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Sassan Asgari, Dennis K. Bideshi, Yves Bigot, Brian A. Federici and Xiao-Wen Cheng
A summary of this ICTV Report chapter has been published as an ICTV Virus Taxonomy Profile article in the Journal of General Virology, and should be cited when referencing this online chapter as follows:
Asgari, S., Bideshi, D.K., Bigot, Y., Federici, B.A., Cheng, X. and ICTV Report Consortium, 2017, ICTV Virus Taxonomy Profile: Ascoviridae, Journal of General Virology, 98:4–5.
The family Ascoviridae includes viruses with circular dsDNA genomes of 100-200 kilobase pairs (kbp) characterized by oblong enveloped virions of 200-400 nm in length. Members of this family mainly infect lepidopteran larvae and are mechanically transmitted by parasitoid wasps in which they may also replicate. They cause high mortality among economically important insect pests thereby contributing to their natural ability to control insect populations.
Table 1.Ascoviridae. Characteristics of the family Ascoviridae.
Spodoptera frugiperda ascovirus 1a (AM398843), species Spodoptera frugiperda ascovirus 1a, genus Ascovirus
Enveloped, 130 nm in diameter by 200-400 nm in length, at least 20 polypeptides
100-200 kbp of circular dsDNA with 117-180 genes
Nuclear, with cell cleavage into virion-containing vesicles that turn the host haemolymph milky white
From transcribed mRNAs
Lepidopteran insect larvae, mostly members of the family Noctuidae
Two genera Ascovirus and Toursvirus
Members of this family are classified into two genera with distinct evolutionary lineages and genome characteristics:
Ascovirus. This genus includes three species whose members infect various members of the insect family Noctuidae, many species of which are economically important. Ascoviruses are difficult to transmit orally, and experimental studies as well as field observations indicate virions are mechanically transmitted horizontally by endoparasitic wasps of the families Braconidae and Ichneumonidae (Hymenoptera) through their contaminated ovipositor (Bideshi et al., 2010).
Toursvirus. This genus includes only one species, Diadromus pulchellus toursvirus (previously named Diadromus pulchellus ascovirus 4a). Diadromus pulchellus toursvirus (DpTV) is so far only found in species of the lepidopteran family Yponomeutidae, but it replicates also in its ichneumonid vector, Diadromus pulchellus. Replication in the wasp vector is limited in comparison to the titers produced in the lepidopteran host (Bigot et al., 1997a). In the wasp, DpTV is transmitted vertically when the virus genome is carried as unintegrated DNA in the nuclei of infected cells.
Virions of ascoviruses are either bacilliform, ovoidal or allantoid in shape, and depending on the species, have complex symmetry, and are large, measuring approximately 130 nm in diameter by 200-400 nm in length. The virion consists of an inner particle surrounded by an outer envelope. The inner particle typically measures 80 x 300 nm and contains a DNA/protein core bounded by an apparent lipid bilayer, the external surface of which bears a distinctive layer of protein subunits. The virion, therefore, appears to contain two lipid membranes, one associated with the inner particle and the other forming the envelope. In negatively stained preparations, virions have a distinctive reticulate appearance thought to result from superimposition of protein subunits on the surface of the internal particle with those in the external envelope (Figure 1.Ascoviridae). Virions of DpTV of the genus Toursvirus have a similar size: about 220 nm long and 150 nm wide. They are multilayered, with two clear 7-nm-thick outer layers and one 15-nm-thick inner layer surrounding an electron-dense core (155-110 nm). However, the flattened rice-grain shape and fragility of the DpTV particles are unlike that of ascoviruses.
Virions are sensitive to organic solvents and detergents.
The inner particle contains a single molecule of circular dsDNA ranging from 100 to 200 kbp. The G + C content ranges from 42% to 60% depending on the species. Ascovirus genomes contain from 117 to 180 genes, of which 40 are common among them (Bigot et al., 2009).
