Department of Entomology and Interdepartmental Program in Genetics, Iowa State University, Ames, IA 50011, USA
Correspondence
Bryony Bonning
bbonning{at}iastate.edu
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ABSTRACT |
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INTRODUCTION |
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A number of NPV genes influence the species-specific virulence or host range of NPVs by affecting the ability to infect and replicate in cells of specific species, the dose required to cause mortality or the survival time of infected hosts (Chen & Thiem, 1997; Chen et al., 1998
; Clem et al., 1991
; Clem & Miller, 1993
; Croizier et al., 1994
; Lu & Miller, 1996
; Maeda et al., 1993
; Popham et al., 1998
). In most of these cases, the species-specific effect of a gene on virulence or host range was discovered after expression of the gene had been eliminated by ORF disruption or deletion. Eliminating or reducing virulence against one species upon knocking out a gene suggests that acquisition of new genes during evolution (by recombination) can shape NPV host range. However, in a single case, individual amino acid replacements in a gene encoding an essential DNA helicase expanded the host range of AcMNPV to include a normally refractory species (Argaud et al., 1998
; Kamita & Maeda, 1997
). This example raises the possibility that nucleotide substitutions in key genes also influence virulence and host range.
Nonsynonymous (amino acid-changing) nucleotide substitutions in NPV genes may lead to alterations in the activity of the encoded protein that facilitate adaptation to a new host species, or overcome the defences of a current host. Such mutations would confer a fitness advantage and would be expected to be fixed in the population at a higher rate than synonymous (silent) substitutions, which are generally invisible to natural selection. When the rate of nonsynonymous substitutions per potential nonsynonymous site in a gene is greater than the rate of synonymous substitutions per potential synonymous site, the gene is said to be undergoing positive selection (Yang, 2001). This concept is expressed as the ratio of nonsynonymous to synonymous substitution rates,
, which is greater than one for positively selected genes. The value of
is less than one for genes undergoing negative or purifying selection, in which nonsynonymous mutations are deleterious and are eliminated at a faster rate than synonymous mutations. Most genes appear to be subject to negative selection most of the time (Endo et al., 1996
; Yang, 2002
).
Maximum-likelihood models that estimate the value of for aligned sequences have been used to identify sites within viral envelope glycoprotein genes that map to regions previously found to be involved in host immune recognition and receptor binding (Holmes et al., 2002
; Twiddy et al., 2002
; Woelk & Holmes, 2001
; Woelk et al., 2001
), suggesting that this method can be used to identify viral genes involved in adapting to new or current hosts. A similar evaluation of the selection pressures on NPV genes may help identify genes involved in species-specific virulence and host range, although positively selected sites may also result from selection for improved stability or transmission, or from compensatory changes triggered by variation in other genes. We applied maximum-likelihood models of codon substitution to examine the selection pressures on 83 group I nucleopolyhedovirus genes that are either widespread in distribution or for which protein expression had been previously demonstrated.
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METHODS |
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Analysis of selection pressure.
The PAML (phylogenetic analysis by maximum-likelihood) software package (Yang, 1997; http://abacus.gene.ucl.ac.uk/software/paml.html) was used to evaluate selection pressures on NPV genes. This software uses a maximum-likelihood approach with codon-based models to estimate the ratio (
) of dN, the rate of nonsynonymous substitutions per nonsynonymous site, to dS, the ratio of synonymous substitutions per synonymous site.
All nucleotide sequence alignments were fitted to six models with different hypotheses about the distribution of estimated values of (Yang et al., 2000
): (1) M0 assumes one
value for all codons; (2) M1 divides codons into an invariant class p0, where
is set at zero (purifying selection) and a neutral class p1, where
is set at one (neutral evolution); (3) M2 includes p0 and p1 from M1, and adds a third class (p2), where
is estimated from the underlying data and can be greater than one; (4) M3 divides codons among three classes of sites (p0, p1, and p2) and
is estimated independently for all three classes and can be greater than one; (5) M7 features ten classes modelled with a discrete beta distribution. The shape of the distribution is determined by parameters p and q, and
values for these classes cannot be greater than one; and (6) M8 includes the ten classes of M7 (collectively referred to as p0), and uses an additional class (p1) where
can be greater than one.
