Genome sequence of Chrysodeixis chalcites nucleopolyhedrovirus, a baculovirus with two DNA photolyase genes

Monique M. van Oers1, Marleen H. C. Abma-Henkens2, Elisabeth A. Herniou3, Joost C. W. de Groot4, Sander Peters2 and Just M. Vlak1

1 Laboratory of Virology, Wageningen University, Binnenhaven 11, 6709 PD Wageningen, The Netherlands
2 Greenomics, Plant Research International BV, Wageningen, The Netherlands
3 Department of Biological Sciences, Imperial College London, UK
4 Applied Bioinformatics, Plant Research International BV, Wageningen, The Netherlands

Correspondence
Monique M. van Oers
monique.vanoers{at}wur.nl


   ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS AND DISCUSSION
REFERENCES
 
The complete genome sequence of a single nucleocapsid nucleopolyhedrovirus recently isolated from Chrysodeixis chalcites (ChchNPV) was determined. The viral genome has a size of 149 622 bp and an overall G+C content of 39·1 mol%. The sequence contains 151 predicted open reading frames (ORFs) with a minimal size of 50 codons. The similarity of these ORFs with those of other completely sequenced baculoviruses was calculated using a newly developed database, named GECCO. Phylogenetic analysis of the whole genome confirmed the evolutionary relationship of ChchNPV with group II NPVs, as did the absence of the NPV group I-specific gp64 gene. It is the first group II NPV to encode proliferating cell nuclear antigen. Most noteworthy is the presence of two ORFs encoding a class II cyclobutane pyrimidine dimer DNA photolyase. These two ORFs share only 45 % amino acid identity and have different promoter motifs. Twenty-two additional unique baculovirus genes were identified, including a gene encoding a novel putative RING finger protein with a possible homologue in poxviruses.

The GenBank/EMBL/DDBJ accession number of the sequence reported in this paper is AY864330.


   INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS AND DISCUSSION
REFERENCES
 
The Baculoviridae form a large family of rod-shaped, invertebrate-infecting viruses with a large double-stranded, covalently closed circular DNA genome. The members of the virus family are taxonomically divided over the genera Nucleopolyhedrovirus (NPV) and Granulovirus (GV), based on occlusion body morphology (van Regenmortel et al., 2000). The NPVs are further divided in group I and II NPVs (Bulach et al., 1999; Zanotto et al., 1993). More recent phylogenetic analyses indicated that the NPVs infecting lepidopteran species are more closely related to GVs, than to NPVs which infect dipteran or hymenopteran insect species (Herniou et al., 2004), like the mosquito-infecting Culex nigra NPV or the NPVs from two Neodiprion species (Afonso et al., 2001; Garcia-Maruniak et al., 2004; Lauzon et al., 2004).

Recently, a novel NPV was identified in larvae of the moth Chrysodeixis chalcites (Noctuidae, Plusiinae) a major pest in Dutch greenhouses on tomato and sweet pepper (van Oers et al., 2004). Chrysodeixis chalcites appears to infect Trichoplusia ni larvae as well, and may be a candidate for a broad spectrum biological control agent against larvae of Plusiinae. Electronmicrosopy showed that this virus occludes singly enveloped nucleocapsids and hence is an SNPV. The virus was named Chrysodeixis chalcites NPV (ChchNPV). Its polyhedrin sequence was obtained by PCR and was most closely related to that of group II NPVs, especially to those that infected other members of the subfamily Plusiinae, within the Noctuidae, like the Canadian (David Theilman, personal communication) and South-African (GenBank accession no. AF093405) isolates of Trichoplusia ni (Tn) SNPV, and Plusia orichalcea NPV (AF019882). Its taxonomical exclusion from group I NPVs was confirmed by phylogeny on concatenated lef-8 and pif-2 (ac22) sequences (van Oers et al., 2004).

The sequence analysis of complete baculovirus genomes has shown that 29 genes, the core genes, are probably shared between all baculoviruses either of lepidopteran, hymenopteran or dipteran origin (Garcia-Maruniak et al., 2004; Lauzon et al., 2004). These core genes can be used for phylogenetic analysis on whole genomes (Herniou et al., 2003). The number of genes present in all baculoviruses infecting lepidopteran insects was originally set at 63 (Herniou et al., 2001), but is currently 62, after sod (superoxide dismutase) was found to be absent in Spodoptera litura (Splt) NPV (Pang et al., 2001) and Epiphyas postvittana (Eppo) NPV (Hyink et al., 2002). An additional set of 14 genes is shared by lepidopteran NPVs (Herniou et al., 2003).

