Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA
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{"title"=>"Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA", "type"=>"journal", "authors"=>[{"first_name"=>"Andrea D.", "last_name"=>"McCue", "scopus_author_id"=>"46062277300"}, {"first_name"=>"Saivageethi", "last_name"=>"Nuthikattu", "scopus_author_id"=>"55159792900"}, {"first_name"=>"Sarah H.", "last_name"=>"Reeder", "scopus_author_id"=>"55158243300"}, {"first_name"=>"R. Keith", "last_name"=>"Slotkin", "scopus_author_id"=>"16047951700"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"364547156", "sgr"=>"84859199684", "pmid"=>"22346759", "scopus"=>"2-s2.0-84859199684", "isbn"=>"1553-7404 (Electronic)\\n1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1002474", "issn"=>"15537390"}, "id"=>"9566f7fc-7600-3514-bd1d-c55406e3e1ed", "abstract"=>"The epigenetic activity of transposable elements (TEs) can influence the regulation of genes; though, this regulation is confined to the genes, promoters, and enhancers that neighbor the TE. This local cis regulation of genes therefore limits the influence of the TE's epigenetic regulation on the genome. TE activity is suppressed by small RNAs, which also inhibit viruses and regulate the expression of genes. The production of TE heterochromatin-associated endogenous small interfering RNAs (siRNAs) in the reference plant Arabidopsis thaliana is mechanistically distinct from gene-regulating small RNAs, such as microRNAs or trans-acting siRNAs (tasiRNAs). Previous research identified a TE small RNA that potentially regulates the UBP1b mRNA, which encodes an RNA-binding protein involved in stress granule formation. We demonstrate that this siRNA, siRNA854, is under the same trans-generational epigenetic control as the Athila family LTR retrotransposons from which it is produced. The epigenetic activation of Athila elements results in a shift in small RNA processing pathways, and new 21-22 nucleotide versions of Athila siRNAs are produced by protein components normally not responsible for processing TE siRNAs. This processing results in siRNA854's incorporation into ARGONAUTE1 protein complexes in a similar fashion to gene-regulating tasiRNAs. We have used reporter transgenes to demonstrate that the UPB1b 3' untranslated region directly responds to the epigenetic status of Athila TEs and the accumulation of siRNA854. The regulation of the UPB1b 3' untranslated region occurs both on the post-transcriptional and translational levels when Athila TEs are epigenetically activated, and this regulation results in the phenocopy of the ubp1b mutant stress-sensitive phenotype. This demonstrates that a TE's epigenetic activity can modulate the host organism's stress response. In addition, the ability of this TE siRNA to regulate a gene's expression in trans blurs the lines between TE and gene-regulating small RNAs.", "link"=>"http://www.mendeley.com/research/gene-expression-stress-response-mediated-epigenetic-regulation-transposable-element-small-rna-1", "reader_count"=>202, "reader_count_by_academic_status"=>{"Unspecified"=>8, "Professor > Associate Professor"=>16, "Researcher"=>43, "Student > Doctoral Student"=>16, "Student > Ph. D. Student"=>59, "Student > Postgraduate"=>3, "Student > Master"=>27, "Other"=>9, "Student > Bachelor"=>11, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>8, "Professor > Associate Professor"=>16, "Researcher"=>43, "Student > Doctoral Student"=>16, "Student > Ph. D. Student"=>59, "Student > Postgraduate"=>3, "Student > Master"=>27, "Other"=>9, "Student > Bachelor"=>11, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>12, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>17, "Agricultural and Biological Sciences"=>159, "Medicine and Dentistry"=>3, "Neuroscience"=>2, "Design"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Psychology"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>159}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>17}, "Unspecified"=>{"Unspecified"=>12}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>4, "United Kingdom"=>3, "Portugal"=>2, "Spain"=>1, "New Zealand"=>2, "Canada"=>1, "Czech Republic"=>1, "Austria"=>1, "Netherlands"=>1, "Brazil"=>3, "Bulgaria"=>1, "France"=>5, "Germany"=>2}, "group_count"=>14}

