Transmission of Ascovirus from<i>Heliothis virescens</i>(Lepidoptera: Noctuidae) by Three Parasitoids and Effects of Virus on Survival of Parasitoid<i>Cardiochiles nigriceps</i>(Hymenoptera: Braconidae)

Tillman, P. Glynn; Styer, Eloise L.; Hamm, John J.

doi:10.1603/0046-225x-33.3.633

Cited by 32 publications

(28 citation statements)

References 18 publications

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“…Another explanation might be linked with the life-history traits of the wasps themselves: endoparasitoid wasps insert their ovipositors in several individuals of a lepidopteran population either to probe the host quality before oviposition or to feed on the host. This behaviour may have favoured encounters with viruses, which can themselves use the wasps as vectors for horizontal transmission, as is the case for ascoviruses [51,52]. It should be noted that pathogenic virus infection induced during oviposition may benefit the development of parasitoid larvae by inhibiting host defences [53].…”

Section: (D) Endogenous Viral Element Domestication Convergencementioning

confidence: 99%

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Herniou

Huguet

Thézé

et al. 2013

Phil. Trans. R. Soc. B

157

172

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International audienceThe Polydnaviridae (PDV), including the Bracovirus (BV) and Ichnovirus genera, originated from the integration of unrelated viruses in the genomes of two parasitoid wasp lineages, in a remarkable example of convergent evolution. Functionally active PDVs represent the most compelling evolutionary success among endogenous viral elements (EVEs). BV evolved from the domestication by braconid wasps of a nudivirus 100 Ma. The nudivirus genome has become an EVE involved in BV particle production but is not encapsidated. Instead, BV genomes have co-opted virulence genes, used by the wasps to control the immunity and development of their hosts. Gene transfers and duplications have shaped BV genomes, now encoding hundreds of genes. Phylogenomic studies suggest that BVs contribute largely to wasp diversification and adaptation to their hosts. A genome evolution model explains how multidirectional wasp adaptation to different host species could have fostered PDV genome extension. Integrative studies linking ecological data on the wasp to genomic analyses should provide new insights into the adaptive role of particular BV genes. Forthcoming genomic advances should also indicate if the associations between endoparasitoid wasps and symbiotic viruses evolved because of their particularly intimate interactions with their hosts, or if similar domesticated EVEs could be uncovered in other parasites

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Section: (D) Endogenous Viral Element Domestication Convergencementioning

confidence: 99%

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Herniou

Huguet

Thézé

et al. 2013

Phil. Trans. R. Soc. B

157

172

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“…Contamination of the ovipositor results in very high levels of infection, typically greater than 80%, in larvae subsequently probed by these wasps. That this mechanism of transmission operates under field conditions is supported by studies showing that ascovirus isolates can be obtained by allowing field-collected wasps to probe laboratory-reared larvae (46,103).Whereas field studies of ascoviruses indicate that they occur commonly, particularly in populations of lepidopteran species …”

mentioning

confidence: 98%

Genomic Sequence of Spodoptera frugiperda Ascovirus 1a , an Enveloped, Double-Stranded DNA Insect Virus That Manipulates Apoptosis for Viral Reproduction

Bideshi

Demattei

Rouleux‐Bonnin

et al. 2006

J Virol

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Ascoviruses (family Ascoviridae) are double-stranded DNA viruses with circular genomes that attack lepidopterans, where they produce large, enveloped virions, 150 by 400 nm, and cause a chronic, fatal disease with a cytopathology resembling that of apoptosis. After infection, host cell DNA is degraded, the nucleus fragments, and the cell then cleaves into large virion-containing vesicles. These vesicles and virions circulate in the hemolymph, where they are acquired by parasitic wasps during oviposition and subsequently transmitted to new hosts. To develop a better understanding of ascovirus biology, we sequenced the genome of the type species Spodoptera frugiperda ascovirus 1a (SfAV-1a). The genome consisted of 156,922 bp, with a G؉C ratio of 49.2%, and contained 123 putative open reading frames coding for a variety of enzymes and virion structural proteins, of which tentative functions were assigned to 44. Among the most interesting enzymes, due to their potential role in apoptosis and viral vesicle formation, were a caspase, a cathepsin B, several kinases, E3 ubiquitin ligases, and especially several enzymes involved in lipid metabolism, including a fatty acid elongase, a sphingomyelinase, a phosphate acyltransferase, and a patatin-like phospholipase. Comparison of SfAV-1a proteins with those of other viruses showed that 10% were orthologs of Chilo iridescent virus proteins, the highest correspondence with any virus, providing further evidence that ascoviruses evolved from a lepidopteran iridovirus. The SfAV-1a genome sequence will facilitate the determination of how ascoviruses manipulate apoptosis to generate the novel virion-containing vesicles characteristic of these viruses and enable study of their origin and evolution.The family Ascoviridae was erected recently to accommodate several new species of large double-stranded DNA (dsDNA) viruses with circular genomes that attack insects of the order Lepidoptera at the larval and pupal stages, causing a chronic, fatal disease (38). Viruses of this family are characterized by large, enveloped virions with a distinctive reticulate surface pattern. Depending on the species, virions are either bacilliform or allantoid (sausage shaped), contain an internal lipid membrane surrounding the DNA/protein core, and are composed of at least 12 structural proteins, ranging in mass from 10 to 200 kDa (40).These structural characteristics of the virions are sufficient to distinguish ascoviruses from all other large dsDNA viruses. However, the most novel feature of ascoviruses is not their virion structure, but rather their unusual cellular pathology and transmission. Unlike for all other viruses, a variety of evidence suggests that ascoviruses induce apoptosis as part of a mechanism that enhances their reproduction and transmission. A typical pattern of cytopathology, as exemplified by Spodoptera frugiperda ascovirus 1a (SfAV-1a), the type species, begins with nuclear hypertrophy and cleavage of host DNA, followed by lysis of the nucleus and fragmentation of the nuclear memb...