Besides these conserved genes, each baculovirus has genes that are present in only a small number of related viruses or are even unique to that virus. These additional genes may give each baculovirus its unique features in terms of pathogenicity, virulence, host range and competitive fitness. The identification of new virus genomes is likely to reveal new genes, so far unknown in other baculovirus species.

Initial sequence analysis of a restriction fragment library of the ChchNPV genome revealed the presence of a class II cyclobutane pyrimidine (CPD) DNA photolyase (van Oers et al., 2004). The putative function of this gene is repairing pyrimidine dimers, which occur in UV-damaged DNA. This repair process, requiring visible light, is known as photo-reactivation (Bennett et al., 2003; Carell et al., 2001; Deisenhofer, 2000). This class of genes is termed phr in cellular organisms (Sancar & Rupert, 1978), but was called dpl in ChchNPV (van Oers et al., 2004). These genes have also been reported for Poxviridae, i.e. Melanoplus sanguinipes entomopoxvirus (MSEV) and shope fibroma virus (SFV) (Afonso et al., 1999; Willer et al., 1999). The present analysis of the complete genome sequence of ChchNPV revealed additional features unique to this virus, including a second DNA photolyase gene.


   METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS AND DISCUSSION
REFERENCES
 
Purification of viral DNA.
To isolate ChchNPV DNA, infected larvae were macerated and filtered through cheese cloth. Additional cellular debris was removed by centrifugation over a 30 % sucrose cushion. To that aim 2 ml of a polyhedra suspension (1x10E9 polyhedra ml–1) were layered onto 4 ml of 30 % sucrose and centrifuged for 15 min at 5300 r.p.m. in a Hereaus centrifuge with a fixed angle rotor (#3571) at 4 °C. The polyhedra were washed twice with water, and dissolved in a total volume of 5·4 ml 1x DAS (0·1 M Na2CO3, 0·16 M NaCl, 0·01 M EDTA, pH 10·5) for 10 min at room temperature. The pH was neutralized with 540 µl 10 mM Tris/HCl, pH 8·0. After centrifugation for 8 min at 5300 r.p.m. (same rotor as above), the supernatant containing the occluded virus particles (ODVs) was collected in SW55 tubes and centrifuged at 25 000 r.p.m. in a SW55 rotor for 1·5 h at 4 °C in a Beckman ultracentrifuge. The virus particles were suspended in a total of 360 µl 10 mM Tris/HCl, pH 8·0 overnight at 4 °C. DNA was isolated from these ODVs with the DNeasy tissue kit (Qiagen) following the protocol for tissue DNA purification.

Sequence analysis.
The full genome sequence was determined by shotgun cloning of 10 µg sheared DNA of 1–1·5 kb. The DNA fragments were cloned into pBluescript II SK(+) (Stratagene) using Escherichia coli XL2 blue ultracompetent cells (Stratagene). Sequencing was performed on a 3730xl DNA analyser (Applied Biosystems) and a 3100 Genetic analyser (Applied Biosystems), and assembled with Gap4 from the Staden-Solaris-1-5-3 software package and then checked in detail manually. Genes were detected with Genemark software and open reading frame (ORF) finder (NCBI). All ORFs with a minimal size of 150 nt (50 aa), which did not overlap for major parts with other ORFs, were analysed. In addition, the genome was checked in detail for the presence of any ORFs identified for Mamestra configurata (Maco) NPV or Spodoptera exigua (Se) MNPV (IJkel et al., 1999; Li et al., 2002a, b). Similarity searches were performed using BLAST.

