Bracovirus gene products are highly divergent from insect proteins

Abstract

Recently, several polydnavirus (PDV) genomes have been completely sequenced. The dsDNA circles enclosed in virus particles and injected by wasps into caterpillars appear to mainly encode virulence factors potentially involved in altering host immunity and/or development, thereby allowing the survival of the parasitoid larvae within the host tissues. Parasitoid wasps generally inject virulence factors produced in the venom gland. As PDV genomes are inherited vertically by wasps through a proviral form, wasp virulence genes may have been transferred to this chromosomal form, leading to their incorporation into virus particles. Indeed, many gene products from Cotesia congregata bracovirus (CcBV), such as PTPs, IkappaB-like, and cystatins, contain protein domains conserved in metazoans. Surprisingly however, CcBV virulence gene products are not more closely related to insect proteins than to human proteins. To determine whether the distance between CcBV and insect proteins is a specific feature of BV proteins or simply reflects a general high divergence of parasitoid wasp products, which might be due to parasitic lifestyle, we have analyzed the sequences of wasp genes obtained from a cDNA library. Wasp sequences having a high similarity with Apis mellifera genes involved in a variety of biological functions could be identified indicating that the high level of divergence observed for BV products is a hallmark of these viral proteins. We discuss how this divergence might be explained in the context of the current hypotheses on the origin and evolution of wasp-bracovirus associations.

Origin and evolution of symbiotic viruses associated with parasitoid wasps

“…Indeed, a recent high through-put transcriptomic analysis confirmed the prediction that a majority of CcBV genes possess at least one intron and also revealed that they harbour arthropod transcription start sites and exhibit GC contents similar to wasp genes -in contrast to the nudivirus genes that do not contain introns and are slightly more AT-rich [21 ]. Despite these structural similarities, the formal demonstration of gene transfer between insects and BVs is in most cases difficult to obtain because of divergence of BV sequences with the original insect genes [37]. Ancient gene transfers (86 million years ago) occurring very early in the history of the BV-wasp associations are, for example, probably at the origin of the Ankyrin and PTP BV gene families, as no clear phylogenetic link can be established with corresponding insect genes [22,36,38] and as they are shared by nearly all BVs (except Chelonus inanitus BV).…”

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

“…Three of these new genes could be mapped to the integrated genome (CcBV_3.9, CcBV_20.6, and CcBV_28. 22), whereas the remaining four genes (bv3-4, bv5-9, bv7-8, and ep1-like7) belonged to known BV multigenic families but were not present in the integrated or packaged genome previously sequenced, suggesting that either certain segments were not perfectly assembled or a few proviral segments remain unidentified. Organization of CcBV genes expressed in immune tissues.…”

“…However, phylogenetic analyses suggesting viral genes could be of hymenopteran origin have so far been performed for only a few genes (20). Indeed, most genes appear to have diverged considerably in their sequence from insect genes (22). The encapsidated genomes of BVs from closely related wasps share many conserved genes (20), whereas distantly related wasps share very few genes (17).…”

Exogenous JH and ecdysteroid applications alter initiation of polydnaviral replication in an endoparasitoid wasp, Cotesia plutellae (Braconidae: Hymenoptera)

“…However, no PDV-possessing DNA polymerase has been identified since its gene is not likely to be encapsulated in viral particles (32). Current approaches for identifying PDV genomes using ovarian EST or analysis of BAC clones containing PDV segments clearly suggest that viral coat protein genes, which are not encapsulated, are actively expressed during viral replication (33,34). Viral DNA amplification during replication has not been observed for PDVs.…”