Satellite DNA Modulates Gene Expression in the Beetle Tribolium castaneum after Heat Stress
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{"title"=>"Satellite DNA Modulates Gene Expression in the Beetle Tribolium castaneum after Heat Stress", "type"=>"journal", "authors"=>[{"first_name"=>"Isidoro", "last_name"=>"Feliciello", "scopus_author_id"=>"6506469897"}, {"first_name"=>"Ivana", "last_name"=>"Akrap", "scopus_author_id"=>"55682827100"}, {"first_name"=>"Đurđica", "last_name"=>"Ugarković", "scopus_author_id"=>"7004156916"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-84940784753", "sgr"=>"84940784753", "doi"=>"10.1371/journal.pgen.1005466", "pui"=>"605889663", "pmid"=>"26275223", "issn"=>"15537404"}, "id"=>"36591c09-f736-39fd-b63e-be67b3451113", "abstract"=>"Non-coding repetitive DNAs have been proposed to perform a gene regulatory role, however for tandemly repeated satellite DNA no such role was defined until now. Here we provide the first evidence for a role of satellite DNA in the modulation of gene expression under specific environmental conditions. The major satellite DNA TCAST1 in the beetle Tribolium castaneum is preferentially located within pericentromeric heterochromatin but is also dispersed as single repeats or short arrays in the vicinity of protein-coding genes within euchromatin. Our results show enhanced suppression of activity of TCAST1-associated genes and slower recovery of their activity after long-term heat stress relative to the same genes without associated TCAST1 satellite DNA elements. The level of gene suppression is not influenced by the distance of TCAST1 elements from the associated genes up to 40 kb from the genes' transcription start sites, but it does depend on the copy number of TCAST1 repeats within an element, being stronger for the higher number of copies. The enhanced gene suppression correlates with the enrichment of the repressive histone marks H3K9me2/3 at dispersed TCAST1 elements and their flanking regions as well as with increased expression of TCAST1 satellite DNA. The results reveal transient, RNAi based heterochromatin formation at dispersed TCAST1 repeats and their proximal regions as a mechanism responsible for enhanced silencing of TCAST1-associated genes. Differences in the pattern of distribution of TCAST1 elements contribute to gene expression diversity among T. castaneum strains after long-term heat stress and might have an impact on adaptation to different environmental conditions.", "link"=>"http://www.mendeley.com/research/satellite-dna-modulates-gene-expression-beetle-tribolium-castaneum-after-heat-stress-2", "reader_count"=>31, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>19}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United States"=>2, "Uruguay"=>1, "Brazil"=>1, "United Kingdom"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2213230", "https://ndownloader.figshare.com/files/2213231", "https://ndownloader.figshare.com/files/2213232", "https://ndownloader.figshare.com/files/2213233", "https://ndownloader.figshare.com/files/2213234", "https://ndownloader.figshare.com/files/2213235"], "description"=>"<div><p>Non-coding repetitive DNAs have been proposed to perform a gene regulatory role, however for tandemly repeated satellite DNA no such role was defined until now. Here we provide the first evidence for a role of satellite DNA in the modulation of gene expression under specific environmental conditions. The major satellite DNA TCAST1 in the beetle <i>Tribolium castaneum</i> is preferentially located within pericentromeric heterochromatin but is also dispersed as single repeats or short arrays in the vicinity of protein-coding genes within euchromatin. Our results show enhanced suppression of activity of TCAST1-associated genes and slower recovery of their activity after long-term heat stress relative to the same genes without associated TCAST1 satellite DNA elements. The level of gene suppression is not influenced by the distance of TCAST1 elements from the associated genes up to 40 kb from the genes’ transcription start sites, but it does depend on the copy number of TCAST1 repeats within an element, being stronger for the higher number of copies. The enhanced gene suppression correlates with the enrichment of the repressive histone marks H3K9me2/3 at dispersed TCAST1 elements and their flanking regions as well as with increased expression of TCAST1 satellite DNA. The results reveal transient, RNAi based heterochromatin formation at dispersed TCAST1 repeats and their proximal regions as a mechanism responsible for enhanced silencing of TCAST1-associated genes. Differences in the pattern of distribution of TCAST1 elements contribute to gene expression diversity among <i>T</i>. <i>castaneum</i> strains after long-term heat stress and might have an impact on adaptation to different environmental conditions.</p></div>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511533, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1005466.s001", "https://dx.doi.org/10.1371/journal.pgen.1005466.s002", "https://dx.doi.org/10.1371/journal.pgen.1005466.s003", "https://dx.doi.org/10.1371/journal.pgen.1005466.s004", "https://dx.doi.org/10.1371/journal.pgen.1005466.s005", "https://dx.doi.org/10.1371/journal.pgen.1005466.s006"], "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Satellite_DNA_Modulates_Gene_Expression_in_the_Beetle_Tribolium_castaneum_after_Heat_Stress/1511533", "title"=>"Satellite DNA Modulates Gene Expression in the Beetle <i>Tribolium castaneum</i> after Heat Stress", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213226"], "description"=>"<p>Transcripts of TCAST1 satellite DNA, specifically induced after heat stress, are processed into siRNA which target via sequence identity dispersed TCAST1 elements associated with genes. By guiding chromatin modifiers TCAST1 siRNAs increase the level of silent heterochromatin marks at dispersed TCAST1 elements and proximal regions. Temporary assembly and spreading of heterochromatin suppresses activity of nearby genes. Genes associated with elements 2 and 21 are schematically shown: exons are represented by rectangles, elements TCAST1 by arrows and complex containing TCAST1 siRNAs by a circle.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511529, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g005", "stats"=>{"downloads"=>4, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_for_satellite_DNA_mediated_suppression_of_genes_/1511529", "title"=>"Model for satellite DNA- mediated suppression of genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213225"], "description"=>"<p>Elements 10, 11, 13, 14, 15, 23, 25, 27, 30, 39, 41, 42, 52, 57, 59 and 67 in population GA2 at standard conditions (blue) and at 1 hour of recovery after long-term heat stress (red). No represents normalized average No value for each gene. Columns show average of two different qRT-PCR experiments performed in triplicate and error bars represent standard deviations.