Genome sequence of Erinnyis ello granulovirus (ErelGV), a natural cassava hornworm pesticide and the first sequenced sphingid-infecting betabaculovirus
© Ardisson-Araújo et al.; licensee BioMed Central Ltd. 2014
Received: 1 March 2014
Accepted: 25 September 2014
Published: 4 October 2014
Cassava (Manihot esculenta) is the basic source for dietary energy of 500 million people in the world. In Brazil, Erinnyis ello ello (Lepidoptera: Sphingidae) is a major pest of cassava crops and a bottleneck for its production. In the 1980s, a naturally occurring baculovirus was isolated from E. ello larva and successfully applied as a bio-pesticide in the field. Here, we described the structure, the complete genome sequence, and the phylogenetic relationships of the first sphingid-infecting betabaculovirus.
The baculovirus isolated from the cassava hornworm cadavers is a betabaculovirus designated Erinnyis ello granulovirus (ErelGV). The 102,759 bp long genome has a G + C content of 38.7%. We found 130 putative ORFs coding for polypeptides of at least 50 amino acid residues. Only eight genes were found to be unique. ErelGV is closely related to ChocGV and PiraGV isolates. We did not find typical homologous regions and cathepsin and chitinase homologous genes are lacked. The presence of he65 and p43 homologous genes suggests horizontal gene transfer from Alphabaculovirus. Moreover, we found a nucleotide metabolism-related gene and two genes that could be acquired probably from Densovirus.
The ErelGV represents a new virus species from the genus Betabaculovirus and is the closest relative of ChocGV. It contains a dUTPase-like, a he65-like, p43-like genes, which are also found in several other alpha- and betabaculovirus genomes, and two Densovirus-related genes. Importantly, recombination events between insect viruses from unrelated families and genera might drive baculovirus genomic evolution.
Cassava (Manihot esculenta) is the basic source for dietary energy of 500 million people in tropical and subtropical areas of Africa, Asia, and Latin America . In Brazil, the hornworm Erinnyis ello ello (Lepidoptera: Sphingidae) is one of the most important pests  occurring throughout the year and greatly impacting cassava production [3, 4]. This pest has been observed in 35 plant species, especially in the Euphorbiaceae family [5, 6]. In large infestations, the cassava pest may reduce by 50% the roots yield. In the 1980s, a naturally occurring baculovirus was isolated from this pest and applied as a bio-pesticide in Brazil . The biological control program has proven to be safe and economical [5, 6]. However, genomic and structural information about this virus is lacking.
The Baculoviridae is a family of insect viruses with circular double-stranded genomic DNA [7–9] that have been successfully applied for the control of agricultural and forest pests . So far, Alpha and Betabaculovirus are the most studied baculovirus genera; both infect Lepidoptera . The infection is initiated when larvae feed on foliage contaminated with orally infectious occlusion bodies (OBs)  that release occlusion derived-virions (ODVs) in the midgut . Early after primary midgut epithelial cell infection, budded virions (BV) are produced and cause systemic infection. Infection symptoms include cuticle discoloration, movement loss, and incapability for feeding [13, 14].
Few full-length betabaculovius genome sequences are available compared to those from Alphabaculovirus and none of them was isolated from sphingid host. In this context, identification and sequencing of virus species from different lepidopteran families will provide a wider empirical database to help understand baculovirus evolution [15, 16]. Here, we presented the morphological characterization, the complete genome sequence, and the phylogenetic analyses of the natural cassava hornworm pesticide, the first completely sequenced betabaculovirus isolated from a sphingid host.
