Department of Microbiology, Otago School of Medical Sciences, University of Otago, PO Box 56, Dunedin, New Zealand1
Department of Biological Sciences, Imperial College of Science, Technology and Medicine, London SW7 2AZ, UK2
Ecology and Biocontrol Group, Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR, UK3
Author for correspondence: Vernon Ward. Fax +64 3 4798540. e-mail vernon.ward{at}stonebow.otago.ac.nz
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Abstract |
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Introduction |
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Epiphyas postvittana MNPV (EppoMNPV) is a multiply embedded (unpublished data) NPV pathogenic for the light brown apple moth, Epiphyas postvittana, which is part of a major horticultural pest complex comprising seven species of leafroller insects present in New Zealand. EppoMNPV has a genome of under 120 kbp, making it the smallest group I NPV genome characterized to date (Hyink et al., 1998 ). The small size of the EppoMNPV genome and the economic importance of its host make EppoMNPV an important virus to study.
To better understand the evolution of baculoviruses and the molecular mechanisms behind baculovirus infection and replication, the sequencing of baculovirus genomes has been undertaken by a number of research groups. Six NPVs, Autographa californica MNPV (AcMNPV) (Ayres et al., 1994 ), Bombyx mori NPV (BmNPV) (Gomi et al., 1999
), Orgyia pseudotsugata MNPV (OpMNPV) (Ahrens et al., 1997
), Lymantria dispar MNPV (LdMNPV) (Kuzio et al., 1999
), Spodoptera exigua MNPV (SeMNPV) (IJkel et al., 1999
) and Helicoverpa armigera SNPV (HaSNPV) (Chen et al., 2001
), and three GVs, Xestia c-nigrum GV (XecnGV) (Hayakawa et al., 1999
), Plutella xylostella GV (PxGV) (Hashimoto et al., 2000
) and Cydia pomonella GV (CpGV) (Luque et al., 2001
), have now been completely sequenced. The genomes of these baculoviruses range in size from 101 to 179 kbp.
Phylogenetic analyses using the EppoMNPV polyhedrin (polh) and ecdysteroid UDP-glucosyltransferase (egt) genes place EppoMNPV in the group I NPVs (Caradoc-Davies et al., 2001 ; Hyink et al., 1998
). Baculovirus phylogeny has traditionally been performed using the sequences of single genes (Zanotto et al., 1993
) and conflicts between phylogenies based on different genes are often observed (Federici & Hice, 1997
). The growing number of whole genome sequences available has allowed the development of phylogenetic methods based on these complete genomes using genes common to all viruses, gene order and total gene content as the base data sets. Phylogeny studies using these data sets support the divisions between the GVs and the NPVs and between the group I and II NPVs (Herniou et al., 2001
).
We have undertaken a project to characterize EppoMNPV, including the sequencing of its entire genome. In this report, we present the sequence of the EppoMNPV genome and the analysis of the encoded open reading frames (ORFs). Whole genome phylogenetic analyses are presented for the ten baculoviruses that have now been completely sequenced.
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Methods |
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Sequencing strategy.
A targeted sequencing strategy was used to sequence the EppoMNPV genome. The genome-priming system (New England Biolabs) sequencing method was used for HindIII fragments BD, G, H, K and P and EcoRI fragments D, H and K. Subcloning from existing restriction fragments and sequencing using universal primers, or sequencing using specifically designed primers, was used to sequence the remainder of the EppoMNPV genome. Where restriction fragment junctions could not be confirmed through sequencing from an overlapping restriction fragment, PCR primers were designed to amplify the junction region from EppoMNPV genomic DNA. The PCR products were then sequenced. Both strands of the entire genome of EppoMNPV were completely sequenced. Sequencing was carried out at the Centre for Gene Research, University of Otago, New Zealand using an ABI 377 DNA Sequencer.
Sequence analysis.
Assembly and analysis of sequence information was performed using DNASTAR. Identification of ORFs was carried out using the BLAST algorithm and the PREDICTPROTEIN application (http://cubic.bioc.columbia.edu/predictprotein/) (Rost, 1996 ). A signal peptide prediction program was used to identify ORFs encoding proteins with probable secretion signals (http://www.cbs.dtu.dk/services/SignalP/) (Nielsen et al., 1997
). The EppoMNPV repeat regions were identified using the FINDPATTERNS and TANDEM applications in GCG (http://angis.otago.ac.nz).
