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Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus.

Desjardins CA, Gundersen-Rindal DE, Hostetler JB, Tallon LJ, Fuester RW, Schatz MC, Pedroni MJ, Fadrosh DW, Haas BJ, Toms BS, Chen D, Nene V - BMC Microbiol. (2007)

Bottom Line: By analyzing sequence polymorphisms in the 8 GiBV viral segment sequences, we found evidence for widespread selection acting on both protein-coding and non-coding DNA.Contrary to current concepts of bracovirus proviral genome organization our results demonstrate that some but not all GiBV proviral segment sequences exist in a tandem array.We hypothesize that selection acting on GiBV proviral sequences maintains the genetic island-like nature of the cluster of proviral genome segments described herein.

View Article: PubMed Central - HTML - PubMed

Affiliation: The Institute for Genomic Research, J. Craig Venter Institute, Rockville, Maryland, USA. cdesjar3@mail.rochester.edu

ABSTRACT

Background: Bracoviruses (BVs), a group of double-stranded DNA viruses with segmented genomes, are mutualistic endosymbionts of parasitoid wasps. Virus particles are replication deficient and are produced only by female wasps from proviral sequences integrated into the wasp genome. Virus particles are injected along with eggs into caterpillar hosts, where viral gene expression facilitates parasitoid survival and therefore perpetuation of proviral DNA. Here we describe a 223 kbp region of Glyptapanteles indiensis genomic DNA which contains a part of the G. indiensis bracovirus (GiBV) proviral genome.

Results: Eighteen of ~24 GiBV viral segment sequences are encoded by 7 non-overlapping sets of BAC clones, revealing that some proviral segment sequences are separated by long stretches of intervening DNA. Two overlapping BACs, which contain a locus of 8 tandemly arrayed proviral segments flanked on either side by ~35 kbp of non-packaged DNA, were sequenced and annotated. Structural and compositional analyses of this cluster revealed it exhibits a G+C and nucleotide composition distinct from the flanking DNA. By analyzing sequence polymorphisms in the 8 GiBV viral segment sequences, we found evidence for widespread selection acting on both protein-coding and non-coding DNA. Comparative analysis of viral and proviral segment sequences revealed a sequence motif involved in the excision of proviral genome segments which is highly conserved in two other bracoviruses.

Conclusion: Contrary to current concepts of bracovirus proviral genome organization our results demonstrate that some but not all GiBV proviral segment sequences exist in a tandem array. Unexpectedly, non-coding DNA in the 8 proviral genome segments which typically occupies ~70% of BV viral genomes is under selection pressure suggesting it serves some function(s). We hypothesize that selection acting on GiBV proviral sequences maintains the genetic island-like nature of the cluster of proviral genome segments described herein. In contrast to large differences in the predicted gene composition of BV genomes, sequences that appear to mediate processes of viral segment formation, such as proviral segment excision and circularization, appear to be highly conserved, supporting the hypothesis of a single origin for BVs.

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Neighbor-joining clustering of the regions of proviral locus 1 based on relative dinucleotide frequencies. All proviral genome segments (1p-8p) group together, as do the regions outside the flanking repeats (I and IV). The scale represents the normalized Euclidean distance between regions. Regions < 500 bp (isg1–3, 5) and the flanking repeats (L1R1 and L1R2) were excluded from the analysis, as they have skewed dinucleotide frequencies.
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Figure 2: Neighbor-joining clustering of the regions of proviral locus 1 based on relative dinucleotide frequencies. All proviral genome segments (1p-8p) group together, as do the regions outside the flanking repeats (I and IV). The scale represents the normalized Euclidean distance between regions. Regions < 500 bp (isg1–3, 5) and the flanking repeats (L1R1 and L1R2) were excluded from the analysis, as they have skewed dinucleotide frequencies.

Mentions: A variety of nucleotide compositional differences exist between the flanking regions I-IV, inter-segmental regions, and proviral genome segments. The latter sequences and L1R1/L1R2 have the highest average G+C content (37%), followed by the flanking regions (32%) while the inter-segmental regions have the lowest G+C content (26%). The difference in G+C content between coding and non-coding DNA is greater in flanking regions I-IV (44% vs. 28%) than in proviral genome segment sequences (41% vs. 34%) (Table 2). Relative dinucleotide frequencies which correct for background G+C composition were calculated for each region > 500 bp in length, except L1R1 and L1R2 as tandemly repetitive sequences have highly biased dinucleotide frequencies. Neighbor-joining clustering of the distances derived from these data (Figure 2) revealed that all of the proviral genome segments cluster together and have a highly similar dinucleotide composition, which is distinct from flanking DNA. Regions I and IV clustered together and the most distantly from proviral genome segments, whereas regions II and III and the inter-segmental regions clustered between the proviral genome segments and regions I and IV.


Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus.