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  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349086/Figure_S1.eps", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349132/Figure_S2.eps", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349173/Figure_S3.eps", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349235/Figure_S4.tif", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349299/Figure_S5.eps", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349364/Figure_S6.tif", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349462/Figure_S7.eps", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/349501/Table_S1.xls"], "description"=>"<div><p>The epigenetic activity of transposable elements (TEs) can influence the regulation of genes; though, this regulation is confined to the genes, promoters, and enhancers that neighbor the TE. This local <em>cis</em> regulation of genes therefore limits the influence of the TE's epigenetic regulation on the genome. TE activity is suppressed by small RNAs, which also inhibit viruses and regulate the expression of genes. The production of TE heterochromatin-associated endogenous small interfering RNAs (siRNAs) in the reference plant <em>Arabidopsis thaliana</em> is mechanistically distinct from gene-regulating small RNAs, such as microRNAs or <em>trans</em>-acting siRNAs (tasiRNAs). Previous research identified a TE small RNA that potentially regulates the <em>UBP1b</em> mRNA, which encodes an RNA–binding protein involved in stress granule formation. We demonstrate that this siRNA, siRNA854, is under the same <em>trans</em>-generational epigenetic control as the <em>Athila</em> family LTR retrotransposons from which it is produced. The epigenetic activation of <em>Athila</em> elements results in a shift in small RNA processing pathways, and new 21–22 nucleotide versions of <em>Athila</em> siRNAs are produced by protein components normally not responsible for processing TE siRNAs. This processing results in siRNA854's incorporation into ARGONAUTE1 protein complexes in a similar fashion to gene-regulating tasiRNAs. We have used reporter transgenes to demonstrate that the <em>UPB1b</em> 3′ untranslated region directly responds to the epigenetic status of <em>Athila</em> TEs and the accumulation of siRNA854. The regulation of the <em>UPB1b</em> 3′ untranslated region occurs both on the post-transcriptional and translational levels when <em>Athila</em> TEs are epigenetically activated, and this regulation results in the phenocopy of the <em>ubp1b</em> mutant stress-sensitive phenotype. This demonstrates that a TE's epigenetic activity can modulate the host organism's stress response. In addition, the ability of this TE siRNA to regulate a gene's expression in <em>trans</em> blurs the lines between TE and gene-regulating small RNAs.</p> </div>", "links"=>[], "tags"=>["mediated", "epigenetic", "transposable", "rna"], "article_id"=>129035, "categories"=>["Molecular Biology", "Genetics", "Cell Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.s001", "http://dx.doi.org/10.1371/journal.pgen.1002474.s002", "http://dx.doi.org/10.1371/journal.pgen.1002474.s003", "http://dx.doi.org/10.1371/journal.pgen.1002474.s004", "http://dx.doi.org/10.1371/journal.pgen.1002474.s005", "http://dx.doi.org/10.1371/journal.pgen.1002474.s006", "http://dx.doi.org/10.1371/journal.pgen.1002474.s007", "http://dx.doi.org/10.1371/journal.pgen.1002474.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/Gene_Expression_and_Stress_Response_Mediated_by_the_Epigenetic_Regulation_of_a_Transposable_Element_Small_RNA/129035", "title"=>"Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-09 02:30:35"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683416/Figure_1.tif"], "description"=>"<p>(A) qRT-PCR of the <i>Athila6</i> retrotransposon, using primers specific for a location 3′ of the <i>gag/pol</i> protein coding region. Expression in wt Col inflorescences (infl) is activated in <i>ddm1</i> and <i>met1</i> mutants (left). Expression is also significantly activated (although to a lesser degree) in Col pollen compared to Col whole seedling, leaf and infl. <i>Athila6</i> transcript accumulation increases >80-fold in wt pollen compared to wt Col infl. <i>Athila6</i> transcript accumulation increases >24,000-fold in <i>ddm1</i> mutants compared to wt Col infl expression. (B) Northern blot detecting siRNA854 and the flanking 3′ region of <i>Athila6</i> (<i>Athila6</i> 3′) in <i>ddm1</i> and <i>met1</i> mutant infl. 21–22 nt <i>Athila6</i> siRNAs and siRNA854 only accumulate when the retrotransposon is transcriptionally activated. The DNA oligonucleotide probe used to detect siRNA854 is 21 nt in length, and is shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002474#pgen.1002474.s008\" target=\"_blank\">Table S1</a>. (C) qRT-PCR of the <i>Athila6</i> retrotransposon region 3′ of <i>gag/pol</i>, demonstrating that higher retrotransposon expression levels accumulate when <i>ddm1</i> is maintained as a homozygote over several generations. (D) Small RNA Northern blot detecting siRNA854 and the <i>Athila6</i> 3′ region. Increased levels of <i>Athila6</i> 21–22 nt siRNAs and siRNA854 correspond to samples with higher transcript levels. For Northern blots in parts B and D, microRNA161 (miR161) and a heterochromatic-region 24 nt siRNA (siRNA02) are shown as loading controls.