Phylogenetic analyses.
The baculovirus repeated ORF (bro) genes were not included in any of these analyses because of the difficulty of establishing orthology between family members.
Phylogeny based on gene sequences.
The amino acid sequences of each of the 62 genes common to all ten baculovirus genomes were aligned using CLUSTALW and the alignments refined by eye. These 62 alignments were then concatenated to form a single alignment of 25682 amino acids. This was analysed using both maximum parsimony (heuristic search with 20 random additions) and neighbour joining in PAUP* (Felsenstein, 1995 ). Branch support was evaluated by 1000 bootstrap replicates.
Phylogeny based on gene order.
Breakpoint analysis was undertaken between all sequenced baculoviruses. The number of breakpoints (points in the gene order where there is a discontinuity) was calculated for every possible pair of genomes and then divided by the number of genes shared by each pair to obtain a matrix of relative breakpoint distances. A phylogenetic tree was calculated based on this matrix using the program NEIGHBOR (from the PHYLIP software package) (Felsenstein, 1995 ).
Neighbour pair analysis of baculovirus genes was undertaken as described by Herniou et al. (2001) . Gene order among the 62 shared genes was evaluated by examining each genome for the presence of all possible neighbouring pairs of genes. For each genome, the presence or absence of each possible gene pair was coded as either 1 or 0, respectively. Neighbour gene pairs resulting in constant characters (present in all genomes or absent from all genomes) were not taken into account. This gave a binary matrix of 99 characters, of which 71 were parsimony informative. A maximum-parsimony analysis (exhaustive search) of this data matrix was performed using PAUP*. Branch support was evaluated by 1000 bootstrap replicates.
Phylogeny based on gene content.
A matrix was generated recording the presence or absence of each baculovirus gene in each genome. A total of 417 distinct genes were recorded in this matrix. Of these, 144 were parsimony informative. Phylogenetic analyses were performed using maximum parsimony in PAUP* (exhaustive search). Branch support was evaluated by 1000 bootstrap replicates.
GenBank accession numbers.
The GenBank accession numbers for the NPV and GV sequences reported previously are as follows: AcMNPV, L22858 (Ayres et al., 1994 ); BmNPV, L33180 (Gomi et al., 1999
); CpGV, U53466 (Luque et al., 2001
); HaSNPV, AF271059 (Chen et al., 2001
); LdMNPV, AF081810 (Kuzio et al., 1999
); OpMNPV, U75930 (Ahrens et al., 1997
); PxGV, AF270937 (Hashimoto et al., 2000
); SeMNPV, AF169823 (IJkel et al., 1999
); and XecnGV, AF162221 (Hayakawa et al., 1999
).
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Results and Discussion |
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Phylogenetic analysis of baculoviruses based on gene sequences, order and content
Phylogeny of baculoviruses has usually been performed using the highly conserved polh gene. Some of the limitations of using this single gene have been discussed previously (Federici & Hice, 1997 ). Phylogeny analysis based on gene sequences for the ten baculovirus sequences available to date was performed using a concatenated alignment of all 62 genes shared by all the viruses. A single most parsimonious tree, strongly supported by high bootstrap scores, was obtained from this analysis (Fig. 2A
). It shows that the ten baculoviruses can be subdivided into three groups, the group I and II NPVs and the GVs, with EppoMNPV belonging to the group I NPVs and most closely related to OpMNPV. The relationships among the other baculoviruses are in agreement with the conclusions drawn in a previous study of baculovirus phylogeny using complete genomes (Herniou et al., 2001
).