In addition, the DNA helicase gene (dnahel) was further analysed with the free-ratios model, which allows to be independently estimated for each individual branch in a phylogenetic tree (Yang, 1998
).
Models M0 and M1 are nested with models M2 and M3, and model M7 is nested with M8. Models which are nested together can be compared statistically using a likelihood ratio test, in which twice the difference between the log-likelihood values for two models is compared with a 2 distribution table with the degrees of freedom equal to the difference in the number of parameters between the two models (Yang et al., 2000
). This comparison supplies a P value for the probability that the null hypothesis (no positive selection, embodied in models M1 and M7) is an equally good or better fit for the data when compared to the nested models that allow for the possibility of positive selection. Positive selection can be inferred from this analysis when (1) models M2, M3 or M8 indicate a group of codons with an
ratio greater than one, and (2) the likelihood of the positive selection model is significantly higher than that of the nested null hypothesis model (at P<0·05). The M0 model, which assumes a single
ratio for all lineages, and the free-ratios model can also be compared in this manner.
The empirical Bayes procedure is used to calculate the probabilities for individual codons belonging to each of the site classes and can be used to predict which codons are under positive selection. The program output lists the codon sites with a probability 0·5 of being in the positively selected class.
Codon frequency bias was accounted for using the F61 model of codon frequency, in which frequencies for each codon are calculated individually. The transition/transversion ratio () was estimated from the underlying data. For each data set, the analysis was run using each MP, ME and ML tree saved by PAUP* that possessed a unique topology.
Alignments and output files from these analyses can be downloaded from http://www.ent.iastate.edu/dept/faculty/bonningb/selection_pressure-group1.zip.
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RESULTS AND DISCUSSION |
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Most data sets consisted of sequences from AcMNPV, RoMNPV, BmNPV, OpMNPV and EppoMNPV. Phylogenetic analysis of these sequences, irrespective of the method used, divided them into two clades, one consisting of AcMNPV, RoMNPV and BmNPV, and the other consisting of OpMNPV and EppoMNPV. In data sets containing sequences from other viruses (e.g. Choristoneura fumiferana MNPV), these sequences grouped with the clade containing OpMNPV and EppoMNPV.
Selection pressure analysis
Models M3 or M8 were the best fit (in terms of having the highest log-likelihood scores) for 81 of the 83 data sets (Table 1). The strictly neutral model (M1) was a poor fit for many of the data sets. For 70 genes, the log-likelihood scores for M1 were lower than the scores for M0 (the model assuming a single
value for all sites). For 4 of these 70 data sets, the M2 model (which includes two classes from M1) also fit the data less well than M0.
For 52 genes, none of the models designed to detect positive selection identified a class with >1. At least one model identified a class of positively selected sites in the remaining 31 data sets. For 18 of 21 data sets for which the M3 model detected a class of positively selected sites, the M2 model did not identify positively selected sites. Because M2 has two fixed-value classes (p0 and p1, with
set at 0 and 1, respectively), the extra category p2 optimally accounts for codon sites with
values lying between 0 and 1 (Yang et al., 2000
).
For nine genes, models M2, M3 or M8 identified a class of positively selected sites and rejected null hypothesis models at P<0·05. For many of the remaining 22 data sets, the nested null hypothesis models could not be rejected at this significance level. In some cases, M3 contained a positively selected site class but was not a significantly better fit for the data than M2, which failed in these cases to identify positively selected sites. These genes were not considered to be positively selected.
Of the data sets for which more than one tree topology was obtained, the models differed in identifying positively selected classes under different tree topologies in only one instance. This result is consistent with previous results indicating that the ability to detect positive selection is not strongly affected by tree topology (Yang et al., 2000).
Positively selected structural genes
Three genes encoding proteins that are components of the virion were identified as being positively selected (Table 2).
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odv-e56.
M3 and M8 both contained site classes in odv-e56 consisting of approximately 4 % of the sites with >3. The other models were rejected at P
0·01. Like ODV-E18, ODV-E56 is found in the envelope of occluded virus. None of the positively selected sites identified by Bayesian analysis were found in a hydrophobic domain hypothesized to be involved in the viral envelope localization of this protein (Braunagel et al., 1996a
).