Virions contain at least 20 proteins ranging in size from 6 to 200 kilodaltons (kDa) (Tan et al., 2009).
Ultrastructural evidence and detergent sensitivity indicate the presence of lipid in both the outer envelope and inner particle of the virion. The specific lipid composition is not known.
The genomes of five members of the genus Ascovirus, Heliothis virescens ascovirus 3e (HvAV-3e) (Asgari et al., 2007), HvAV-3f (Wei et al., 2014), HvAV-3g (Huang et al., 2012), Spodoptera frugiperda ascovirus 1a (SfAV-1a) (Bideshi et al., 2006) and Trichoplusia ni ascovirus 6a (TnAV-6a; previously named TnAV-2c) (Wang et al., 2006), and one member of the genus Toursvirus, Diadromus wulchellus toursvirus (DpTV) (Bigot et al., 2009) have been completely sequenced.
Members of the family Ascoviridae initiate replication in the nucleus. The nucleus enlarges and ruptures, after which the plasmalemma invaginates, forming internal membranous folds that cleave the cell into a cluster of virion-containing vesicles (Federici and Govindarajan 1990). Virion assembly becomes apparent after the nucleus ruptures. The first recognizable structural component of the virion to form is the multilaminar layer of the inner particle. Based on its ultrastructure, this layer consists of a unit membrane and an exterior layer of protein subunits. As the multilaminar layer forms, the dense DNA/protein core assembles along the inner surface. While this process continues, the allantoid, ovoidal or bacilliform shape of the inner particle becomes apparent. After the inner particle is assembled, it is enveloped by a membrane, synthesized de novo, or derived from cell membranes, within the cell or vesicle. In the case of SfAV-1a, virions are occluded in an occlusion body composed of minivesicles and protein (Federici et al., 1990).
Members of the Ascovirus genus cause disease in lepidopteran larvae and pupae, and have been reported most commonly from species of the family Noctuidae, including Trichoplusia ni, Heliothis virescens, Helicoverpa zea, Spodoptera frugiperda and Autographa precationis. TnAV-2a and HvAV-3a have been shown to have a broad experimental host range among larvae of the lepidopteran family Noctuidae, but the host range of SfAV-1a is restricted primarily to species of Spodoptera (Hamm et al., 1986). However, ascoviruses may have an expanded host range that includes non-noctuid insects. For example, recent studies have demonstrated that HvAV-3e is able to productively propagate in Crocidolomia pavonana and Plutella xylostella larva, lepidopteran species belonging to families Crambidae and Plutellidae, respectively (Smede et al., 2008, Furlong and Asgari 2010).
DpTV, the only member of the Toursvirus genus, so far has only been found in species of the lepidopteran family Yponomeutidae, in which it replicates extensively. There is also a limited replication of the virus in its ichneumonid vector, Diadromus pulchellus, but is substantially less than its replication in the lepidopteran host (Bigot et al., 1997a).
Members of the family Ascoviridae are difficult to transmit orally, and experimental studies as well as field observations indicate most are transmitted horizontally by endoparasitic wasps (Hymenoptera), many species of which belong to the families Braconidae and Ichneumonidae (Federici and Govindarajan 1990, Tillman et al., 2004). During egg-laying, the ovipositor of female wasps becomes contaminated with virions and virion-containing vesicles that circulate in the blood (hemolymph) of infected caterpillars. Wasps contaminated in this manner subsequently transmit ascovirus virions to new caterpillar hosts during oviposition. DpTV is transmitted vertically in the wasp D. pulchellus when the virus genome is carried as extrachromosomal DNA in the nuclei of infected cells.
Members of the family Ascoviridae are known from the United States, Europe, Australia, Indonesia, Japan, China and Mexico, and likely occur worldwide, that is, wherever species of Lepidoptera and their hymenopteran parasites occur. These viruses cause a chronic, fatal disease that markedly retards larval development, but which typically exhibits little other gross pathology. This lack of easily recognizable gross pathology probably accounts for the lack of host records from many geographical regions.
