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Virologica Sinica

, Volume 33, Issue 4, pp 359–368 | Cite as

Genome Characteristics of the Cyclophragma Undans Nucleopolyhedrovirus: A Distinct Species in Group I of Alphabaculovirus

  • Zheng Zhu
  • Jun Wang
  • Qianran Wang
  • Feifei Yin
  • Xiaoping Liu
  • Dianhai Hou
  • Lei Zhang
  • Haizhou Liu
  • Jiang Li
  • Basil M. Arif
  • Hualin Wang
  • Fei Deng
  • Zhihong Hu
  • Manli Wang
Research Article

Abstract

The Cyclophragma undans nucleopolyhedrovirus (CyunNPV), a potential pest control agent, was isolated from Cyclophragma undans (Lepidoptera: Lasiocampidae), an important forest pest. In the present study, we performed detailed genome analysis of CyunNPV and compared its genome to those of other Group I alphabaculoviruses. Sequencing of the CyunNPV genome using the Roche 454 sequencing system generated 142,900 bp with a G + C content of 45%. Genome analysis predicted a total of 147 hypothetical open reading frames comprising 38 baculoviral core genes, 24 lepidopteran baculovirus conserved genes, nine Group I Alphabaculovirus conserved genes, 71 common genes, and five genes that are unique to CyunNPV. In addition, the genome contains 13 homologous repeated sequences (hrs). Phylogenetic analysis groups CyunNPV under a distinct branch within clade “a” of Group I in the genus Alphabaculovirus. Unlike other members of Group I, CyunNPV harbors only nine of the 11 genes previously determined to be specific to Group I viruses. Furthermore, the CyunNPV lacks the tyrosine phosphatase gene and the ac30 gene. The CyunNPV F-like protein contains two insertions of continuous polar amino acids, one at the conventional fusion peptide and a second insertion at the pre-transmembrane domain. The insertions are likely to affect the fusion function and suggest an evolutionary process that led to inactivation of the F-like protein. The above findings imply that CyunNPV is a distinct species under Group I Alphabaculovirus.

Keywords

Cyclophragma undans nucleopolyhedrovirus (CyunNPV) Baculovirus Group I Alphabaculovirus F protein 

Notes

Acknowledgements

This work was supported by the National Key R&D Program of China (Grant No. 2017YFD0200400) and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB11030400). We acknowledge the technical support and core facility of the Wuhan Institute of Virology for their technical assistance.

Author Contributions

Conceived and designed the experiments: ZZ, MW, ZH, FD, HW, and FY. Viral nucleic acid extraction and 454 sequencing: ZZ, DH, FY, XL, and ZL. Genome assembly, annotation and data analysis: ZZ, XL, JW, QW, and HL. Wrote the paper: ZZ, BA, ZH, and MW.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Animal and Human Rights Statement

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

12250_2018_47_MOESM1_ESM.pdf (284 kb)
Supplementary material 1 (PDF 284 kb)
12250_2018_47_MOESM2_ESM.xlsx (28 kb)
Supplementary material 2 (XLSX 28 kb)

