Skip to main content
SpringerLink
Log in

Genomic analysis of a Trichoplusia ni Betabaculovirus (TnGV) with three different viral enhancing factors and two unique genes

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The complete genome of a Trichoplusia ni granulovirus (TnGV) is described and analyzed. The genome contains 175,360 bp (KU752557), becoming the third largest genome within the genus Betabaculovirus, smaller only than the Xestia c-nigrum GV (XecnGV) (178,733 pb) and the Pseudaletia unipuncta GV (PsunGV) (176,677 pb) genomes. The TnGV genome has a 39.81% C+G content and a total of 180 ORFs were identified, 96 of them in the granulin gene direction and 84 in the opposite direction. A total of 94.38% of the ORFs showed high identity with those of ClanGV, HaGV, and SlGV. Eight homologous regions (hrs) were identified as well as one apoptosis inhibitor (IAP-3). Interestingly, three viral enhancing factors (VEFs) were located in TnGV genome: VEF-1 (orf153), VEF-3 (orf155), and VEF-4 (orf164), additional to another metalloprotease (orf37). Two ORFs were unique to TnGV (orf100 and orf101) and another one was shared by only TnGV and AgseGV (orf2). Eleven of the deduced proteins showed high identity with proteins from nucleopolyhedroviruses, three with proteins from ascoviruses, and one with an entomopoxvirus protein. The largest deduced protein contains 1,213 amino acids (orf43) and the smallest deduced protein contains only 50 amino acids (orf143). Sequence identity and phylogenetic analyses showed that the closest related genomes to TnGV are, to date, those of PsunGV and XecnGV. This genome analysis may contribute to functional research on TnGV, and may form the bases for the utilization of this betabaculovirus as a pest control agent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ardisson-Araujo DMP, de Melo FL, Andrade MD, Sihler W, Bao SN, Ribeiro BM, de Souza ML (2014) Genome sequence of Erinnyis ello granulovirus (ErelGV), a natural cassava hornworm pesticide and the first sequenced sphingid-infecting betabaculovirus. BMC Genom 15:856

    Article  Google Scholar 

  2. Ardisson-Araujo DMP, Melo FL, Clem RJ, Wolff JLC, Ribeiro BM (2016) A Betabaculovirus-encoded gp64 homolog codes for a functional envelope fusion protein. J Virol 90:1668–1672

    Article  CAS  PubMed Central  Google Scholar 

  3. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, Stockinger H (2012) ExPASy: SIB bioinformatics resource portal. Nucl Acids Res 40:W597–W603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bideshi DK, Hice RH, Ge B, Federici BA (1998) Molecular characterization and expression of the Trichoplusia ni granulovirus helicase gene. J Gen Virol 79:1309–1319

    Article  CAS  PubMed  Google Scholar 

  5. Birnbaum MJ, Clem RJ, Miller LK (1994) An apoptosis-inhibiting gene from a nuclear polyhedrosis-virus encoding a polypeptide with Cys/His sequence motif. J Virol 68:2521–2528

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Braunagel SC, Russell WK, Rosas-Acosta G, Russell DH, Summers MD (2003) Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci USA 100:9797–9802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Capinera JL (2001) Handbook of Vegetable Pests. Academic Press, San Diego, California

    Google Scholar 

  8. Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. Proc Ger Conf Bioinf 99:45–56

    Google Scholar 

  9. Conesa A, Götz S (2007) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genom 2008:1–12

    Google Scholar 

  10. Cuartas PE, Barrera GP, Belaich MN, Barreto E, Ghiringhelli PD, Villamizar LF (2015) The complete sequence of the first Spodoptera frugiperda Betabaculovirus genome: a natural multiple recombinant virus. Viruses Basel 7:394–421

    Article  Google Scholar 

  11. Danquah JO, Botchway S, Jeshtadi A, King LA (2012) Direct interaction of baculovirus capsid proteins VP39 and EXON0 with Kinesin-1 in insect cells determined by fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy. J Virol 86:844–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Escasa SR, Lauzon HAM, Mathur AC, Krell PJ, Arif BM (2006) Sequence analysis of the Choristoneura occidentalis granulovirus genome. J Gene Virol 87:1917–1933

    Article  CAS  Google Scholar 

  13. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Sonnhammer EL (2013) Pfam: the protein families database. Nucl Acids Res:281–288

  14. Friesen DP (1997) Regulation of baculovirus early gene expression. In: Miller KL (ed) The baculoviruses. Springer, New York, pp 141–170

    Chapter  Google Scholar 

  15. Garavaglia MJ, Miele SAB, 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 86:12069–12079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. Humana Press, New York, pp 571–607

    Google Scholar 

  17. Gordon D, Green P (2013) Consed: a graphical editor for next-generation sequencing. Bioinformatics 29:2936–2937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Guarino LA, Smith M (1992) Regulation of delayed-eartly gene-transcription by dual TATA boxes. J Virol 66:3733–3739

