Widespread Genome Reorganization of an Obligate Virus Mutualist
Publication Date
September 18, 2014
Journal
PLOS Genetics
Authors
Gaelen R. Burke, Kimberly K. O. Walden, James B. Whitfield, Hugh M. Robertson, et al
Volume
10
Issue
9
Pages
e1004660
DOI
https://dx.plos.org/10.1371/journal.pgen.1004660
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1004660
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25232843
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4169385
Europe PMC
http://europepmc.org/abstract/MED/25232843
Web of Science
000343009600057
Scopus
84907588635
Mendeley
http://www.mendeley.com/research/widespread-genome-reorganization-obligate-virus-mutualist
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Mendeley | Further Information

{"title"=>"Widespread Genome Reorganization of an Obligate Virus Mutualist", "type"=>"journal", "authors"=>[{"first_name"=>"Gaelen R.", "last_name"=>"Burke", "scopus_author_id"=>"8577115800"}, {"first_name"=>"Kimberly K.O.", "last_name"=>"Walden", "scopus_author_id"=>"6701692502"}, {"first_name"=>"James B.", "last_name"=>"Whitfield", "scopus_author_id"=>"7202654691"}, {"first_name"=>"Hugh M.", "last_name"=>"Robertson", "scopus_author_id"=>"7203066280"}, {"first_name"=>"Michael R.", "last_name"=>"Strand", "scopus_author_id"=>"56920367300"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84907588635", "doi"=>"10.1371/journal.pgen.1004660", "pui"=>"600082856", "issn"=>"15537404", "pmid"=>"25232843", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "scopus"=>"2-s2.0-84907588635"}, "id"=>"7a1c492d-9bce-3fcc-a5ec-4e63cb342d24", "abstract"=>"The family Polydnaviridae is of interest because it provides the best example of viruses that have evolved a mutualistic association with their animal hosts. Polydnaviruses in the genus Bracovirus are strictly associated with parasitoid wasps in the family Braconidae, and evolved ∼100 million years ago from a nudivirus. Each wasp species relies on its associated bracovirus to parasitize hosts, while each bracovirus relies on its wasp for vertical transmission. Prior studies establish that bracovirus genomes consist of proviral segments and nudivirus-like replication genes, but how these components are organized in the genomes of wasps is unknown. Here, we sequenced the genome of the wasp Microplitis demolitor to characterize the proviral genome of M. demolitor bracovirus (MdBV). Unlike nudiviruses, bracoviruses produce virions that package multiple circular, double-stranded DNAs. DNA segments packaged into MdBV virions resided in eight dispersed loci in the M. demolitor genome. Each proviral segment was bounded by homologous motifs that guide processing to form mature viral DNAs. Rapid evolution of proviral segments obscured homology between other bracovirus-carrying wasps and MdBV. However, some domains flanking MdBV proviral loci were shared with other species. All MdBV genes previously identified to encode proteins required for replication were identified. Some of these genes resided in a multigene cluster but others, including subunits of the RNA polymerase that transcribes structural genes and integrases that process proviral segments, were widely dispersed in the M. demolitor genome. Overall, our results indicate that genome dispersal is a key feature in the evolution of bracoviruses into mutualists.", "link"=>"http://www.mendeley.com/research/widespread-genome-reorganization-obligate-virus-mutualist", "reader_count"=>35, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Ph. D. Student"=>13, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Ph. D. Student"=>13, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>29}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>29}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United States"=>1, "Brazil"=>1, "United Kingdom"=>1, "Spain"=>1, "India"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1680591"], "description"=>"<p>Five scaffolds containing nudivirus-like genes arranged from largest (1.6 Mb) to smallest (660 Kb) are shown in in gray. Named nudivirus-like genes (red) are separated by large stretches of DNA containing predicted <i>M. demolitor</i> genes (white). Wasp genes are depicted without indicating introns, exons, and untranslated regions.</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173502, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g006", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_nudivirus_like_genes_in_loosely_associated_clusters_in_the_M_demolitor_genome_/1173502", "title"=>"Distribution of nudivirus-like genes in loosely associated clusters in the <i>M. demolitor</i> genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680588"], "description"=>"<p>Alignment of HIM sequences with similarity for each site colored in shades of blue. Maximum likelihood analysis shows that three segment groups contain HIMs that form monophyletic groups (segments N and J; segments P, K1 and K; segments A and B) but other relationships could not be resolved.