Archives of Virology

, Volume 156, Issue 7, pp 1185–1198 | Cite as

Genomic sequencing and analysis of Clostera anachoreta granulovirus

  • Zhenpu Liang
  • Xiaoxia Zhang
  • Xinming Yin
  • Sumei Cao
  • Feng Xu
Original Article

Abstract

The complete genome of Clostera anachoreta granulovirus (ClanGV) from an important pest of poplar, Clostera anachoreta (Lepidoptera: Notodontidae), was sequenced and analyzed. The circular double-stranded genome is 101,487 bp in size with a C+G content of 44.4%. It is predicted to contain 123 open reading frames (ORFs), covering 93% of the whole genome sequence. One hundred eleven ClanGV ORFs are homologues of previously reported baculovirus genes, two ORFs only exist in nucleopolyhedroviruses (NPVs), and 10 ORFs are unique to ClanGV, accounting for 3.9% of the genome in total. The average amino acid sequence identities between ClanGV and other granulovirus (GV) homologues ranged from 55.5% (PiraGV) to 43.1% (HearGV and PsunGV). ClanGV includes 16 DNA replication- and transcription-related genes, including ie-1, dnapol, helicase, lef-1, lef-2, lef-3, lef-4, lef-5, lef-6, lef-8, lef-9, lef-10, lef-11, 39K, p47 and vlf-1. Seventeen conserved structural genes and two types of apoptosis suppression proteins (P35 and IAP) have also been identified. To date, ClanGV is the second identified GV that contains the p35 gene, which is present in eight NPVs and ChocGV. Genes of chitinase and cathepsin, which are involved in the liquefaction of the host, were found in the ClanGV genome, consistent with the typical insecticidal properties of ClanGV. In the ClanGV genome, there are four homologous repeat regions, each one of which contains only 2-3 direct repeats. Phylogenetic analysis, based on the 29 core baculovirus genes, indicates that ClanGV is closely related to PhopGV, AdorGV, CpGV, CrleGV, PiraGV and ChocGV, and this agrees with the results of homology analysis and gene parity plot analysis.

Notes

Acknowledgments

This project was supported by grants from the National Natural Science Foundation of China (30700540 and 30901152).