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Guarino LA, Mistretta TA, Dong W (2002) DNA binding activity of the baculovirus late expression factor PP31. Virus Res 90:187–195

    Article  CAS  PubMed  Google Scholar 

  20. Haase S, Sciocco-Cap A, Romanowski V (2015) Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses Basel 7:2230–2267

    Article  CAS  Google Scholar 

  21. Harrison RL, Popham HJR (2008) Genomic sequence analysis of a granulovirus isolated from the Old World bollworm, Helicoverpa armigera. Virus Genes 36:565–581

    Article  CAS  PubMed  Google Scholar 

  22. Harrison RL, Rowley DL, Mowery J, Bauchan GR, Theilmann DA, Rohrmann GF, Erlandson MA (2017) The complete genome sequence of a second distinct betabaculovirus from the True Armyworm, Mythimna unipuncta. PLos One:12

  23. Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD (1997) Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology 238:243–253

    Article  CAS  PubMed  Google Scholar 

  24. Hayakawa T, Ko R, Okano K, Seong SI, Goto C, Maeda S (1999) Sequence analysis of the Xestia c-nigrum granulovirus genome. Virology 262:277–297

    Article  CAS  PubMed  Google Scholar 

  25. 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 151:1257–1266

    Article  CAS  PubMed  Google Scholar 

  26. Ko R, Okano K, Maeda S (2000) Structural and functional analysis of the Xestia c-nigrum granulovirus matrix metalloproteinase. J Virol 74:11240–11246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kumar S, Tamura K, Nei M (1994) MEGA—molecular evolutionary genetics analysis software for microcomputeres. Comput Appl Biosci 10:189–191

    CAS  PubMed  Google Scholar 

  28. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  29. Lange M, Jehle JA (2003) The genome of the Cryptophlebia leucotreta granulovirus. Virology 317:220–236

    Article  CAS  PubMed  Google Scholar 

  30. Li Y, Tang P, Zhang Z, Zhang H, Qin Q Genome sequence analysis of the Pseudaletia unipuncta granulovirus which was propagated in Pseudaletia separate larvae (in Press)

  31. Li ZF, Li CB, Yang K, Wang LH, Yin C, Gong YX, Pang Y (2003) Characterization of a chitin-binding protein GP37 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Res 96:113–122

    Article  CAS  PubMed  Google Scholar 

  32. Liang ZP, Zhang XX, Yin XM, Cao SM, Xu F (2011) Genomic sequencing and analysis of Clostera anachoreta granulovirus. Arch Virol 156:1185–1198

    Article  CAS  PubMed  Google Scholar 

  33. Lu A, Krell JP, Vlak MJ, Rohrmann FG (1997) Baculovirus DNA replication. In: Miller KL (ed) The baculoviruses. Springer, New York, pp 171–191

    Chapter  Google Scholar 

  34. Lu A, Miller KL (1997) Regulation of baculovirus late and very late gene expression. In: Miller KL (ed) The baculoviruses, New York, pp 193-216

  35. Luque T, Finch R, Crook N, O’Reilly DR, Winstanley D (2001) The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol 82:2531–2547

    Article  CAS  PubMed  Google Scholar 

  36. Minion FC, Coons L, Broome JR (1979) Characterization of the polyhedral evelope of the nuclear plyhedrosis virus of Heliothis virescens. J Invertebr Pathol 34:303–307

    Article  CAS  Google Scholar 

  37. Okonechnikov K, Golosova O, Fursov M, Team U (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167

    Article  CAS  PubMed  Google Scholar 

  38. Olszewski J, Miller LK (1997) A role for Baculovirus GP41 in budded virus production. Virology 233:292–301

    Article  CAS  PubMed  Google Scholar 

  39. Ono C, Kamagata T, Taka H, Sahara K, Asano SI, Bando H (2012) Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res 165:197–206

    Article  CAS  PubMed  Google Scholar 

  40. Oreilly DR, Miller LK (1989) A baculovirus blocks insect molting by producing ecdysteroid udp-glucosyl transferase. Science 245:1110–1112

    Article  CAS  Google Scholar 

  41. O´Reilly RD (1997) Auxiliary genes of baculoviruses. In: Miler KL (ed) The baculoviruses. Springer, New York, pp 267–300

    Chapter  Google Scholar 

  42. Peng JX, Zhong J, Granados RR (1999) A baculovirus enhancin alters the permeability of a mucosal midgut peritrophic matrix from lepidopteran larvae. J Insect Physiol 45:159–166

    Article  CAS  PubMed  Google Scholar 

  43. Prestridge DS (1995) Predicting POL-ll promoter sequences using transcription factor-binding sites. J Mol Biol 249:923–932

    Article  CAS  PubMed  Google Scholar 

  44. Rohrmann FG (2013) Baculovirus molecular biology. Bethesda (MD): Natonal Library of Medicine (US), National Center for Biotechnology Information

