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Volume 98, Issue 2

Midgut-based resistance to oral infection by a nucleopolyhedrovirus in the laboratory-selected strain of the smaller tea tortrix, (Lepidoptera: Tortricidae) Free

Abstract

A strain of resistant to Adoxophyes honmai nucleopolyhedrovirus (AdhoNPV) was established from a field-collected colony by repeated selection. Fifth-instar larvae of this resistant strain (R-strain) had over 66 666-fold greater resistance in terms of 50 % lethal concentration values to oral infection of AdhoNPV than non-selected strain larvae (susceptible for AdhoNPV; S2-strain). In this study, the mechanism of resistance to AdhoNPV was determined in R-strain larvae. An assessment of viral genome replication in AdhoNPV-infected S2- and R-strain larvae by quantitative PCR showed no viral genome replication occurring in R-strain larvae. Transcription of AdhoNPV , and genes was also not detected in R-strain midgut cells. Besides, a fluorescent brightener had no effect on AdhoNPV infection in either S2- or R-strain. However, binding and fusion of occlusion-derived virus with R-strain were significantly lower than those of S2-strain. These findings suggest that R-strain larvae possess a midgut-based resistance to oral infection by AdhoNPV in which midgut epithelial cells are infected less efficiently.

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Keyword(s): Adoxophyes honmai , baculovirus , midgut , nucleopolyhedrovirus and resistance
© 2017 The Authors
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2017-02-01
2024-04-25
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References

