Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in Neurospora
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{"title"=>"Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in Neurospora", "type"=>"journal", "authors"=>[{"first_name"=>"Cigdem", "last_name"=>"Sancar", "scopus_author_id"=>"26634157500"}, {"first_name"=>"Nati", "last_name"=>"Ha", "scopus_author_id"=>"55164138600"}, {"first_name"=>"Rüstem", "last_name"=>"Yilmaz", "scopus_author_id"=>"42662684300"}, {"first_name"=>"Rafael", "last_name"=>"Tesorero", "scopus_author_id"=>"35189606400"}, {"first_name"=>"Tamas", "last_name"=>"Fisher", "scopus_author_id"=>"7402051682"}, {"first_name"=>"Michael", "last_name"=>"Brunner", "scopus_author_id"=>"36096555700"}, {"first_name"=>"Gencer", "last_name"=>"Sancar", "scopus_author_id"=>"26634404100"}], "year"=>2015, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"25822411", "sgr"=>"84926296713", "doi"=>"10.1371/journal.pgen.1005105", "scopus"=>"2-s2.0-84926296713", "pui"=>"603513955", "issn"=>"15537404"}, "id"=>"502e0bfa-d5fa-3109-bf83-3902b5b2436c", "abstract"=>"Light is an important environmental cue that affects physiology and development of Neurospora crassa. The light-sensing transcription factor (TF) WCC, which consists of the GATA-family TFs WC1 and WC2, is required for light-dependent transcription. SUB1, another GATA-family TF, is not a photoreceptor but has also been implicated in light-inducible gene expression. To assess regulation and organization of the network of light-inducible genes, we analyzed the roles of WCC and SUB1 in light-induced transcription and nucleosome remodeling. We show that SUB1 co-regulates a fraction of light-inducible genes together with the WCC. WCC induces nucleosome eviction at its binding sites. Chromatin remodeling is facilitated by SUB1 but SUB1 cannot activate light-inducible genes in the absence of WCC. We identified FF7, a TF with a putative O-acetyl transferase domain, as an interaction partner of SUB1 and show their cooperation in regulation of a fraction of light-inducible and a much larger number of non light-inducible genes. Our data suggest that WCC acts as a general switch for light-induced chromatin remodeling and gene expression. SUB1 and FF7 synergistically determine the extent of light-induction of target genes in common with WCC but have in addition a role in transcription regulation beyond light-induced gene expression.", "link"=>"http://www.mendeley.com/research/combinatorial-control-light-induced-chromatin-remodeling-gene-activation-neurospora", "reader_count"=>18, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>9, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}}, "reader_count_by_country"=>{"Chile"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1995187"], "description"=>"<p><b>A</b>. Heat-maps showing the 189 light-inducible genes with significantly lower light-induced RNA levels in Δ<i>sub1</i> compared to <i>wt</i>. <b>B</b>. Quantification of light-induced RNA levels of <i>rds1</i> and <i>hyr1</i> by RT-PCR (± SEM, n = 4). 28s rRNA was used for normalization. <i>wt</i> RNA levels in dark were normalized to 1. <b>C</b>. ChIP-PCR analysis of SUB1 showing binding of SUB1 to the <i>rds1</i> (upper panel) and <i>hyr1</i> promoters (lower panel) determined by two-step FLAG-HIS ChIP. <i>wt</i><sub><i>9718</i></sub> was used as a control. 28s rDNA was used for normalization. SUB1 binding at t = 60 min was set to 1 (± SEM, n = 3). <b>D</b>. ChIP-PCR analysis of WC2 showing light-induced binding of the WCC to the <i>rds1</i> (upper panel) and <i>hyr1</i> promoters (lower panel) in <i>wt</i> and Δ<i>sub1</i> strains. 28s rDNA was used for normalization. WC2 ChIP at t = 60 min in <i>wt</i> was set to 1 (± SEM, n = 4).</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361036, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SUB1_is_required_for_efficient_recruitment_of_WCC_and_light_induction_of_a_subset_of_genes_/1361036", "title"=>"SUB1 is required for efficient recruitment of WCC and light-induction of a subset of genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995196"], "description"=>"<p><b>A-B</b>. Western blots showing co-immunoprecipitation (co-IP) of <b>(A)</b> SUB1 with FF7<sub>FLAG-HIS</sub> and <b>(B)</b> FF7<sub>FLAG-HIS</sub> with SUB1. FLAG antibody was used for FF7<sub>FLAG-HIS</sub> IP and α-SUB1 antibody was used for SUB1 IP. The asterisks (*) indicate cross-reactions of the FLAG antibody. <b>C</b>. FF7 binding motifs identified by MEME. The top 200 binding sites identified by FF7 ChIP-seq