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1 School of Integrative Biology, University of Queensland, St Lucia, QLD 4072, Australia
2 Australian Genome Research Facility, University of Queensland, St Lucia, QLD 4072, Australia
Correspondence
Sassan Asgari
s.asgari{at}uq.edu.au
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the sequence reported in this paper is EF133465.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). AVs have large, enveloped virions (130x400 nm) that are allantoid to bacilliform in shape and have a complex symmetry (Federici et al., 1991). The size of the circular genome ranges from 100 to 180 kbp (Bigot et al., 1997b; Cheng et al., 1999; Federici et al., 2005). The pathology of AVs is distinguished from that of other viruses by producing a milky-white discoloration of the haemolymph in the infected host, caused by accumulation of a high concentration of virion-containing vesicles. The vesicles are formed by the cleavage of the host-cell membrane, a unique sign of AV infection (Federici, 1983).
Four species of AV are currently recognized: Spodoptera frugiperda AV (SfAV-1), Trichoplusia ni AV (TnAV-2), Heliothis virescens AV (HvAV-3) and Diadromus pulchellus AV (DpAV-4). Phylogenetic studies based on several genes characterized from the AVs indicate that SfAV-1, TnAV-2 and HvAV-3 cluster together on the same branch, whereas DpAV is found on a separate branch (Federici & Bigot, 2003). This is probably a reflection of the biology and association of the viruses with their parasitoid vector. Members of the former group are transferred mechanically by parasitoids and are antagonistic, leading to the death of the developing parasitoid (Stasiak et al., 2005), whereas DpAV is transmitted vertically and has a mutualistic association with its wasp vector (Bigot et al., 1997a). Further phylogenetic studies revealed that invertebrate iridoviruses are related closely to AVs (Stasiak et al., 2003), despite major differences in their cell biology.
An Australian AV was isolated from Helicoverpa armigera larvae in south-east Queensland (Newton, 2003). Here, by using DNA hybridization, we show that little hybridization occurs between TnAV-2 and the Australian isolate under high-stringency conditions. However, HvAV-3 genomic DNA (gDNA) hybridized strongly to all restriction fragments from the Australian isolate. This isolate was previously designated HvAV-3e, a variant of HvAV, based only on the DNA polymerase and the major capsid protein sequences (Stasiak et al., 2005). The hybridization results confirmed the identity of the isolate as a variant of HvAV-3.
Recently, the complete genome sequences of SfAV-1a (156 922 bp) and TnAV-2c (174 059 bp) were determined (Bideshi et al., 2006; Wang et al., 2006). TnAV is very AT-rich (G+C content, 35.4 mol%) and contains two homologous regions (hrs), whereas SfAV has a G+C content of 49.2 mol% with four complete repeats and a partial one. Here, we present the complete genome sequence of HvAV-3e, with a G+C content of 45.8 mol%. The genome is significantly larger than those of TnAV-2c and SfAV-1a, with five hr regions containing transposase domains that are not present in the TnAV-2c genome. In addition, the HvAV-3e genome contains 23 baculovirus repeated ORF (Bro) proteins, compared with three in TnAV-2c and seven in SfAV-1a. Only one copy of the major capsid protein and thymidine kinase were found in HvAV-3e, compared with two copies of each gene in TnAV-2c.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. Briefly, vesicles were mixed with 10 ml 1 % Triton X-100 and pipetted several times by force to break the vesicles and release the virions (about 1 min). The suspension was centrifuged at 2000 g for 10 min at 4 °C and the supernatant was layered onto a sucrose gradient (20–55 % in sodium phosphate buffer, pH 7.4) and centrifuged at 75 000 g at 4 °C for 1 h. The virus band was taken out by using a glass Pasteur pipette, diluted several times with sodium phosphate buffer and centrifuged at 110 000 g at 4 °C for 1 h. The pellet was incubated overnight at 4 °C with 0.5 ml sodium phosphate buffer to resuspend the virions. Viral DNA was isolated from the virions by using Qiagen's Genomic Tip 100/G according to the manufacturer's instructions.
