1887

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Volume 101, Issue 6

A novel cypovirus found in a betabaculovirus co-infection context contains a poxvirus immune nuclease (poxin)-related gene Free

Abstract

The cassava hornworm (Lepidoptera: Sphingidae) is an important pest in Brazil. This insect feeds on host plants of several species, especially (cassava) and (rubber tree). Cassava hornworm outbreaks are quite common in Brazil and can cause great impact over crop production. Granulare and polyhedral-shaped occlusion bodies (OBs) were observed in extracts of dead larvae from rubber-tree plantations by light and scanning electron microscopy (SEM), suggesting a mixed infection. The polyhedral-shaped OB surface revealed indentations that resemble those found in cypovirus polyhedra. After OB nucleic acid extraction followed by cDNA production and Illumina deep-sequencing analysis, the results confirmed for the presence of a putative novel cypovirus that carries ten segments and also a betabaculovirus (Erinnyis ello granulovirus, ErelGV). Phylogenetic analysis of the predicted segment 1-enconded RdRP showed that the new cypovirus isolate is closely related to a member of species , which was isolated from (Lepidoptera: Nymphalidae). Therefore, we named this new isolate Erinnyis ello cypovirus 2 (ErelCPV-2). Genome analyses showed that ErelCPV-2 segment 8 (S8) has a predicted amino acid identity of 35.82 % to a hypothetical protein of betabaculoviruses. This putative protein has a cGAMP-specific nuclease domain related to the poxvirus immune nucleases (poxins) from the 2′,3′-cGAMP-degrading enzyme family.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): 3'-cGAMP-degrading enzyme , betabaculo virus , Cypovirus , genomic convergence , horizontal gene transfer; 2' and mixed infection
Funding
This study was supported by the:
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 305756/2017-6)
    • Principle Award Recipient: Bergmann Morais Ribeiro
  • Fundação de Apoio à Pesquisa do Distrito Federal (Award 193.001532/2016)
    • Principle Award Recipient: Bergmann Morais Ribeiro
© 2020 The Authors
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2020-04-30
2024-04-20
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References