</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173499, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g003", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relatedness_of_Host_Integration_Motif_HIM_sequences_for_all_MdBV_proviral_segments_/1173499", "title"=>"Relatedness of Host Integration Motif (HIM) sequences for all MdBV proviral segments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680590"], "description"=>"<p>The <i>M. demolitor</i> nudivirus-like gene cluster is indicated in the lower portion of the figure by the two white boxes, while flanking domains containing predicted <i>M. demolitor</i> genes are indicated by the gray background. Regions of synteny between the <i>M. demolitor</i> nudivirus-like gene cluster and <i>C. congregata</i> nudivirus-like cluster are indicated by light blue. Black regions in gene models represent UTRs, black lines indicate introns, while red and white regions represent exons for nudivirus-like genes and wasp genes respectively. Scale bar indicates the size of these clusters in kilobase pairs (Kbp). Accession numbers are FM212911 for the <i>C. congregata</i> nudivirus-like cluster, and KK043480 for the <i>M. demolitor</i> cluster.</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173501, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g005", "stats"=>{"downloads"=>0, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_nudivirus_like_gene_cluster_in_the_genome_of_M_demolitor_shares_features_with_the_partial_nudivirus_like_gene_cluster_from_C_congregata_/1173501", "title"=>"The nudivirus-like gene cluster in the genome of <i>M. demolitor</i> shares features with the partial nudivirus-like gene cluster from <i>C. congregata</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680589"], "description"=>"<p>(A) The area surrounding segments N and J in <i>M. demolitor</i> Locus 3 is homologous to the regions surrounding segment 25 in Locus 5 of <i>G. flavicoxis</i> and <i>G. indiensis</i> and segment 1 in Locus 5 of <i>C. congregata.</i><i>M. demolitor</i> loci are oriented to match the orientation of sequence scaffolds and similarity between flanking regions reported in prior studies. Although the genes in the proviral segments themselves are usually not recognizably homologous (black background with genes in white), the regions flanking these proviral segments (gray background with genes in white) are conserved as indicated by regions of synteny shaded in light blue. To the right of the figure is shown the phylogenetic relationships between these wasp species and estimated divergence times. (B) The downstream region flanking segment P in <i>M. demolitor</i> Locus 1 is similar to the region between Locus 1 and 2 in <i>G. flavicoxis, G. indiensis, C. congregata</i> and <i>C. sesamiae Kitale</i>. Genes and segments are depicted as in (A) except for <i>odv-e66-like1</i> homologs are indicated in red in the <i>Glyptapanteles</i> and <i>Cotesia</i> genomes. Although the <i>odv-e66</i> homologs are located in an area of synteny, no <i>odv-e66</i> homologs exist in this region for <i>M. demolitor</i>. Accession numbers for sequences are MdL3 (KK043340), GiL5 (EF710656), GfL5 (EF710650), CcL5 (HF586476), MdL1 (KK044729), GfL1 (EF710644), GiL1 (EF710657), GiL2 (AC191960), CcL2 (HF586473), CcL1 (HF586472), CsL2 (EF710635), CsL1 (EF710629).</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173500, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g004", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_genomic_regions_flanking_proviral_segments_are_conserved_among_BV_carrying_wasps_/1173500", "title"=>"Two genomic regions flanking proviral segments are conserved among BV-carrying wasps.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680586"], "description"=>"<p>(A) Alignment of 200 nucleotides (nt) surrounding the 5′ WIM site of each segment with similarity for each site colored in shades of blue. Red box highlights the tetramer AGCT. 31 nt are conserved in each proviral segment following the AGCT motif (red box), while the 5′ flanking region upstream of this motif is AT rich and not well conserved. (B) Alignment of 200 nt surrounding the 3′ WIM site for proviral segments shows that the flanking region preceding the WIM site is AT rich but not conserved, whereas the first 100 nt of each proviral segment downstream of the WIM site shows high conservation. Maximum likelihood analyses indicated that the relationships between segments for the WIM sites (A) and 3′ flanking regions (B) cannot be resolved.