  1. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA et al. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 2006; 151:1257–1266 [View Article][PubMed]
     [Google Scholar]
  2. Harrison RL, Hoover K. Baculovirus and other occluded insect viruses. In Vega FE, Kaya HK. (editors) Insect Pathology, 2nd ed. London, UK: Academic Press; 2012 pp. 73–131 [CrossRef]
     [Google Scholar]
  3. Briese DT, Mende HA. Selection for increased resistance to a granulosis virus in the potato moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Bull Entomol Res 1983; 73:1–9 [View Article]
     [Google Scholar]
  4. Boots M, Begon M. Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct Ecol 1993; 7:528–534 [CrossRef]
     [Google Scholar]
  5. Fuxa JR, Mitchell FL, Richter AR. Resistance of Spodoptera frugiperda [Lep.: Noctuidae] to a nuclear polyhedrosis virus in the field and laboratory. Entomophaga 1988; 33:55–63 [CrossRef]
     [Google Scholar]
  6. Abot AR, Moscardi F, Fuxa JR, Sosa-Gómez DR, Richter AR. Development of resistance by Anticarsia gemmatalis from Brazil and the United States to a nuclear polyhedrosis virus under laboratory selection pressure. Biol Control 1996; 7:126–130 [CrossRef]
     [Google Scholar]
  7. Milks ML, Myers JH. The development of larval resistance to a nucleopolyhedrovirus is not accompanied by an increased virulence in the virus. Evol Ecol 2000; 14:645–664 [CrossRef]
     [Google Scholar]
  8. Milks ML, Theilmann DA. Serial selection for resistance to a wild-type and to a genetically modified nucleopolyhedrovirus in Trichoplusia ni. Biol Control 2000; 19:283–289 [CrossRef]
     [Google Scholar]
  9. Asser-Kaiser S, Fritsch E, Undorf-Spahn K, Kienzle J, Eberle KE et al. Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science 2007; 317:1916–1918 [View Article][PubMed]
     [Google Scholar]
  10. Berling M, Blachere-Lopez C, Soubabere O, Lery X, Bonhomme A et al. Cydia pomonella granulovirus genotypes overcome virus resistance in the codling moth and improve virus efficiency by selection against resistant hosts. Appl Environ Microbiol 2009; 75:925–930 [View Article][PubMed]
     [Google Scholar]
  11. Zichová T, Stará J, Kundu JK, Eberle KE, Jehle JA. Resistance to Cydia pomonella granulovirus follows a geographically widely distributed inheritance type within Europe. BioControl 2013; 58:525–534 [CrossRef]
     [Google Scholar]
  12. Asser-Kaiser S, Heckel DG, Jehle JA. Sex linkage of CpGV resistance in a heterogeneous field strain of the codling moth Cydia pomonella (L.). J Invertebr Pathol 2010; 103:59–64 [View Article][PubMed]
     [Google Scholar]
  13. Berling M, Sauphanor B, Bonhomme A, Siegwart M, Lopez-Ferber M. A single sex-linked dominant gene does not fully explain the codling moth's resistance to granulovirus. Pest Manag Sci 2013; 69:1261–1266 [View Article][PubMed]
     [Google Scholar]
  14. Uchiyama T, Ozawa A. Rapid development of resistance to diamide insecticides in the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae), in the tea fields of Shizuoka Prefecture, Japan. Appl Entomol Zool 2014; 49:529–534 [CrossRef]
     [Google Scholar]
  15. Mochizuki F, Fukumoto T, Noguchi H, Sugie H, Morimoto T et al. Resistance to a mating disruptant composed of (Z)-11-tetradecenyl acetate in the smaller tea tortrix, Adoxophyes honmai (Yasuda) (Lepidoptera: Tortricidae). Appl Entomol Zool 2002; 37:299–304 [CrossRef]
     [Google Scholar]
  16. Guarino LA, Summers MD. Nucleotide sequence and temporal expression of a baculovirus regulatory gene. J Virol 1987; 61:2091–2099[PubMed]
     [Google Scholar]
  17. Boucias DG, Pendland JC. Principles of Insect Pathology Boston, MA: Kluwer Academic Publishers; 1998 p 537 [CrossRef]
     [Google Scholar]
  18. Hoekstra D, de Boer T, Klappe K, Wilschut J. Fluorescence method for measuring the kinetics of fusion between biological membranes. Biochemistry 1984; 23:5675–5681[PubMed] [CrossRef]
     [Google Scholar]
  19. Horton HM, Burand JP. Saturable attachment sites for polyhedron-derived baculovirus on insect cells and evidence for entry via direct membrane fusion. J Virol 1993; 67:1860–1868[PubMed]
     [Google Scholar]
  20. Haas-Stapleton EJ, Washburn JO, Volkman LE. P74 mediates specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to primary cellular targets in the midgut epithelia of Heliothis virescens larvae. J Virol 2004; 78:6786–6791 [View Article][PubMed]
     [Google Scholar]
  21. Ohkawa T, Washburn JO, Sitapara R, Sid E, Volkman LE. Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of pif genes Ac119 and Ac022 but not by Ac115. J Virol 2005; 79:15258–15264 [View Article][PubMed]
     [Google Scholar]
  22. Sparks WO, Harrison RL, Bonning BC. Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. Virology 2011; 409:69–76 [View Article][PubMed]
     [Google Scholar]
  23. Haas-Stapleton EJ, Washburn JO, Volkman LE. Spodoptera frugiperda resistance to oral infection by Autographa californica multiple nucleopolyhedrovirus linked to aberrant occlusion-derived virus binding in the midgut. J Gen Virol 2005; 86:1349–1355 [View Article][PubMed]
     [Google Scholar]
  24. Chikhalya A, Luu DD, Carrera M, De La Cruz A, Torres M et al. Pathogenesis of Autographa californica multiple nucleopolyhedrovirus in fifth-instar Anticarsia gemmatalis larvae. J Gen Virol 2009; 90:2023–2032 [View Article][PubMed]
     [Google Scholar]
  25. Ikeda M, Yamada H, Hamajima R, Kobayashi M. Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells. Virology 2013; 435:1–13 [View Article][PubMed]