Results and discussion
Virus characterization and genome features
All species from the genus Betabaculovirus completely sequenced to date
Adoxophyes orana granulovirus
Agrotis segetum granulovirus Xinjiang
Agrotis segetum granulovirus L1
Choristoneura occidentalis granulovirus
Clostera anachoreta granulovirus
Clostera anastomosis L. granulovirus
Cryptophlebia leucotreta granulovirus
Cydia pomonella granulovirus
Epinotia aporema granulovirus
Erinnyis ello granulovirus
Helicoverpa armigera granulovirus
Phthorimaea operculella granulovirus
Pieris rapae granulovirus China
Pieris rapae granulovirus E3
Pieris rapae granulovirus South Korea
Plutella xylostella granulovirus
Pseudaletia unipuncta granulovirus
Spodoptera litura granulovirus
Xestia c-nigrum granulovirus
Lack of cathepsin and chitinasegenes
ErelGV lacks cathepsin and chitinase genes, despite of their importance for promoting baculovirus horizontal transmission . This feature can explain the integrity of caterpillar flesh and light color after death (Figure 1A). Other betabaculovirus genomes also lack both enzymes: complete deletion in ChocGV , Adoxophyes orana granulovirus (AdorGV) , Phthorimaea opercullela granulovirus (PhopGV) (unpublished), PlxyGV  and Spodoptera litura granulovirus (SpliGV) ; Cryptophlebia leucotreta granulovirus (CrleGV)  chitinase has an interruption; and in Helicoverpa armigera granulovirus (HearGV)  only cathepsin is absent. Interestingly, most of these deletions seem to have occurred independently of each other within Betabaculovirus (data not shown), aside from ChocGV and ErelGV in which is strongly supported an ancestral lacking. Thus, it is reasonable to expect that AnbiGV, the closest relative to ErelGV, might also lack both cathepsin and chitinase. Taken together, these results reinforce the notion that both genes are most likely non-essential for the persistence of baculoviruses in the environment. Conversely, previous work from our research team has shown that introduction of cathepsin and chitinase from Choristoneura fumiferana defective nucleopolyhedrovirus into AgMNPV (which naturally lacks both genes) increases pathogenicity and occlusion body production relative to the wild type virus .
ErelOrf-5 codes for a nucleotide metabolism-related gene homologous to Orgyia pseudotsugata multiple nucleopolyhedrovirus (OpMNPV) Orf-31. The gene seems to be composed of a fusion between two distinct ORFs; the C-terminal portion is related to a baculovirus thymidylate kinase-like gene and the N-terminal portion is related to several dUTPase-like genes. The thymidylate kinase enzyme catalyzes a critical step in the biosynthesis of deoxythymidine triphosphate . dUTPase catalyses dUTP dephosphorylation to generate dUMP . High levels of dUTP can be deleterious for virus genomic DNA replication since dTTP can be substituted for dUTP during DNA synthesis . A high dUTP/dTTP ratio promotes uracil incorporation into DNA. Uracils in DNA are then targeted by uracil DNA glycosylase and excised, leading to futile repair cycles and DNA breakage and or translesional DNA synthesis [53, 54]. Nucleotide metabolism-related enzyme acquisition is common in baculoviruses  and could avoid this deleterious response by decreasing the dUTP/dTTP ratio, however how these genes alter the virus fitness is not clear .
The he65-like and p43-like genes
Furthermore, we found in ErelGV genome a p43-like gene (ErelOrf-105) whose homologues were found only in baculovirus species from the genus Alphabaculovirus (Figure 4B) with conserved amino acid sequence and position in the genome . Deletion of p43 in AcMNPV does not affect virus replication in cell culture and the reason for gene acquisition and preservation is not clear . Two hypotheses can be raised for p43 introduction in ErelGV: (i) ErelGV acquired the p43-like gene from Group I Alphabaculovirus, specifically from AcMNPV-related viruses; or (ii) ErelGV acquired from Group II Alphabaculovirus, specifically from a baculovirus (e.g. Clanis bilineata nucleopolyhedrovirus - ClbiNPV ) during co-infection of a sphingid host.