To easily compare sequence information from different baculovirus genomes and calculate the percentages of identity with ChchNPV, the GECCO program (http://appliedbioinformatics.wur.nl/) was exploited. GECCO is a novel gene content comparison tool able to quickly align large amounts of sequences using the standard ncbi BLAST (Altschul et al., 1997). GECCO consists of pipeline software and a web based user interface. The pipeline performs cross species BLASTs on supplied sequences, in this case ORFs of baculovirus genomes. For our analysis, only a selection of baculovirus genomes (Autographa californica (Ac) MNPV, ChchNPV, Lymantria dispar (Ld) MNPV, SeMNPV, Helicoverpa armigera (Hear) NPV and MacoNPV B) was incorporated in the program, but this number can easily be extended. Boolean values for absence or presence of a certain sequence in other species can be set. The BLAST results of every individual sequence versus all other supplied species are stored in a database matrix table. Using the GECCO interface source, target species can be selected and different settings can be applied during the query (e.g. ratio-ed expectation values or the minimal percentage of identity). In this study, a search with an expectation value of e–10 revealed most genes. Genes with low identity levels needed to be pulled out with expectation values (e–5 to 1). To detect homologous regions DOTPLOT analysis (DNAstar) was applied under various stringency conditions. Further analysis was directed towards identifying tandem repeat units (Krishnan & Tang, 2004), which were then compared to the whole ChchNPV genome sequence to search for homologues using BLAST (Altschul et al., 1997).

Phylogenetic analysis and gene parity plots.
For the phylogenetic analysis, protein sequences were aligned with CLUSTALW (EBI) and edited in MacClade 4.0. Maximum-likelihood (ML) analyses were performed in PHYML version 2.3 (Guindon & Gascuel, 2003). Maximum-parsimony (MP) analysis was performed using PAUP* (Swofford, 2001) with heuristic searches including branch swapping by tree-bisection reconnections. Bootstrap analyses were performed to evaluate the robustness of the phylogenies with 100 replicates for both ML and MP analyses.

The DNA photolyase sequences used for these analyses were obtained by using the ChchNPV phr-2 sequence as the query for the BLAST link program at NCBI. Sequences with a BLAST score above 850 were included. The ML tree was searched using PHYML under the following conditions: JTT amino acid substitution model, {gamma} shaped distribution (Yang, 1994) estimated at 0·907 and proportion of invariable sites estimated as 0·001.

The phylogenetic tree for baculoviruses was based on the concatamer of the 29 baculovirus core genes of the 27 baculoviruses, which were completely sequenced at the time of analyses. The ML tree was obtained as described above with {gamma} shaped distributions estimated at 1·284 and proportion of invariable sites estimated as 0.

Pairwise gene order analyses were performed by making gene parity plots as described previously (Hu et al., 1998). For these analyses, we used both shared and non-shared genes. bro genes were excluded from this analysis since it is difficult to determine the evolutionary relationships between individual bro genes from various species (see Herniou et al., 2003) due to the presence of a varying number of bro genes per genome.


   RESULTS AND DISCUSSION
Top
ABSTRACT
INTRODUCTION
METHODS
RESULTS AND DISCUSSION
REFERENCES
 
Nucleotide sequence of ChchNPV
The genome of ChchNPV has a size of 149 622 bp. With a G+C content of 39·1 mol%, ChchNPV has a highly AT-rich genome. Within the NPVs HearNPV, Helicoverpa zea (Hz) and Rachiplusia ou (Ro) MNPV (Chen et al., 2001, 2002b; Harrison & Bonning, 2003) have a similar low G+C content (Table 1). The ChchNPV genome contains 151 putative ORFs with a minimal size of 150 bp (50 aa), and with minimal overlap with other ORFs (Fig. 1, Table 2). The 62 genes conserved in other lepidopteran baculoviruses are all present. ChchNPV does not have the group I specific gp64 gene, but it has a baculovirus F protein gene (chch150), which is in line with its previous classification as a group II NPV (van Oers et al., 2004). ChchNPV has 59 ORFs preceded by a baculovirus early promoter motif (CAGT) within the 150 bp upstream of the ATG start codon. A late promoter motif (TAAG) is found for 75 ChchNPV ORFs. Twenty-eight of these ORFs carry both early- and late-promoter motifs. The number of ORFs with a sense orientation (similar to polyhedrin) is 73, and almost equals the number of ORFs with an opposite orientation (78). Typical homologous regions (hrs) were not detected in ChchNPV using DOTPLOT analysis and computational searches for tandem repeats. Tandem repeats were found at several locations, but these regions were not repeated in other parts of the genome. In this respect, ChchNPV appears to be different from other NPVs and more similar to Cydia pomonella (Cp) GV and Adoxophyes orana (Ador) GV also lacking typical hr regions (Luque et al., 2001; Wormleaton et al., 2003).