Members of the family Ascoviridae vary in tissue tropism, with some attacking most host tissues, such as TnAV-2a and HvAV-3a, whereas others, such as SfAV-1a, are restricted to the fat body (Federici and Govindarajan 1990). The unique property of ascovirus infection is a cytopathology in which host cells cleave to form virion-containing vesicles by a developmental process utilizing a modified form of apoptosis (Bideshi et al., 2005). Infection results in nuclear hypertrophy followed by lysis. The anucleate cell enlarges 5–10-fold and then cleaves into 10–30 virion-containing vesicles. Membranes delimiting vesicles form by invagination of the plasmalemma and membrane synthesis. Millions of vesicles (ca. 107–108 vesicles ml-1) accumulate in the hemolymph, turning it milky white. Opaque white hemolymph containing refractile virion vesicles is unique and diagnostic for ascovirus disease (Federici 1983).
The following list of criteria is used to differentiate genera in the family:
The virions of most Ascovirus isolates are similar in size and shape (Federici et al., 1990), but the Toursvirus DpTV virions are more flattened rice-grain shape rather than allantoid found in other ascoviruses (Bigot et al., 1997b). There should be no DNA/DNA hybridization between members of the genera Ascovirus and Toursvirus. DpTV, as the sole member of Toursvirus, is mostly transmitted by the parasitoid wasp, Diadromous pulchellus, whereas members of the genus Ascovirus can be transmitted by a variety of parasitoid wasp species. DpTV has been mainly isolated from the host pupae in the lepidopteran family of Yponomeutidae, but members of the Ascovirus genus have been isolated mostly from larvae of the lepidopteran family Noctuidae.
Asco: from the Greek for “sac”, referring to the virion-containing vesicles produced by cleavage of host cells, which are characteristic for all known viruses of this family.
Tours: from Tours, France, where DpTV was first isolated.
The family appears to have evolved into two lineages in which DpTV sits within a lineage distinct to that of the Ascovirus genus (Piegu et al., 2015) (Figure 2.Ascoviridae).
Phylogenetic analyses using nine core genes shared by the members of Ascoviridae, Iridoviridae and Marseilleviridae revealed that all iridoviruses and members of Ascoviridae have evolved from a common ancestor that they share with members of the family Marseilleviridae (Figure 2.Ascoviridae).
Ascoviruses typically replicate in lepidopteran larvae of the family Noctuidae producing virion-containing vesicles, which give a milky white colouration to the haemolymph. Virions of ascoviruses are either bacilliform, ovoidal or allantoid in shape measuring 130 nm in diameter by 200–400 nm in length.
See discussion under family description.
The following list of characters is used in combination to differentiate species in the genus:
Members of the family Ascoviridae, in particular members of the genus Ascovirus, can have broad host ranges among the larvae of lepidopteran species, and the fat body tissue is a major site of replication for most species (Federici and Govindarajan 1990). The above characters are therefore used in combination to distinguish existing and new ascovirus species from one another. Hybridization studies have proven particularly useful, and when combined with RFLPs and phylogenetics can also be used to distinguish variants within a species. For example, SfAV-1a DNA does not hybridize with HvAV-3a or TnAV-2a DNAs under conditions of low stringency. TnAV-2a DNA hybridizes to some extent with HvAV-3a DNA, but not as strongly as it does with homologous DNA. In addition, TnAV-2a replicates in a range of larval tissues including the fat body, tracheal matrix and epidermis, but SfAV-1a and HvAV-3a appear to replicate, respectively, only or primarily in the fat body tissue of most hosts. SfAV-1a virions are bacilliform and are occluded in vesiculate occlusion bodies, whereas TnAV-2a virions are allantoid and are not occluded in occlusion bodies. HvAV-3a virions vary from allantoid to bacilliform, and are not occluded in occlusion bodies.
