1887

Abstract

The family is a recently described virus family whose members are transmitted by parasitoids and cause chronic and lethal infections in lepidopteran insects. Little is known about the biology and ecology of ascoviruses, and few isolates have been found outside the United States. We report here the isolation of a new ascovirus variant from in Japan. Full genome sequence and phylogenetic analyses showed that this virus was closely related to variants in , and it was named HvAV-3j. HvAV-3j has a DNA genome of 191 718 bp, with 189 putative ORFs and a GC content of 45.6 %, and is highly similar to HvAV-3h, which was isolated in China. In a field survey, the endoparasitoid caused a high percentage of parasitization in populations of larvae, and under laboratory conditions was able to transmit HvAV-3j from infected to uninfected larvae by oviposition. is thus likely to be a major vector for HvAV-3j transmission in Japan. This species is recognized here for the first time as a vector of ascoviruses that parasitizes a range of host species that extends across families.

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2018-04-01
2020-01-18
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References

  1. Jones RA. Using epidemiological information to develop effective integrated virus disease management strategies. Virus Res 2004;100:5–30 [CrossRef][PubMed]
    [Google Scholar]
  2. Mackenzie JS, Jeggo M. Reservoirs and vectors of emerging viruses. Curr Opin Virol 2013;3:170–179 [CrossRef][PubMed]
    [Google Scholar]
  3. Federici BA. Enveloped double-stranded DNA insect virus with novel structure and cytopathology. Proc Natl Acad Sci USA 1983;80:7664–7668 [CrossRef][PubMed]
    [Google Scholar]
  4. Federici BA, Bideshi DK, Tan Y, Spears T, Bigot Y. Ascoviruses: superb manipulators of apoptosis for viral replication and transmission. Curr Top Microbiol Immunol 2009;328:171–196
    [Google Scholar]
  5. Bigot Y, Asgari S, Bideshi DK, Cheng XW, Federici BA et al. Family Ascoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. I Amsterdam, the Netherlands: Elsevier; 2012; pp.147–152
    [Google Scholar]
  6. Asgari S, Bideshi DK, Bigot Y, Federici BA, Cheng XW et al. ICTV virus taxonomy profile: Ascoviridae. J Gen Virol 2017;98:4–5 [CrossRef][PubMed]
    [Google Scholar]
  7. Federici BA. A new type of insect pathogen in larvae of the clover cutworm, Scotogramma trifolii. J Invertebr Pathol 1982;40:41–54 [CrossRef]
    [Google Scholar]
  8. Cheng XW, Carner GR, Arif BM. A new ascovirus from Spodoptera exigua and its relatedness to the isolate from Spodoptera frugiperda. J Gen Virol 2000;81:3083–3092 [CrossRef][PubMed]
    [Google Scholar]
  9. Asgari S, Davis J, Wood D, Wilson P, McGrath A. Sequence and organization of the Heliothis virescens ascovirus genome. J Gen Virol 2007;88:1120–1132 [CrossRef][PubMed]
    [Google Scholar]
  10. Huang GH, Garretson TA, Cheng XH, Holztrager MS, Li SJ et al. Phylogenetic position and replication kinetics of Heliothis virescens ascovirus 3h (HvAV-3h) isolated from Spodoptera exigua. PLoS One 2012;7:e40225 [CrossRef][PubMed]
    [Google Scholar]
  11. Huang GH, Hou DH, Wang M, Cheng XW, Hu Z. Genome analysis of Heliothis virescens ascovirus 3h isolated from China. Virol Sin 2017;32:147–154 [CrossRef][PubMed]
    [Google Scholar]
  12. Bigot Y, Rabouille A, Sizaret PY, Hamelin MH, Periquet G. Particle and genomic characteristics of a new member of the Ascoviridae: Diadromus pulchellus ascovirus. J Gen Virol 1997;78:1139–1147 [CrossRef][PubMed]
    [Google Scholar]
  13. Huang GH, Wang YS, Wang X, Garretson TA, Dai LY et al. Genomic sequence of Heliothis virescens ascovirus 3g isolated from Spodoptera exigua. J Virol 2012;86:12467–12468 [CrossRef][PubMed]
    [Google Scholar]
  14. Bideshi DK, Demattei MV, Rouleux-Bonnin F, Stasiak K, Tan Y et al. Genomic sequence of Spodoptera frugiperda ascovirus 1a, an enveloped, double-stranded DNA insect virus that manipulates apoptosis for viral reproduction. J Virol 2006;80:11791–11805 [CrossRef][PubMed]
    [Google Scholar]
  15. Wang L, Xue J, Seaborn CP, Arif BM, Cheng XW. Sequence and organization of the Trichoplusia ni ascovirus 2c (Ascoviridae) genome. Virology 2006;354:167–177 [CrossRef][PubMed]
    [Google Scholar]
  16. Bideshi DK, Renault S, Stasiak K, Federici BA, Bigot Y. Phylogenetic analysis and possible function of bro-like genes, a multigene family widespread among large double-stranded DNA viruses of invertebrates and bacteria. J Gen Virol 2003;84:2531–2544 [CrossRef][PubMed]
    [Google Scholar]
  17. Li SJ, Wang X, Zhou ZS, Zhu J, Zhao YP et al. A comparison of growth and development of three major agricultural insect pests infected with Heliothis virescens ascovirus 3h (HvAV-3h). PLoS One 2013;8:1–12