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Table 1. Characteristics of baculovirus genomes

 


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Fig. 1. Linear presentation of the genomic map of ChchNPV with annotated genes. Arrows indicate the direction of the predicted genes: (+) orientation in dark shading (–), orientation in light shading. Numbers refer to the nucleotide position in kbp relative to the start codon of polyhedrin.

 

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Table 2. ORFs predicted in the genome of ChchNPV

 
Phylogenetic characterization and gene content
The gene sequences of the 29 baculovirus core genes were used for phylogenetic analysis comparing ChchNPV to the other completely sequenced lepidopteran baculoviruses (Fig. 2). The phylogenetic analysis showed a close relationship of ChchNPV with SeMNPV and the Maco NPVs, which is supported by high bootstrap values. This is correlated with the high number of genes shared with these viruses. ChchNPV has 120 and 119 genes in common with MacoNPV A and B, respectively, and 111 with SeMNPV, compared with 101 genes with HearNPV and 99 genes with AcMNPV. Genes shared with both SeMNPV and the MacoNPVs include among others dUTPase, ptp2, rr1, rr2, inhibitor of apoptosis (iap)-3 and a second p26 gene copy. The degree of identity with the corresponding ORFs in these other NPVs is depicted in Table 2 and is in general the highest with SeMNPV and MacoNPVs. Gene order data also support the phylogenetic relationships of ChchNPV. Gene parity plot analysis (Hu et al., 1998) in which the gene order of ChchNPV was compared with that of AcMNPV, HearNPV, SeMNPV and MacoNPV B (Fig. 3), showed that the genome synteny of ChchNPV is most similar to that of SeMNPV and MacoNPV, and differs most from that of AcMNPV. The region between ORFs 60 and 80 has been rearranged in ChchNPV compared with the other viruses used in this analysis, including inversions (HearNPV) and translocations (SeMNPV, MacoNPV). Inversions are also seen in the ORF 130–150 region when compared with SeMNPV and MacoNPV.



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Fig. 2. Phylogeny of baculovirus genomes. The tree was obtained by ML analysis using the 29 baculovirus core gene protein sequences. Numbers indicate bootstrap scores above 50 for ML and MP analyses (ML boot/MP boot). **, Symbolize 100 bootstrap scores for ML and MP analyses.

 


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Fig. 3. Pairwise comparison of gene content and position of ChchNPV with AcMNPV, SeMNPV, HearNPV and MacoNPV B using gene parity plot analysis. Genes present in only one of the two viruses in the pair-wise comparison appear on the x or y axes. bro genes were not included in these plots.

 
Genes with homologues in group I NPVs or GVs
Chch66 is a pcna gene (proliferating cell nuclear antigen), a gene reported only from AcMNPV, RoMNPV and Orgyia pseudostugata (Op) MNPV. This is therefore the first report of a pcna gene in a group II NPV. In ChchNPV, it is flanked by chitinase and gp37, which is different from the position of this gene in AcMNPV and OpMNPV, where pcna is neighboured by lef-8 and etm.

The three contiguous ORFs chch112, 113 and 114 have homologues in Xestia c-nigrum (Xecn) GV (Hayakawa et al., 1999). ORF 112 (Xecn83) is also present in both MacoNPV isolates. ORF 113 shows amino acid similarity with the XecnGV ORFs 59 and 138 (49 and 44 %, respectively), and to a lesser extent with the Amsacta moorei entemopoxvirus (Bawden et al., 2000) DNA helicase (40 %). ORF 114 is most similar to XecnGV ORF60, a baculovirus repeat ORF (bro). Since ORFs 113 and 114 are also neighbouring genes in XecnGV, these genes may have been inserted in a single event into the ancestor of the ChchNPV genome from a virus also harbouring a homologue of ORF 112/Xecn83 in this region. The XecnGV genes referred to here are not part of the group of genes conserved among all GVs (Wormleaton et al., 2003).