were used for the motif analysis. The upper motif is found in 117 / 200 binding sites whereas the lower motif is found in 36 / 200 binding sites. <b>D</b>. Occurrence of the major FF7 motif at FF7 binding sites. The grey area shows the occupancy of FF7 binding sites determined by ChIP-seq. The red line shows the occurrence of the FF7 binding motif “t/c AAGCG c/a”. <b>E</b>. Wig file showing MNase-WC2, SUB1 and FF7 ChIP-seq signals at the <i>rds1</i> promoter. Numbers on the ChIP-seq panels correspond the maximum coverage shown in the wig file. <b>F</b>. Venn-diagram showing the overlap between SUB1, WC2 and FF7 ChIP-seq signals. <b>G</b>. Heat-map showing light-inducible genes with significantly lower RNA levels in Δ<i>sub1</i> and in Δ<i>ff7</i> strains in comparison to <i>wt</i>. <b>H</b>. Wig file (left panel) showing the nucleosome position and occupancy at the <i>rds1</i> promoter in <i>wt</i> and Δ<i>ff7</i> strains in the dark and after light-exposure. The MNase-WC2 ChIP-seq (blue) is shown below the nucleosome signals. Numbers on the ChIP-seq panels show the maximum coverage shown in the wig file. ChIP-PCR analysis (right panel) of H2A occupancy at the binding sites of WCC and SUB1 at <i>rds1</i> promoter in the dark and 20 min after light-exposure (± SEM, n = 4). a<i>ctin</i> DNA was used for normalization. w<i>t</i> dark level was set to 1. <b>I</b>. Nucleosome occupancy at binding sites of WCC (n = 92) and in Δ<i>ff7</i> in dark (dotted lines) and 20 min after light-exposure (solid lines).</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361045, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g006", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_FF7_interacts_weakly_with_SUB1_and_co_regulates_light_inducible_and_non_light_inducible_genes_/1361045", "title"=>"FF7 interacts weakly with SUB1 and co-regulates light-inducible and non light-inducible genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995193"], "description"=>"<p><b>A</b>. Line graphs showing the averaged nucleosome occupancy in transcribed genes and promoters of all annotated <i>Neurospora</i> genes (n = 9733) in <i>wt</i>, Δ<i>sub1</i> and Δ<i>wc2</i> strains in dark (red) and 20 min (blue) after light-exposure of cultures. The center of the +1 nucleosome (nucleosome overlapping the annotated transcription start site) was used for alignment of sequence coverage of MNase-resistant fragments >100bp. <b>B</b>. Wig file showing the nucleosome position and occupancy at the <i>rds1</i> promoter in <i>wt</i>, Δ<i>sub1</i> and Δ<i>wc2</i> strains in the dark and after light-exposure. MNase-WC2 ChIP-seq (blue) is shown below the nucleosome signals. Numbers on the ChIP-seq panels show the maximum read coverage shown in the wig file. <b>C</b>. ChIP-PCR analysis showing H2A occupancy in the dark and 20 min after light exposure at the binding sites of WCC and SUB1 in the <i>rds1</i> promoter. ChIP was performed by immunoprecipitation with H2A antibody (± SEM, n = 4). a<i>ctin</i> gene was used for normalization. <i>wt</i> dark level was set to 1. <b>D</b>. Transcription-independent light-induced nucleosome eviction at WCC binding sites (BS). Four examples (wig files) of nucleosome position and occupancy at WCC BS in <i>wt</i>, Δ<i>sub1</i> and Δ<i>wc2</i> strains are shown. WCC binding (TAP-WC2 ChIP-seq) is shown above the nucleosome signals. The positions of GATC motifs are shown in the lower panels. Numbers on the ChIP-seq panels indicate the maximum nucleosome coverage shown in the Wig file. Regions used for ChIP-PCR analysis are indicated by black lines. <b>E</b>. ChIP-PCR analysis showing H2A occupancy in the regions shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005105#pgen.1005105.g004\" target=\"_blank\">Fig. 4D</a>. Occupancy of H2A was determined by immunoprecipitation with H2A antibody (± SEM, n = 4). a<i>ctin</i> gene was used for normalization. w<i>t</i> dark level was set to 1.</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361041, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g004", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Light_and_WCC_dependent_nucleosome_eviction_is_transcription_independent_/1361041", "title"=>"Light- and WCC-dependent nucleosome eviction is transcription independent.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995190"], "description"=>"<p><b>A</b>. Heat-map showing the light-induced WCC occupancy at 92 binding sites identified by both, MNase-WC2 ChIP-seq and TAP-WC2 ChIP-seq. 5 kb region covering the binding sites are shown. Left panel: WCC binding in the dark. Right panel: WCC binding 30 min after light-exposure. <b>B</b>. Occurrence of tandem GATC motifs with the indicated spacing at WCC binding sites. 