PDV genomics reveal signatures of mutualist and parasitic lifestyles

Since these early observations several potential virulence genes have been characterized through likely produced by duplications of segments of the viral genome and tandem duplications of an initial copy (Friedman and Hughes, 2006; C. Serbielle et al., unpublished results). In CcBV, for example, almost half of the genes are organized in gene families (Dupuy et al., 2006), including the protein tyrosine phosphatase (PTPs; 27 genes), cactus/ inhibitory kB (IKB)-like (six genes), cystatin (three genes), and cysteine-motif (cysteine-rich protein (CRP); four genes) gene families. In addition, several bracovirus gene families encode conserved proteins that show no similarities to entries in the sequence databases. Few of these factors have been studied due to the difficulty of predicting and thus assessing their possible roles, but they are likely to represent new potential functions.

Strikingly, few PDV genes share significant similarities with genes from other viruses. The paucity of 'virus-like' genes may be explained by the fact that the virus does not replicate in the host tissues (Wyder et al., 2003). Therefore the genes involved in the production of calyx-fluid virus particles are not required to be present on the DNA circles themselves, and might reside permanently in the wasp genome, as shown for a gene coding a structural protein of CsIV particles (Deng et al., 2000). Recently, we have identified the viral machinery producing bracovirus particles and confirmed that none of the genes involved are encoded in the DNA of the particles (Bezier et al, 2009). Thus most of the genes delivered by the particles appear to be exclusively devoted to the production of factors involved in the manipulation of lepidopteran physiology (Dupuy et al, 2006).

9.2.3 Origin of PDVs

Important progress has been made recently towards the understanding of the origin of PDVs and their relationship with other viruses. Detailed phylogen-etic studies have shown that bracovirus-associated wasps form a monophyletic group: the microgas-troid complex (Whitfield, 2002). This finding led to the hypothesis that all current associations involving bracoviruses originate from a unique integration event of a viral genome as a provirus in a chromosome of the ancestral braconid wasp. The vertically transmitted viral DNA would then have been maintained because of its contribution to successful parasitism. Subsequently, viral DNA encapsidated in the PDV particles has presumably evolved differently depending on the wasp lineage, thus contributing to the diversification of the microgastroid complex, which now comprises at least 17 500 species (Whitfield, 2002). It has been estimated from fossils preserved in amber that the ancestral wasp lived during the Cretaceous period approximately 100 million years ago (Murphy et al., 2008). Recently, the use of transcriptomic and prote-omic approaches to identify viral structural genes expressed in wasp ovaries offered us the opportunity to reveal that the virus ancestor was most probably a nudivirus (nudiviruses constitute a sister group of baculoviruses) (Bezier et al, 2009). Indeed, using these approaches we characterized the machinery producing CcBV and CiBV particles and showed that the genes involved are related to those of nudiviruses. Different subunits of the nudiviral RNA polymerase are expressed in wasp ovaries and about one-third of CiBV particle components have retained similarities with nudiviral proteins (B. Lanzrein, personal communication). The same approach did not allow the characterization of virus-related genes producing ichnovirus particles from Hyposoter dydimator ichnovirus (HdIV), indicating that the ancestor of ichnoviruses, if it ever existed, was not a nudivirus nor any other virus characterized to date. The picture has become even more complex with the recent characterization of viruses associated with wasps from the subfamily of Banchinae, which are proposed to form a third group. These viruses associated with ichneumonid wasps differ in morphology from ichnoviruses and contain PTPs, which so far have only been identified in bracoviruses (Lapointe et al, 2007). These viruses are therefore likely to originate from a third ancestral event of wasp-virus association indicating that the domestication of viruses was selected several times during the evolution of parasitoid wasps. The association with viruses allowing gene transfer might have been selected repeatedly because it allows the production of a larger set of factors at a lower physiological cost for the wasp compared to the synthesis of proteins directly by the ovaries or the venom gland. This larger arsenal could also limit the selection of host resistance.

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