Acquisitions of Densovirus-related genes in Betabaculovirus
ErelGV is a new betabaculovirus species closely related to ChocGV and PiraGV isolates. Its genome encodes 130 ORFs, eight of which are unique. We found evidence suggesting horizontal gene transfers from Alphabaculovirus and Densovirus to Betabaculovirus. The he65-like gene was independently acquired tree times from Alphabaculovirus. We found a dUTPase-like gene homologous to OpMNPV Orf-31 and two Densovirus-related genes. The contribution of these genes to baculovirus fitness is not clear and is being experimentally tested in our lab. Importantly, recombination events between insect viruses from unrelated families and genera might drive baculovirus genomic evolution.
Nucleotide sequence accession number
The ErelGV genome sequence was submitted to GenBank under accession number KJ406702.
Availability of supporting data
The complete ErelGV genome sequence has been submitted to GenBank (accession number KJ406702). All supporting data is included as additional files.
Insect cadavers of the hornworm E. ello ello with baculovirus infection symptoms were collected in cassava crops in the South of Brazil (Itajaí, Santa Catarina) in 1986. They were kindly provided by Dr. Renato Arcanjo Pegoraro (EPAGRI). The cadavers were kept in the freezer and later used for OBs purification. Insect cadavers were homogenized with ddH2O (w/v), filtered through three layers of gauze, and centrifuged at 7,000 x g for 10 min. The pellet was resuspended in 0.5% (w/v) SDS and again centrifuged at 7,000 x g for 10 min. The dilution and centrifugation steps were repeated four times, and the final pellet was washed in 0.5 M NaCl. The pellet was resuspended in ddH2O, loaded onto a continuous 40-65% sucrose gradient, and centrifuged at 104.000 x g for 40 min at 4°C. The OB band was collected, diluted 4-fold in ddH2O, and centrifuged at 7,000 x g for 15 min at 4°C.
For scanning electron microscopy (SEM), 100 μl of the OB-containing solution (109 OBs/ml) were incubated with 300 μl of acetone at 25°C for 1 hour. The solution was loaded in a metallic stub, dried overnight at 37°C, coated with gold in a Sputter Coater (Balzers) for 3 min, and observed in a scanning electron microscope Jeol JSM 840 A at 10 kV. For transmission electron microscopy (TEM) pellets of purified granules were fixed in Karnovsky fixative (2.5% glutaraldehyde, 2% paraformaldehyde, in 0.1 M, cacodylate buffer, pH 7.2) for 2 h, post-fixed in 1% osmium tetroxide in the same buffer for 1 h and then stained en bloc with 0.5% aqueous uranyl acetate, dehydrated in acetone, and embedded in Spurr’s low viscosity embedding medium. The ultrathin sections were contrasted with 2% uranyl acetate and observed in a ZEISS TEM 109 at 80 kV.
Genomic DNA restriction analyses
Purified granules (109 OBs/ml) were dissolved in an alkaline solution and used to extract DNA according to O’Reilly et al. . The quantity and quality of the isolated DNA were determined by electrophoresis on 0.8% agarose (data not shown). The viral DNA (1–2 μg) was individually cleaved with the restriction enzymes HindIII, EcoRI, and BamHI (Promega) according to manufacturer’s instructions. The DNA fragments generated were analyzed by 0.8% agarose gel electrophoresis , visualized, and photographed in AlphaImager® Mini (Alpha Innothech).
Genome sequencing, assembly, and annotation
ErelGV genomic DNA was sequenced with the 454 Genome Sequencer (GS) FLX™ Standard (Roche) at the Centro de Genômica de Alto Desempenho do Distrito Federal (Brasília, Brazil). The genome was assembled de novo using Geneious 6.0  and confirmed using restriction enzyme digestion profile. The annotation was performed using Geneious 6.0 to identify the open reading frames (ORFs) that started with a methionine codon (ATG) encoding at least 50 amino acids and blastp  to identify homologues.
