Elsevier

Virus Research

Volume 117, Issue 1, April 2006, Pages 81-89
Virus Research

Unfolding the evolutionary story of polydnaviruses

https://doi.org/10.1016/j.virusres.2006.01.001Get rights and content

Abstract

Polydnaviruses (PDVs) are fascinating viruses. Described in thousands of parasitoid wasp species they are unique viruses having both a segmented DNA genome in viral particles and an integrated form that persists as a provirus in the wasp genome. Parasitoid wasps inject their eggs in another insect host typically a lepidopteran. In these host–parasitoid interactions, the virus particles are co-injected along with the eggs and are essential to ensure wasp parasitism success. PDVs do not replicate in the lepidopteran host, but expression of viral gene products confers protection from the host immune defence response. Two genera of PDVs phylogenetically unrelated exist, the bracoviruses (BVs) and the ichnoviruses (IVs), associated with braconid and ichneumonid wasps, respectively. New data on the genomes of two bracoviruses (Microplitis demolitor BV and Cotesia congregata BV) and an ichnovirus associated with Campoletis sonorensis (CsIV) offers us new elements to discuss the central questions concerning the origin of these viral entities and how they have evolved. The results of sequencing approaches indicate that the tens of millions of years of mutualistic associations between PDVs and wasps have had a strong impact on PDV genomes that now ressemble eukaryotic regions both in organization and gene content.

Introduction

Advances in the knowledge of viral particle structure and the mechanisms by which viruses reproduce in their host cells have lead to their definition as obligate intracellular parasites that are replicated and transcribed by cells to form progeny virions that can infect adjacent host cells and organisms. The recent description of “giant” viral genomes (mimivirus and polydnavirus) is however breaking the classical vision we have of viruses and raising new questions concerning their evolution and biology (Desjardins et al., 2005, Espagne et al., 2004, Raoult et al., 2004).

Polydnaviruses (PDVs) are fascinating due to many aspects of their biology and to their unresolved but evidently complex evolution. Polydnaviridae are named after the unique segmented structure of their packaged double stranded DNA genome. Described in numerous parasitoid wasps of the Ichneumonidae (ichnovirus) and Braconidae (bracovirus) families (Fleming and Krell, 1993, Whitfield and Asgari, 2003), they have an unusual obligate mutualistic association with these eukaryotic organisms. The parasitoid wasps lay their eggs into another insect host, typically lepidopteran (Quicke, 1997). The parasitic eggs complete embryonic development, hatch, emerge from the parasitized lepidopteran, spin cocoons and emerge as adults (Fig. 1). Wasp larvae that develop within the tissues of the parasitized hosts must face the challenge such a habitat presents. In particular, insect hosts have the capacity to fight macroscopic intruders with an immune response consisting in surrounding the foreign body with a cellular sheath of hemocytes (Kanost et al., 1994, Lavine and Strand, 2003). To circumvent this immune response certain parasitic hymenoptera have developed an original strategy consisting in a mutualistic association with viruses of the Polydnaviridae family.

The PDV life cycle is highly unconventional compared to typical virus life cycles in that a replicative infection in which the virus infects a cell, replicates and produces viral progeny for transmission never occurs. Although PDVs exhibit all stages of virus replication (infection, replication, transmission to new host), these stages are distributed between the wasp and its parasitized lepidopteran host, replication being restricted to the wasp host (Drezen et al., 2003, Kroemer and Webb, 2004). In parasitic wasps, the PDV exists as a provirus integrated in the wasp chromosome and amplification of segments and particle production occurs only in the wasp ovaries (Albrecht et al., 1994, Belle et al., 2002, Drezen et al., 2003, Fleming and Summers, 1991, Gruber et al., 1996, Pasquier-Barre et al., 2002, Savary et al., 1999). Viral particles containing circular episomal forms of the integrated genome are co-injected with eggs into parasitized lepidoptera during oviposition. In the absence of replication in the lepidopteran host, the virus is maintained only by vertical transmission of the provirus.

