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The Pattern of R2 Retrotransposon Activity in Natural Populations of Drosophila simulans Reflects the Dynamic Nature of the rDNA Locus

Publication Date: February 20, 2009
Journal: PLOS Genetics
Authors: Jun Zhou & Thomas H. Eickbush
Volume: 5
Issue: 2
Pages: e1000386
DOI: https://dx.plos.org/10.1371/journal.pgen.1000386
Publisher URL: http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1000386
PubMed: http://www.ncbi.nlm.nih.gov/pubmed/19229317
PubMed Central: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2637433
Europe PMC: http://europepmc.org/abstract/MED/19229317
Web of Science: 000266320000026
Scopus: 61449167094
Mendeley: http://www.mendeley.com/research/pattern-r2-retrotransposon-activity-natural-populations-drosophila-simulans-reflects-dynamic-nature

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{"title"=>"The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus", "type"=>"journal", "authors"=>[{"first_name"=>"Jun", "last_name"=>"Zhou", "scopus_author_id"=>"56908579700"}, {"first_name"=>"Thomas H.", "last_name"=>"Eickbush", "scopus_author_id"=>"57197803006"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"61449167094", "pmid"=>"19229317", "scopus"=>"2-s2.0-61449167094", "pui"=>"354253470", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1000386"}, "id"=>"5ae0cbbe-5b47-30c2-8974-9c0b68f27ec6", "abstract"=>"The pattern and frequency of insertions that enable transposable elements to remain active in a population are poorly understood. The retrotransposable element R2 exclusively inserts into the 28S rRNA genes where it establishes long-term, stable relationships with its animal hosts. Previous studies with laboratory stocks of Drosophila simulans have suggested that control over R2 retrotransposition resides within the rDNA loci. In this report, we sampled 180 rDNA loci of animals collected from two natural populations of D. simulans. The two populations were found to have similar patterns of R2 activity. About half of the rDNA loci supported no or very low levels of R2 transcripts with no evidence of R2 retrotransposition. The remaining half of the rDNA loci had levels of R2 transcripts that varied in a continuous manner over almost a 100-fold range and did support new retrotransposition events. Structural analysis of the rDNA loci in 18 lines that spanned the range of R2 transcript levels in these populations revealed that R2 number and rDNA locus size varied 2-fold; however, R2 activity was not readily correlated with either of these parameters. Instead R2 activity was best correlated with the distribution of elements within the rDNA locus. Loci with no activity had larger contiguous blocks of rDNA units free of R2-insertions. These data suggest a model in which frequent recombination within the rDNA locus continually redistributes R2-inserted units resulting in changing levels of R2 activity within individual loci and persistent R2 activity within the population.", "link"=>"http://www.mendeley.com/research/pattern-r2-retrotransposon-activity-natural-populations-drosophila-simulans-reflects-dynamic-nature", "reader_count"=>37, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>34, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>2, "Japan"=>2, "Brazil"=>2, "Germany"=>1}, "group_count"=>3}