Restriction fragment-length polymorphism (RFLP) analysis and Southern hybridization.
Four hundred nanograms of AV gDNA was digested with BamHI, EcoRI, HindIII, PstI, XbaI and XhoI and run on 0.7 % TAE/agarose gel. DNA fragments were then transferred onto a nylon membrane by Southern hybridization as described by Sambrook et al. (1989). The membrane was fixed with UV light and probed with HvAV-3 and TnAV-2c purified gDNA, kindly donated by Xiao-Wen Cheng (Miami University, Oxford, OH, USA). Viral gDNA (50 ng) used as probe was digested with Sau3AI for 2 h, denatured and labelled with [32P]dCTP by using a Ready-to-Go labelling kit (Amersham). Hybridization was carried out overnight at 65 °C, followed by four washes with 2x SSC/0.1 % SDS (20 min twice) and 0.2x SSC/0.1 % SDS (20 min twice) at 65 °C. For reusing the membrane, the old probe was removed by incubating the membrane in 0.4 M NaOH at 42 °C for 30 min, followed by washing with 2x SSC/0.1 % SDS for a further 15 min.
DNA cloning and sequencing.
Purified viral DNA was sheared into fragments of 4–8 kb by a GeneMachines Hydroshear and then cloned into pSMART-LC (Lucigen Corp.). DNA templates for sequencing were prepared by using an in-house alkaline lysis method. Plasmids were sequenced with Applied Biosystems (ABI) BigDye Terminator v3.1 sequencing chemistry and analysed on ABI 3730xl sequencers. The combination of shotgun cloning, primer walking and PCR gap-closure reactions generated a 9.5x sequence coverage.
Sequence analysis.
Shotgun sequence reads were quality-scored by using PHRED and assembled by using PHRAP. Assemblies were viewed and finishing reactions were designed within CONSED. All programs are available at http://www.phrap.org. Open reading frames (ORFs) were identified by using GLIMMER 2.13 (Delcher et al., 1999), ORF finder (NCBI) and VectorNTI (Invitrogen). ORFs encoding >50 aa with minimal overlap were considered as putative genes. Functional assignments were made by similarity searches of each of the putative ORFs in GenBank and its viral subdivision and in UniRef100, using RPSBLAST to search against the conserved-domain database. Repetitive regions were identified by using the MIROPEATS program (Parsons, 1995). Similarity between AV genomes was investigated by using BLASTP (NCBI) analysis of predicted ORFs against the SfAV-1a and TnAV-2c predicted proteins. Genes with 25 % or more overall amino acid identity were considered homologues. Gene-parity plots were produced by comparing the HvAV-3e genome with the SfAV-1a and TnAV-2c genomes as described previously (Hu et al., 1998).
Confirmation of the assembled gDNA sequence.
The genome assembly was confirmed by comparison of restriction digests of the viral gDNA with BamHI and NotI restriction enzymes to the in silico-predicted digestion patterns.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), was named HvAV-3e based only on sequence comparison of the DNA polymerase and major capsid protein genes with those of other AVs (Stasiak et al., 2005). Phylogenetic studies using these two genes showed that HvAV-3e is related closely to SeAV-5a and other HvAV-3 strains (Stasiak et al., 2005). A more recent investigation indicated that SeAV-5a is in fact a variant of HvAV-3, as Southern hybridization under high-stringency conditions revealed that HvAV-3 total gDNA hybridized to all restriction fragments from SeAV-5a and vice versa (Cheng et al., 2005).
To confirm the identity of the Australian isolate further, Southern hybridizations were carried out by using TnAV-2c and HvAV-3 total gDNA as probes. When restriction fragments of the Australian isolate were probed with TnAV-2 gDNA under high-stringency conditions, only weak hybridizations to one or two fragments were detected (Fig. 1a). However, when HvAV-3 gDNA was used as a probe, it hybridized strongly to all fragments from the Australian isolate, although differences in the banding patterns of restriction digests by BamHI and HindIII were observed (Fig. 1b). This confirmed that the Australian isolate is a variant of HvAV-3. Therefore, we confirm the identity of the isolate and use the previous designation HvAV-3e. The number behind the viral species refers to the chronological order of discovery and the lower-case letter to the genotype (Federici et al., 2005).