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“…As the cell enlarges, the plasma membrane invaginates as part of process that cleaves the cell into numerous virion-containing vesicles, 5-10 µm in diameter, which subsequently disperse to the hemolymph (Federici 1983). Virion assembly continues in these vesicles as they circulate in the hemolymph, where they contaminate the ovipositor of parasitic wasps during oviposition for transmission to the next host Tillman et al 2004).In eucaryotic cells, apoptosis is a common response to virus infection that limits virus replication and dissemination (O'Brien 1998;Roulston et al 1999;Barber 2001;Clarke and Clem 2003;Imajoh et al 2004). To counter this response, many viruses have acquired genes during evolution that encode anti-apoptotic proteins to inhibit apoptosis.…”

mentioning

confidence: 99%

“…The ovipositor of the female wasp becomes contaminated with virions and virion-containing vesicles when inserted into an infected host to lay eggs. Subsequent oviposition in other caterpillars transfers virions to new hosts, resulting in their infection and death as well as the death of wasp progeny (Hamm et al 1985;Govindarajan and Federici 1990;Tillman et al 2004). An interesting exception to this transmission pattern is the ascovirus that attacks pupae of the leak moth, Acrolepiosis assectella.…”

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confidence: 99%

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confidence: 99%

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A viral caspase contributes to modified apoptosis for virus transmission

Bideshi¹,

Tan²,

Bigot³

et al. 2005

Genes Dev.

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The Spodoptera frugiperda ascovirus, a DNA virus that attacks lepidopterans, codes for an executioner caspase synthesized by 9 h after infection of Sf21 cells. This caspase alone induces apoptosis in insect cells and, during viral replication in vivo, contributes to a novel cell cleavage process in which developing apoptotic bodies are rescued by the virus and differentiate to form large vesicles in which virions assemble. These viral vesicles disseminate to the blood, where they are acquired during egg-laying by parasitic wasps that transmit the virus. No other viruses encode caspases or form such modified apoptotic bodies, suggesting this caspase plays a direct role in cell partitioning that facilitates viral reproduction and transmission.Supplemental material is available at http://www.genesdev.org. Ascoviruses are complex double-stranded DNA viruses that attack lepidopterans, most commonly species of the family Noctuidae. Virions of these viruses are enveloped, bacilliform to allantoid in shape and 400 nm in length, and contain circular genomes, which, depending on the species, range from 116 to 180 kbp (Federici et al. 2000). An unusual feature of ascoviruses in comparison to most other viruses that attack invertebrates is that they are poorly infectious per os . Instead, laboratory experiments and ecological studies have shown that these viruses are transmitted mechanically by female parasitic wasps during oviposition. The ovipositor of the female wasp becomes contaminated with virions and virion-containing vesicles when inserted into an infected host to lay eggs. Subsequent oviposition in other caterpillars transfers virions to new hosts, resulting in their infection and death as well as the death of wasp progeny (Hamm et al. 1985;Govindarajan and Federici 1990;Tillman et al. 2004). An interesting exception to this transmission pattern is the ascovirus that attacks pupae of the leak moth, Acrolepiosis assectella. The genome of this ascovirus is carried unintegrated in the nuclei of males and females of its wasp vector, Diadromus pulchellus, and virions are transmitted vertically during oviposition by the wasp, which is highly dependent on this virus for parasitic success (Bigot et al. 1997).While the transmission of ascoviruses is unusual for an insect virus, the most novel feature of these viruses compared with all others is their reproductive cellular biology. After infecting a cell, these viruses initiate a cytopathology that resembles apoptosis, but in vivo differs significantly in several features. Within a few hours of infection, the nuclear membrane invaginates and then fragments (Federici 1983;Federici and Govindarajan 1990). Subsequently, rather than shrink and form characteristic apoptotic bodies by blebbing as cell death proceeds, the cell hypertrophies, enlarging as much as 10 times the size of healthy cells . As the cell enlarges, the plasma membrane invaginates as part of process that cleaves the cell into numerous virion-containing vesicles, 5-10 µm in diameter, which subsequently disperse ...

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Transmission of Ascovirus fromHeliothis virescens(Lepidoptera: Noctuidae) by Three Parasitoids and Effects of Virus on Survival of ParasitoidCardiochiles nigriceps(Hymenoptera: Braconidae)

Cited by 32 publications

References 18 publications

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Genomic Sequence of Spodoptera frugiperda Ascovirus 1a , an Enveloped, Double-Stranded DNA Insect Virus That Manipulates Apoptosis for Viral Reproduction

A viral caspase contributes to modified apoptosis for virus transmission

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