References

  1. 1.
    Afonso CL, Tulman ER, Lu Z, Balinsky CA, Moser BA, Becnel JJ, Rock DL, Kutish GF (2001) Genome sequence of a baculovirus pathogenic for Culex nigripalpus. J Virol 75:11157–11165PubMedCrossRefGoogle Scholar
  2. 2.
    Ayres MD, Howard SC, Kuzio J, Lopez-Ferber M, Possee RD (1994) The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586–605PubMedCrossRefGoogle Scholar
  3. 3.
    Birnbaum MJ, Clenm RJ, Miller LK (1994) An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 68:2521–2528PubMedGoogle Scholar
  4. 4.
    Blissard GW, Kogan PH, Wei R, Rohrmann GF (1992) A synthetic early promoter from a baculovirus: roles of the TATA box and conserved start site CAGT sequence in basal levels of transcription. Virology 190:783–793PubMedCrossRefGoogle Scholar
  5. 5.
    Chang JH, Choi JY, Jin BR, Roh JY, Olszewski JA, Seo SJ, O’Reilly DR, Je YH (2003) An improved baculovirus insecticide producing occlusion bodies that contain Bacillus thuringiensis insect toxin. J Invertebr Pathol 84:30–37PubMedCrossRefGoogle Scholar
  6. 6.
    Chen XW, Ijkel WFJ, Tarchini R, Sun XL, Sandbrink H, Wang HZ, Zuidema D, Lankhorst RK, Vlak JM, Hu ZH (2001) The sequence of the Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus genome. J Gen Virol 82:241–257PubMedGoogle Scholar
  7. 7.
    Chen XW, Zhang WJ, Wong J, Chun G, Lu A, McCutchen BF, Presnail JK, Herrmann R, Dolan M, Tingey S, Hu ZH, Vlak JM (2002) Comparative analysis of the complete genome sequences of Helicoverpa zea and Helicoverpa armigera single-nucleocapsid nucleopolyhedroviruses. J Gen Virol 83:673–684PubMedGoogle Scholar
  8. 8.
    Eldridge R, O’Reilly DR, Miller LK (1992) Efficacy of a baculovirus pesticide expressing an eclosion hormone gene. Biol Control 2:104–110CrossRefGoogle Scholar
  9. 9.
    Escasa SR, Lauzon HAM, Mathur AC, Krell PJ, Arif BM (2006) Sequence analysis of the Choristoneura occidentalis granulovirus genome. J Gen Virol 87:1917–1933PubMedCrossRefGoogle Scholar
  10. 10.
    Federici BA (1997) Baculovirus pathogenesis. In: Miller LK (ed) The baculoviruses. Plenum, New York, pp 33–59Google Scholar
  11. 11.
    Friesen PD (1997) Regulation of baculovirus early gene expression. In: Miller LK (ed) The baculoviruses. Plenum, New York, pp 141–170Google Scholar
  12. 12.
    Fuchs LY, Woods MS, Weaver RF (1983) Viral transcription during Autographa californica nuclear polyhedrosis virus infection: a novel RNA polymerase induced in infected Spodoptera frugiperda cells. J Virol 48:641–646PubMedGoogle Scholar
  13. 13.
    Garcia-Maruniak A, Maruniak JE, Zanotto PMA, Doumbouya AE, Liu JC, Merritt TM, Lanoie JS (2004) Sequence analysis of the genome of the Neodiprion sertifer nucleopolyhedrovirus. J Virol 78:7036–7051PubMedCrossRefGoogle Scholar
  14. 14.
    Garcia-Maruniak A, Pavan OHO, Maruniak JE (1996) A variable region of Anticarsia gemmatalis nuclear polyhedrosis virus contains tandemly repeated DNA sequences. Virus Res 41:123–132PubMedCrossRefGoogle Scholar
  15. 15.
    Gomi S, Majima K, Maea S (1999) Sequence analysis of the genome of Bombys mori nucleopolyhedrovirus. J Gen Virol 80:1323–1337PubMedGoogle Scholar
  16. 16.
    Gomi S, Zhou CE, Yih W, Majima K, Maeda S (1997) Deletion analysis of four of eighteen late gene expression factor gene homologues of the baculovirus, BmNPV. Virology 230:35–47PubMedCrossRefGoogle Scholar
  17. 17.
    Guarino LA, Smith M (1992) Regulation of delayed-early gene transcription by dual TATA boxes. J Virol 66:3733–3739PubMedGoogle Scholar
  18. 18.
    Harrison RL, Puttler B, Popham HJR (2008) Genomic sequence analysis of a fast-killing isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus. J Gen Virol 89:775–790PubMedCrossRefGoogle Scholar
  19. 19.
    Hashimoto Y, Harakawa T, Ueno Y, Fujita T, Sano Y, Matsumoto T (2000) Sequence analysis of the Plutella xylostella granulovirus genome. Virology 275:358–372PubMedCrossRefGoogle Scholar
  20. 20.
    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 238:243–253PubMedCrossRefGoogle Scholar
  21. 21.