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; Cheng et al., 1999; Federici et al., 2005). However, HvAV-3 seems to be the largest AV sequenced so far, as the TnAV-2c complete genome is 174 059 bp in length and that of SfAV-1a is 156 922 bp. The size of predicted restriction fragments in the genome for BamHI, NotI and AvrII matched the size of the fragments produced by restriction digestion of the purified DNA (data not shown). Based on these restriction patterns, the circular arrangement of the genome was also confirmed, as shown previously (Cheng et al., 1999). The G+C content of the HvAV-3e genome is 45.8 mol%, which is higher than those for TnAV-2c (35.4 mol%) and Chilo suppressalis iridovirus (CIV), the closest relative of AVs (28.63 mol%), but closer to that for SfAV-1a (49.2 mol%) (Table 1). The adenine residue at the translational initiation codon of the gene encoding the DNA polymerase protein was designated the start point of the physical map of HvAV DNA (Fig. 2) and, therefore, the DNA polymerase gene determines the orientation of the physical map.
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). The number and orientation of ORFs are shown in Table 2 and Fig. 2
. The 180 predicted ORFs account for 86.8 % of the total genome. The longest ORF is 3465 nt, encoding RNA polymerase. Interestingly, only two genes were found to show similarity to a Cotesia congregata polydnavirus (PDV) putative protein (ORF2, 23 % identity; ORF112, 36 % identity), which was not found in any other PDV genome sequence available in GenBank. A copy of this gene was also found in the TnAV-2c genome; however, none were found in the SfAV-1a genome. It has been postulated that AVs are perhaps the closest relative of PDVs (Federici & Bigot, 2003; Whitfield & Asgari, 2003). AV and PDV genome analyses indicate that not only are PDVs and AVs unrelated, but also that PDVs are probably not related to any other group of viruses (Espagne et al., 2004; Webb et al., 2006).
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). ORF11 showed 31 % identity to Lymphocystis disease virus 1, containing domains 1, 3, 5, part of 4, subunit A N terminus (RPOLA-N) and RPOC (
subunit). ORF64 showed 35 % identity to Chilo iridescent virus Ddrp, covering 848 aa. It contained Rpb-2 and Rpo8 of the subunit plus domains 6 and 7. ORF82 showed 27 % similarity to Singapore grouper iridovirus Ddrp and contained two parts of Rpb-1 domain 5. A homologue of the gene was also found in the CIV genome (34 % identity).
Three nucleases were found that are normally involved in DNA repair (ORF71), inhibiting host-cellular gene expression (ORF80; homologous to virion host shutoff from various herpesviruses) and RNA or DNA cleavage with no base specificity (ORF134; an S1/P1 nuclease) (Marchler-Bauer et al., 2005).
HvAV-3e encodes only one copy of thymidine kinase (tk, ORF55), which is similar to SfAV-1a but contrasts with the TnAV-2c genome, which contains two ORFs of this gene. This enzyme catalyses the phosphorylation of deoxyribonucleosides to produce monophosphates. The gene encoding tk has also been found in DpAV (28 % identity).
bro genes.
bro genes comprise a multigene family and occur as multiple copies per genome of certain insect dsDNA viruses, including baculoviruses (Ayres et al., 1994), entomopoxviruses (Bawden et al., 2000), entomoiridoviruses (Jakob et al., 2001) and AVs (Bideshi et al., 2003). There is little known about the function of Bro-like proteins in virus biology or virus–host interactions, despite their common occurrence among insect DNA viruses. However, they are assumed to be involved in DNA replication or transcription, functioning as DNA-binding proteins that modulate chromatin structure in the host cells (Zemskov et al., 2000). In addition to insect viruses, bro-like genes have been found in bacteriophages (Kang et al., 1999) and the phycodnavirus Ectocarpus siliculosus virus (Delaroque et al., 2000). Partial sequencing of SfAV-1a and DpAV-4 viruses showed that they contain 11 and three bro ORFs, respectively (Bideshi et al., 2003). However, the complete genome sequence recently deposited in GenBank indicates the presence of only four bro genes in SfAV-1a (GenBank accession no. AM398843
[GenBank]
). In the TnAV-2c complete genome sequence, only three bro homologues were found (Wang et al., 2006). Analysis of the HvAV-3e genome sequence indicated the presence of 23 bro ORFs. The role of bro proteins in AV biology remains to be determined.