References

  1. Bulach DM, Kumar CA, Zaia A, Liang B, Tribe DE (1999) Group II nucleopolyhedrovirus subgroups revealed by phylogenetic analysis of polyhedrin and DNA polymerase gene sequences. J Invertebr Pathol 73:59–73CrossRefPubMedGoogle Scholar
  2. Carstens EB, Ball LA (2009) Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2008). Arch Virol 154:1181–1188CrossRefPubMedGoogle Scholar
  3. Conant GC, Wolfe KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24:861–862CrossRefPubMedGoogle Scholar
  4. Deng F, Wang R, Fang M, Jiang Y, Xu X, Wang H, Chen X, Arif BM, Guo L, Wang H, Hu Z (2007) Proteomics analysis of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus identified two new occlusion-derived virus-associated proteins, HA44 and HA100. J Virol 81:9377–9385CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ferrelli ML, Salvador R, Biedma ME, Berretta MF, Haase S, Sciocco-Cap A, Ghiringhelli PD, Romanowski V (2012) Genome of Epinotia aporema granulovirus (EpapGV), a polyorganotropic fast killing betabaculovirus with a novel thymidylate kinase gene. BMC Genom 13:548CrossRefGoogle Scholar
  6. Garavaglia MJ, Miele SA, Iserte JA, Belaich MN, Ghiringhelli PD (2012) The ac53, ac78, ac101, and ac103 genes are newly discovered.core genes in the family Baculoviridae. J Virol 86:12069–12079CrossRefPubMedPubMedCentralGoogle Scholar
  7. Gross CH, Shuman S (1998) Characterization of a baculovirus-encoded RNA 5’-triphosphatase. J Virol 72:7057–7063PubMedPubMedCentralGoogle Scholar
  8. Guarino LA, Gonzalez MA, Summers MD (1986) Complete sequence and enhancer function of the homologous DNA regions of Autographa californica nuclear polyhedrosis virus. J Virol 60:224–229PubMedPubMedCentralGoogle Scholar
  9. Habib S, Hasnain SE (2000) Differential activity of two non-hr origins during replication of the baculovirus Autographa californica nuclear polyhedrosis virus genome. J Virol 74:5182–5189CrossRefPubMedPubMedCentralGoogle Scholar
  10. Hayakawa T, Ko R, Okano K, Seong SI, Goto C, Maeda S (1999) Sequence analysis of the Xestia c-nigrum granulovirus genome. Virology 262:277–297CrossRefPubMedGoogle Scholar
  11. Herniou EA, Olszewski JA, Cory JS, O’Reilly DR (2003) The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48:211–234CrossRefPubMedGoogle Scholar
  12. Hu ZH, Arif BM, Jin F, Martens JW, Chen XW, Sun JS, Zuidema D, Goldbach RW, Vlak JM (1998a) Distinct gene arrangement in the Buzura suppressaria single-nucleocapsid nucleopolyhedrovirus genome. J Gen Virol 79:2841–2851CrossRefPubMedGoogle Scholar
  13. Hu ZH, Arif BM, Sun JS, Chen XW, Zuidema D, Goldbach RW, Vlak JM (1998b) Genetic organization of the HindIII-I region of the single-nucleocapsid nucleopolyhedrovirus of Buzura suppressaria. Virus Res 55:71–82CrossRefPubMedGoogle Scholar
  14. Huang JP, Tang WQ, Shu QH (1983) A study on cyclophragma undans nuclear polyhedrosis virus. J Cent South Univ For Technol 3:136–142 (In Chinese) Google Scholar
  15. Huang J, Hao B, Deng F, Sun X, Wang H, Hu Z (2008) Open reading frame Bm21 of Bombyx mori nucleopolyhedrovirus is not essential for virus replication in vitro, but its deletion extends the median survival time of infected larvae. J Gen Virol 89:922–930CrossRefPubMedGoogle Scholar
  16. Ijkel WFJ, Westenberg M, Goldbach RW, Blissard GW, Vlak JM, Zuidema D (2000) A novel baculovirus envelope fusion protein with a proprotein convertase cleavage site. Virology 275:30–41CrossRefPubMedGoogle Scholar
  17. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266CrossRefPubMedGoogle Scholar
  18. Jiang Y, Deng F, Rayner S, Wang H, Hu Z (2009) Evidence of a major role of GP64 in group I alphabaculovirus evolution. Virus Res 142:85–91CrossRefPubMedGoogle Scholar
  19. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences Computer applications in the biosciences. CABIOS 8:275–282PubMedGoogle Scholar