As ODV envelope proteins, ODV-E18 and ODV-E56 may interact with midgut cell surface proteins and mediate binding and internalization of ODV. Substitutions in key sites of these proteins may enhance binding and internalization in different species.
vp80.
Classes of positively selected codons with >2 were present in both M3 and M8 in the vp80 data set. M3 rejected M1 and M2 (which did not identify positively selected sites) at P<<0·01, but M8 could not reject M7 at P<0·05. For both M3 and M8, Bayesian empirical analysis identified three positively selected sites that are located in the conserved N and C termini of the predicted protein sequence (Li et al., 1997b
).
vp80 encodes a protein associated with the NPV nucleocapsid (Lu & Carstens, 1992; Li et al., 1997b
). It is unclear how changes in a nucleocapsid protein like VP80 would modulate virulence or host range. Positive selection detected with this gene may represent co-variation to compensate for sequence alterations occurring elsewhere in the genome, or it may reflect adaptation that stabilizes virions under different environmental conditions.
Positively selected genes encoding replication and expression factors
Three genes with previously characterized roles in virus replication and gene expression were identified as being positively selected (Table 3).
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lef-7 was found to be necessary for late promoter-driven reporter gene expression in a transient assay in a Spodoptera frugiperda cell line, but not in a Trichoplusia ni cell line (Lu & Miller, 1995a). lef-7 knockout mutant viruses exhibited impaired replication in S. frugiperda and Spodoptera exigua cell lines but not in a T. ni cell line (Chen & Thiem, 1997
). Substitutions in this gene may modulate the ability of NPVs to replicate in the cells of different hosts.
lef-10.
Models M2, M3, and M8 all indicated positively selected categories of sites in lef-10. For M3 and M8, these categories contained approximately 18 % of the sites in this small ORF, and exhibited values of approximately 6·5. Null hypothesis models were rejected for both M3 and M8, and the same eight codon sites were placed into the positively selected category.
lef-12.
Positively selected categories for M3 and M8 each contained approximately 12 % of total sites with similar values (approximately 9·79·8). M3 and M8 rejected the other models at P
0·01. A single codon site (position 153) was identified as being positively selected by both models at P>0·99.
lef-10 and lef-12 were identified as genes that supported late promoter-driven reporter gene expression in a transient assay (Lu & Miller, 1994; Rapp et al., 1998
). lef-12 was found to be essential for expression in assays performed with S. frugiperda-derived Sf21 cells, but not in High 5 cells derived from T. ni, suggesting that LEF-12 operates as a species-specific late gene expression factor (Rapp et al., 1998
). Further analysis revealed that lef-12 was itself a late gene (Guarino et al., 2002
). In contrast to results obtained with transient expression assays, viral mutants in which expression of lef-12 had been eliminated were able to express late genes and replicate in S. frugiperda-derived Sf9 cells, albeit at reduced levels (Guarino et al., 2002
). With both lef-10 and lef-12, mutations may facilitate efficient late gene expression in different species.
Positively selected auxiliary genes and genes of unknown function
Two uncharacterized but widespread ORFs and one gene involved in actin rearrangement were identified as undergoing positive selection (Table 4).
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ac66 and arif-1.
Positively selected sites were identified by M3 and M8 for both ac66 and arif-1, but the parameter estimates for the categories containing these sites were different for the two models. For both ac66 and arif-1, the positively selected categories under M8 were smaller with higher values. For arif-1, M2 (which did not identify positively selected sites) was not rejected by M3.
ac38 and ac66 are present in all lepidopteran NPV genomes sequenced to date. However, these ORFs remain uncharacterized. The ac38 predicted amino acid sequences have no significant sequence identity with proteins with a known function, while ac66 specifies an amino acid sequence with significant identity to desmoplakin, a structural component of intercellular junctions called desmosomes that link the intermediate filaments of cells together (Ruhrberg & Watt, 1997).