Apoptosis-related genes.
HvAV-3e contains one inhibitor of apoptosis (iap)-like gene (ORF28), containing one degenerate baculovirus iap repeat (BIR) and a RING-finger domain, with 24 % identity to the Epiphyas postvittana nucleopolyhedrovirus (NPV) iap-2. In addition, there are four other iap-like genes with a RING-finger domain, but lacking the BIR domain (ORFs 23, 51, 63 and 89). The genome contains a caspase-like gene (ORF165) with 35 % identity to the SfAV-1a caspase 3/7-like protein (Bideshi et al., 2005). This gene seems to be absent in the TnAV-2c genome (Wang et al., 2006). The pathology caused by AVs is unique in that it leads to cleavage of host cells into vesicles, a phenomenon resembling apoptosis. This led to the assumption that perhaps AVs manipulate the host apoptotic pathway for their own benefit (Miller, 1998). A recent study showed that the caspase 3/7-like protein from SfAV-1a has caspase properties and plays a direct role in cell cleavage and induction of apoptosis, facilitating virus replication and dissemination (Bideshi et al., 2005). Caspases have not been reported from any other viruses, indicating that it is perhaps a host-derived gene.
Repeat regions.
Five repeat regions were found in the entire genome of HvAV-3e, with 94–100 % identity among the repeats (Figs 2, 3a; Table 2). Almost the entire repeat region (approx. 1820 bp) consists of an ORF encoding a putative protein of approximately 608 aa (Table 2). Surprisingly, a region within the protein from aa 292 to the end shows 90 % identity to a hypothetical protein from Mamestra configurata NPV (MacoNPV) that is not found in any other NPVs (Fig. 3b; Li et al., 2002). Interestingly, a conserved transposase domain was found in the C terminus of all repeats within the MacoNPV-homologous region. This putative domain is found at the C terminus of a large number of transposase proteins. The domain contains four conserved cysteines, suggestive of a zinc-binding domain hypothesized to be a DNA-binding domain. These conserved residues were also found in the HvAV-3e repeat regions (Fig. 3c). The presence of the putative transposable element within the repeat regions suggests that the DNA might have been transferred to the AV genome either from the host or from MacoNPV. The element might also be responsible for duplication of the gene in the genome. Two copies of the repeat regions were found in SfAV-1a (ORFs 34 and 77), but not in TnAV-2c. No homologue of the 2.9 kb repeat regions in SfAV-1a, which are non-coding, was found in HvAV-3e.
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). The plots revealed that gene order was more conserved between HvAV-3e and SfAV-1a (Fig. 4a) than between HvAV-3e and TnAV-2c (Fig. 4b). TnAV-2c showed a gene arrangement very different from those of the other two AVs (Fig. 4b). In addition, mean identity of TnAV-2c and SfAV-1a homologous ORFs to HvAV-3e ORFs was found to be 39.7 and 52.3 %, respectively (see Table 2), indicating that HvAV-3e is related more closely to SfAV-1a than to TnAV-2c. When phylogenetic trees based on single genes (major capsid protein and DNA polymerase) were evaluated, it was suggested that SfAV-1a is related more closely to HvAV-3e than TnAV-2c (Cheng et al., 2005), which is consistent with our analysis. DNA hybridizations presented here and by Cheng et al. (2005) indicate that, under high-stringency conditions, there is little hybridization among the three AVs (HvAV-3e, SfAV-1a and TnAV-2c), suggesting that they probably belong to three different species.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Received 18 October 2006;
accepted 30 November 2006.
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) vs SfAV-1 (
); (b) HvAV-3 (