     [Google Scholar]
  26. Nakai M, Goto C, Kang W, Shikata M, Luque T et al. Genome sequence and organization of a nucleopolyhedrovirus isolated from the smaller tea tortrix, Adoxophyes honmai. Virology 2003; 316:171–183[PubMed] [CrossRef]
     [Google Scholar]
  27. Katou Y, Ikeda M, Kobayashi M. Abortive replication of Bombyx mori nucleopolyhedrovirus in Sf9 and high five cells: defective nuclear transport of the virions. Virology 2006; 347:455–465 [View Article][PubMed]
     [Google Scholar]
  28. Hamajima R, Ito Y, Ichikawa H, Mitsutake H, Kobayashi J et al. Degradation of rRNA in BM-N cells from the silkworm Bombyx mori during abortive infection with heterologous nucleopolyhedroviruses. J Gen Virol 2013; 94:2102–2111 [View Article][PubMed]
     [Google Scholar]
  29. Jayachandran B, Hussain M, Asgari S. RNA interference as a cellular defense mechanism against the DNA virus baculovirus. J Virol 2012; 86:13729–13734 [View Article][PubMed]
     [Google Scholar]
  30. Kanginakudru S, Royer C, Edupalli SV, Jalabert A, Mauchamp B et al. Targeting ie-1 gene by RNAi induces baculoviral resistance in lepidopteran cell lines and in transgenic silkworms. Insect Mol Biol 2007; 16:635–644 [View Article][PubMed]
     [Google Scholar]
  31. Levy SM, Falleiros AM, Moscardi F, Gregório EA. Susceptibility/resistance of Anticarsia gemmatalis larvae to its nucleopolyhedrovirus (AgMNPV): structural study of the peritrophic membrane. J Invertebr Pathol 2007; 96:183–186 [View Article][PubMed]
     [Google Scholar]
  32. Levy SM, Falleiros AM, Moscardi F, Gregório EA. The role of peritrophic membrane in the resistance of Anticarsia gemmatalis larvae (Lepidoptera: Noctuidae) during the infection by its nucleopolyhedrovirus (AgMNPV). Arthropod Struct Dev 2011; 40:429–434 [View Article][PubMed]
     [Google Scholar]
  33. Wang P, Granados RR. Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J Invertebr Pathol 1998; 72:57–62 [View Article][PubMed]
     [Google Scholar]
  34. Mukawa S, Nakai M, Okuno S, Takatsuka J, Kunimi Y. Nucleopolyhedrovirus enhancement by a fluorescent brightener in Mythimna separata (Lepidoptera: Noctuidae). Appl Entomol Zool 2003; 38:87–96 [CrossRef]
     [Google Scholar]
  35. Okuno S, Takatsuka J, Nakai M, Ototake S, Masui A et al. Viral-enhancing activity of various stilbene-derived brighteners for a Spodoptera litura (Lepidoptera: Noctuidae) nucleopolyhedrovirus. Biol Control 2003; 26:146–152 [CrossRef]
     [Google Scholar]
  36. Wang P, Granados RR. Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 2000; 30:135–143[PubMed] [CrossRef]
     [Google Scholar]
  37. Morales L, Moscardi F, Sosa-Gómez DR, Paro FE, Soldorio IL. Fluorescent brighteners improve Anticarsia gemmatalis (Lepidoptera: Noctuidae) nucleopolyhedrovirus (AgMNPV) activity on AgMNPV-susceptible and resistant strains of the insect. Biol Control 2001; 20:247–253 [CrossRef]
     [Google Scholar]
  38. El-Salamouny S. Observations on the peritrophic membrane of tortricid and noctuid insects and its role in susceptibility and enhancement. J Agric Urban Entomol 2007; 24:195–204 [CrossRef]
     [Google Scholar]
  39. Cheng Y, Wang XY, du C, Gao J, Xu JP. Expression analysis of several antiviral related genes to BmNPV in different resistant strains of silkworm, Bombyx mori. J Insect Sci 2014; 14:76 [View Article][PubMed]
     [Google Scholar]
  40. Ponnuvel KM, Nakazawa H, Furukawa S, Asaoka A, Ishibashi J et al. A lipase isolated from the silkworm Bombyx mori shows antiviral activity against nucleopolyhedrovirus. J Virol 2003; 77:10725–10729 [View Article][PubMed]
     [Google Scholar]
  41. Nakazawa H, Tsuneishi E, Ponnuvel KM, Furukawa S, Asaoka A et al. Antiviral activity of a serine protease from the digestive juice of Bombyx mori larvae against nucleopolyhedrovirus. Virology 2004; 321:154–162 [View Article][PubMed]
     [Google Scholar]
  42. Jiang L, Wang G, Cheng T, Yang Q, Jin S et al. Resistance to Bombyx mori nucleopolyhedrovirus via overexpression of an endogenous antiviral gene in transgenic silkworms. Arch Virol 2012; 157:1323–1328 [View Article][PubMed]
     [Google Scholar]
  43. Asser-Kaiser S, Radtke P, El-Salamouny S, Winstanley D, Jehle JA. Baculovirus resistance in codling moth (Cydia pomonella L.) caused by early block of virus replication. Virology 2011; 410:360–367 [View Article][PubMed]
     [Google Scholar]
  44. Ishii T, Nakai M, Okuno S, Takatsuka J, Kunimi Y. Characterization of Adoxophyes honmai single-nucleocapsid nucleopolyhedrovirus: morphology, structure, and effects on larvae. J Invertebr Pathol 2003; 83:206–214[PubMed] [CrossRef]
     [Google Scholar]
  45. Russell RM, Robertson JL, Savin NE. POLO: a new computer program for probit analysis. Bull Entomol Soc Amer 1977; 23:209–213 [CrossRef]
     [Google Scholar]
  46. Nussbaum O, Loyter A. Quantitative determination of virus-membrane fusion events. Fusion of influenza virions with plasma membranes and membranes of endocytic vesicles in living cultured cells. FEBS Lett 1987; 221:61–67 [View Article][PubMed]
     [Google Scholar]
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Midgut-based resistance to oral infection by a nucleopolyhedrovirus in the laboratory-selected strain of the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae)
J. Gen. Virol. 98, 296 (2017); https://doi.org/10.1099/jgv.0.000684
/content/journal/jgv/10.1099/jgv.0.000684
/content/journal/jgv/10.1099/jgv.0.000684
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