossRef] [PubMed]
    [Google Scholar]
  38. Staden R. , Judge D. P. , Bonfield J. K. . ( 2003; ). Sequence assembly and finishing method. . In Bioinformatics, a Practical Guide to the Analysis of Genes and Proteins, pp. 303–322. Edited by Baxevanis A. D. , Ouellette B. F. F. . . New York:: John Wiley & Sons;.
    [Google Scholar]
  39. Steinhaus E. A. . ( 1958; ). Crowding as a possible stress factor in insect disease. . Ecol 39:, 503–514. [CrossRef]
    [Google Scholar]
  40. Swaine G. . ( 1966; ). Generation-to-generation passage of the nuclear polyhedral virus of Spodoptera exempta (Wlk.). . Nature 210:, 1053–1054. [CrossRef] [PubMed]
    [Google Scholar]
  41. Thompson J. D. , Gibson T. J. , Plewniak F. , Jeanmougin F. , Higgins D. G. . ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. . Nucleic Acids Res 25:, 4876–4882. [CrossRef] [PubMed]
    [Google Scholar]
  42. Vilaplana L. , Redman E. M. , Wilson K. , Cory J. S. . ( 2008; ). Density-related variation in vertical transmission of a virus in the African armyworm. . Oecologia 155:, 237–246. [CrossRef] [PubMed]
    [Google Scholar]
  43. Vilaplana L. , Wilson K. , Redman E. M. , Cory J. S. . ( 2010; ). Pathogen persistence in migratory insects: high levels of vertically-transmitted virus infection in field populations of the African armyworm. . Evol Ecol 24:, 147–160. [CrossRef]
    [Google Scholar]
  44. Wang J.-H. , Valanne S. , Rämet M. . ( 2010; ). Drosophila as a model for antiviral immunity. . World J Biol Chem 1:, 151–159. [CrossRef]
    [Google Scholar]
  45. Yampolsky L. Y. , Webb C. T. , Shabalina S. A. , Kondrashov A. S. . ( 1999; ). Rapid accumulation of a vertically transmitted parasite triggered by relaxation of natural selection among hosts. . Evol Ecol Res 1:, 581–589.
    [Google Scholar]
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Supplements

vol. , part 5, pp. 1061 - 1070

q-PCR positive individuals for breeding lines and the developmental stage tested ( =10)

Breeding lines schedule and NPV mortality records

SeMNPV intergenic region sequence generated by PCR from either covertly (Cx) or overtly (Ox) infected insects [Single PDF file](110 KB)



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