Phylogeny, genome, and gene comparisons
For Baculoviridae phylogenetic analysis, a MAFFT alignment  was carried out with concatenated amino acid sequences predicted for 37 baculovirus core genes. A maximum likelihood tree was inferred using PhyML with 100 repetitions of a non parametric bootstrap , implemented in Geneious, with LG + I + G + F model selected by Prottest 2.4 . Moreover, a genomic comparison was performed using the protein dataset of all the complete Betabaculovirus genomes available in Genbank. The dataset was compared using CGView Comparison Tool  and the results were plotted using CIRCOS . We also compared ChocGV and PiraGV genomes with ErelGV genome using Mauve alignment . The horizontal gene transfer (HGTs) events were investigated comparing the maximum likelihood phylogenetic tree inferred using the RAxML method  and a MAFT alignment of homologues for he65-like and p43-like, and Densovirus-related genes with 100 repetitions of a non parametric bootstrap for branch support.
Conceived and designed the experiments: DMPAA, FLM, BMR, MLS; Performed the experiments: DMPAA, FLM, MSA, WS; Analyzed the data: DMPAA, FLM, BMR; Contributed reagents/materials/analysis tools: BMR, DMPAA, FLM, MSA, SNB, MLS; Wrote the paper: DMPAA, FLM, BMR, MLS. All authors read and approved the final manuscript.
We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and EMBRAPA Recursos Genéticos e Biotecnologia for the financial support; José Osmar Lorenzi for the picture of E. ello ello infected by ErelGV; Ingrid Gracielle Martins da Silva for kindly helping with the sample for microscopy; and Jeffrey J. Hodgson for kindly reviewing the English writing style.
- El-Sharkawy MA: Cassava biology and physiology. Plant Mol Biol. 2004, 56 (4): 21-View ArticleGoogle Scholar
- Pietrowski V, Ringenberger R, Rheinheimer AR, Bellon PP, Gazola D, Miranda AM: Insetos-praga da cultura da mandioca na região Centro-Sul do Brasil. 2010, Marechal Cândido Rondon - Parana: EMBRAPA, 1:Google Scholar
- Bellotti AC, Arias B, Guzman OL: Biological control of the cassava hornworm erinnyis ello (Lepidoptera: Sphingidae). The Florida Entomologist. 1992, 75 (4): 10-View ArticleGoogle Scholar
- Fazolin M, Estrela JLV, Filho MDC, Santiago ACC, Frota FS: Manejo Integrado do Mandarová-da-Mandioca Erinnyis ello (L.) (Lepidoptera: Sphingidae): Conceitos e Experiências na Região do Vale do Rio Juruá, Acre. Edited by: Embrapa. 2007, Rio Branco, Brasil: EmbrapaGoogle Scholar
- Schmitt AT: Eficiência da aplicação de Baculovirus erinnyis no controle do mandarová da mandioca. 1985, Florianópolis, Santa Catarina - Brasil: EMPASC Comunicado Técnico edn, 88:Google Scholar
- Schmitt AT: Principais insetos pragas da mandioca e seu controle. Cultura de tuberosas amiláceas Latino Americanas. Edited by: Cereda MP. 2002, São Paulo: Fundação Cargill, 2: 7-Google Scholar
- Rohrmann GF: Baculovirus Molecular Biology, Third Edition [Internet] edn. 2011, Bethesda (MD): National Center for Biotechnology Information (US), Available from: http://www.ncbi.nlm.nih.gov/books/NBK49500/Google Scholar
- Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM: On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol. 2006, 151 (7): 1257-1266. 10.1007/s00705-006-0763-6.PubMedView ArticleGoogle Scholar
