The history of the discovery of baculoviruses is intimately related to the development of the silk industry that occurred in China as early as 5000 years ago. The culture of silkworms spread throughout Asia and reached Japan via Korea by about 300 C.E. and arrived in Europe by about 550 C.E. By the 12th century it was established in Italy and Spain and eventually spread to France and England and to Mexico by the 1500s. Silk production has been of major cultural significance in both China and Japan. It was a major item of commerce and in Japan is extensively documented in historic prints (1). Although no longer a major industry, silk production is still practiced symbolically by the Japanese royal family. (For a review of the history of silkworm culture, see (2)). As with any agricultural enterprise, problems were encountered caused by a variety of diseases, and these had to be confronted in order for the industry to flourish. Even before the germ theory of disease was introduced, a variety of different types of illnesses afflicting silkworms had been described, and methods to mitigate the effects of these diseases had been developed. With the advent of light microscopy, a prominent feature of one of the types of diseases was characterized by the presence of highly refractile occlusion bodies that were symptomatic of the affected insects. These were commonly polyhedron shaped (Figure 1) and led to the naming of the diseases associated with these structures as 'polyhedroses' by the mid-1800s. Although the presence of infectious particles within occlusion bodies had been suggested earlier, it was not until the late 1940s that the presence of rod-shaped virions was convincingly demonstrated by electron microscopy (3). This and other investigations also established the crystalline nature of the occlusion body structure. Subsequently, two different types of polyhedrosis diseases were distinguished: those in which the polyhedra developed in nuclei and were called nuclear polyhedroses (NPVs), and those with occlusion bodies present in the cytoplasm (Figure 2). These were called cytoplasmic polyhedroses (CPVs) (4). In contrast to the rod-shaped, DNA-containing NPVs, the CPVs were observed to have icosahedral capsids and were placed in the Reoviridae (genus Cypovirus), a family of viruses with segmented, double-stranded RNA genomes. A second category of baculovirus characterized by the presence of small, granular, ellipsoidal-shaped occlusion bodies was originally reported in the 1920s (5) and was named granulosis viruses (GVs). The division of the baculoviruses into two major groups, the nuclear polyhedrosis viruses (now called nucleopolyhedroviruses (NPV)) (Figure 3) and the granulosis viruses (now called granuloviruses (GVs)) (Figure 4), based on occlusion body morphology defined the major taxonomical divisions of these viruses until the advent of molecular biology.

Figure 1

Baculovirus occlusion bodies. Scanning EM by K. Hughes and R. B. Addison.

Figure 2

Comparison of cells infected with a cypovirus (CPV – Reoviridae) and a baculovirus. Left panel: CPV of Orgyia pseudotsugata. Photo by G. S. Beaudreau. Right Panel: AcMNPV infected T. ni cells. From Volkman and Summers (65). Copyright 1975 American (more...)

Figure 3

Two nucleopolyhedroviruses pathogenic for Orgyia pseudotsugata showing single (top panel) and multiple (bottom panel) nucleocapsids/envelope. Top panel: OpSNPV. Bottom panel: OpMNPV. From Hughes and Addison (33). Copyright 1970 Elsevier. Reproduced with (more...)

Figure 4

Cross section of a granulovirus of Plodia interpunctella. From Arnott and Smith (66). Copyright Elsevier 1967. Reproduced with permission via Copyright Clearance Center.

The terminology for these viruses went through a series of names, and it was not until 1973 that a nomenclature that included Borrelinavirus, Bergolidavirus, Smithiavirus, Moratorvirus and Vagoiavirus in honor of various historic individuals who had done early research on NPVs and GVs was changed and unified into the Baculoviridae (6). The name baculovirus was proposed by Mauro Martignoni, who because of his Italian-Swiss heritage was a Latin scholar. He suggested that they be named baculoviruses (family Baculoviridae) because of the rod-shape of their virions, which is derived from Latin baculum — cane, walking stick, staff.

The significance of baculoviruses in Nature

Although much of the early interest in baculoviruses was due to the threat they posed to the silk industry, baculoviruses play a major role in the control of natural insect populations. For example, they are a major regulator of gypsy moth populations in North America and in some instances have been shown to be responsible for over 50% of the mortality observed (7). They also are major contributors to the collapse of Douglas-fir tussock moth outbreaks (8). In addition to forest insect populations, they also appear to be important in the natural control of agricultural pests of human food crops, and as a result they may be a substantial contaminant of the human diet. For example, in one study it was found that cabbage purchased from 5 different supermarkets in the Washington D.C. area were all contaminated with baculoviruses to such an extent that each serving (about 100 cm² of leaf material) would contain up to 10⁸ polyhedra of an NPV pathogenic for the cabbage looper, Trichoplusia ni (9)!