    Hayakawa T, Ko R, Okano K, Seong SI, Goto C, Maeda S (1999) Sequence analysis of the Xestia c-nigrum granulovirus genome. Virology 262:277–297PubMedCrossRefGoogle Scholar
  22. 22.
    Herniou EA, Olszewski JA, Cory JS, O’Reilly DR (2003) The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48:211–234PubMedCrossRefGoogle Scholar
  23. 23.
    Hilton S, Winstanley D (2007) Identification and functional analysis of the origins of DNA replication in the Cydia pomonella granulovirus genome. J Gen Virol 88:1496–1504PubMedCrossRefGoogle Scholar
  24. 24.
    Hilton S, Winstanley D (2008) Genomic sequence and biological characterization of a nucleopolyhedrovirus isolated from the summer fruit tortrix, Adoxophyes orana. J Gen Virol 89:2898–2908PubMedCrossRefGoogle Scholar
  25. 25.
    Hu ZH, Arif BM, Jin F, Martens JWM, Chen XW, Sun JS, Zuidema D, Goldbach RW, Vlak JM (1998) Distinct gene arrangement in the Buzura suppressaria single-nucleocapsid nucleopolyhedrovirus genome. J Gen Virol 79:2841–2851PubMedGoogle Scholar
  26. 26.
    Hyink O, Dellow RA, Olsen MJ, Caradoc-Davies KMB, Drake K, Herniou EA, Cory JS, O’Reilly DR, Ward VK (2002) Whole genome analysis of the Epiphyas postvittana nucleopolyhedrovirus. J Gen Virol 83:957–971PubMedGoogle Scholar
  27. 27.
    Ijkel WFJ, van Strien EA, Heldens JGM, Broer R, Zuidema D, Goldbach RW, Vlak JM (1999) Sequence and organization of the Spodoptera exigua multicapsid nucleopolyhedrovirus genome. J Gen Virol 80:3289–3304PubMedGoogle Scholar
  28. 28.
    Ikeda M, Yanagimoto K, Kobayashi M (2004) Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321:359–371PubMedCrossRefGoogle Scholar
  29. 29.
    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 151:1257–1266PubMedCrossRefGoogle Scholar
  30. 30.
    Kuzio J, Pearson MN, Harwood SH, Funk CJ, Evans JT, Slavicek JM, Rohrmann George F (1999) Sequence and analysis of the genome of a baculovirus pathogenic for Lymantria dispar. Virology 253:17–34PubMedCrossRefGoogle Scholar
  31. 31.
    Lange M, Jehle JA (2003) The genome of Cryptophlebia leucotreta granulovirus. Virology 317:220–236PubMedCrossRefGoogle Scholar
  32. 32.
    Lauzon HA, Lucarotti CJ, Krell PJ, Feng Q, Retnakaran A, Arif BM (2004) Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J Virol 78:7023–7035PubMedCrossRefGoogle Scholar
  33. 33.
    Lu A, Krell P, Vlak J, Rohrmann G (1997) Baculovirus DNA replication. In: Miller LK (ed) The baculoviruses. Plenum, New York, pp 171–192Google Scholar
  34. 34.
    Lu A, Miller LK (1997) Regulation of baculovirus late and very late gene expression. In: Miller LK (ed) The baculoviruses. Plenum, New York, pp 193–216Google Scholar
  35. 35.
    Luque T, Finch R, Crook N, O’Reilly DR, Winstanley D (2001) The complete sequence of Cydia pomonella granulovirus genome. J Gen Virol 82:2531–2547PubMedGoogle Scholar
  36. 36.
    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 77:328–339PubMedCrossRefGoogle Scholar
  37. 37.
    McCarthy CB, Theilmann DA (2008) AcMNPV ac143 (odv-e18) is essential for mediating budded virus production and is the 30th baculovirus core gene. Virology 375:277–291PubMedCrossRefGoogle Scholar
  38. 38.
    Morris TD, Lk Miller (1994) Mutational analysis of a baculovirus major late promoter. Gene 140:147–153PubMedCrossRefGoogle Scholar
  39. 39.
    Morris TD, Todd JW, Fisher B, Miller LK (1994) Identification of lef-7: a baculovirus gene affecting late gene expression. Virology 200:360–369PubMedCrossRefGoogle Scholar
  40. 40.
    Moscardi F (1999) Assessment of the applications of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289PubMedCrossRefGoogle Scholar
  41. 41.
    Nakai M, Goto C, Kang WK, Shikata M, Luque T, Kunimi Y (2003) Genome sequence and organization of a nucleopolyhedrovirus isolated from the smaller tea tortrix, Adoxophyes honmai. Virology 316:171–183PubMedCrossRefGoogle Scholar
  42. 42.
    O’Reilly DR (1997) Auxiliary genes of baculoviruses. In: Miller LK (ed) The baculoviruses. Plenum, New York, pp 276–300Google Scholar
  43. 43.
    O’Reilly DR, Miller LK (1991) Improvement of a baculovirus pesticide by deletion of the EGT Gene. Nat Biotechnol 9:1086–1089CrossRefGoogle Scholar