  20. Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, Kobayashi M, Maeda S, Hammock BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci USA 102:2584–2589CrossRefPubMedGoogle Scholar
  21. Kool M, Voeten JT, Goldbach RW, Tramper J, Vlak JM (1993) Identification of seven putative origins of Autographa californica multiple nucleocapsid nuclear polyhedrosis virus DNA replication. J Gen Virol 74:2661–2668CrossRefPubMedGoogle Scholar
  22. Landais I, Vincent R, Bouton M, Devauchelle G, Duonor-Cerutti M, Ogliastro M (2006) Functional analysis of evolutionary conserved clustering of bZIP binding sites in the baculovirus homologous regions (hrs) suggests a cooperativity between host and viral transcription factors. Virology 344:421–431CrossRefPubMedGoogle Scholar
  23. Lauzon HA, Lucarotti CJ, Krell PJ, Feng Q, Retnakaran A, Arif BM (2004) Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J Virol 78:7023–7035CrossRefPubMedPubMedCentralGoogle Scholar
  24. Li Y, Miller LK (1995) Properties of a baculovirus mutant defective in the protein phosphatase gene. J Virol 69:4533–4537PubMedPubMedCentralGoogle Scholar
  25. Liu X, Yin F, Zhu Z, Hou D, Wang J, Zhang L, Wang M, Wang H, Hu Z, Deng F (2014) Genomic sequencing and analysis of Sucra jujuba nucleopolyhedrovirus. PLoS ONE 9:e110023CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lorizate M, Huarte N, Saez-Cirion A, Nieva JL (2008) Interfacial pre-transmembrane domains in viral proteins promoting membrane fusion and fission. Biochem Biophys Acta 1778:1624–1639CrossRefPubMedGoogle Scholar
  27. Lung OY, Cruz-Alvarez M, Blissard GW (2003) Ac23, an envelope fusion protein homolog in the baculovirus Autographa californica multicapsid nucleopolyhedrovirus, is a viral pathogenicity factor. J Virol 77:328–339CrossRefPubMedPubMedCentralGoogle Scholar
  28. Pearson MN, Bjornson RM, Ahrens C, Rohrmann GF (1993) Identification and characterization of a putative origin of DNA replication in the genome of a baculovirus pathogenic for Orgyia pseudotsugata. Virology 197:715–725CrossRefPubMedGoogle Scholar
  29. Pearson MN, Groten C, Rohrmann GF (2000) Identification of the lymantria dispar nucleopolyhedrovirus envelope fusion protein provides evidence for a phylogenetic division of the Baculoviridae. J Virol 74:6126–6131CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pearson MN, Russell RL, Rohrmann GF (2001) Characterization of a baculovirus-encoded protein that is associated with infected-cell membranes and budded virions. Virology 291:22–31CrossRefPubMedGoogle Scholar
  31. Rodems SM, Friesen PD (1995) Transcriptional enhancer activity of hr5 requires dual-palindrome half sites that mediate binding of a dimeric form of the baculovirus transregulator IE1. J Virol 69:5368–5375PubMedPubMedCentralGoogle Scholar
  32. Rohrmann GF, Karplus PA (2001) Relatedness of baculovirus and gypsy retrotransposon envelope proteins. BMC Evol Biol 1:1CrossRefPubMedPubMedCentralGoogle Scholar
  33. Sainz B Jr, Rausch JM, Gallaher WR, Garry RF, Wimley WC (2005) The aromatic domain of the coronavirus class I viral fusion protein induces membrane permeabilization: putative role during viral entry. Biochemistry 44:947–958CrossRefPubMedGoogle Scholar
  34. Salzwedel K, West JT, Hunter E (1999) A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J Virol 73:2469–2480PubMedPubMedCentralGoogle Scholar
  35. Sheng Z, Charbonneau H (1993) The baculovirus Autographa californica encodes a protein tyrosine phosphatase. J Biol Chem 268:4728–4733PubMedGoogle Scholar
  36. Solovyev VV, Salamov AA (1999) INFOGENE: a database of known gene structures and predicted genes and proteins in sequences of genome sequencing projects. Nucleic Acids Res 27:248–250CrossRefPubMedPubMedCentralGoogle Scholar