Baculoviruses are normally named for the initial host from which they were isolated. Consequently, the type NPV species, AcMNPV, was named for its host, the alfalfa looper, Autographa californica (Ac). This naming would be straightforward except that AcMNPV infects a wide variety of lepidopteran insects and its name originated because of its initial association. Consequently, a variety of other virus isolates e.g., Galleria mellonella (GmNPV), Rachiplusia ou (RoNPV), and Plutella xylostella (PlxyNPV), although having unique names, are closely related (~96-98.5% at the amino acid sequence level) variants of AcMNPV. In addition, viruses were originally named by the first letter of the genus and species of their host. However, as more viruses were discovered, some infected different insects that had names with the same first letters. This resulted in different viruses with the same descriptor. Consequently, the first two letters of the genus and species have become the convention, i.e., AcMNPV should really be AucaMNPV. However, since AcMNPV, GmMNPV and RoMNPV have been used so extensively, the original abbreviations have been retained.

The recent proliferation of baculovirus genome sequences has greatly expanded our understanding of their diversity and evolution. This has yielded distinct patterns of virus relatedness (Figure 5) in which virus lineages are associated by the host that they infect. The Baculoviridae are divided into four genera (23). The viruses of Lepidoptera are divided into Alpha- and Betabaculoviruses encompassing the NPVs and GVs, respectively, and those infecting Hymenoptera and Diptera would be named Gamma- and Deltabaculoviruses, respectively (Table 2). Such patterns of host-associated virus diversity were first observed for small DNA viruses (papilloma and polyoma viruses) of mammals (24) and suggested for baculoviruses based on N-terminal polyhedrin and granulin sequences (25). In this process, viruses associate with a host, and as their host becomes genetically isolated and speciates, so does the virus in a process called host-dependent evolution. As more sequence data has become available, this process has been more convincingly demonstrated for baculoviruses (26) and is clearly reflected in Figure 5 in which the major lineages are clustered into clades based on the host insect that they infect. In GVs, host-dependent evolution has been suggested on the level of insect families (27). A major division has been observed in the lepidopteran NPVs that has resulted in the separation of this lineage into two major Groups, I and II (28). These two groups differ significantly in gene content, most notably Group I NPVs use GP64 as their BV fusion protein, whereas Group II NPVs lack gp64 and utilize a protein called F (29). There are also 11 other genes in addition to gp64 that appear to be found only in Group I NPVs (Table 3). It has been suggested that the Group I lineage originated when a NPV variant uniquely containing these genes incorporated gp64 which stimulated their evolution as a distinct lineage (30, 31). Although the list of host insects provides information on baculovirus distribution, sequence analysis of common sets of genes from a wide variety of baculoviruses has provided a picture of the actual extent of their diversity (32). From this data, a picture of the lepidopteran viruses has emerged. However, more information on viruses from the other insect orders is needed to complete our understanding of baculovirus evolution.

Figure 5

Phylogenetic relatedness of LEF8 from selected baculoviruses. Neighbor joining; bootstrap analysis (1000 reps).

Gene content and organization

Although there are major differences in the sizes of baculovirus genomes, a few patterns are evident (Table 4). The viruses of members of the Hymenoptera contain the smallest genomes at a little over 80 kb. In contrast, the GV genomes vary from 101 kb (PlxyGV) up to 178 kb (XecnGV). Group I NPVs cluster around 130 kb, whereas Group II show a much higher degree of diversity, varying from about 130 to almost 170 kb. The small size of the hymenopteran NPV genomes might be attributed to a restricted life cycle confined to replication in insect gut cells (40). Consequently, unlike other baculoviruses that cause systemic infections, genes required for spread throughout the insect, where the virus encounters and replicates in a variety of tissues, might not be necessary. In contrast, the large size of a Group II NPV (LdMNPV), which at 161 kb is about 30 kb larger than many other NPV genomes, can be attributed to a combination of repetitive genes (16 bro [baculovirus repeated orf] genes) that add about half of the additional 30 kb, while genes not found in smaller genomes add most of the remainder. These additional genes encode ribonucleotide reductase subunits and two enhancin genes (41). In other viruses with large genomes (e.g., XecnGV), repeated genes including 10 bro and 4 enhancin genes, comprise up to 17% (30 kb) of the genome (42). Despite the large difference in gene content in GV genomes as reflected in their size range, their genomes are surprisingly collinear (43). In contrast, NPVs even from the same order (Lepidoptera) show a high degree of variation (44).