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Gene content comparison of EppoMNPV with other group I NPVs
Table 1 summarizes the gene content of EppoMNPV in comparison to the other fully sequenced baculoviruses. EppoMNPV is the fourth group I NPV to be sequenced and a total of 116 ORFs are conserved between all the members of this group of NPVs. EppoMNPV shares 126 ORFs with OpMNPV and 120 with AcMNPV, with average identities of 64·7 and 53·5%, respectively. EppoMNPV shares 119 ORFs with BmNPV, the fourth fully sequenced group I NPV. A number of ORFs have now been identified as unique to this group of NPVs (Table 4
), including some which encode well-characterized proteins. For example, gp64 is an essential glycoprotein found on the surface of budded virions and functions in the fusion of these virus particles to cells (Blissard & Rohrmann, 1989
). Previous research has suggested that the acquisition of this gene by the group I NPVs has promoted virus diversification (Pearson et al., 2000
). Also unique to group I NPVs are the ie2 and lef-7 genes, which are involved in viral gene expression (Carson et al., 1991
; Kool et al., 1994
; Morris et al., 1994
). The iap-1 gene, a member of the apoptosis inhibitor family of proteins, has been shown to inhibit apoptosis (Maguire et al., 2000
). The remainder of the ORFs unique to group I NPVs have not been functionally characterized. The gene named gta, EppoMNPV ORF 39 from database homologies, contains seven motifs common to the SNF2/SWI2 family of proteins which are involved in chromatin remodelling (for reviews see Pazin & Kadonaga, 1997
; Peterson, 1996
; Tsukiyama & Wu, 1997
). EppoMNPV ORF 30 shows homology to a set of repeated ORFs, designated the tryptophan repeat family of proteins, in the Amsacta moorei entomopoxvirus (Bawden et al., 2000
). EppoMNPV ORF 108 encodes a protein predicted to contain membrane-spanning regions, indicating that it encodes a transmembrane protein.
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Six ORFs identified previously as being unique to OpMNPV have homologues on the EppoMNPV genome (Table 4). The EppoMNPV ORF 27 and 99 gene products both have multiple predicted membrane-spanning regions, indicating that they could encode transmembrane proteins. The EppoMNPV ORF 92 gene product, as described by Ahrens et al. (1997)
, has a truncated BIR domain and a RING-finger motif and was therefore designated iap-4. The predicted proteins encoded by EppoMNPV ORFs 2, 3 and 29 have no recognizable motifs that can be attributed to function. Overall, the EppoMNPV genome shows close similarity to the genome of OpMNPV, with phylogenetic analysis consistently and strongly supporting the grouping of these two viruses.
The main differences between the EppoMNPV and OpMNPV genomes occur at two points on the OpMNPV genome, where OpMNPV has additional genes (Fig. 3). The largest of these clusters includes OpMNPV ORFs 2834, which include the sod and conotoxin-like (ctl-2) genes, plus a dUTPase and two ribonucleotide reductase genes. Comparison of the OpMNPV and AcMNPV genomes reveals a larger cluster of genes, OpMNPV ORFs 3037, all absent in AcMNPV. The last three ORFs (ORFs 3537) do have homologues in EppoMNPV. The question that arises is have AcMNPV and EppoMNPV lost these genes or has OpMNPV gained them? One possible model for the loss of sod from EppoMNPV is that the OpMNPV/EppoMNPV lineage contained the OpMNPV ORFs 3037 gene cluster and that EppoMNPV then lost the homologues of OpMNPV ORFs 2834, thus losing sod. OpMNPV ORFs 147150 also lack homologues in EppoMNPV. The proteins encoded by OpMNPV ORFs 147149, opep-3, opep-2 and p8.9 have been described previously by Wu et al. (1993)
and Shippam et al. (1997)
. These ORFs occur between the odv-e56 and ie2 genes in OpMNPV, where ie2 is followed by an hr region. In EppoMNPV, the odv-e56 gene is followed by an hr region and ie2 faces in the opposite orientation to the ie2 gene on the OpMNPV genome. Interestingly, AcMNPV has the odv-e56 and ie2 genes in the same orientation as EppoMNPV, with two small ORFs between them instead of an hr region. This suggests a rearrangement has occurred in OpMNPV with the acquisition of the ORF 147150 gene cluster. The BmNPV genome is identical to AcMNPV in gene order in these two regions, with the exception of the bro-a gene found upstream of the sod gene homologue. These two gene clusters account for 7·9 kbp of the 13·4 kbp size difference between EppoMNPV and OpMNPV. The remainder of the size difference between EppoMNPV and OpMNPV can be attributed to extra ORFs at apparently random locations around the OpMNPV genome and the OpMNPV I-R and GT repeat regions.