  37. Takagi T, Taylor GS, Kusakabe T, Charbonneau H, Buratowski S (1998) A protein tyrosine phosphatase-like protein from baculovirus has RNA 5′-triphosphatase and diphosphatase activities. Proc Natl Aca Sci USA 95:9808–9812CrossRefGoogle Scholar
  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tan Y, Jiang L, Wang M, Yin F, Deng F, Liu M, Hu Z, Wang H (2008) Mutagenesis and nuclear magnetic resonance analyses of the fusion peptide of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus F protein. J Virol 82:8138–8148CrossRefPubMedPubMedCentralGoogle Scholar
  40. Theilmann DA, Stewart S (1992) Tandemly repeated sequence at the 3’ end of the IE-2 gene of the baculovirus Orgyia pseudotsugata multicapsid nuclear polyhedrosis virus is an enhancer element. Virology 187:97–106CrossRefPubMedGoogle Scholar
  41. van Oers MM, Vlak JM (2007) Baculovirus genomics. Curr Drug Targets 8:1051–1068CrossRefPubMedGoogle Scholar
  42. Wang M, Tan Y, Yin F, Deng F, Vlak JM, Hu Z, Wang H (2008) The F-like protein Ac23 enhances the infectivity of the budded virus of gp64-null Autographa californica multinucleocapsid nucleopolyhedrovirus pseudotyped with baculovirus envelope fusion protein F. J Virol 82:9800–9804CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wang M, Wang J, Yin F, Tan Y, Deng F, Chen X, Jehle JA, Vlak JM, Hu Z, Wang H (2014) Unraveling the entry mechanism of baculoviruses and its evolutionary implications. J Virol 88:2301–2311CrossRefPubMedPubMedCentralGoogle Scholar
  44. Westenberg M, Wang H, Ijkel WFJ, Goldbach RW, Vlak JM, Zuidema D (2002) Furin is involved in baculovirus envelope fusion protein activation. J Virol 76:178–184CrossRefPubMedPubMedCentralGoogle Scholar
  45. Westenberg M, Veenman F, Roode EC, Goldbach RW, Vlak JM, Zuidema D (2004) Functional analysis of the putative fusion domain of the baculovirus envelope fusion protein F. J Virol 78:6946–6954CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wu Y, Carstens EB (1996) Initiation of baculovirus DNA replication: early promoter regions can function as infection-dependent replicating sequences in a plasmid-based replication assay. J Virol 70:6967–6972PubMedPubMedCentralGoogle Scholar
  47. Xiao KJ, Shu QH (1984) Biology of the oak caterpillar Cyclophragma undans (Walker). J Cent South Univ For Technol 4:59–64 (In Chinese) Google Scholar
  48. Yin F, Zhu Z, Liu X, Hou D, Wang J, Zhang L, Wang M, Kou Z, Wang H, Deng F, Hu Z (2015) The complete genome of a new Betabaculovirus from Clostera anastomosis. PLoS ONE 10:e0132792CrossRefPubMedPubMedCentralGoogle Scholar
  49. Yu IL, Lin YC, Robinson JH, Lung O (2009) Transduction of vertebrate cells with Spodoptera exigua multiple nucleopolyhedrovirus F protein-pseudotyped gp64-null Autographa californica multiple nucleopolyhedrovirus. J Gen Virol 90:2282–2287CrossRefPubMedGoogle Scholar
  50. Zanotto PM, Kessing BD, Maruniak JE (1993) Phylogenetic interrelationships among baculoviruses: evolutionary rates and host associations. J Invertebr Pathol 62:147–164CrossRefPubMedGoogle Scholar
  51. Zhu Z, Yin F, Liu X, Hou D, Wang J, Zhang L, Arif B, Wang H, Deng F, Hu Z (2014) Genome sequence and analysis of Buzura suppressaria nucleopolyhedrovirus: a group II Alphabaculovirus. PLoS ONE 9:e86450CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Zheng Zhu
    • 1
  • Jun Wang
    • 1
  • Qianran Wang
    • 1
  • Feifei Yin
    • 1
  • Xiaoping Liu
    • 1
  • Dianhai Hou
    • 1
  • Lei Zhang
    • 1
  • Haizhou Liu
    • 1
  • Jiang Li
    • 1
  • Basil M. Arif
    • 2
  • Hualin Wang
    • 1
  • Fei Deng
    • 1
  • Zhihong Hu
    • 1
  • Manli Wang
    • 1
  1. 1.State Key Laboratory of Virology and China Center for Virus Culture Collection, Wuhan Institute of VirologyChinese Academy of SciencesWuhanChina
  2. 2.Canadian Forest ServiceGreat Lakes Forestry CentreSault Ste MarieCanada

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