</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173497, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wasp_Integration_Motifs_WIMs_for_all_MdBV_proviral_segments_/1173497", "title"=>"Wasp Integration Motifs (WIMs) for all MdBV proviral segments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680609", "https://ndownloader.figshare.com/files/1680610", "https://ndownloader.figshare.com/files/1680612", "https://ndownloader.figshare.com/files/1680613", "https://ndownloader.figshare.com/files/1680614", "https://ndownloader.figshare.com/files/1680615", "https://ndownloader.figshare.com/files/1680616"], "description"=>"<div><p>The family Polydnaviridae is of interest because it provides the best example of viruses that have evolved a mutualistic association with their animal hosts. Polydnaviruses in the genus <i>Bracovirus</i> are strictly associated with parasitoid wasps in the family Braconidae, and evolved ∼100 million years ago from a nudivirus. Each wasp species relies on its associated bracovirus to parasitize hosts, while each bracovirus relies on its wasp for vertical transmission. Prior studies establish that bracovirus genomes consist of proviral segments and nudivirus-like replication genes, but how these components are organized in the genomes of wasps is unknown. Here, we sequenced the genome of the wasp <i>Microplitis demolitor</i> to characterize the proviral genome of <i>M. demolitor</i> bracovirus (MdBV). Unlike nudiviruses, bracoviruses produce virions that package multiple circular, double-stranded DNAs. DNA segments packaged into MdBV virions resided in eight dispersed loci in the <i>M. demolitor</i> genome. Each proviral segment was bounded by homologous motifs that guide processing to form mature viral DNAs. Rapid evolution of proviral segments obscured homology between other bracovirus-carrying wasps and MdBV. However, some domains flanking MdBV proviral loci were shared with other species. All MdBV genes previously identified to encode proteins required for replication were identified. Some of these genes resided in a multigene cluster but others, including subunits of the RNA polymerase that transcribes structural genes and integrases that process proviral segments, were widely dispersed in the <i>M. demolitor</i> genome. Overall, our results indicate that genome dispersal is a key feature in the evolution of bracoviruses into mutualists.</p></div>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173514, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004660.s001", "https://dx.doi.org/10.1371/journal.pgen.1004660.s002", "https://dx.doi.org/10.1371/journal.pgen.1004660.s003", "https://dx.doi.org/10.1371/journal.pgen.1004660.s004", "https://dx.doi.org/10.1371/journal.pgen.1004660.s005", "https://dx.doi.org/10.1371/journal.pgen.1004660.s006", "https://dx.doi.org/10.1371/journal.pgen.1004660.s007"], "stats"=>{"downloads"=>15, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Widespread_Genome_Reorganization_of_an_Obligate_Virus_Mutualist_/1173514", "title"=>"Widespread Genome Reorganization of an Obligate Virus Mutualist", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-09-18 02:56:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1680585"], "description"=>"<p>The upper part of the figure presents the eight proviral loci identified (L1–L8) and the corresponding <i>M. demolitor</i> genome scaffolds where they are located. Only the portion of the scaffold where the proviral locus resides is shown. For each locus, the upper scale bar in kilobases (k) names the scaffold(s). Below the scale bar, colored bars indicate the segments identified by deep sequencing DNA from MdBV virions (Encapsidated segments) and their corresponding orientation and location in a given locus as a proviral segment in the <i>M. demolitor</i> genome. Average coverage in thousands of reads is indicated above each segment in brackets, while below each segment is shown read coverage per nucleotide relative to the scale indicated to the right of the graph. Gaps in read coverage indicate regions flanking individual proviral segments that are not amplified, excised and packaged into virions. The gap seen in segment S (L6) is due to a region of N's in the reference sequence. Below each MdBV proviral segment is shown predicted genes in forward (black) and reverse (white) orientation. Individual introns, exons and untranslated regions are not shown. The lower part of the figure shows each scaffold containing MdBV proviral loci in their entirety. Scaffolds are drawn to scale and organized from largest (L3) to smallest (L5). Scale bar is in megabases (M).</p>", "links"=>[], "tags"=>["MdBV proviral loci", "process proviral segments", "wasp Microplitis demolitor", "gene", "bracoviru", "dna", "rna", "proviral segments", "demolitor genome", "Widespread Genome Reorganization", "Obligate Virus Mutualist"], "article_id"=>1173496, "categories"=>["Biological Sciences"], "users"=>["Gaelen R. Burke", "Kimberly K. O. Walden", "James B. Whitfield", "Hugh M. Robertson", "Michael R. Strand"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004660.g001", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_organization_of_MdBV_proviral_segment_loci_/1173496", "title"=>"Genomic organization of MdBV proviral segment loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-18 02:56:26"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
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  • {"unique-ip"=>"16", "full-text"=>"13", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"14", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}

Relative Metric

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