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{"files"=>["https://ndownloader.figshare.com/files/907657"], "description"=>"High molecular weight DNA was prepared from 0–23 hr old embryo nuclei, digested with NotI, which cleaves only in the R2 element (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g001\" target=\"_blank\">Figure 1</a>), and separated by pulsed-field electrophoresis. Six lines with high levels of R2 transcripts (High) and six lines with little or no R2 transcripts (Low) were used in the analysis. After transfer to nitrocellulose the DNA was probed with a segment from the 18S rRNA gene <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen.1000386-Eickbush3\" target=\"_blank\">[26]</a>. The DNA marker standard corresponds to a 50 kb ladder. Two samples (CS115 and A56) were analyzed on a separate gel under identical conditions. Also because of a lower DNA concentration in the nuclear plug, the CS22 lane represents a longer exposure of the DNA blot.", "links"=>[], "tags"=>["r2", "elements", "rdna"], "article_id"=>578112, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g008", "stats"=>{"downloads"=>3, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_R2_elements_in_the_rDNA_locus_/578112", "title"=>"Distribution of R2 elements in the rDNA locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:48:30"}
{"files"=>["https://ndownloader.figshare.com/files/907452"], "description"=>"The 18 iso-rDNA lines described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g003\" target=\"_blank\">Figures 3</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g004\" target=\"_blank\">4</a> were assayed for R2 retrotransposition activity after eight generations. The R2 5′ truncation profiles of 16 males from the eighth generation were compared to the R2 profile from the original male used to establish each line. Because R2 deletions are also associated with R2 activity <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen.1000386-Zhang3\" target=\"_blank\">[25]</a> loss of pre-existing insertions were also classified as R2 events. Because multiple R2 elements can be eliminated by a single deletion, all losses of R2 copies were scored as single events regardless of the number of R2 elements involved. For each line the total number of R2 events in all eighth generation males was plotted versus the R2 transcript level of that line.", "links"=>[], "tags"=>["r2", "transcript", "levels"], "article_id"=>577911, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_between_R2_transcript_levels_and_the_rate_of_R2_retrotransposition_/577911", "title"=>"Correlation between R2 transcript levels and the rate of R2 retrotransposition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:47:17"}
{"files"=>["https://ndownloader.figshare.com/files/907318"], "description"=>"The 3,600 nt full-length R2 transcript detected on RNA blots of adult female RNA (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g002\" target=\"_blank\">Figure 2</a>) were quantified on Phosphorimager scan and ImageQuant software. To control for RNA loading and possible degradation the R2 signal was standardized to the alcohol dehydrogenase signal from the same blot. RNA from line58, an active laboratory stock, was also present on every RNA blot as a standard to enable comparisons between blots. The 18 lines selected for further analysis to monitor R2 retrotranspositions and to determine the compositions of their rDNA loci are indicated with asterisks and labeled.", "links"=>[], "tags"=>["transcript", "levels", "180", "iso-rdna", "lines", "derived", "populations", "san", "diego"], "article_id"=>577767, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R2_transcript_levels_of_180_iso_rDNA_lines_derived_from_populations_in_San_Diego_and_Atlanta_/577767", "title"=>"R2 transcript levels of 180 iso-rDNA lines derived from populations in San Diego and Atlanta.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:46:29"}
{"files"=>["https://ndownloader.figshare.com/files/907735"], "description"=>"FL, full-length R2 copies; 5′ Trun, 5′ truncated R2 copies; Un, uninserted rDNA units; R1, R1-inserted units; R2, R2-inserted units.*Values include both single and R1+R2 (double) inserted units.", "links"=>[], "tags"=>["elements", "locus", "18"], "article_id"=>578199, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.t001", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R2_elements_and_locus_composition_in_18_D_simulans_lines_/578199", "title"=>"R2 elements and locus composition in 18 D. simulans lines.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 06:48:59"}
{"files"=>["https://ndownloader.figshare.com/files/907164"], "description"=>"The top panel shows the tandemly repeated rDNA transcription units with or without R1 and R2 insertions in the 28S rRNA gene. Every unit is composed of an 18S, 5.8S and 28S gene (black boxes) and transcribed spacer regions (white boxes). The R2 insertion site is located in the 28S rRNA gene 60 bp upstream of the R1 site. The bottom two diagrams show the R1 and R2 insertions in greater detail. The black boxes represent the 28S gene, the grey boxes represent the open reading frames of the R1 and R2 elements, and the white boxes represent the 5′ and 3′ untranslated regions of R1 and R2. ClaI, NotI, PstI and MspA1I restriction enzyme cleavage sites used in this report, and the locations of the hybridization probes used for the RNA blots (probe1) and genomic DNA blots (probes 2 and 3) are indicated. NotI cleaves only the R2 elements but not R1 or the rDNA units.", "links"=>[], "tags"=>["rdna", "locus", "site-specific", "retrotransposable", "r1"], "article_id"=>577616, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g001", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_rDNA_locus_of_D_simulans_and_the_site_specific_retrotransposable_elements_R1_and_R2_/577616", "title"=>"The rDNA locus of D. simulans and the site-specific retrotransposable elements, R1 and R2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:45:40"}