Table 4

Genome size and predicted ORF content* of selected baculoviruses

Conservation of baculovirus genes: core genes

Despite the diversity in gene content present in different baculovirus genomes, a set of about 31 genes that are present in all sequenced baculovirus genomes has been identified (Table 5). This set should be viewed with caution, however, as it is likely that many shared genes have diverged to such an extent that their relatedness cannot be readily determined. This is particularly true of the dipteran virus that is most distant from the baculoviruses of Lepidoptera and Hymenoptera. Of the conserved genes, about half are virion-associated proteins that are involved in capsid structure, the occlusion-derived virus envelope, and larval infectivity. Most of the others are related to DNA replication or processing, and late or very late transcription. Despite this limited set of genes that baculoviruses share, they do provide insight into some of the major functions required of all baculoviruses such as a common virion structure, the necessity to infect gut cells, and the use of a novel polymerase for the expression of late genes. Furthermore, there are sets of genes specific to, and conserved in, each clade of viruses such as gp64 in Group I NPVs and a number of GV-specific genes (see below). These genes likely reflect major recombination events that altered the properties of the viruses to such an extent that they subsequently developed along distinctive phylogenetic pathways. The observation that different types of NPVs and GVs and other types of DNA viruses (e.g., entomopox, ascovirus, nudivirus) have the potential to simultaneously infect the same insect indicates how via recombination, genes can be transferred between different viruses and between viruses and the host insect.

Table 5

Conserved genes¹ in baculoviruses and nudiviruses

Lepidopteran baculovirus (NPV and GV) core genes

In addition to the core genes found in all baculoviruses, lepidopteran baculoviruses encode an additional set of genes that appear to be present in all their genomes, and about half are also found in Gammabaculovirus (hymenopteran virus) genomes (Table 6). Homologs or functional analogs of many of these genes are likely present in all baculoviruses, but the relationships cannot be detected due to the extent of divergence the genes. Since they appear to be so central to the replication of the baculoviruses, the single-stranded DNA binding protein, LEF-3, and the transcriptional activator IE-1 may be examples of gene divergence which prevents their detection in the more distantly related viruses. In contrast, homologs of Ac38, an ADP-ribose phosphatase, belong to a family found in many organisms and would likely be detected outside the lepidopteran baculoviruses, if it were present. It acts as a decapping enzyme in vaccinia virus (53) and its presence suggests that the lepidopteran viruses employ molecular strategies significantly different from the other baculovirus genera. Polyhedrin appears to be an example of possible convergent evolution since the occlusion body protein of the dipteran virus appears to encode a novel protein (54).

Table 6

Additional Core genes present in all Lepidopteran (Alpha- and Beta-) and some Gammabaculoviruses

A few genes are present in all Alphabaculoviruses but are found in some but not all Betabaculoviruses (Table 7). The most well-characterized of these is Ac9 (orf1629), which is a homolog of WASP proteins that are involved in movement of the virus based on actin polymerization (see Chapter 3). This would suggest that other baculoviruses have major differences in their pathogenesis.

Table 7

Genes present in all Alphabaculoviruses (lepidopteran NPVs) and some Betabaculoviruses (GVs)

In addition to baculoviruses, there are a number of viruses pathogenic for invertebrates that have large double-stranded DNA genomes. These include nudiviruses, ascoviruses, irridoviruses, and entomopox viruses. However, with the exception of nudiviruses, all these viruses replicate in the cytoplasm or exhibit a combination of both nuclear and cytoplasmic replication (ascoviruses) (reviewed in (56)). In addition, although nudiviruses are an unassigned genus of viruses, they closely resemble baculoviruses and were originally classified as non-occluded baculoviruses, although occlusion bodies have been occasionally reported (e.g., see (57)). Their similarity to baculoviruses includes nuclear replication and rod-shaped, enveloped nucleocapsids. They have double-strand, circular DNA genomes varying in size from 97–230 kb (14). They were removed from the Baculoviridae because they are nonoccluded. Hence the etymology of their name (latin nudi = naked, bare, uncovered), because they lack occlusion bodies. They also have a somewhat different host range than baculoviruses, having been characterized not only from Lepidoptera, but also from Coleoptera (a rhinoceros beetle) and Orthoptera (a cricket).

As more genome sequence data has become available, homologs of baculovirus genes have been found in many different categories of invertebrate viruses. These appear to be the result of lateral transfer, probably during co-infection of the same host (58). However, the nudiviruses share a significant number of the conserved core genes found in all baculoviruses and therefore their presence does not appear to be a result of lateral gene transfer. As shown in Table 5, nudivirus genomes contain homologs of 20 of the 31 core conserved baculovirus genes. These include homologs of genes encoding the novel baculovirus RNA polymerase subunits, virion structural proteins, and a set of genes required for infection of gut tissue. In addition, genes such as DNA helicase are present in many large DNA virus genomes, and LEF-8 has homology to RNA polymerase subunits from many organisms. However, homology searches group these genes from baculoviruses and nudiviruses together. Therefore, based on morphology and molecular phylogeny, these two groups of viruses clearly share membership in a distinct viral lineage.

