The Bracovirus Genome of the Parasitoid Wasp Cotesia congregata Is Amplified within 13 Replication Units, Including Sequences Not Packaged in the Particles

Abstract

bThe relationship between parasitoid wasps and polydnaviruses constitutes one of the few known mutualisms between viruses and eukaryotes. Viral particles are injected with the wasp eggs into parasitized larvae, and the viral genes thus introduced are used to manipulate lepidopteran host physiology. The genome packaged in the particles is composed of 35 double-stranded DNA (dsDNA) circles produced in wasp ovaries by amplification of viral sequences from proviral segments integrated in tandem arrays in the wasp genome. These segments and their flanking regions within the genome of the wasp Cotesia congregata were recently isolated, allowing extensive mapping of amplified sequences. The bracovirus DNAs packaged in the particles were found to be amplified within more than 12 replication units. Strikingly, the nudiviral cluster, the genes of which encode particle structural components, was also amplified, although not encapsidated. Amplification of bracoviral sequences was shown to involve successive head-to-head and tail-to-tail concatemers, which was not expected given the nudiviral origin of bracoviruses.

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

“…First viral DNA sequences have to be amplified within wasp cells in nuclear virus factories. Contrary to initial hypotheses [44,45], it is not the circles themselves that are amplified from proviral segment excision but larger molecules [46] that are replicated linearly [36]. In C. congregata, two segments were found to amplify together within the same molecule as well as sequences not packaged in the particles [46].…”

“…Other nudiviral genes are now dispersed in the C. congregata genome [10]. This scattering could be expected 100 myr after the ancestral nudivirus integration if there is no particular selective pressure to maintain these genes together [36]. The other part of the BV genome located within the wasp chromosomes is composed of proviral segments used to produce the multiple dsDNA circles packaged in the particles, which encodes virulence genes ensuring wasp larval development (figure 2).…”

“…The region is characterized by high gene density and contains intronless genes. This cluster encodes VP39 and 38K, the most abundant proteins in CiBV particles [28] and is amplified during CcBV virus particle production [36]. Other nudiviral genes are now dispersed in the C. congregata genome [10].…”

Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata : insights into the evolutionary dynamics of bracoviruses

“…Proviral segments were separated by spacer sequences more than 114 bp long that are not packaged in the particles [43], and surprisingly segments separated by short spacers (less than 500 bp) were often in opposite directions. This particular organization could derive from physical constraints as adjacent segments are amplified together in the same molecule [43] before their separation and circularization by recombination of the DRJs, which is likely coupled with viral DNA entry into the nucleocapsids. When spacers are short, opposite orientation of segments may permit capsid access to the amplified DNA molecule from opposite sides, whereas segments in the same orientation will induce capsid competition for space.…”

Microplitis demolitor Bracovirus Proviral Loci and Clustered Replication Genes Exhibit Distinct DNA Amplification Patterns during Replication

“…The first is DNA domains in the wasp genome called proviral segments, which contain several virulence genes plus noncoding sequence. Proviral segments are amplified and processed in calyx cells during replication to produce multiple circular dsDNAs of large aggregate size that are packaged into nucleocapsids (4)(5)(6)(7)(8)(9). Almost none of the genes on these segments are transcribed in wasps, although many or most are transcribed in parasitized hosts (10).…”