  1. Serge Belloncik HM. Cypoviruses. In: Baii LKM and LA (editor). The viruses 1998337–369
     [Google Scholar]
  2. Metcalf P. Reoviridae. Perspect Med Virol 1987; 3:135–145
     [Google Scholar]
  3. King A. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier. https://limo.libis.be/primo-explore/fulldisplay?docid=LIRIAS1956485&context=L&vid=Lirias&search_scope=Lirias&tab=default_tab&lang=en_US&fromSitemap=1 ; 2012
  4. Shapiro A, Green T, Rao S, White S, Carner G et al. Morphological and molecular characterization of a cypovirus (Reoviridae) from the mosquito Uranotaenia sapphirina (Diptera: Culicidae). J Virol 2005; 79:9430–9438 [View Article][PubMed]
     [Google Scholar]
  5. Chen YP, Becnel JJ, Valles SM. RNA viruses infecting pest insects. Insect Pathology 2012 pp 133–170
     [Google Scholar]
  6. Green TB, Shapiro A, White S, Rao S, Mertens PPC et al. Molecular and biological characterization of a cypovirus from the mosquito Culex restuans. J Invertebr Pathol 2006; 91:27–34 [View Article]
     [Google Scholar]
  7. Silva LA, Ardisson-Araújo DMP, Morgado FS, Horta AB, Lemos MVF et al. Cell-line-dependent crystal morphology and sublocalization of the Thyrinteina arnobia cypovirus polyhedrin expressed from a recombinant baculovirus. Arch Virol 2019; 164:1677–1682 [View Article]
     [Google Scholar]
  8. Horta AB, Ardisson-Araujo DMP, da Silva LA, de Melo FL, da Silva Morgado F et al. Genomic analysis of a cypovirus isolated from the Eucalyptus brown looper, Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae). Virus Res 2018; 253:62–67 [View Article]
     [Google Scholar]
  9. Zhang G, Yang J, Qin F, Xu C, Wang J et al. A reverse genetics system for cypovirus based on a bacmid expressing T7 RNA polymerase. Viruses 2019; 11:314 [View Article]
     [Google Scholar]
  10. Ji X, Axford D, Owen R, Evans G, Ginn HM et al. Polyhedra structures and the evolution of the insect viruses. J Struct Biol 2015; 192:88–99 [View Article]
     [Google Scholar]
  11. Horta AB, Ardisson-Araujo DMP, da Silva LA, de Melo FL, da Silva Morgado F et al. Genomic analysis of a cypovirus isolated from the Eucalyptus brown looper, Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae). Virus Res 2018; 253:62–67 [View Article]
     [Google Scholar]
  12. Bellotti AC, V. BA, Guzman OL. Biological control of the cassava hornworm Erinnyis ello (Lepidoptera: Sphingidae). The Florida Entomologist 1992; 75:506–515 [View Article]
     [Google Scholar]
  13. Fazolin M, Estrela JL V, Campos Filho MD, Santiago ACC, Frota F de S. Manejo integrado do mandarová-da-mandioca Erinnyis ello (L.) (Lepidoptera: Sphingidae): conceitos E experiências Na região do Vale do Rio Juruá, ACRE. Embrapa Acre Doc
     [Google Scholar]
  14. Cuartas PE, Villamizar LF, Barrera GP, Ruiz JC, Campos JC et al. Novel biopesticide based on Erinnyis ello betabaculovirus: characterization and preliminary field evaluation to control Erinnyis ello in rubber plantations. Pest Manag Sci 2019; 75:1391–1399 [View Article]
     [Google Scholar]
  15. El-Sharkawy MA. Cassava biology and physiology cassava: a crop for sustainable agriculture and food security in developing countries. Plant Mol Biol 2004; 56:481–501
     [Google Scholar]
  16. McKey D, Cavagnaro TR, Cliff J, Gleadow R. Chemical ecology in coupled human and natural systems: people, manioc, multitrophic interactions and global change. Chemoecology 2010; 20:109–133 [View Article]
     [Google Scholar]
  17. Gabrys B, Capinera JL, Legaspi JC, Legaspi BC, Long LS et al. Cassava Pests and their Management. In: Encyclopedia of Entomology . Springer Netherlands 2008 pp. 764–794
     [Google Scholar]
  18. Venkatachalam P, Geetha N, Sangeetha P, Thulaseedharan A. Natural rubber producing plants: an overview. African J Biotechnol 2013; 12:1297–1310
     [Google Scholar]
  19. Bellotti AC, Smith L, Lapointe SL. Recent advances in cassava pest management. Annu Rev Entomol 1999; 44:343–370 [View Article]
     [Google Scholar]
  20. Haase S, Sciocco-Cap A, Romanowski V. Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 2015; 7:2230–2267 [View Article]
     [Google Scholar]
  21. Villamizar L, Cuartas P, Correal C, Lopez-Ferber M. Virus entomopatógenos en el control biológico de insectos. Control biológico de fitopatógenos, insectos y ácaros 2018 pp 372–409
     [Google Scholar]
  22. Brito AF, Melo FL, Ardisson-Araújo DMP, Sihler W, Souza ML et al. Genome-Wide diversity in temporal and regional populations of the betabaculovirus Erinnyis ello granulovirus (ErelGV) 06 biological sciences 0604 genetics. BMC Genomics 2018; 19:273672
     [Google Scholar]
  23. O’Reilly DR, Miller LK, Luckow VA. Baculovirus Expression Vectors. a Laboratory Manual New York: Freeman and Company; 1992
     [Google Scholar]
  24. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
     [Google Scholar]
  25. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
     [Google Scholar]
  26. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005; 21:951–960 [View Article]
     [Google Scholar]
  27. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article]
     [Google Scholar]