  45. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38:D161–D166

    Article  CAS  PubMed  Google Scholar 

  47. Sugiura N, Setoyama Y, Chiba M, Kimata K, Watanabe H (2011) Baculovirus envelope protein ODV-E66 is a novel chondroitinase with distinct substrate specificity. J Biol Chem 286:29026–29034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Summers MD (2006) Milestones leading to the genetic engineering of baculoviruses as expression vector systems and viral pesticides. Insect Viruses Biotechnol Appl 68:3–73

    Article  CAS  Google Scholar 

  49. Tomalski MD, Eldridge R, Miller LK (1991) A baculovirus homolog of a Cu/Zn superoxide-dismutase gene. Virology 184:149–161

    Article  CAS  PubMed  Google Scholar 

  50. VanOers MM, Vlak JM (1997) The baculovirus 10-kDa protein. J Invertebr Pathol 70:1–17

    Article  CAS  Google Scholar 

  51. Vaux DL, Strasser A (1996) The molecular biology of apoptosis. Proc Natl Acad Sciences USA 93:2239–2244

    Article  CAS  Google Scholar 

  52. Wang P, Granados RR (1998) Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J Invertebr Pathol 72:57–62

    Article  CAS  PubMed  Google Scholar 

  53. Wang RR, Deng F, Hou DH, Zhao Y, Guo L, Wang HL, Hu ZH (2010) Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 84:7233–7242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wolgamot GM, Gross CH, Russell RLQ, Rohrmann GF (1993) Immunocytochemical characterization of P24, a baculovirus capsid-associated protein. J Gen Virol 74:103–107

    Article  CAS  PubMed  Google Scholar 

  55. Wormleaton S, Kuzio J, Winstanley D (2003) The complete sequence of the Adoxophyes orana granulovirus genome. Virology 311:350–365

    Article  CAS  PubMed  Google Scholar 

  56. Wu WB, Passarelli AL (2010) Autographa californica multiple nucleopolyhedrovirus Ac92 (ORF92, P33) is required for budded virus production and multiply enveloped occlusion-derived virus formation. J Virol 84:12351–12361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Yin FF, Zhu Z, Liu XP, Hou DH, Wang J, Zhang L, Wang ML, Kou Z, Wang HL, Deng F, Hu ZH (2015) The complete genome of a new betabaculovirus from Clostera anastomosis. PLos One:10

  58. Yuan MJ, Wu WB, Liu C, Wang YJ, Hu ZY, Yang K, Pang Y (2008) A highly conserved baculovirus gene p48 (ac103) is essential for BV production and ODV envelopment. Virology 379:87–96

    Article  CAS  PubMed  Google Scholar 

  59. Zemskov EA, Kang WY, Maeda S (2000) Evidence for nucleic acid binding ability and nucleosome association of Bombyx mori nucleopolyhedrovirus BRO proteins. J Virol 74:6784–6789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhang S, Zhu Z, Sun SF, Chen QJ, Deng F, Yang K (2015) Genome sequencing and analysis of a granulovirus isolated from the Asiatic rice leafroller, Cnaphalocrocis medinalis. Virol Sin 30:417–424

    Article  CAS  PubMed  Google Scholar 

  61. Zhu SM, Wang W, Wang Y, Yuan MJ, Yang K (2013) The baculovirus core gene ac83 is required for nucleocapsid assembly and per os infectivity of Autographa californica nucleopolyhedrovirus. J Virol 87:10573–10586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are in debt to Javier Luévano-Borroel and Leandro Gabriel Ordóñez-Acevedo for their technical support. This research was founded by CONACYT (Grant 166586) and the University of Guanajuato (Grant 964/2016).

Author information

Authors and Affiliations

  1. Posgrado en Biociencias, División de Ciencias de la Vida, Departamento de Alimentos, Campus Irapuato-Salamanca, Universidad de Guanajuato, Ex Hacienda El Copal Km. 9.0, Carretera Irapuato-León, Irapuato, Guanajuato, Mexico

    Ma. de los Ángeles Bivian-Hernández, Everardo Mares-Mares & María Cristina Del Rincón-Castro

  2. CINVESTAV-Irapuato, Apartado Postal 629, 36500, Irapuato, Guanajuato, Mexico

    Juventino López-Tlacomulco & Jorge E. Ibarra

Authors
  1. Ma. de los Ángeles Bivian-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juventino López-Tlacomulco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Everardo Mares-Mares
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge E. Ibarra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María Cristina Del Rincón-Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Cristina Del Rincón-Castro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de los Ángeles Bivian-Hernández, M., López-Tlacomulco, J., Mares-Mares, E. et al. Genomic analysis of a Trichoplusia ni Betabaculovirus (TnGV) with three different viral enhancing factors and two unique genes. Arch Virol 162, 3705–3715 (2017). https://doi.org/10.1007/s00705-017-3506-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3506-y

Search

Navigation