Movatterモバイル変換

[0]ホーム
URL:

Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
Thehttps:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

NIH NLM Logo
Log inShow account info
Access keysNCBI HomepageMyNCBI HomepageMain ContentMain Navigation
pubmed logo
Advanced Clipboard
User Guide

Full text links

Atypon full text link Atypon Free PMC article
Full text links

Actions

Share

.2015 Sep;89(17):8909-21.
doi: 10.1128/JVI.01001-15. Epub 2015 Jun 17.

Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if Not Identical, Viral Ancestors

Affiliations

Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if Not Identical, Viral Ancestors

Catherine Béliveau et al. J Virol.2015 Sep.

Abstract

Polydnaviruses form a group of unconventional double-stranded DNA (dsDNA) viruses transmitted by endoparasitic wasps during egg laying into caterpillar hosts, where viral gene expression is essential to immature wasp survival. A copy of the viral genome is present in wasp chromosomes, thus ensuring vertical transmission. Polydnaviruses comprise two taxa, Bracovirus and Ichnovirus, shown to have distinct viral ancestors whose genomes were "captured" by ancestral wasps. While evidence indicates that bracoviruses derive from a nudivirus ancestor, the identity of the ichnovirus progenitor remains unknown. In addition, ichnoviruses are found in two ichneumonid wasp subfamilies, Campopleginae and Banchinae, where they constitute morphologically and genomically different virus types. To address the question of whether these two ichnovirus subgroups have distinct ancestors, we used genomic, proteomic, and transcriptomic analyses to characterize particle proteins of the banchine Glypta fumiferanae ichnovirus and the genes encoding them. Several proteins were found to be homologous to those identified earlier for campoplegine ichnoviruses while the corresponding genes were located in clusters of the wasp genome similar to those observed previously in a campoplegine wasp. However, for the first time in a polydnavirus system, these clusters also revealed sequences encoding enzymes presumed to form the replicative machinery of the progenitor virus and observed to be overexpressed in the virogenic tissue. Homology searches pointed to nucleocytoplasmic large DNA viruses as the likely source of these genes. These data, along with an analysis of the chromosomal form of five viral genome segments, provide clear evidence for the relatedness of the banchine and campoplegine ichnovirus ancestors.

Importance: Recent work indicates that the two recognized polydnavirus taxa, Bracovirus and Ichnovirus, are derived from distinct viruses whose genomes integrated into the genomes of ancestral wasps. However, the identity of the ichnovirus ancestor is unknown, and questions remain regarding the possibility that the two described ichnovirus subgroups, banchine and campoplegine ichnoviruses, have distinct origins. Our study provides unequivocal evidence that these two ichnovirus types are derived from related viral progenitors. This suggests that morphological and genomic differences observed between the ichnovirus lineages, including features unique to banchine ichnovirus genome segments, result from evolutionary divergence either before or after their endogenization. Strikingly, analysis of selected wasp genomic regions revealed genes presumed to be part of the replicative machinery of the progenitor virus, shedding new light on the likely identity of this virus. Finally, these genes could well play a role in ichnovirus replication as they were overexpressed in the virogenic tissue.

Copyright © 2015, American Society for Microbiology. All Rights Reserved.