- Herniou EA, Arif BM, Becnel JJ, Blissard GW, Bonning B, Harrison R, Jehle JA, Theilmann DA, Vlak JM: Baculoviridae. Virus taxonomy Ninth Report of the International Committee on Taxonomy of Viruses. Edited by: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 2012, San Diego: Elsevier-Academic Press, 163-173.Google Scholar
- Moscardi F: Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol. 1999, 44: 257-289. 10.1146/annurev.ento.44.1.257.PubMedView ArticleGoogle Scholar
- Ji X, Sutton G, Evans G, Axford D, Owen R, Stuart DI: How baculovirus polyhedra fit square pegs into round holes to robustly package viruses. EMBO J. 2010, 29 (2): 505-514. 10.1038/emboj.2009.352.PubMed CentralPubMedView ArticleGoogle Scholar
- Slack J, Arif BM: The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res. 2007, 69: 99-165.PubMedView ArticleGoogle Scholar
- Wang R, Deng F, Hou D, Zhao Y, Guo L, Wang H, Hu Z: Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol. 2010, 84 (14): 7233-7242. 10.1128/JVI.00040-10.PubMed CentralPubMedView ArticleGoogle Scholar
- Washburn JO, Chan EY, Volkman LE, Aumiller JJ, Jarvis DL: Early synthesis of budded virus envelope fusion protein GP64 enhances Autographa californica multicapsid nucleopolyhedrovirus virulence in orally infected Heliothis virescens. J Virol. 2003, 77 (1): 280-290. 10.1128/JVI.77.1.280-290.2003.PubMed CentralPubMedView ArticleGoogle Scholar
- Herniou EA, Olszewski JA, Cory JS, O'Reilly DR: The genome sequence and evolution of baculoviruses. Annu Rev Entomol. 2003, 48: 211-234. 10.1146/annurev.ento.48.091801.112756.PubMedView ArticleGoogle Scholar
- Herniou EA, Luque T, Chen X, Vlak JM, Winstanley D, Cory JS, O'Reilly DR: Use of whole genome sequence data to infer baculovirus phylogeny. J Virol. 2001, 75 (17): 8117-8126. 10.1128/JVI.75.17.8117-8126.2001.PubMed CentralPubMedView ArticleGoogle Scholar
- Hoover K, Grove M, Gardner M, Hughes DP, McNeil J, Slavicek J: A gene for an extended phenotype. Science. 2011, 333 (6048): 1401-10.1126/science.1209199.PubMedView ArticleGoogle Scholar
- Ackermann H, Smirnoff W: A morphological investigation of 23 baculoviruses. J Invertebr Pathol. 1983, 41: 12-View ArticleGoogle Scholar
- Finnerty CM, Li G, Granados RR: Characterization of a granulovirus from the cassava hornworm (Erinnyis ello: Sphingidae). J Invertebr Pathol. 2000, 75 (4): 273-278. 10.1006/jipa.2000.4929.PubMedView ArticleGoogle Scholar
- Jehle JA, Lange M, Wang H, Hu Z, Wang Y, Hauschild R: Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology. 2006, 346 (1): 180-193. 10.1016/j.virol.2005.10.032.PubMedView ArticleGoogle Scholar
- Escasa SR, Lauzon HA, Mathur AC, Krell PJ, Arif BM: Sequence analysis of the Choristoneura occidentalis granulovirus genome. J Gen Virol. 2006, 87 (Pt 7): 1917-1933.PubMedView ArticleGoogle Scholar
- Garavaglia MJ, Miele SA, Iserte JA, Belaich MN, Ghiringhelli PD: The ac53, ac78, ac101, and ac103 genes are newly discovered core genes in the family Baculoviridae. J Virol. 2012, 86 (22): 12069-12079. 10.1128/JVI.01873-12.PubMed CentralPubMedView ArticleGoogle Scholar
- Wormleaton S, Kuzio J, Winstanley D: The complete sequence of the Adoxophyes orana granulovirus genome. Virology. 2003, 311 (2): 350-365. 10.1016/S0042-6822(03)00149-1.PubMedView ArticleGoogle Scholar