Desjardins CA, Gundersen-Rindal DE, Hostetler JB, Tallon LJ, Fuester RW, Schatz MC, Pedroni MJ, Fadrosh DW, Haas BJ, Toms BS, Chen D, Nene V - BMC Microbiol. (2007)

Neighbor-joining clustering of the regions of proviral locus 1 based on relative dinucleotide frequencies. All proviral genome segments (1p-8p) group together, as do the regions outside the flanking repeats (I and IV). The scale represents the normalized Euclidean distance between regions. Regions < 500 bp (isg1–3, 5) and the flanking repeats (L1R1 and L1R2) were excluded from the analysis, as they have skewed dinucleotide frequencies.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1919376&req=5

Figure 2: Neighbor-joining clustering of the regions of proviral locus 1 based on relative dinucleotide frequencies. All proviral genome segments (1p-8p) group together, as do the regions outside the flanking repeats (I and IV). The scale represents the normalized Euclidean distance between regions. Regions < 500 bp (isg1–3, 5) and the flanking repeats (L1R1 and L1R2) were excluded from the analysis, as they have skewed dinucleotide frequencies.
Mentions: A variety of nucleotide compositional differences exist between the flanking regions I-IV, inter-segmental regions, and proviral genome segments. The latter sequences and L1R1/L1R2 have the highest average G+C content (37%), followed by the flanking regions (32%) while the inter-segmental regions have the lowest G+C content (26%). The difference in G+C content between coding and non-coding DNA is greater in flanking regions I-IV (44% vs. 28%) than in proviral genome segment sequences (41% vs. 34%) (Table 2). Relative dinucleotide frequencies which correct for background G+C composition were calculated for each region > 500 bp in length, except L1R1 and L1R2 as tandemly repetitive sequences have highly biased dinucleotide frequencies. Neighbor-joining clustering of the distances derived from these data (Figure 2) revealed that all of the proviral genome segments cluster together and have a highly similar dinucleotide composition, which is distinct from flanking DNA. Regions I and IV clustered together and the most distantly from proviral genome segments, whereas regions II and III and the inter-segmental regions clustered between the proviral genome segments and regions I and IV.

Bottom Line: By analyzing sequence polymorphisms in the 8 GiBV viral segment sequences, we found evidence for widespread selection acting on both protein-coding and non-coding DNA.Contrary to current concepts of bracovirus proviral genome organization our results demonstrate that some but not all GiBV proviral segment sequences exist in a tandem array.We hypothesize that selection acting on GiBV proviral sequences maintains the genetic island-like nature of the cluster of proviral genome segments described herein.

View Article: PubMed Central - HTML - PubMed

Affiliation: The Institute for Genomic Research, J. Craig Venter Institute, Rockville, Maryland, USA. cdesjar3@mail.rochester.edu

ABSTRACT

Background: Bracoviruses (BVs), a group of double-stranded DNA viruses with segmented genomes, are mutualistic endosymbionts of parasitoid wasps. Virus particles are replication deficient and are produced only by female wasps from proviral sequences integrated into the wasp genome. Virus particles are injected along with eggs into caterpillar hosts, where viral gene expression facilitates parasitoid survival and therefore perpetuation of proviral DNA. Here we describe a 223 kbp region of Glyptapanteles indiensis genomic DNA which contains a part of the G. indiensis bracovirus (GiBV) proviral genome.

Results: Eighteen of ~24 GiBV viral segment sequences are encoded by 7 non-overlapping sets of BAC clones, revealing that some proviral segment sequences are separated by long stretches of intervening DNA. Two overlapping BACs, which contain a locus of 8 tandemly arrayed proviral segments flanked on either side by ~35 kbp of non-packaged DNA, were sequenced and annotated. Structural and compositional analyses of this cluster revealed it exhibits a G+C and nucleotide composition distinct from the flanking DNA. By analyzing sequence polymorphisms in the 8 GiBV viral segment sequences, we found evidence for widespread selection acting on both protein-coding and non-coding DNA. Comparative analysis of viral and proviral segment sequences revealed a sequence motif involved in the excision of proviral genome segments which is highly conserved in two other bracoviruses.

Conclusion: Contrary to current concepts of bracovirus proviral genome organization our results demonstrate that some but not all GiBV proviral segment sequences exist in a tandem array. Unexpectedly, non-coding DNA in the 8 proviral genome segments which typically occupies ~70% of BV viral genomes is under selection pressure suggesting it serves some function(s). We hypothesize that selection acting on GiBV proviral sequences maintains the genetic island-like nature of the cluster of proviral genome segments described herein. In contrast to large differences in the predicted gene composition of BV genomes, sequences that appear to mediate processes of viral segment formation, such as proviral segment excision and circularization, appear to be highly conserved, supporting the hypothesis of a single origin for BVs.

Show MeSH
Related in: MedlinePlus