</p>", "links"=>[], "tags"=>["retrotransposon", "leads", "accumulation", "nt"], "article_id"=>353897, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Expression_of_the_Athila6_retrotransposon_leads_to_accumulation_of_Athila_21_22_nt_siRNAs_including_siRNA854_/353897", "title"=>"Expression of the <i>Athila6</i> retrotransposon leads to accumulation of <i>Athila</i> 21–22 nt siRNAs, including siRNA854.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:04:57"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683501/Figure_2.tif"], "description"=>"<p>All parts correspond to Northern blots detecting siRNA854 and a flanking region of <i>Athila6</i> 3′ of the <i>gag/pol</i> protein coding region. (A) In wt Col, only the 24 nt versions of siRNA854 and <i>Athila6</i> siRNAs accumulate, while in <i>ddm1</i> seedling, leaf and infl, 21 nt and 22 nt versions of siRNA854 and flanking <i>Athila6</i> siRNAs accumulate. (B) Biogenesis pathway of the 24 nt <i>Athila6</i> siRNAs. <i>hen1</i>, <i>rdr2</i> and <i>nrpD1A</i> mutants fail to accumulate <i>Athila6</i> 24 nt siRNAs. (C) Biogenesis pathway of the 21–22 nt <i>Athila6</i> siRNAs that accumulate upon transcriptional activation. <i>ddm1</i> double mutants were generated for mutants involved in known siRNA production pathways. 21–22 nt <i>Athila6</i> 3′ siRNAs and siRNA854 fail to accumulate in <i>ddm1;rdr6</i> double mutants, while the 21 nt siRNAs shift to 22 nt in <i>ddm1;dcl4</i> double mutants. (D) Higher resolution Northern showing that the 21 nt version of siRNA854 and <i>Athila6</i> 3′ siRNAs are absent in <i>ddm1;dcl4</i> double mutants, while the 22 nt version is absent in <i>ddm1;dcl2</i> double mutants. (E) The accumulation of <i>Athila6</i> 3′ siRNAs in a <i>ddm1;ago1</i> segregating family produced from <i>ddm1</i> homozygote P1 plants. <i>AGO1</i> is necessary for the accumulation of 21–22 nt siRNA854 and <i>Athila6</i> 3′ siRNAs from both <i>ddm1</i> homozygotes and <i>ddm1</i> heterozygotes (<i>ddm1</i>/+). (F) 21–22 nt <i>Athila6</i> 3′ siRNAs and siRNA854 accumulate in <i>ddm1</i> heterozygotes produced by crossing wt to an individual homozygous for the recessive <i>ddm1-2</i> allele (Col x <i>ddm1</i>). <i>ddm1/+</i> heterozygous plants produced from parents that have not been homozygous for <i>ddm1</i> for at least 6 generations do not accumulate <i>Athila6</i> 21–22 nt siRNAs and are shown as a control (<i>ddm1/+</i> in segregating family).</p>", "links"=>[], "tags"=>["sirnas"], "article_id"=>353993, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Biogenesis_of_Athila6_siRNAs_and_siRNA854_/353993", "title"=>"Biogenesis of <i>Athila6</i> siRNAs and siRNA854.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:06:33"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683644/Figure_3.tif"], "description"=>"<p>(A) Plants homozygous for a transgene constitutively expressing the GUS reporter protein fused to the <i>UBP1b</i> 3′ UTR (35S:GUS-<i>UBP1b</i> 3′UTR) were transformed with an artificial microRNA (amiRNA) with the siRNA854 sequence (35S:amiRNA-854), or a second control sequence that does not target <i>UBP1b</i> (35S-amiRNA-control). GUS activity was monitored using a quantitative assay (left) and inflorescence staining (right). Plants expressing the siRNA854 sequence as an artificial microRNA show significantly reduced GUS levels. (B) Col and <i>ddm1</i> plants homozygous for a constitutively expressed GUS transgene (35S:GUS) or the same reporter transgene with the <i>UBP1b</i> 3′ UTR from part A. As in A, GUS activity was monitored using a quantitative assay (left) and plant staining (right). Wt Col plants show no differential regulation between the two transgene variations, while in the <i>ddm1</i> mutant background the GUS activity of the <i>UBP1b</i> 3′ UTR transgene is significantly less than the control 35S:GUS transgene. (C) A 35S:GUS-<i>UBP1b</i> 3′UTR transgene in the wt Col background was crossed to a <i>ddm1</i> homozygote, and the GUS activity was measured in the F1 plant. GUS activity of the same hemizygous transgene in the wt Col background is shown as a control. (D) RT-PCR of the same transgenic individuals from part B. The GUS activity differences observed in part B are not reflected in transgene transcript levels, demonstrating that this regulation is not due to post-transcriptional mRNA degradation. In A, B and C, the box plot whiskers represent the minimum and maximum of the dataset, the top and bottom of the box are the 75<sup>th</sup> and 25<sup>th</sup> percentile (respectively), the middle line is the median, and + is the mean. The number of individuals assayed (n) is shown in or near the box.