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EppoMNPV lacks homologues of three other genes common to all the other group I NPVs. These are homologues of the AcMNPV ORFs 47, 87 (p15) and 122. The protein encoded by BmNPV p15 has been proposed to be a capsid-associated protein (Lu & Iatrou, 1997 ). EppoMNPV also lacks homologues of 13 ORFs that are found in two of the other three group I NPVs. Like BmNPV, no homologue of the ctl gene, pcna or AcMNPV ORF 85 were identified on the EppoMNPV genome. AcMNPV and OpMNPV both have these ORFs, with OpMNPV encoding two ctl genes (Ahrens et al., 1997
; Ayres et al., 1994
). Homologues of the ctl ORF have also been identified in LdMNPV, XecnGV and Buzura suppressaria SNPV (Hayakawa et al., 1999
; Hu et al., 1998
; Kuzio et al., 1999
). Ten ORFs shared between AcMNPV and BmNPV have no homologues in either EppoMNPV or OpMNPV (Table 3
).
The size of some of the larger baculoviruses has been attributed to the presence of repeated genes (Hayakawa et al., 2000 ). Approximately 10% of the genome of LdMNPV, the largest NPV genome, encodes copies of the bro genes (Kuzio et al., 1999
). The XecnGV genome has four copies of an enhancin gene, three variants of p10, seven copies of bro genes, four ORFs with homology to the AcMNPV ORF 145150 group and a further five ORFs that have similarity to each other but not to other genes in GenBank (Hayakawa et al., 1999
). EppoMNPV has just one gene, ORF 103, with homology to the bro genes. This gene is 174 amino acids in length and shows 72·7% identity to OpMNPV ORF 116, which is even smaller at only 88 amino acids in length. The EppoMNPV bro homologue shows weak homology to other bro genes, with the best identity being 24·1% to one of the BmNPV bro genes. The iap genes have been classified as repeated ORFs (Hayakawa et al., 2000
) and EppoMNPV, despite its small size, has four of these (iap14) (Maguire et al., 2000
). The functions of the different classes of iap have still to be elucidated but both IAP1 and IAP2 are anti-apoptotic (Maguire et al., 2000
) and IAP3 from OpMNPV is also a functional apoptosis inhibitor.
Repeat regions identified on EppoMNPV
EppoMNPV, like most other baculoviruses, has hr regions dispersed throughout its genome. Five hr sequences have been identified with a 30 bp imperfect palindrome inside a directly repeated sequence, with the number of palindromes per hr region varying from two to eight (Fig. 4A). The consensus palindrome sequence was obtained by taking bases that occurred at a frequency of greater than 70% at a given position. The EppoMNPV hr regions show considerably more variation than those of OpMNPV and AcMNPV (Fig. 4B
). The similarity between the consensus palindrome sequences of EppoMNPV, AcMNPV and OpMNPV shows little correlation to the overall relatedness of these viruses, with the EppoMNPV palindromes being more similar to those of AcMNPV than OpMNPV. The hr sequences have been identified as enhancer elements for gene expression and can act as origins of replication (Leisy & Rohrmann, 1993
). The baculovirus early gene transactivator has been shown to bind the 8 bp, three bases in from the ends of the palindrome sequence in AcMNPV (Fig. 4B
) (Rodems & Friesen, 1995
). It would be expected that the IE1 proteins from EppoMNPV and OpMNPV bind the same regions of the palindrome sequences in these viruses. Fig. 3
highlights two highly variable regions between EppoMNPV, OpMNPV and AcMNPV. Hr regions are present in or around these regions, suggesting a possible role for hr regions in recombination events in baculoviruses. LdMNPV, the most divergent of the NPVs sequenced to date, has more hr regions than any of the other completely sequenced baculoviruses (Hayakawa et al., 2000
).
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Summary
EppoMNPV is the tenth baculovirus to have been fully sequenced and is the smallest group I NPV genome sequenced to date. EppoMNPV shares 116 ORFs with the three fully sequenced group I NPVs and 62 ORFs with all other sequenced baculoviruses. The EppoMNPV genome contains eight randomly dispersed, unique ORFs and lacks a homologue of the sod gene, which is present in nine fully sequenced baculoviruses. The only repeated genes present are the four iap genes. EppoMNPV has five hr regions and two of these are located in the regions showing the most variability with OpMNPV. Phylogenetic analysis of the whole genomes of baculoviruses places EppoMNPV in the group I NPVs, closely related to OpMNPV.
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Acknowledgments |
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Footnotes |
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Received 26 September 2001;
accepted 14 December 2001.