  44. 44.
    Pearson MN, Russell RLQ, Rohrmann GF (2002) Functional analysis of a conserved region of the baculovirus envelope fusion protein, LD130. Virology 304:81–88PubMedCrossRefGoogle Scholar
  45. 45.
    Pham DQ, Hicea RH, Sivasubramaniana N, Federicia BA (1993) The 1629-bp open reading frame of the Autographa californica multinucleocapsid nuclear polyhedrosis virus encodes a virion structural protein. Gene 137:275–280PubMedCrossRefGoogle Scholar
  46. 46.
    Pham DQ, Sivasubramaniana N (1992) Sequence and in vitro translational analysis of a 1629-nucleotide ORF in Autographa californica nuclear polyhedrosis virus strain E2. Gene 122:345–348PubMedCrossRefGoogle Scholar
  47. 47.
    Possee RD, Sun TP, Howarda SC, Ayresa MD, Michéle HP, Gearing KL (1991) Nucleotide sequence of the Autographa californica nuclear polyhedrosis 9.4 kbp EcoRI-I and -R (Polyhedrin gene) region. Virology 185:229–241PubMedCrossRefGoogle Scholar
  48. 48.
    Rapp JC, Wilson JA, Miller LK (1998) Nineteen baculovirus open reading frames, including LEF-12, support late gene expression. J Virol 72:10197–10206PubMedGoogle Scholar
  49. 49.
    Slack JM, Kuzio J, Faulkner P (1995) Characterization of v-cath, a cathepsin L-like proteinase expressed by the baculovirus Autographa californica multiple nuclear polyhedrosis virus. J Gen Virol 76:1091–1098PubMedCrossRefGoogle Scholar
  50. 50.
    Theilmann DA, Stewart S (1992) Tandemly repeated sequence at the 3’ end of the IE-2 gene of the baculovirus Orgyia pseudosugata multicapsid nuclear polyhedrosis virus is an enhancer element. Virology 187:97–106PubMedCrossRefGoogle Scholar
  51. 51.
    Van OMM, Vlak JM (1997) The baculovirus 10-kDa protein. J Inverteb Pathol 70:1–17CrossRefGoogle Scholar
  52. 52.
    Vaux DL, Strasser A (1996) The molecular biology of apoptosis. Proc Natl Acad Sci USA 93:2239–2244PubMedCrossRefGoogle Scholar
  53. 53.
    Vucic D, Kaiser WJ, Harvey AJ, Miller LK (1997) Inhibition of reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc Natl Acad Sci USA 94:10183–10188PubMedCrossRefGoogle Scholar
  54. 54.
    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 78:6946–6954PubMedCrossRefGoogle Scholar
  55. 55.
    Westenberg M, Wang HL, IJkel WFJ, Goldbach RW, Vlak JM, Zuidema D (2002) Furin is involved in baculovirus envelope fusion protein activation. J Virol 76:178–184PubMedCrossRefGoogle Scholar
  56. 56.
    Williams GV, Rohel DZ, Kuzio J, Faulkner P (1989) A cytopathological investigation of Autographa californica nuclear polyhedrosis virus p10 gene function using insertion/deletion mutants. J Gen Virol 70:187–202PubMedCrossRefGoogle Scholar
  57. 57.
    Winstanley D, Crook NE (1993) Replication of Cydia pomonella granulosis virus in cell cultures. J Gen Virol 74:1599–1609PubMedCrossRefGoogle Scholar
  58. 58.
    Wormleaton S, Kuzio J, Winstanley D (2003) The complete sequence of the Adoxophyes orana granulovirus genome. Virology 311:350–365PubMedCrossRefGoogle Scholar
  59. 59.
    Zhang D, Zhang Z, Yang K, Li B (2004) Genetic mapping in (Populus tomentosa × Populus bolleana) and P. tomentosa Carr. using AFLP markers. Theor Appl Genet 108:657–662PubMedCrossRefGoogle Scholar
  60. 60.
    Zhang XX, Liang ZP, Peng HY, Zhang ZX, Tang XC, Liu TQ (2005) Characterization and partial genome sequence analysis of Clostera anachoreta granulovirus. Virus Res 113:36–43PubMedCrossRefGoogle Scholar
  61. 61.
    Zhang XX, Liang ZP, Peng HY, Zhang ZX, Tang XC, Zhao SL, Xiao YZ, Zhang WJ (2006) Location and phylogenetic analysis of the region immediately upstream of the granulin gene of the Clostera anachoreta granulovirus. Virus Res 121:97–102PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Zhenpu Liang
    • 1
  • Xiaoxia Zhang
    • 1
  • Xinming Yin
    • 2
  • Sumei Cao
    • 1
  • Feng Xu
    • 1
  1. 1.College of Life SciencesHenan Agricultural UniversityZhengzhouChina
  2. 2.College of Plant ProtectionHenan Agricultural UniversityZhengzhouChina

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