Unique ORFs
The genome of ChchNPV contains 24 ORFs, so far, unique to this virus (Table 2). Among those, chch6 contains an MDN-1 domain, typical for eukaryotic AAA+ ATPases, which play a role in protein (un)folding processes (Martin et al., 2004). The degree of similarity with these proteins is around 50 % over 200 aa. Chch24 is homologous to MSEV ORF 156 (42 % similarity) and to ATP-dependent proteases from Plasmodium (43 %) and an ABC transporter ATP-binding protein from Mycoplasma (38 %) (GenBank accession no. NC_001993; GenBank protein database EAA20911 YP_015854). Chch68 and 72 represent DNA photolyase genes (see below). Chch103 shows 50 % similarity over 100 aa with members of the Borrelia Bdr gene family, which contains inner membrane proteins of unknown function (GenBank protein database; AAF19138. Chch118 contains a RING domain and is discussed further below. The other ORFs do not have clear homologues in GenBank and their possible functions are hence unknown.

A new RING finger protein
ChchNPV ORF 118 encodes a putative protein with a C-terminal RING domain (‘Really Interesting New Gene’ NCBI conserved domain cd00162). The predicted protein contains 172 aa and has a predicted molecular mass of 20 kDa. A RING domain is a specialized Zn-finger of 40–60 residues that putatively binds two atoms of zinc and is characterized by the motif C-X2-C-X(9-39)-C-X(1-3)-H-X(2-3)-(N/C/H)-X2-C-X(4-48)C-X2-C. RING domains are probably involved in mediating protein–protein interactions. Chch118 is most similar to a putative RING finger host range protein from the poxvirus lumpy skin disease virus (Kara et al., 2003) (51 % similarity over 100 aa). A low degree of similarity was also found with MacoNPV A and B ORF 97 and 96, respectively, which also have a RING finger domain at the C terminus. In this case, only the RING finger domain showed similarity, not the preceding 82 aa, suggesting that chch118 and the Maco97/96 might not be true homologues. Known baculovirus RING finger proteins also include exon-0, essential for budded virus production (Dai et al., 2004) and the iap genes, neither of which are homologous to chch118. The RING domain of the OpMNPV IAP-3 protein was shown to be crucial for the functioning of IAP-3 as an E3 ubiquitin ligase (Green et al., 2004). ChchNPV ORF 39 is an iap-3 homologue and also encodes a RING domain. In addition, it contains the typical iap BIR domain.

dUTPase
Previous analysis of dUTPase genes in baculoviruses has shown that dUTPase has been gained several times during baculovirus evolution (Herniou et al., 2003). The ChchNPV dUTPase gene is embedded within unique genes (chch116–118 and chch120) and is related to the MacoNPV and SeMNPV dUTPase (identities of 52 and 50 %). The function of dUTPase is to prevent mutagenic incorporation of uracyl into DNA (Chen et al., 2002a). Furthermore, the genes ld138, rr1 and rr2 are all present in ChchNPV, as ORFs 106, 151 and 122, respectively. This is reinforcing the hypothesis of a putative baculovirus enzyme system preventing mutations in the viral genome, proposed in view of the phylogenetic linkage of these genes (Herniou et al., 2003).

DNA photolyase genes
The complete genome analysis revealed that ChchNPV has not one (van Oers et al., 2004), but two ORFs that encode putative class II cyclobutane pyrimidine photolyases (phr/dpl). These genes are now labelled phr-1 (chch68) and phr-2 (chch72) based on their position in the ChchNPV genome, relative to the polyhedrin gene. The previously reported dpl sequence (van Oers et al., 2004) corresponds to phr-2. The two phr genes are separated by a genome fragment of 3700 bp, containing three ORFs: bro-b, bro-c and ORF 71 (ac111). Both ChchNPV phr genes appear to encode complete DNA photolyase enzymes as both the DNA photolyase and FAD-binding domains (Deisenhofer, 2000) are conserved.

Phylogenetic analyses were conducted to address the origin of the two ChchNPV phr genes, as homologues are found in many cellular organisms, including Eubacteria, Archea and Eukaryotes (except placental mammals) and in the virus family Poxviridae. The tree (Fig. 4) shows that the phr gene recovers the monophyly of the major cellular lineages, except in bacteria where paralogous genes might be present.