- Zhang X, Liang Z, Yin X, Wang J, Shao X: Complete genome sequence of Agrotis segetum granulovirus Shanghai strain. Arch Virol. 2014, http://dx.doi.org/10.1007/s00705-014-2001-y,Google Scholar
- Liang Z, Zhang X, Yin X, Cao S, Xu F: Genomic sequencing and analysis of Clostera anachoreta granulovirus. Arch Virol. 2011, 156 (7): 1185-1198. 10.1007/s00705-011-0977-0.PubMedView ArticleGoogle Scholar
- Lange M, Jehle JA: The genome of the Cryptophlebia leucotreta granulovirus. Virology. 2003, 317 (2): 220-236. 10.1016/S0042-6822(03)00515-4.PubMedView ArticleGoogle Scholar
- Luque T, Finch R, Crook N, O'Reilly DR, Winstanley D: The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol. 2001, 82 (Pt 10): 2531-2547.PubMedView ArticleGoogle Scholar
- Ferrelli ML, Salvador R, Biedma ME, Berretta MF, Haase S, Sciocco-Cap A, Ghiringhelli PD, Romanowski V: Genome of Epinotia aporema granulovirus (EpapGV), a polyorganotropic fast killing betabaculovirus with a novel thymidylate kinase gene. BMC Genomics. 2012, 13: 14-10.1186/1471-2164-13-14.View ArticleGoogle Scholar
- Harrison RL, Popham HJ: Genomic sequence analysis of a granulovirus isolated from the Old World bollworm, Helicoverpa armigera. Virus Genes. 2008, 36 (3): 565-581. 10.1007/s11262-008-0218-0.PubMedView ArticleGoogle Scholar
- Zhang BQ, Cheng RL, Wang XF, Zhang CX: The Genome of Pieris rapae Granulovirus. J Virol. 2012, 86 (17): 9544-10.1128/JVI.01431-12.PubMed CentralPubMedView ArticleGoogle Scholar
- Hashimoto Y, Hayakawa T, Ueno Y, Fujita T, Sano Y, Matsumoto T: Sequence analysis of the Plutella xylostella granulovirus genome. Virology. 2000, 275 (2): 358-372. 10.1006/viro.2000.0530.PubMedView ArticleGoogle Scholar
- Wang Y, Choi JY, Roh JY, Liu Q, Tao XY, Park JB, Kim JS, Je YH: Genomic sequence analysis of granulovirus isolated from the tobacco cutworm, Spodoptera litura. PLoS One. 2011, 6 (11): e28163-10.1371/journal.pone.0028163.PubMed CentralPubMedView ArticleGoogle Scholar
- Hayakawa T, Ko R, Okano K, Seong SI, Goto C, Maeda S: Sequence analysis of the Xestia c-nigrum granulovirus genome. Virology. 1999, 262 (2): 277-297. 10.1006/viro.1999.9894.PubMedView ArticleGoogle Scholar
- Darling AC, Mau B, Blattner FR, Perna NT: Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004, 14 (7): 1394-1403. 10.1101/gr.2289704.PubMed CentralPubMedView ArticleGoogle Scholar
- Lange M, Wang H, Zhihong H, Jehle JA: Towards a molecular identification and classification system of lepidopteran-specific baculoviruses. Virology. 2004, 325 (1): 36-47. 10.1016/j.virol.2004.04.023.PubMedView ArticleGoogle Scholar
- Grant JR, Arantes AS, Stothard P: Comparing thousands of circular genomes using the CGView Comparison Tool. BMC Genomics. 2012, 13: 8-10.1186/1471-2164-13-8.View ArticleGoogle Scholar
- Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA: Circos: an information aesthetic for comparative genomics. Genome Res. 2009, 19 (9): 1639-1645. 10.1101/gr.092759.109.PubMed CentralPubMedView ArticleGoogle Scholar
- Pearson MN, Rohrmann GF: Transfer, incorporation, and substitution of envelope fusion proteins among members of the Baculoviridae, Orthomyxoviridae, and Metaviridae (insect retrovirus) families. J Virol. 2002, 76 (11): 5301-5304. 10.1128/JVI.76.11.5301-5304.2002.PubMed CentralPubMedView ArticleGoogle Scholar