</p>", "links"=>[], "tags"=>["nt", "sirna854", "negatively", "regulates", "transgene", "transcripts"], "article_id"=>354125, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Accumulation_of_21_22_nt_siRNA854_negatively_regulates_transgene_transcripts_with_the_UBP1b_3_UTR_/354125", "title"=>"Accumulation of 21–22 nt siRNA854 negatively regulates transgene transcripts with the <i>UBP1b</i> 3′ UTR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:08:45"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683769/Figure_4.tif"], "description"=>"<p>GFP transgenes with pollen-specific expression were used to assay the activity of endogenous siRNA854 in pollen. Background corrected GFP fluorescence levels are shown on the left, while representative pollen images are on the right. On each image, an asterisk marks non-fluorescent pollen grains that did not inherit the transgene from the hemizygous parent that were used for background correction. The addition of the <i>UBP1b</i> 3′UTR to a GFP transgene results in reduced fluorescence. Abrogation of the perfectly complementary base pairing in the predicted siRNA854 target sites of the <i>UBP1b</i> 3′UTR (MOD), or removal of these target sites altogether (DEL), alleviates this repression. The repression of the <i>UBP1b</i> 3′ UTR in pollen is lost in <i>rdr6</i> mutant plants. Box plot whiskers represent the 90<sup>th</sup> and 10<sup>th</sup> percentile of the dataset, the top and bottom of the box are the 75<sup>th</sup> and 25<sup>th</sup> percentile (respectively), the middle line is the median, and + is the mean. Number of pollen grains measured and the number of transgenic individuals they came from (in parentheses) is shown in or near the box. Scale bars = 10 µm.</p>", "links"=>[], "tags"=>["nt", "sirna854", "wt", "pollen", "regulates", "transgene", "transcripts"], "article_id"=>354246, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Accumulation_of_21_22_nt_siRNA854_in_wt_pollen_regulates_transgene_transcripts_with_the_UBP1b_3_UTR_/354246", "title"=>"Accumulation of 21–22 nt siRNA854 in wt pollen regulates transgene transcripts with the <i>UBP1b</i> 3′UTR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:10:46"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683857/Figure_5.tif"], "description"=>"<p>(A) qRT-PCR of <i>UBP1b</i> in inflorescence tissue and mature pollen. In inflorescence tissue, <i>UBP1b</i> transcript accumulation is not affected in <i>ddm1</i> mutants. In wt Col pollen, <i>UBP1b</i> expression significantly increases in <i>rdr6</i> mutants and in a pool of pollen that is segregating 1∶1 <i>ago1</i> mutant pollen (seg <i>ago1</i>). (B) qRT-PCR of FLAG-tagged <i>UBP1b</i> transgenes with and without the <i>UBP1b</i> 3′UTR and under control of their native promoters. In inflorescence tissue, the addition of the <i>UBP1b</i> 3′UTR results in increased transcript levels. In pollen, the <i>UBP1b</i> promoter is active, and addition of the <i>UBP1b</i> 3′UTR results in significantly decreased levels of mRNA. (C) qRT-PCR of small RNAs from AGO1-IP biological replicates demonstrating that in the plant body of <i>ddm1</i> mutants siRNA854 is enriched in AGO1 protein complexes, while it is not in wt Col. Relative enrichment values over 1.0 indicate AGO1-enrichment, whereas relative enrichment values under 1.0 indicate no enrichment. Relative enrichment was calculated based on amplification of the input sample for each IP. MiR161 and TAS3a-D8 are shown as positive controls while siRNA02 and siRNA1003 are 24 nt siRNA negative controls not bound by AGO1. qRT-PCR melting curves for siRNA854 amplification products from the AGO1-IP demonstrate that the non-enriched siRNA854 in wt Col is the larger 24 nt version (higher melting temperature), while the AGO1-enriched siRNA854 in <i>ddm1</i> is the 21–22 nt version (lower melting temperature).