PubMed Disclaimer

Figures

FIG 1
FIG 1
Examples of campoplegine and banchine IV virions and nucleocapsids. Negatively stained nucleocapsids of Hyposoter exiguae IV (A) and Glypta fumiferanae IV (D) are shown. Diagrams show typical campoplegine (B) and banchine (C) IV virion structures; inner and outer membranes are shown in red and purple, respectively. Longitudinal (E and F) and cross (G, H) sections of representative Hyposoter fugitivus (Campopleginae) and A. simplicipes (Banchinae) virions, as seen in the lumen of the oviduct. Arrows indicate positively stained nucleocapsids; the arrow on the left side of panel F points to a particle budding from the apical surface of a calyx epithelial cell.
FIG 2
FIG 2
SDS-PAGE fractionation of GfIV virion proteins. Molecular mass markers (kDa) are shown on the left. The protein bands (1 to 6) that were excised from the gel for proteomics analysis are shown on the right; the remaining bands were not submitted to proteomics analysis.
FIG 3
FIG 3
Schematic representation of G. fumiferanae genomic regions that were sequenced and annotated following PCR screening of a G. fumiferanae fosmid library using primers targeting putative GfIV structural proteins identified through proteomic/EST library analysis. Each region shown here represents individual or overlapping fosmid clones. The top three panels show genomic regions that contain CDSs displaying homology to CDSs identified in H. didymator IVSPERs (17); these regions are designated Gf-IVSPER1, Gf-IVSPER2, and Gf-IVSPER3. Black arrows, replicative machinery genes from a putative NCLDV ancestor; pink and blue arrows, CDSs that display significant similarity to known genes identified in H. didymator IVSPERs (blue arrows designate CDSs that were targeted for PCR screening of the fosmid library); gray arrows, unknown proteins apparently unique to Gf-IVSPERs. The names of CDSs that have homologs in H. didymator contain an “L” (“like”) at the end (e.g., U16L is a homolog of H. didymator U16). A hyphen between two CDS names (e.g., U2-U7) indicates that both were found on a single transcript in the EST library. As a rule, only CDSs encoding ≥100 amino acids are shown here; however, smaller ones that had a match in the EST library or in H. didymator were also included. Among U proteins, some displayed significant similarity to one another: U10 and U39 (7E−56), U14 and U26 (9E−38), U29 and U31 (5E−57), U30 and U31 (2E−37), U32 and U33 (3E−29), and U23La and U23Lb (3E−54). The bottom panel shows the genomic region that contains the baculoviral p26-like CDS; none of the neighboring sequences display similarity to H. didymator IVSPER genes, and all appear to be insect genes: Gf-slp6 and Gf-uncharacterized have introns (3 and 2, respectively), and the closest homologs of the Ank repeats are from the wasp Nasonia vitripennis, with E values ranging from E−70 to E−154. Two p26-positive fosmid clones were selected for sequencing, and one of them contained a retrotransposon (red arrow) immediately downstream from the p26L CDS.
FIG 4
FIG 4
qPCR assessment of transcript abundance for a subset of genes, shown in Fig. 3, in G. fumiferanae ovarioles and lateral oviducts, which contain the calyx region where GfIV virions are produced. Values presented here are the means + standard deviations of four biological replicates, each containing tissue dissected from two to six individual female wasps of various ages. Absolute transcript amounts were assessed using the LRE analyzer (22–24) and normalized against values obtained for two housekeeping genes (β-tubulin 1 and EF1g; absolute transcript amounts for these two genes are shown at the right end of the histogram) using the geNorm algorithm (48). Five transcripts that correspond to proteins identified through proteomic analysis (Fig. 2) are labeled Prot 1 to Prot 5. CDSs U13L* and U17L* were found on a single transcript in the EST library. The inset shows transcript abundance for four of the five genes presumed to be part of the replicative machinery of the progenitor virus, shown on a different scale.
FIG 5
FIG 5
G sequences and direct repeats within chromosomal copies of GfIV genome segments and their proposed role in genome segment excision/circularization. (A) Three recognizable motifs (shaded in yellow) within an ∼250- to 280-bp region (G sequence) conserved among packaged GfIV and AsIV genome segments are shown; below are shown BV motifs resembling those found in GfIV and AsIV, including the DRJ motif, AGCTTT. (B) Alignment of the G sequences of the five GfIV genome segments examined here. A sample from AsIV is also included for comparison. Sequences shaded in yellow are those highlighted in panel A. (C) Schematic representation of the direct repeats (DRs) and associated G sequence found in proviral homologs of GfIV genome segments, along with a model for their involvement in segment excision/circularization. The DRs are represented by an arrow at each end of the integrated segment. Each DR contains a recombination region (indicated by an R and white box) whose position varies among segments (Table 3). The G sequence is represented by a black box. For genome segment excision, the DRs come in close proximity to allow recombination through the recombination regions; following recombination and excision, the circle contains a single, hybrid DR whose 3′ and 5′ ends come from the 5′ DR and the 3′ DR of the proviral genome segment, respectively. The exact role of the G sequence in this process, if any, is unclear at this stage. (D) Identification of the R region, using genome segment A7 as an example. The full 5′ and 3′ DRs are 313 and 312 bp long, respectively (Table 3); only their central portion is shown here. The R region was identified by aligning the two DRs and the homologous portion of the corresponding circle. The R region displayed perfect sequence identity among the three aligned sequences, while sequence variation was observed on either side of it (arrows). This sequence variation enabled identification of DR regions retained in the circle following recombination (the color scheme is the same as that shown in panel C).
FIG 6
FIG 6
Two hypothetical evolutionary scenarios to explain the homology between banchine and campoplegine IVSPERs (15). (A) Single IV ancestor. The dsDNA genome of a putative NCLDV integrated (red arrow) into the genome of an ancestor of banchine and campoplegine wasps; following genome integration, IVs of banchine and campoplegine wasps took different evolutionary courses, resulting in virions with distinct morphological and genomic features. To date, no PDV has been observed in wasps belonging to the intervening subfamilies; if this absence were to be confirmed, the present scenario would imply a loss of the capacity to produce PDV particles in these subfamilies although traces of IVSPERs could remain in their genomes. (B) Independent acquisition of closely related IV ancestors. Here, two separate integration events involving two very similar but distinct putative NCLDVs took place in ancestors of banchine and campoplegine wasps. Note that in this scenario, the integration event depicted on the right-hand side could have taken place in a more basal ancestor (dashed arrows).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Strand MR. 2010. Polydnaviruses, p 216–241. In Asgari S, Johnson KN (ed), Insect Virology Caister Academic Press, Norwich.
    1. Murphy N, Banks JC, Whitfield JB, Austin AD. 2008. Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol 47:378–395. doi:10.1016/j.ympev.2008.01.022. - DOI - PubMed
    1. Whitfield JB. 2002. Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 99:7508–7513. doi:10.1073/pnas.112067199. - DOI - PMC - PubMed
    1. Whitfield JB, O'Connor JM. 2012. Molecular systematics of wasp and polydnavirus genomes and their coevolution, p 89–97. In Beckage NE, Drezen J-M (ed), Parasitoid viruses: symbionts and pathogens. Elsevier, Inc., London, United Kingdom.
    1. Stoltz DB, Vinson SB, MacKinnon EA. 1976. Baculovirus-like particles in the reproductive tracts of female parasitoid wasps. Can J Microbiol 22:1013–1023. doi:10.1139/m76-148. - DOI - PubMed

Publication types

MeSH terms

Substances

Associated data

Related information

LinkOut - more resources

Full text links
Atypon full text link Atypon Free PMC article
Cite
Send To

NCBI Literature Resources

MeSHPMCBookshelfDisclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

[8]ページ先頭
©2009-2025 Movatter.jp