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511528, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g004", "stats"=>{"downloads"=>1, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_genes_associated_with_nonpolymorphic_TCAST1_elements_after_heat_stress_/1511528", "title"=>"Expression of genes associated with nonpolymorphic TCAST1 elements after heat stress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213223"], "description"=>"<p><b>a)</b> Dynamics of expression of gene associated with element 21 in strain GA2 (red) and of the same gene without element 21 in strain 61 (blue) under standard conditions (no HS), immediately after long-term heat stress and at 30 min, 1 hr, 1.5 hrs and 3 hrs of recovery period. Expression of genes associated with: <b>b)</b> element 21 in strains with (GA2) and without (61, 55, GA1) insert, <b>c)</b> element 46 in strains with (GA2, GA1 and 55) and without (43) insert, <b>d)</b> element 2 in the form of trimer (GA2 strain), dimer (57 strain) and monomer (43 strain). Blue columns in <b>b</b>, <b>c</b> and <b>d</b> represent expression at standard conditions, while red columns represent expression at 1 hour of recovery after long-term heat stress. No represents normalized average No value for each gene. Columns show average of two different qRT-PCR experiments performed in triplicate and error bars represent standard deviations.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511526, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g003", "stats"=>{"downloads"=>0, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_genes_associated_with_polymorphic_TCAST1_elements_after_heat_stress_/1511526", "title"=>"Expression of genes associated with polymorphic TCAST1 elements after heat stress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213228"], "description"=>"<p>Types of dispersed elements with a number of TCAST1 monomers within each element, positions of TCAST1 elements relative to the genes and their distance from TSS are indicated. The P values were calculated using the unpaired t-test.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511531, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.t001", "stats"=>{"downloads"=>4, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_genes_NCBI_GeneIDs_associated_with_TCAST1_elements_and_their_level_of_suppression_after_long_term_heat_stress_in_different_strains_of_T_castaneum_/1511531", "title"=>"List of genes (NCBI-GeneIDs) associated with TCAST1 elements and their level of suppression after long-term heat stress in different strains of <i>T</i>. <i>castaneum</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213227"], "description"=>"<p>Level of H3K9me2 and H3K9me3 within region proximal to: <b>a)</b> element 46 in strain GA2 (blue) and within the same region in strain 43 (red) without element 46, <b>b</b>) element 21 in strain GA2 (blue) and within the same region in strain 61 (red) without element 21, <b>c)</b> element 2 in strain GA2 (blue) with element 2 in the form of trimer and within the same region in strain 43 (red) with element 2 as a monomer. H3K9me2/3 levels were measured by ChIP at standard conditions (no HS) and at 45 min and 1.5 hours of recovery period after long-term heat stress. Data show average of three independent replicate experiments and error bars indicate the standard error.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511530, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g006", "stats"=>{"downloads"=>0, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_H3K9me2_and_H3K9me3_levels_within_regions_flanking_dispersed_polymorphic_TCAST1_elements_/1511530", "title"=>"Analysis of H3K9me2 and H3K9me3 levels within regions flanking dispersed polymorphic TCAST1 elements.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213222"], "description"=>"<p><b>a)</b> Expression of gene associated with element 21 in strains with (GA2) and without (61, GA1) element 21. <b>b</b>) Expression of gene associated with element 46 in strains with (GA2, GA1 and 55) and without (43) element 46. <b>c</b>) Expression of gene associated with TCAST1 element 2 in strains where element 2 is in the form of trimer and monomer. No represents normalized average No value for each gene. Columns show average of two different qRT-PCR experiments performed in triplicate and error bars represent standard deviations.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511525, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g002", "stats"=>{"downloads"=>1, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_gene_expression_measured_by_qRT_PCR_under_standard_physiological_conditions_/1511525", "title"=>"Analysis of gene expression measured by qRT-PCR under standard physiological conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2213221"], "description"=>"<p>Blue and red arrows represent repeats belonging to subfamilies Tcast1a and Tcast2b, respectively, while flanking sequences are shown in black.</p>", "links"=>[], "tags"=>["gene expression diversity", "satellite DNA Modulates Gene Expression", "satellite DNA TCAST 1", "histone marks H 3K", "gene suppression correlates", "TCAST 1 satellite DNA", "TCAST 1 satellite DNA elements", "beetle Tribolium castaneum", "heat stress", "TCAST 1 elements", "satellite DNA", "TCAST 1"], "article_id"=>1511524, "categories"=>["Biological Sciences"], "users"=>["Isidoro Feliciello", "Ivana Akrap", "Đurđica Ugarković"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005466.g001", "stats"=>{"downloads"=>1, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_representation_of_dispersed_TCAST1_elements_2_12_46_and_21_in_T_castaneum_strains_/1511524", "title"=>"Schematic representation of dispersed TCAST1 elements 2, 12, 46 and 21 in <i>T</i>. <i>castaneum</i> strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-08-14 03:26:01"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"18", "full-text"=>"29", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"14", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
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  • {"unique-ip"=>"5", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
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  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"9"}
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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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