When the genome of a new isolate cross-hybridizes with that of an existing species member, RFLPs can be used to distinguish variants. Numerous ascovirus isolates, for example, have been obtained from larvae of different noctuid species, including Heliothis virescens, Helicoverpa zea, Autographa precationis and Spodoptera exigua in the United States, as well as from Helicoverpa and Spodoptera species in Australia, China and Indonesia. The DNA of many of these isolates shows strong reciprocal hybridization with HvAV-3a DNA under conditions of high stringency. RFLP profiles of these isolates, however, often show variations from HvAV-3a that range from minor to major. Because these isolates cross-hybridize strongly with HvAV-3a, they are considered variants of this viral species. Moreover, experimentally these isolates have been shown to have host ranges that overlap with HvAV-3a, providing additional evidence that they are variants of the same species. A similar situation occurs with isolates of TnAV-2a and TnAV-2b.
Trichoplusia ni ascovirus 6a
(formerly Trichoplusia ni ascovirus 2c)
Currently, there is only one species within this genus, Diadromous pulchellus toursvirus. The single known member of this species, Diadromous puchellus toursvirus (DpTV) is transmitted by the parasitoid wasp Diadromous pulchellus, which typically parasitizes pupae of the lepidopteran family Yponomeutidae.
Virions of Toursvirus are flattened rice-grain shape, and fragile relative to members of the genus Ascovirus. Virions are typically 220 nm long and 150 nm wide.
Genome consists of a circular dsDNA of about 119 kbp with a GC% of 49.7 encoding 119 putative genes. The genome of DpTV is the smallest within the family Ascoviridae.
Eleven virion proteins are shared with members of the genus Ascovirus (Bigot et al., 2009).
The genome of the only member of this genus, DpTV (Bigot et al., 2009) has been sequenced. Replication is largely similar to members of the genus Ascovirus.
Similar to ascoviruses, toursvirus DpTV, is transmitted by a parasitoid wasp, Diadromus pulchellus. DpTV infection has mainly been found in the pupae of members of the lepidopteran family of Yponomeutidae. The virus also has a limited replication in the ovaries of the female wasp and is vertically transmitted as extrachromosomal DNA. Compared to the lepidopteran host, replication of DpTV in the parasitoid wasp is very limited (Bigot et al., 1997).
Sassan Asgari*Ascoviridae Study Group ChairSchool of Biological Sciences The University of Queensland Brisbane QLD 4072 Australia Tel: 617-33652043 E-mail: email@example.com
Dennis K. Bideshi California Baptist University Department of Natural and Mathematical Sciences 8432 Magnolia Avenue Riverside, CA 92504 USA Tel: 951-343-4397 E-mail: firstname.lastname@example.org
Yves Bigot UMR INRA-CNRS 7247, PRC Centre INRA de Nouzilly 37380 Nouzilly France Tel: 33-0-247427566 E-mail: email@example.com
Brian A. Federici Department of Entomology Department of Interdepartmental Graduate Programs in Microbiology and Cell, Molecular and Developmental Biology University of California Riverside, CA 92521 USA Tel: 951-827-5006 E-mail: firstname.lastname@example.org
Xiao-Wen Cheng Department of Microbiology 32 Pearson Hall Miami University Oxford, OH 45056 USA Tel: (513) 529-5429 E-mail: chengx@MiamiOH.edu
* to whom correspondence should be addressed
The chapter in the Ninth ICTV Report, which served as the template for this chapter, was contributed by Bigot, Y., Asgari, S., Bideshi, D.K., Cheng X.W., Federici, B.A. and Renault, S.
Tree file (nexus format)
Alignment file (fasta format)
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A summary of this ICTV Report chapter has been published as an ICTV Virus Taxonomy Profile article in the Journal of General Virology, and should be cited when referencing this online chapter as follows:
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