The arif-1 ORF encodes the 48 kDa actin rearrangement-inducing factor, a protein that localizes to vesicular structures at the plasma membrane of infected cells (Roncarati & Knebel-Mörsdorf, 1997). ARIF-1 mediates the dissociation of the host cell actin network and of the virus-induced actin cables that form early during infection, as well as the subsequent formation of actin aggregates at the plasma membrane (Dreschers et al., 2001
). Mutations in AcMNPV arif-1 had no effect upon replication in S. frugiperda or T. ni cells in vitro (Roncarati & Knebel-Mörsdorf, 1997
; Dreschers et al., 2001
). However, ARIF-1 could be required in some way for the in vivo replication cycle.
Analysis of the DNA helicase gene
dnahel encodes a DNA helicase (P143) required for viral DNA replication and late gene expression (Gordon & Carstens, 1984; Lu & Carstens, 1991
; Lu & Miller, 1995b
; McDougal & Guarino, 2000
). Substitution of part of the AcMNPV dnahel gene with the homologous sequence from BmNPV dnahel resulted in recombinant AcMNPV that could replicate in a B. mori cell line and kill B. mori larvae, a species normally refractory to AcMNPV infection (Maeda et al., 1993
; Croizier et al., 1994
). Substitutions at two sites encoding different amino acids in the AcMNPV and BmNPV dnahel gene products were found to be minimally required for the expanded host range of the recombinant AcMNPV (Argaud et al., 1998
; Kamita & Maeda, 1997
). This result suggests that P143 works in a host-specific fashion to facilitate virus replication, and that non-synonymous substitutions in dnahel may contribute to the capacity of NPVs to replicate in different hosts.
However, selection pressure analysis with models that allow to vary among sites failed to detect positive selection in this gene (Table 5
). A category of codons with
=1·213 was indicated in M8, but the null hypothesis model M7 could not be rejected (P=0·333). The two sites in dnahel (positions 564 and 577) identified as being minimally required for expansion of the AcMNPV host range to include B. mori had average
values in M8 of 0·099 and 0·08, respectively.
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The likelihood ratio tests used to compare models determine whether sequences in an alignment contain sites under positive selection and are very conservative (Anisimova et al., 2001). The power of the likelihood ratio tests to detect positive selection decreases with decreasing number of sequences in a data set. Because our data sets often consisted of only five sequences, it is likely that not all of the positively selected NPV genes of the group of 83 examined in this study were detected. In addition, the inclusion of the OpMNPV sequences likely resulted in higher values of dS, which would have increased the difficulty of identifying genes with
>1. The OpMNPV genome has an overall G+C composition of 55 %, while the G+C compositions of EppoMNPV, AcMNPV, RoMNPV, and BmNPV are approximately 3941 %. This difference in nucleotide frequencies is especially pronounced in the third (wobble) codon position of coding sequences, where the G+C % ranges from approximately 7080 % for OpMNPV genes and 4852 % for genes from the other viruses. As a result, homologous codon sites that code for the same amino acid are frequently expected to have a G or a C in the wobble position of the OpMNPV sequence, while an A or a T is more likely to occur at the same position in the other sequences. The sequence differences at the wobble positions of such codons would be scored as synonymous substitutions, when in fact the differences in some cases may be a function of the different nucleotide frequencies between OpMNPV and the other sequences.
The ability of the empirical Bayes method to identify sites occurring in positively selected classes suffers from reduced accuracy when a low number of sequences are analysed (Anisimova et al., 2002). Although the empirical Bayes method often identified the same residues as being positively selected with different models (M3 and M8), the identification of positively selected sites in this study should be regarded with caution because of the relatively low number of sequences in the data sets.
This analysis identified nine genes that have undergone positive selection amongst group 1 NPVs. Two of these genes (odv-e18 and arif-1) were previously identified as being positively selected when the same codon substitution models were applied to alignments of AcMNPV and RoMNPV genes (Harrison & Bonning, 2003). Genes under positive selection pressure may account for differences in species-specific virulence or host range among NPVs, although contributions to environmental stability or transmission efficiency cannot be ruled out. It is also possible that some of these genes, such as vp80, are not responding directly to selection pressure but are exhibiting co-variation to compensate with changes elsewhere in the genome. Empirical studies will be required to assess the contribution of the positively selected genes identified in this study to species-specific virulence and host range.
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ACKNOWLEDGEMENTS |
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Received 6 August 2003;
accepted 22 September 2003.
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