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Fig. 4. Phylogenetic analysis of DNA photolyase proteins. The phylogenies were obtained by ML analysis. Numbers indicate bootstrap scores above 50 for ML analysis and MP analysis (ML boot/MP boot, 100 replicates each). The line refers to 0·1 substitutions per site for the branch length. ChchNPV-1, phr-1; ChchNPV-2, phr-2. The Bacillus cereus photolyase was used as an outgroup. Other sequences used in this analysis: Amsacta moorei (Am) EV, Anopheles gambiae, Antonospora locustae, Arabidopsis thaliana, Bacillus cereus, Bombyx mori (Silkworm.genomics.org.cnBmb009672); Carassius auratus, Chlamydomonas reinhardtii, Chlorobium tepidum, Cucumis sativus, Danio rerio, Desulfovibrio desulfuricans, Desulfotalea psychrophila, Drosophila pseudoobscura, Drosophila melanogaster, Gallus gallus, Geobacter sulfurreducens, MSEV, Monodelphis domesticus, Methanosarcina barkeri, Methanosarcina acetivorans, Methanothermobacter thermoautotrophicus, Myxoma virus, Oryza sativa, Oryzias latipes, Pityrogramma austroamericaneo, Potorous tridactylus, SFV, Stellaria longipes, Spinacia oleracea, Tetraodon nigroviridis.

 
The viral phr genes form a monophyletic group both in the ML and the MP trees, although poorly supported by bootstrap analyses. This indicates that ChchNPV and the poxviruses might have acquired their phr gene from a common source. The fact that the virus genes are clearly and robustly nested between the metazoan and fungal clades, shows clearly the eukaryotic origin of these viral genes.

The ChchNPV phr genes form a monophyletic group, suggesting a single acquisition of a phr gene followed by duplication. The fact that both phr copies have relatively low similarity (45 %), as illustrated by the long branch separating them, may suggest that either genetic drifting or diverging selection could have operated on them. The upstream regions of both phr genes do not align and have different putative promoters, which may indicate that these genes have a different regulation pattern, possibly coupled with a different function. The phr-1 upstream region has the characteristics of a typical baculovirus early promoter (TATA box and CAGT) while phr-2 is preceded by several GATA motifs, indicating that these genes may follow different expression profiles. The transcriptional activity of phr-2 has been demonstrated (van Oers et al., 2004) and transcription starts between the most downstream GATA sequence and the ATG.

The presence of a phr gene may be more beneficial for a SNPV than an MNPV, since MNPVs enter the host cell with multiple genome copies per virus particle, which may complement each other for gene deficiencies due to UV damage. Whether these phr genes play an important role in the ecology of ChchNPV has to be established. The presence of a host enzyme with similar activity is a complicating factor when studying these genes in cell culture or insect systems. Therefore, alternative systems need to be explored.

Conclusion
This is the first publication of a whole genome sequence of a group II NPV isolated from a plusiine species. In view of the close relationship of the polyhedrin genes of ChchNPV and TnSNPV (van Oers et al., 2004), and the fact that these viruses both infect Plusiinae, it would be interesting to compare the genomes of these viruses. Unique genes of ChchNPV include a novel RING finger protein and an MND-1 domain protein. ChchNPV is the first group II NPV shown to carry a pcna gene. Furthermore, the presence of a full complement of genes potentially involved in preventing DNA mutations (dUTPase, ld138, rr1 and rr2), as well as two genes (phr-1 and phr-2) encoding DNA photolyase homologues with a predicted role in UV-damage repair, might play an important role in the ecology of this virus and may indicate that the ChchNPV genome is uniquely protected.


   ACKNOWLEDGEMENTS
 
Rene Klein-Lankhorst supervised the sequencing project and Jan van Haarst assisted in the search for homologous repeats. Gerben Messelink supplied the original virus stock. Andre Eker is acknowledged for helpful discussions on DNA repair, and Marcel Westenberg for checking the GenBank annotation. This research was performed with a financial contribution from Applied Plant Research, Naaldwijk, The Netherlands.


   REFERENCES
Top
ABSTRACT
INTRODUCTION
METHODS
RESULTS AND DISCUSSION
REFERENCES
 
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Received 10 February 2005; accepted 5 April 2005.