    [Google Scholar]
  18. Hamm JJ, Pair SD, Marti OG. Incidence and host range of a new ascovirus isolated from fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Fla Entomol 1986;69:524–531 [CrossRef]
    [Google Scholar]
  19. Cheng XW, Wang L, Carner GR, Arif BM. Characterization of three ascovirus isolates from cotton insects. J Invertebr Pathol 2005;89:193–202 [CrossRef][PubMed]
    [Google Scholar]
  20. Tillman PG, Styer EL, Hamm JJ. Transmission of ascovirus from Heliothis virescens (Lepidoptera: Noctuidae) by three parasitoids and effects of virus on survival of parasitoid Cardiochiles nigriceps (Hymenoptera: Braconidae). Environ Entomol 2004;33:633–643 [CrossRef]
    [Google Scholar]
  21. Li SJ, Hopkins RJ, Zhao YP, Zhang YX, Hu J et al. Imperfection works: Survival, transmission and persistence in the system of Heliothis virescens ascovirus 3h (HvAV-3h), Microplitis similis and Spodoptera exigua. Sci Rep 2016;6:21296 [CrossRef][PubMed]
    [Google Scholar]
  22. Hamm JJ, Nordlung DA, Marti OG. Effects of a nonoccluded virus of Spodoptera frugiperda (Lepidoptera: Noctuidae) on the development of a parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae). Environ Entomol 1985;14:258–261 [CrossRef]
    [Google Scholar]
  23. Newton I. The biology and characterisation of the ascoviruses (Ascoviridae: Ascovirus) of Helicoverpa armigera Hubner and Helicoverpa punctigera Wallengren (Lepidoptera: Noctuidae) in Australia. PhD Thesis, The University of Queensland 2004
  24. Murphy N, Banks JC, Whitfield JB, Austin AD. Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol 2008;47:378–395 [CrossRef][PubMed]
    [Google Scholar]
  25. Sharanowski BJ, Dowling APG, Sharkey MJ. Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Syst Entomol 2011;36:549–572 [CrossRef]
    [Google Scholar]
  26. Maeto K. Systematic studies on the tribe Meteorini (Hymenoptera, Braconidae) from Japan : V. The pulchricornis group of the genus Meteorus (1). Japanese J Entomol 1989;57:581–595
    [Google Scholar]
  27. Matsuura H, Naito A. Studies on the cold-hardiness and overwintering of Spodoptera litura F. (Lepidoptera: Noctuidae) : VI. Possible overwingering areas predicted from meteorological data in Japan. Appl Entomol Zool 1997;32:167–177 [CrossRef]
    [Google Scholar]
  28. Li SJ, Huang JP, Chang YY, Quan SY, Yi WT et al. Development of Microplitis similis (Hymenoptera: Braconidae) on two candidate host species, Spodoptera litura and Spodoptera exigua (Lepidoptera: Noctuidae). Fla Entomol 2015;98:736–741[Crossref]
    [Google Scholar]
  29. Harvey JA, Visser B, Lann CL, de Boer J, Ellers J et al. Convergence and divergence in direct and indirect life-history traits of closely related parasitoids (Braconidae: Microgastrinae). Evol Biol 2014;41:134–144 [CrossRef]
    [Google Scholar]
  30. Zheng XL, Wang P, Cheng WJ, Wang XP, Lei CL. Projecting overwintering regions of the beet armyworm, Spodoptera exigua in China using the CLIMEX model. J Insect Sci 2012;12:1–13 [CrossRef][PubMed]
    [Google Scholar]
  31. Pompon J, Morales-Vargas R, Manuel M, Huat Tan C, Vial T et al. A Zika virus from America is more efficiently transmitted than an Asian virus by Aedes aegypti mosquitoes from Asia. Sci Rep 2017;7:1215 doi:10.1038/S41598-017-01282-6 [CrossRef][PubMed]
    [Google Scholar]
  32. Williams T. Ecology of invertebrate pathogens: viruses. In Hajek AE, Shapiro-Ilan DI. (editors) Ecology of Invertebrate Diseases Wiley; 2017; pp.213–285[Crossref]
    [Google Scholar]
  33. Azam A, Kunimi Y, Inoue MN, Nakai M. Effect of granulovirus infection of Spodoptera litura (Lepidoptera: Noctuidae) larvae on development of the endoparasitoid Chelonus inanitus (Hymenoptera: Braconidae). Appl Entomol Zool 2016;51:479–488 [CrossRef]
    [Google Scholar]
  34. Nguyen DH, Nakai M, Takatsuka J, Okuno S, Ishii T et al. Interaction between a nucleopolyhedrovirus and the braconid parasitoid Meteorus pulchricornis (Hymenoptera: Braconidae) in the larvae of Spodoptera litura (Lepidoptera: Noctuidae). Appl Entomol Zool 2005;40:325–334 [CrossRef]
    [Google Scholar]
  35. Williams RC, Backus RC. Macromolecular weights determined by particle counting. J Am Chem Soc 1949;71:4052–4057[Crossref]
    [Google Scholar]
  36. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008;18:821–829 [CrossRef][PubMed]
    [Google Scholar]
  37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/Map format and SAMtools. Bioinformatics 2009;25:2078–2079 [CrossRef][PubMed]
    [Google Scholar]
  38. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011;27:2987–2993 [CrossRef][PubMed]
    [Google Scholar]
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