- Oomens AG, Blissard GW: Requirement for GP64 to drive efficient budding of Autographa californica multicapsid nucleopolyhedrovirus. Virology. 1999, 254 (2): 297-314. 10.1006/viro.1998.9523.PubMedView ArticleGoogle Scholar
- Wang M, Yin F, Shen S, Tan Y, Deng F, Vlak JM, Hu Z, Wang H: Partial functional rescue of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus infectivity by replacement of F protein with GP64 from Autographa californica multicapsid nucleopolyhedrovirus. J Virol. 2010, 84 (21): 11505-11514. 10.1128/JVI.00862-10.PubMed CentralPubMedView ArticleGoogle Scholar
- Wang M, Tan Y, Yin F, Deng F, Vlak JM, Hu Z, Wang H: The F protein of Helicoverpa armigera single nucleopolyhedrovirus can be substituted functionally with its homologue from Spodoptera exigua multiple nucleopolyhedrovirus. J Gen Virol. 2008, 89 (Pt 3): 791-798.PubMedView ArticleGoogle Scholar
- Lung O, Westenberg M, Vlak JM, Zuidema D, Blissard GW: Pseudotyping Autographa californica multicapsid nucleopolyhedrovirus (AcMNPV): F proteins from group II NPVs are functionally analogous to AcMNPV GP64. J Virol. 2002, 76 (11): 5729-5736. 10.1128/JVI.76.11.5729-5736.2002.PubMed CentralPubMedView ArticleGoogle Scholar
- Harrison RL, Lynn DE: Genomic sequence analysis of a nucleopolyhedrovirus isolated from the diamondback moth, Plutella xylostella. Virus Genes. 2007, 35 (3): 857-873. 10.1007/s11262-007-0136-6.PubMedView ArticleGoogle Scholar
- Wennmann JT, Jehle JA: Detection and quantitation of Agrotis baculoviruses in mixed infections. J Virol Methods. 2014, 197: 39-46.PubMedView ArticleGoogle Scholar
- Ko R, Okano K, Maeda S: Structural and functional analysis of the Xestia c-nigrum granulovirus matrix metalloproteinase. J Virol. 2000, 74 (23): 11240-11246. 10.1128/JVI.74.23.11240-11246.2000.PubMed CentralPubMedView ArticleGoogle Scholar
- Means JC, Passarelli AL: Viral fibroblast growth factor, matrix metalloproteases, and caspases are associated with enhancing systemic infection by baculoviruses. Proc Natl Acad Sci U S A. 2010, 107 (21): 9825-9830. 10.1073/pnas.0913582107.PubMed CentralPubMedView ArticleGoogle Scholar
- Lepore LS, Roelvink PR, Granados RR: Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J Invertebr Pathol. 1996, 68 (2): 131-140. 10.1006/jipa.1996.0070.PubMedView ArticleGoogle Scholar
- D'Amico V, Slavicek J, Podgwaite JD, Webb R, Fuester R, Peiffer RA: Deletion of v-chiA from a baculovirus reduces horizontal transmission in the field. Appl Environ Microbiol. 2013, 79 (13): 4056-4064. 10.1128/AEM.00152-13.PubMed CentralPubMedView ArticleGoogle Scholar
- Lima AA, Aragao CW, de Castro ME, Oliveira JV, Sosa Gomez DR, Ribeiro BM: A Recombinant MNPV Harboring and Genes from Defective NPV Induce Host Liquefaction and Increased Insecticidal Activity. PLoS One. 2013, 8 (9): e74592-10.1371/journal.pone.0074592.PubMed CentralPubMedView ArticleGoogle Scholar
- Cui Q, Shin WS, Luo Y, Tian J, Cui H, Yin D: Thymidylate kinase: an old topic brings new perspectives. Curr Med Chem. 2013, 20 (10): 1286-1305. 10.2174/0929867311320100006.PubMedView ArticleGoogle Scholar