  28. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008; 57:758–771 [View Article]
     [Google Scholar]
  29. Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 2011; 60:685–699 [View Article]
     [Google Scholar]
  30. Schwede T, Kopp J, Guex N, Peitsch MC. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 2003; 31:3381–3385 [View Article]
     [Google Scholar]
  31. Hagiwara K, Higashi T, Namba K, Uehara-Ichiki T, Omura T. Assembly of single-shelled cores and double-shelled virus-like particles after baculovirus expression of major structural proteins P3, p7 and p8 of rice dwarf virus. J Gen Virol 2003; 84:981–984 [View Article]
     [Google Scholar]
  32. Embo J. Papillomaviridae . Virus Taxonomy Elsevier; pp 235–248
     [Google Scholar]
  33. Eaglesham JB, Pan Y, Kupper TS, Kranzusch PJ. Viral and metazoan poxins are cGAMP-specific nucleases that restrict cGAS–STING signalling. Nature 2019; 566:259–263 [View Article]
     [Google Scholar]
  34. Kolliopoulou A, Taning CNT, Smagghe G, Swevers L. Viral delivery of dsRNA for control of insect agricultural pests and vectors of human disease: prospects and challenges. Front Physiol 2017; 8:399 [View Article]
     [Google Scholar]
  35. Harrison R, Rowley D, Mowery J, Bauchan G, Burand J. The operophtera brumata nucleopolyhedrovirus (OpbuNPV) represents an early, divergent lineage within genus Alphabaculovirus . Viruses 2017; 9:307 [View Article]
     [Google Scholar]
  36. Bird FT. Infection and mortality of spruce budworm, choristoneura fumiferana, and forest tent caterpillar, malacosoma disstria, caused by nuclear and cytoplasmic polyhedrosis viruses. Can Entomol 1969; 101:1269–1285 [View Article]
     [Google Scholar]
  37. Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA et al. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evol Biol 2012; 12:91 [View Article]
     [Google Scholar]
  38. Graham RI, Rao S, Possee RD, Sait SM, Mertens PPC et al. Detection and characterisation of three novel species of reovirus (Reoviridae), isolated from geographically separate populations of the winter moth Operophtera brumata (Lepidoptera: Geometridae) on Orkney. J Invertebr Pathol 2006; 91:79–87 [View Article]
     [Google Scholar]
  39. Brüssow H. The not so universal tree of life or the place of viruses in the living world. Phil Trans R Soc B 2009; 364:2263–2274 [View Article]
     [Google Scholar]
  40. Thézé J, Takatsuka J, Nakai M, Arif B, Herniou E. Gene acquisition convergence between Entomopoxviruses and baculoviruses. Viruses 2015; 7:1960–1974 [View Article]
     [Google Scholar]
  41. Cory JS, Bishop DHL. Use of baculoviruses as biological insecticides. Mol Biotechnol 1997; 7:303–313 [View Article]
     [Google Scholar]
  42. Lange M, Jehle JA. The genome of the Cryptophlebia leucotreta granulovirus. Virology 2003; 317:220–236 [View Article]
     [Google Scholar]
  43. Lauzon HAM, Lucarotti CJ, Krell PJ, Feng Q, Retnakaran A et al. Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J Virol 2004; 78:7023–7035 [View Article]
     [Google Scholar]
  44. Escasa SR, Lauzon HAM, Mathur AC, Krell PJ, Arif BM. Sequence analysis of the Choristoneura occidentalis granulovirus genome. J Gen Virol 2006; 87:1917–1933 [View Article]
     [Google Scholar]
  45. Ardisson-Araújo DM, de Melo F, Andrade M, Sihler W, Báo S et al. Genome sequence of Erinnyis ello granulovirus (ErelGV), a natural cassava hornworm pesticide and the first sequenced sphingid-infecting betabaculovirus. BMC Genomics 2014; 15:856 [View Article]
     [Google Scholar]
  46. Ardisson-Araújo DMP, Pereira BT, Melo FL, Ribeiro BM, Báo SN et al. A betabaculovirus encoding a gp64 homolog. BMC Genomics 2016; 17:94 [View Article]
     [Google Scholar]
  47. Ishikawa H, Ma Z, Barber GN. Sting regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461:788–792 [View Article]
     [Google Scholar]
  48. Sun W, Li Y, Chen L, Chen H, You F et al. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci U S A 2009; 106:8653–8658 [View Article]
     [Google Scholar]
  49. ASY L, Kranzusch PJ, Cate JHD. Eif3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature 2015; 522:111–114
     [Google Scholar]
  50. Liu Y, Gordesky-Gold B, Leney-Greene M, Weinbren NL, Tudor M et al. Inflammation-Induced, STING-dependent autophagy restricts Zika virus infection in the Drosophila brain. Cell Host Microbe 2018; 24:57–68 [View Article]
     [Google Scholar]
  51. Martin M, Hiroyasu A, Guzman RM, Roberts SA, Goodman AG. Analysis of Drosophila sting reveals an evolutionarily conserved antimicrobial function. Cell Rep 2018; 23:3537–3550 [View Article]
     [Google Scholar]
  52. Woon Shin S, Park S-S, Park D-S, Gwang Kim M, Kim SC et al. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochem Mol Biol 1998; 28:827–837 [View Article]
     [Google Scholar]
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A novel cypovirus found in a betabaculovirus co-infection context contains a poxvirus immune nuclease (poxin)-related gene
J. Gen. Virol. 101, 667 (2020); https://doi.org/10.1099/jgv.0.001413
/content/journal/jgv/10.1099/jgv.0.001413
/content/journal/jgv/10.1099/jgv.0.001413
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