300 bp DNA regions covering the peaks of 92 highly confident WCC binding sites were analyzed. The dashed line corresponds to the occurrence of tandem GATC motifs in a set of randomly chosen 300 bp regions. <b>C</b>. Potential light response elements (LREs) at WCC binding sites contain multiple GATC motifs. GATC motifs in WCC binding sites of the indicated genes are shown. <i>frq</i><sub><i>as</i></sub>: <i>frq</i> antisense [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005105#pgen.1005105.ref019\" target=\"_blank\">19</a>]. <i>vvd</i><sub><i>prox</i></sub> and <i>vvd</i><sub><i>dis</i></sub>: proximal and distal WCC binding sites in <i>vvd</i> promoter (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1005105#pgen.1005105.s008\" target=\"_blank\">S2 Table</a>). <b>D</b>. Distribution of tandem GATC motifs with < 30 bp spacing at WCC binding sites. The grey area represents the sequence coverage of the WCC ChIP (MNase-WC2 ChIP, 30 min) at the highly confident 92 WCC binding sites. The red line shows the occurrence of tandem GATC motifs. <b>E</b>. Heat-map showing the SUB1 occupancy at binding sites. Left panel: SUB1 binding in the dark. Right panel: SUB1 binding 30 min after light-exposure. <b>F</b>. SUB1 binding motifs identified by MEME are shown. The major sequence motif shown in the upper panel is found in 171 sites. The GTA-rich motifs shown in the lower left and right panels are present in 82 and 63 sites, respectively. <b>G</b>. Distribution of the major SUB1 binding motif (a/cGAT-x6-a/cTGc/t) at SUB1 binding sites. The grey area represents the sequence coverage of the SUB1 ChIP (SUB1 30 min) at 617 SUB1 binding sites. The red line shows the occurrence of the SUB1 binding motif.</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361039, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g002", "stats"=>{"downloads"=>0, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cistrome_analysis_of_WCC_and_SUB1_/1361039", "title"=>"Cistrome analysis of WCC and SUB1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995191"], "description"=>"<p><b>A</b>. Nucleosome occupancy at binding sites of WCC (n = 92) and in <i>wt</i> (red), Δ<i>sub1</i> (green) and Δ<i>wc2</i> (blue) strains in dark (dotted lines) and 20 min after light-exposure (solid lines). <b>B</b>. Nucleosome occupancy at binding sites of WCC for SUB1-dependent (upper panel) and SUB1-independent (lower panel) light induced nucleosome loss. <i>wt</i> (red) and Δ<i>sub1</i> (green) strains in dark (dotted lines) and 20 min after light-exposure (solid lines) are shown. <b>C</b>. Nucleosome occupancy at binding sites of SUB1 (n = 617) in <i>wt</i> (red), Δ<i>sub1</i> (green) and Δ<i>wc2</i> (blue) strains in dark (dotted lines) and 20 min after light-exposure (solid lines).</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361040, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Light_promotes_WCC_dependent_nucleosome_eviction_at_WCC_binding_sites_/1361040", "title"=>"Light promotes WCC dependent nucleosome eviction at WCC binding sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995204", "https://ndownloader.figshare.com/files/1995205", "https://ndownloader.figshare.com/files/1995206", "https://ndownloader.figshare.com/files/1995207", "https://ndownloader.figshare.com/files/1995208", "https://ndownloader.figshare.com/files/1995209", "https://ndownloader.figshare.com/files/1995210", "https://ndownloader.figshare.com/files/1995211", "https://ndownloader.figshare.com/files/1995212", "https://ndownloader.figshare.com/files/1995213", "https://ndownloader.figshare.com/files/1995214", "https://ndownloader.figshare.com/files/1995215", "https://ndownloader.figshare.com/files/1995216"], "description"=>"<div><p>Light is an important environmental cue that affects physiology and development of <i>Neurospora crassa</i>. The light-sensing transcription factor (TF) WCC, which consists of the GATA-family TFs WC1 and WC2, is required for light-dependent transcription. SUB1, another GATA-family TF, is not a photoreceptor but has also been implicated in light-inducible gene expression. To assess regulation and organization of the network of light-inducible genes, we analyzed the roles of WCC and SUB1 in light-induced transcription and nucleosome remodeling. We show that SUB1 co-regulates a fraction of light-inducible genes together with the WCC. WCC induces nucleosome eviction at its binding sites. Chromatin remodeling is facilitated by SUB1 but SUB1 cannot activate light-inducible genes in the absence of WCC. We identified FF7, a TF with a putative O-acetyl transferase domain, as an interaction partner of SUB1 and show their cooperation in regulation of a fraction of light-inducible and a much larger number of non light-inducible genes. Our data suggest that WCC acts as a general switch for light-induced chromatin remodeling and gene expression. SUB1 and FF7 synergistically determine the extent of light-induction of target genes in common with WCC but have in addition a role in transcription regulation beyond light-induced gene expression.