- Penades JR, Donderis J, Garcia-Caballer M, Tormo-Mas MA, Marina A: dUTPases, the unexplored family of signalling molecules. Curr Opin Microbiol. 2013, 16 (2): 163-170. 10.1016/j.mib.2013.02.005.PubMedView ArticleGoogle Scholar
- Priet S, Sire J, Querat G: Uracils as a cellular weapon against viruses and mechanisms of viral escape. Curr HIV Res. 2006, 4 (1): 31-42. 10.2174/157016206775197673.PubMedView ArticleGoogle Scholar
- Castillo-Acosta VM, Aguilar-Pereyra F, Bart JM, Navarro M, Ruiz-Perez LM, Vidal AE, Gonzalez-Pacanowska D: Increased uracil insertion in DNA is cytotoxic and increases the frequency of mutation, double strand break formation and VSG switching in Trypanosoma brucei. DNA Repair (Amst). 2012, 11 (12): 986-995. 10.1016/j.dnarep.2012.09.007.View ArticleGoogle Scholar
- Guillet M, Van Der Kemp PA, Boiteux S: dUTPase activity is critical to maintain genetic stability in Saccharomyces cerevisiae. Nucleic Acids Res. 2006, 34 (7): 2056-2066. 10.1093/nar/gkl139.PubMed CentralPubMedView ArticleGoogle Scholar
- Herniou EA, Jehle JA: Baculovirus phylogeny and evolution. Curr Drug Targets. 2007, 8 (10): 1043-1050. 10.2174/138945007782151306.PubMedView ArticleGoogle Scholar
- Ho CK, Shuman S: Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc Natl Acad Sci U S A. 2002, 99 (20): 12709-12714. 10.1073/pnas.192184699.PubMed CentralPubMedView ArticleGoogle Scholar
- Yu M, Carstens EB: Characterization of an Autographa californica multiple nucleopolyhedrovirus mutant lacking the ac39(p43) gene. Virus Res. 2011, 155 (1): 300-306. 10.1016/j.virusres.2010.10.025.PubMedView ArticleGoogle Scholar
- Zhu SY, Yi JP, Shen WD, Wang LQ, He HG, Wang Y, Li B, Wang WB: Genomic sequence, organization and characteristics of a new nucleopolyhedrovirus isolated from Clanis bilineata larva. BMC Genomics. 2009, 10: 91-10.1186/1471-2164-10-91.PubMed CentralPubMedView ArticleGoogle Scholar
- Lauzon HA, Lucarotti CJ, Krell PJ, Feng Q, Retnakaran A, Arif BM: Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J Virol. 2004, 78 (13): 7023-7035. 10.1128/JVI.78.13.7023-7035.2004.PubMed CentralPubMedView ArticleGoogle Scholar
- O'Reilly D, Miller LK, Luckow VA: Baculovirus Expression Vectors: a laboratory manual. 1992, New York: Freeman and CompanyGoogle Scholar
- Sambrook J, Russel DW: Molecular Cloning: a laboratory manual, 3rd ed. edn. 2001, New York: Cold Spring HarborGoogle Scholar
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A: Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012, 28 (12): 1647-1649. 10.1093/bioinformatics/bts199.PubMed CentralPubMedView ArticleGoogle Scholar
- Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25 (17): 3389-3402. 10.1093/nar/25.17.3389.PubMed CentralPubMedView ArticleGoogle Scholar
- 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 (14): 3059-3066. 10.1093/nar/gkf436.PubMed CentralPubMedView ArticleGoogle Scholar
- Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010, 59 (3): 307-321. 10.1093/sysbio/syq010.PubMedView ArticleGoogle Scholar
- Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 2005, 21 (9): 2104-2105. 10.1093/bioinformatics/bti263.PubMedView ArticleGoogle Scholar
- Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol. 2008, 57 (5): 758-771. 10.1080/10635150802429642.PubMedView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.