Research ArticleLIFE SCIENCES

Recurrent DNA virus domestication leading to different parasite virulence strategies

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Science Advances  27 Nov 2015:
Vol. 1, no. 10, e1501150
DOI: 10.1126/sciadv.1501150
  • Fig. 1 VLP morphogenesis in V. canescens calyx cells.

    (A to E) Transmission electron micrographs of (A) calyx cells displaying hypertrophic nuclei (N) containing virogenic stroma (VS) and VLPs; (B) calyx cell nuclei with empty envelopes close to the VS; (C) envelopes filled with VS material giving rise to VLPs; (D) VLPs budding from the calyx cell membrane; (E) immunogold labeling of VS and VLPs in the nucleus with specific antibodies against VLP2 (left) and PIF-0 (right). (Insets) Larger magnifications of VLPs. CYT, cytoplasm; Mv, microvilli of the cytoplasmic membrane; OvL, oviduct lumen; Pm, plasma membrane.

  • Fig. 2 Organization, origin, and putative function of the nudiviral genes of the V. canescens genome.

    (A) Nudiviral genes (in red; named after their OrNV homologs) are grouped into six clusters flanked by regions containing conserved wasp genes (in blue). (B) Phylogenetic tree of insect large double-stranded DNA viruses obtained by maximum likelihood analysis with a concatenated multiple alignment for 37 genes showing that the nudiviruses captured by the V. canescens and braconid wasp lineages belonged to different clades. VcVLP, V. canescens VLP. (C) Genes common to nudiviruses and baculoviruses conserved in V. canescens (red) or wasps carrying bracoviruses (BV) (purple). The products of the helicase gene and of the genes mediating viral gene transcription are not incorporated into the particles (hatched motif). Note that V. canescens lacks capsid genes, consistent with the absence of DNA in the particles.

  • Fig. 3 Overview of the production, function, and origin of V. canescens VLPs.

    (A) VLPs consist of virulence proteins of wasp origin wrapped in nudiviral envelopes. VLPs are released into the oviduct lumen, where they become attached to the wasp egg. Once in the parasitized caterpillar host, VLPs confer immune protection to the egg by impairing capsule formation by the host immune cells. (B) Recurrent virus domestication during parasitic wasp evolution. Two virus genome integration events have occurred during the evolution of campoplegine wasps: the first involved a genome, making it possible to produce ichnoviruses (mediating gene transfer), and the second involved an alphanudivirus genome used for VLP production (mediating the delivery of virulence proteins), which has replaced the ichnovirus in V. canescens. A betanudivirus was independently acquired by a braconid wasp ancestor and gave rise to bracoviruses (DNA delivery).

  • Table 1 Nudiviral and virulence genes expressed in V. canescens ovaries and the presence of their products in VLPs.

    Nudiviral genes of unknown function are detailed in table S1. RPKM, number of Illumina reads per kilobase per million mapped reads. PSM, number of peptide spectrum matches.

    Protein putative functionGene nameTranscript
    abundance
    (RPKM)
    Peptide
    abundance
    (PSM)
    OrNV homologAccession
    number
    BLASTp e value
    Nudiviral genes encoding VLP components
    Envelope componentpif-0 (p74)12,90054P74 protein (OrNV_gp126)YP_0023214371.0 × 10−85
    pif-15,19628PIF-1 (OrNV_gp060)YP_0023213712.0 × 10−94
    pif-21,98034PIF-2 (OrNV_gp017)YP_0023213289.8 × 10−112
    pif-32,65512PIF-3 (OrNV_gp107)YP_0023214182.0 × 10−59
    pif-47,731519-kDa protein (OrNV_gp033)YP_0023213445.0 × 10−44
    pif-5-15275ODV-E56 (OrNV_gp115)YP_0023214261.0 × 10−34
    pif-5-286321ODV-E56 (OrNV_gp115)YP_0023214264.8 × 10−38
    pif-5-31,0489ODV-E56 (OrNV_gp115)YP_0023214261.6 × 10−29
    pif-63,0112Ac68-like (OrNV_gp072)YP_0023213834.0 × 10−40
    vp912,96623VP91 (OrNV_gp106)YP_0023214171.4 × 10−84
    p335,5535Ac92-like (OrNV_gp113)YP_0023214248.6 × 10−48
    Unknown15 other genes related to OrNV
    V. canescens genes encoding VLP components
    VirulencePHGPx VLP11,115134
    RhoGAP VLP223,134400
    Neprylisin VLP33,540138
    Nudiviral genes transcribed in VLP-producing tissue not encoding VLP components
    ReplicationHelicase27DNAHEL (OrNV_gp034)YP_0023213450.0
    TranscriptionRNA polymerase lef-4488LEF-4 (OrNV_gp042)YP_0023213532.8 × 10−92
    RNA polymerase lef-8125LEF-8 (OrNV_gp064)YP_0023213750.0
    RNA polymerase lef-9724LEF-9 (OrNV_gp096)YP_0023214070.0
    RNA polymerase p47916P47 (OrNV_gp020)YP_0023213311.6 × 10−97
    Initiation factor lef-5245LEF-5 (OrNV_gp052)YP_0023213635.5 × 10−18
    Envelope componentpif-5-42,286ODV-E56 (OrNV_gp115)YP_0023214269.1 × 10−22
    Ac81-1272Ac81-like protein (OrNV_gp004)YP_0023213152.0 × 10−34
    Ac81-21,777Ac81-like protein (OrNV_gp004)YP_0023213151.0 × 10−39
    Ac81-31,080Ac81-like protein (OrNV_gp004)YP_0023213159.3 × 10−34
    Unknown18 other genes related to OrNV

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/10/e1501150/DC1

    Fig. S1. Link between nudiviral genes and V. canescens VLPs.

    Fig. S2. Vestiges of the ichnovirus in the V. canescens genome.

    Table S1. Nudiviral and flanking wasp sequences identified in the V. canescens genome scaffolds.

    Table S2. Selected list of ichnovirus-like sequences identified in the V. canescens genome.

    Table S3. List of PCR and quantitative PCR primers used to amplify nudiviral genes and wasp housekeeping genes.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Link between nudiviral genes and V. canescens VLPs.
    • Fig. S2. Vestiges of the ichnovirus in the V. canescens genome.
    • Table S1. Nudiviral and flanking wasp sequences identified in the V. canescens
      genome scaffolds.
    • Table S2. Selected list of ichnovirus-like sequences identified in the V. canescens
      genome.
    • Table S3. List of PCR and quantitative PCR primers used to amplify nudiviral
      genes and wasp housekeeping genes.

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