An occluded baculovirus-like element pathogenic for the pink shrimp P. monodon has been described (16, 17). These viruses produce striking pyramidal-shaped occlusion bodies containing rod-shaped nucleocapsids similar in dimension and appearance to those of baculoviruses (Figure 6). Analysis of several sequences from this virus has indicated that it encodes proteins similar to the baculovirus/nudivirus lineage including LEF-5, LEF-9 and VLF-1 (14, 59) (Figure 7). Completion of the sequence of this genome should definitively clarify its phylogeny.

Figure 6

Polyhedral inclusion body of a virus of the pink shrimp, Penaeus monodon. Arrows indicated nucleocapsids. From Couch (16). Reproduced with permission of Elsevier Limited via Copyright Clearance Center.

Figure 7

Phylogenetic relatedness of VLF-1 from selected viruses and a braconid wasp. Neighbor joining Best Tree; Numbers in bold indicate Bootstrap values (1000 reps) over 50%. Abbreviations: PemoNPV, Penaeus monodon (shrimp); Cotesia inanitus (braconid wasp); (more...)

Polydnaviruses are not true viruses because they do not contain genetic material for their own replication. They are produced in the ovaries of parasitic wasps, and the virion-like particles contain genetic material from the wasp and are injected into host lepidopteran larvae along with the wasp eggs. They are named because they contain multiple circular double-stranded DNA molecules (polydispersed DNA) encompassing up to 560 kb that encode gene products that compromise the target host immune system and other processes and are essential for the successful development of the wasp egg. There are two lineages of parasitic wasps that employ these elements; the braconid and ichneumonids, producing bracovirus and ichnovirus polydnavirus elements, respectively. When cDNAs produced from RNA associated with polydnavirus production in braconid ovaries were analyzed, a number were found to exhibit sequence homology to genes encoded by nudiviruses and baculoviruses (Figure 6). These included per os infectivity factors that are involved in infection of mid-gut cells by baculoviruses. Another group of factors are related to subunits of the baculovirus RNA polymerase and a very late transcription factor, VLF-1. When the structural proteins of the polydnavirus virions were analyzed, proteins related to per os infectivity factors were also identified. The presence of homologs of these factors suggests that they may be involved in a similar role to that played in baculoviruses by delivering the bracovirus DNA into cells of the parasitized larvae. The logic of the production of host viral RNA polymerase subunits in association with virus production remains to be explained (60, 61). These data have been interpreted to indicate that a parasitic wasp was infected by a nudivirus and all or part of the nudivirus genome was incorporated into the wasp genome. Some of these genes were subsequently adapted for the packaging of the polydnavirus DNA, thereby facilitating their transmission into the host larvae.

A similar analysis of an ichnovirus found that polydnavirion-associated proteins did not show relatedness to known proteins. However, because the genes encoding these products were found clustered in specific locations and are amplified along with the DNA that is packaged in the ichnovirus virions, it was suggested that they are derived from a hitherto unknown virus that integrated into the host genome similar to the nudivirus-like element that is present in the genomes of braconid wasps (62).

A phylogenetic tree of VLF-1 from representative baculovirus, nudivirus, polydnavirus (bracovirus) host (Cotesia inanitus), and two nudiviruses is shown in Figure 7. Although there appear to be two distinct lineages with the baculovirus comprising one and the other including the nudiviruses, shrimp virus, and bracovirus host (Cotesia), the latter branch is not well supported, and therefore, it is difficult to draw conclusions regarding the relationships of the non-baculovirus lineages.

Hytrosaviruses include the salivary gland hypertrophy viruses and have been characterized from several Diptera including the tsetse fly, the vector for sleeping sickness. They are non-occluded and contain large double-stranded DNA genomes and have a virion morphology similar in both size and appearance to baculoviruses. They appear to infect the salivary gland and although not particularly virulent, they can result in a significant reduction in reproductive fitness (63).

The genus Whispovirus includes the white spot syndrome virus (WSSV) that causes severe disease outbreaks in cultured penaeid shrimp, particularly in Asia. It is a non-occluded, enveloped, rod-shaped virus with a double-stranded DNA genome of up to 300 kb. It is a highly virulent virus and causes major tissue damage; the infection results in white spots of calcium deposited in the shell (64).

Genomes of both the WSSV and several hytrosaviruses have been sequenced and have been found to encode homologs of four baculovirus/nudivirus genes involved in per os infectivity including pifs 1-3 and p74 (14). It is unclear if these viruses have a direct phylogenetic relatedness to the baculovirus/nudivirus lineage, or whether this is an example of a set of genes important in oral infectivity that was transferred between viruses. The lack of RNA polymerase subunits suggests that their molecular biology may be significantly different from the baculovirus/nudivirus lineage.

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