</p>", "links"=>[], "tags"=>["genetics and genomics", "plant biology", "molecular biology"], "article_id"=>354344, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Tissue_specific_regulation_of_UBP1b_by_siRNA854_/354344", "title"=>"Tissue-specific regulation of <i>UBP1b</i> by siRNA854.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:12:24"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/683960/Figure_6.tif"], "description"=>"<p>(A) Survival of plants grown under conditions of ionic and osmotic stress. Seeds were spotted on plates containing no stressor, increasing levels of NaCl or increasing levels of mannitol. After 11 days the number of surviving plants were counted. Wt plants of the Ws background are more sensitive to the stressors tested than wt Col. Compared to the corresponding wt Ws control, <i>ubp1b</i> mutants are more sensitive to both ionic (100 mM NaCl) and osmotic (300 mM mannitol) stresses. No <i>upb1b</i> seedlings survived under stress conditions of 150 mM NaCl or 400 mM mannitol. <i>ddm1</i> F6 generation plants are also sensitive to both ionic (150 mM NaCl) and osmotic (400 mM mannitol) stresses compared to wt Col. (B) Imaging of a constitutively expressed UBP1b protein fused to GFP (without its native 3′ UTR) in the root cell elongation zone. In unstressed wt Col seedling roots the UBP1b-GFP protein is localized to the nucleus, where specific peri-nuclear bright foci are observed. Growth of the same plants under stress conditions (due to etiolation) results in the relocalization of the UBP1b-GFP fusion protein from the nucleus into the cytosol. In unstressed <i>ddm1</i> mutants, the UBP1b-GFP protein accumulates in the cytosol, while occasional cells display distinct cytoplasmic foci (arrows). For each image, scale bars, magnification, and exposure time (in ms) are shown. (C) Measurements of fluorescence intensity were taken from the lines in B, and a ratio of nuclear to cytosolic fluorescence was calculated. The localization of UBP1b-GFP fluorescence is significantly different in unstressed wt Col compared to unstressed <i>ddm1</i>.</p>", "links"=>[], "tags"=>["localization"], "article_id"=>354453, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_UBP1b_protein_localization_and_stress_sensitivity_of_ddm1_/354453", "title"=>"UBP1b protein localization and stress sensitivity of <i>ddm1</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-09 01:14:13"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/684061/Table_1.xls"], "description"=>"A<p>Does not include tRNA, rRNA, snRNA, snoRNA reads.</p>B<p>Number of siRNA854 reads normalized per 1 million.</p>", "links"=>[], "tags"=>["21", "nt", "sirna854", "sbs", "rna"], "article_id"=>354547, "categories"=>["Molecular Biology", "Genetics", "Plant Biology"], "users"=>["Andrea D. McCue", "Saivageethi Nuthikattu", "Sarah H. Reeder", "R. Keith Slotkin"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002474.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Frequency_of_21_nt_siRNA854_in_SBS_small_RNA_libraries_/354547", "title"=>"Frequency of 21 nt siRNA854 in SBS small RNA libraries.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-09 01:15:47"}

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  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"23", "full-text"=>"15", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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  • {"unique-ip"=>"16", "full-text"=>"11", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"14", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"26", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
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  • {"unique-ip"=>"20", "full-text"=>"19", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[322, 550, 671, 773, 864, 955, 1048, 1135, 1223, 1308, 1387, 1465, 1534, 1602, 1673, 1744, 1813, 1885, 1955, 2026, 2093, 2160, 2228, 2290, 2349]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[319, 556, 679, 785, 881, 970, 1062, 1149, 1236, 1323, 1402, 1474, 1545, 1617, 1681, 1754, 1822, 1892, 1963, 2031, 2099, 2165, 2233, 2299, 2359]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[331, 557, 677, 777, 868, 960, 1050, 1136, 1223, 1307, 1390, 1466, 1536, 1603, 1673, 1741, 1814, 1889, 1954, 2028, 2096, 2164, 2233, 2305, 2362]}, {"subject_area"=>"/Biology and life sciences/Plant science", "average_usage"=>[329, 543, 667, 773, 865, 963, 1066, 1149, 1233, 1323, 1411, 1500, 1588, 1661, 1732, 1803, 1887, 1978, 2057, 2138, 2203, 2283, 2363, 2419, 2493]}]}
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