</p></div>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361053, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1005105.s001", "https://dx.doi.org/10.1371/journal.pgen.1005105.s002", "https://dx.doi.org/10.1371/journal.pgen.1005105.s003", "https://dx.doi.org/10.1371/journal.pgen.1005105.s004", "https://dx.doi.org/10.1371/journal.pgen.1005105.s005", "https://dx.doi.org/10.1371/journal.pgen.1005105.s006", "https://dx.doi.org/10.1371/journal.pgen.1005105.s007", "https://dx.doi.org/10.1371/journal.pgen.1005105.s008", "https://dx.doi.org/10.1371/journal.pgen.1005105.s009", "https://dx.doi.org/10.1371/journal.pgen.1005105.s010", "https://dx.doi.org/10.1371/journal.pgen.1005105.s011", "https://dx.doi.org/10.1371/journal.pgen.1005105.s012", "https://dx.doi.org/10.1371/journal.pgen.1005105.s013"], "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Combinatorial_Control_of_Light_Induced_Chromatin_Remodeling_and_Gene_Activation_in_Neurospora_/1361053", "title"=>"Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in <i>Neurospora</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-03-30 03:43:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/1995194"], "description"=>"<p><b>A</b>. Western blot showing SUB1 expression levels of <i>qa</i> promoter driven FLAG-tagged <i>sub1</i> in <i>wc1</i><sup><i>+</i></sup> and <i>wc1</i><sup><i>mut</i></sup> strains before and 4 h after QA-induction of cultures grown for 24 h in the dark or in constant light. <b>B</b>. Quantification of <i>hyr1</i> RNA levels by RT-PCR (± SEM, n = 4) under the conditions described in (A). <i>tubulin</i> RNA was used for normalization. The <i>hyr1</i> RNA level in <i>wc1</i><sup><i>+</i></sup><i>qa2</i>::<i>sub1</i><sub><i>FLAG</i></sub> in the dark (-QA) was set to 1. <b>C</b>. ChIP-PCR analysis of FLAG-SUB1 showing binding of SUB1 to the <i>hyr1</i> promoter in <i>wc1</i><sup><i>+</i></sup><i>qa2</i>::<i>sub1</i><sub><i>FLAG</i></sub>, <i>wc1</i><sup><i>mut</i></sup><sub><i>_</i></sub><i>qa2</i>::<i>sub1</i><sub><i>FLAG</i></sub> and Δ<i>sub1</i> strains grown 24 h in dark or in constant light. QA-induction, when indicated, was carried out for 4 h. Two-step ChIP was performed using FLAG and SUB1 antibodies. 28s rDNA was used for normalization. The ChIP-PCR signal of light grown <i>wc1</i><sup><i>+</i></sup><i>qa2</i>::<i>sub1</i><sub><i>FLAG</i></sub> was set to 1 (± SEM, n = 3). <b>D</b>. Western blot showing SUB1 levels after light-exposure of <i>wt</i>, <i>tub</i>::<i>sub1</i> and <i>ccg1</i>::<i>sub1</i> strains. <b>E</b>. Quantification by RT-PCR of light-induced accumulation of <i>hyr1</i> RNA levels in <i>wt</i>, Δ<i>sub1</i>, <i>tub</i>::<i>sub1 and ccg1</i>::<i>sub1</i> strains. 28s rRNA was used for normalization. Dark RNA levels of <i>wt</i> were normalized to 1 (± SEM, n = 4).</p>", "links"=>[], "tags"=>["wc", "Sub 1", "FF 7 synergistically", "Light Induced Chromatin Remodeling", "gene", "expression", "regulation", "transcription", "tf", "wcc"], "article_id"=>1361043, "categories"=>["Biological Sciences"], "users"=>["Cigdem Sancar", "Nati Ha", "Rüstem Yilmaz", "Rafael Tesorero", "Tamas Fisher", "Michael Brunner", "Gencer Sancar"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1005105.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SUB1_requires_light_activated_WCC_to_induce_hyr1_gene_expression_/1361043", "title"=>"SUB1 requires light-activated WCC to induce <i>hyr1</i> gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-30 03:43:03"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"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"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"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"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"52", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}

Relative Metric

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