PDV genomes consist of several double stranded DNA segments ranging from 4 to 41,573 Kb (Espagne et al., 2004, Kroemer and Webb, 2004, Webb and Strand, 2005). Viral gene expression in the lepidopteran hosts disrupts major host physiological systems (host cellular defences and host development) thereby ensuring wasp larvae survival and development (Lavine and Beckage, 1995, Strand and Pech, 1995, Webb, 1998). The virus is therefore essential for the wasp's parasitic success and the wasp ensures virus inheritance. This wasp–PDV association is one of the rare examples of mutualism between eukaryotes and viruses.

Until recently, little data was available on the virulence mechanisms or the origin and evolution of these viruses. One of the central and still unsolved questions in this field of research concerns the origin of these viral entities and how they have evolved. In particular, it is questioned whether PDVs are descendents of free-living viruses that are fixed in their mutualistic association or whether PDVs are originally a “wasp creation” with genes provided by the wasp genome but also from different mobile elements and viruses (Drezen et al., 2005). In this latter hypothesis PDVs are viewed as gene secretion systems leading to the delivery and expression of virulence genes into the parasitized host (Federici and Bigot, 2003).

The sequencing and annotation of the entire genome of the bracovirus of Cotesia congregata (CcBV) in our laboratory (Espagne et al., 2004) combined with available sequence data on the genomes of the bracovirus associated with Microplitis demolitor (MdBV) and an ichnovirus associated with Campoletis sonorensis (CsIV) and partial sequence data on other PDVs (Choi et al., 2005, Webb and Strand, 2005, Wyder et al., 2002) give us the opportunity to analyze shared features between PDV lineages in order to unveil evolutionary processes that have acted on these genomes.

Section snippets

Bracoviruses and ichnoviruses have an independent evolutionary story but the same constraints

Ichnovirus and bracovirus particles are produced from specialized cells located in a region of the ovary called the calyx. Transmission electron microscopy analyses revealed that these two PDV genera display morphological differences with each genus showing certain similarities with other known viruses infecting lepidoptera. The nucleocapsids of ichnoviruses show an ellipsoid shape and are of uniform size resembling those of ascoviruses, whereas the rod-shaped nucleocapsids of variable lengths

Bracovirus origin and evolution

Braconid wasp species harboring PDVs have been shown to form a monophyletic group, the microgastroid complex composed of seven subfamilies (Cheloninae, Dirrhoponae, Mendesellinae, Khoikhoiinae, Cardiochilinae, Miracinae and Microgastrinae) and comprising 17,500 species (Whitfield and Asgari, 2003) (Fig. 2). Parallel phylogenetic analyses of wasp sequences in the Cotesia genus based on mtDNA16S and viral sequences using the CrV1 gene (Cotesia rubeculaV1 gene) showed complete statistical

Ancestor virus, are you out there ?

If PDVs are viral derivatives they should share characteristics of other DNA viruses. In an attempt to determine the origin of these astonishing viruses we have searched for viral genes or remnants of viral genes in the genome of CcBV. Bracoviruses have been originally described as unusual baculoviruses and due to similarities in the morphology of the nucleocapsids it was proposed that the bracovirus ancestor was a baculovirus (Federici and Bigot, 2003, Krell and Stoltz, 1979).

The sequence of

Where do the PDV genes come from ?

A hallmark of the two PDV families is that most of the genes encode putative proteins possibly involved in host physiological modification. These genes are organized in genes families contributing to the large expansion of PDV genomes. For example, CsIV encodes four recognizable gene types, MdBV five, and CcBV encodes nine (Espagne et al., 2004, Pennacchio and Strand, 2005).

The question to date is how have the virulence genes described been acquired. The most parsimonious hypothesis is that the

Conclusion

Viruses usually acquire cellular genes to increase their fitness, PDVs acquire genes to increase wasp success. The new virulence factors acquired are thought to have allowed the extensive radiation of the wasp hosts. However, PDVs are not always associated with parasitoid wasps. Only two families use viruses, Ichneumonidae and Braconidae, while the Figitidae have another entity less well characterized called “virus-like particles” (Dupas et al., 1996). All the other families have to develop

Acknowledgements

The work concerning CcBV was supported in part by the Institut de Recherche Federatif “IFR 136Agents Transmissibles et Infectiologie” and by the CNRS “Groupement de Recherche” on mobile elements.

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