{"files"=>["https://ndownloader.figshare.com/files/907514"], "description"=>"(A) The relative R2 transcript level of each line is plotted versus the number of full-length, thus potentially active, R2 elements in that line. (B) The level of R2 transcripts in each line is plotted versus the fraction of the rDNA units inserted with R2 elements. The fraction of the rDNA units inserted with R2 was determined using genomic blots (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#s4\" target=\"_blank\">Materials and Methods</a>). (C) The level of R2 transcripts is plotted versus the size of the rDNA locus. The total number of units is determined by dividing the total number of R2 elements by the fraction of units inserted with R2 for each line.", "links"=>[], "tags"=>["r2", "transcript", "levels", "rdna"], "article_id"=>577970, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_of_R2_transcript_levels_to_the_size_and_composition_of_the_rDNA_locus_/577970", "title"=>"Relationship of R2 transcript levels to the size and composition of the rDNA locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:47:39"}
{"files"=>["https://ndownloader.figshare.com/files/907234"], "description"=>"(A) Representative RNA blot using RNA isolated from 18 iso-rDNA lines and, as a positive control (lane labeled, +), laboratory line 58, known to have high levels of R2 transcription and retrotranspositions <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen.1000386-Eickbush3\" target=\"_blank\">[26]</a>. The arrow indicates the 3,600 nt full-length R2 transcript. For each lane 10 µg of RNA isolated from adult females was fractionated on a 1% agarose gel, transferred to a nylon membrane, and probed with a 300 nt R2 5′ antisense RNA (probe1 in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g001\" target=\"_blank\">Figure 1</a>). (B) As a control for RNA quality and loading the R2 hybridization signal was allowed to decay and the blot was re-probed with a fragment of the alcohol dehydrogenase gene <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen.1000386-Eickbush3\" target=\"_blank\">[26]</a>. (C) Ethidium bromide staining of the RNAs used for the analyses in panels A and B.", "links"=>[], "tags"=>["transcripts", "levels", "iso-rdna", "lines", "derived", "atlanta", "san", "diego"], "article_id"=>577683, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g002", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R2_transcripts_levels_in_the_iso_rDNA_lines_derived_from_the_Atlanta_and_San_Diego_populations_/577683", "title"=>"R2 transcripts levels in the iso-rDNA lines derived from the Atlanta and San Diego populations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:46:04"}
{"files"=>["https://ndownloader.figshare.com/files/907385"], "description"=>"Diagramed at the top is a full-length R2 element with the location of the ORF and 5′ and 3′ untranslated regions indicated. Shown below the R2 diagram are the individual 5′ truncation profiles of each iso-rDNA line. Each horizontal line represents one of the D. simulans lines with the position of the vertical lines indicating the 5′ end point of a truncated R2 element in that line. Because all R2 insertions have an intact 3′ end of the element, each 5′ truncated R2 copy extends from the vertical line to the 3′ end of the R2 element. The collection of the 5′ truncated R2 copies differs for each line. Those 5′ truncations connected by dotted lines are shared between lines with those dotted lines indicated with an asterisk shared between the two populations. Full-length R2 elements in each line can also show small differences in length but are not shown. For each population the lines are arranged from the highest level of R2 transcript (top) to the lowest level of transcripts (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000386#pgen-1000386-g003\" target=\"_blank\">Figure 3</a>).", "links"=>[], "tags"=>["truncation", "profiles", "18"], "article_id"=>577847, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R2_5_truncation_profiles_of_18_representative_D_simulans_lines_/577847", "title"=>"R2 5′ truncation profiles of 18 representative D. simulans lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:46:55"}
{"files"=>["https://ndownloader.figshare.com/files/907590"], "description"=>"Bar heights indicate the total number of rDNA units in each line. The shading of the bar indicates the number of units that are uninserted or inserted with R1, R2 or both elements. Asterisks indicate the six lines with the highest levels of R2 transcripts.", "links"=>[], "tags"=>["rdna", "loci", "18", "iso-rdna", "lines", "was", "genomic", "blot"], "article_id"=>578045, "categories"=>["Evolutionary Biology", "Molecular Biology", "Genetics"], "users"=>["Jun Zhou", "Thomas H. Eickbush"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000386.g007", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Composition_of_the_rDNA_loci_of_18_iso_rDNA_lines_was_determined_by_genomic_blot_analysis_/578045", "title"=>"Composition of the rDNA loci of 18 iso-rDNA lines was determined by genomic blot analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:48:02"}

PMC Usage Stats 61317 Nov 13:45 UTC

PMC Usage Stats | Further Information

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Relative Metric 49550210 May 16:07 UTC

Relative Metric

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F1000Prime13 Nov 11:33 UTC

F1000Prime

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