A Reporter Assay in Lamprey Embryos Reveals Both Functional Conservation and Elaboration of Vertebrate Enhancers
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{"title"=>"A reporter assay in lamprey embryos reveals both functional conservation and elaboration of vertebrate enhancers", "type"=>"journal", "authors"=>[{"first_name"=>"Hugo J.", "last_name"=>"Parker", "scopus_author_id"=>"35726088700"}, {"first_name"=>"Tatjana", "last_name"=>"Sauka-Spengler", "scopus_author_id"=>"6506693180"}, {"first_name"=>"Marianne", "last_name"=>"Bronner", "scopus_author_id"=>"7006767803"}, {"first_name"=>"Greg", "last_name"=>"Elgar", "scopus_author_id"=>"7003707374"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"372730888", "doi"=>"10.1371/journal.pone.0085492", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"24416417", "issn"=>"19326203", "scopus"=>"2-s2.0-84897389631", "sgr"=>"84897389631"}, "id"=>"44e656c0-689c-3ec6-bf73-9a429fed0ec3", "abstract"=>"The sea lamprey is an important model organism for investigating the evolutionary origins of vertebrates. As more vertebrate genome sequences are obtained, evolutionary developmental biologists are becoming increasingly able to identify putative gene regulatory elements across the breadth of the vertebrate taxa. The identification of these regions makes it possible to address how changes at the genomic level have led to changes in developmental gene regulatory networks and ultimately to the evolution of morphological diversity. Comparative genomics approaches using sea lamprey have already predicted a number of such regulatory elements in the lamprey genome. Functional characterisation of these sequences and other similar elements requires efficient reporter assays in lamprey. In this report, we describe the development of a transient transgenesis method for lamprey embryos. Focusing on conserved non-coding elements (CNEs), we use this method to investigate their functional conservation across the vertebrate subphylum. We find instances of both functional conservation and lineage-specific functional evolution of CNEs across vertebrates, emphasising the utility of functionally testing homologous CNEs in their host species.", "link"=>"http://www.mendeley.com/research/reporter-assay-lamprey-embryos-reveals-both-functional-conservation-elaboration-vertebrate-enhancers", "reader_count"=>18, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>13, "Unspecified"=>2}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>3, "France"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1344243", "https://ndownloader.figshare.com/files/1344244", "https://ndownloader.figshare.com/files/1344245", "https://ndownloader.figshare.com/files/1344246"], "description"=>"<div><p>The sea lamprey is an important model organism for investigating the evolutionary origins of vertebrates. As more vertebrate genome sequences are obtained, evolutionary developmental biologists are becoming increasingly able to identify putative gene regulatory elements across the breadth of the vertebrate taxa. The identification of these regions makes it possible to address how changes at the genomic level have led to changes in developmental gene regulatory networks and ultimately to the evolution of morphological diversity. Comparative genomics approaches using sea lamprey have already predicted a number of such regulatory elements in the lamprey genome. Functional characterisation of these sequences and other similar elements requires efficient reporter assays in lamprey. In this report, we describe the development of a transient transgenesis method for lamprey embryos. Focusing on conserved non-coding elements (CNEs), we use this method to investigate their functional conservation across the vertebrate subphylum. We find instances of both functional conservation and lineage-specific functional evolution of CNEs across vertebrates, emphasising the utility of functionally testing homologous CNEs in their host species.</p></div>", "links"=>[], "tags"=>["developmental biology", "Evolutionary developmental biology", "morphogenesis", "Pattern formation", "Evolutionary biology", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Functional genomics", "Genome evolution", "systems biology", "assay", "lamprey", "embryos", "reveals", "elaboration", "vertebrate"], "article_id"=>898661, "categories"=>["Biological Sciences"], "users"=>["Hugo J. Parker", "Tatjana Sauka-Spengler", "Marianne Bronner", "Greg Elgar"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0085492.s001", "https://dx.doi.org/10.1371/journal.pone.0085492.s002", "https://dx.doi.org/10.1371/journal.pone.0085492.s003", "https://dx.doi.org/10.1371/journal.pone.0085492.s004"], "stats"=>{"downloads"=>6, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Reporter_Assay_in_Lamprey_Embryos_Reveals_Both_Functional_Conservation_and_Elaboration_of_Vertebrate_Enhancers_/898661", "title"=>"A Reporter Assay in Lamprey Embryos Reveals Both Functional Conservation and Elaboration of Vertebrate Enhancers", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-01-09 03:36:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1344236"], "description"=>"<p>(<b>A–B</b>) GFP fluorescence in stage 26 transient transgenic lamprey embryos, generated by meganuclease-mediated transgenesis with the pm3285 (<b>A</b>) and dr3285 enhancers (<b>B</b>). GFP expression is seen in the cranial ganglia (arrowheads), hindbrain and spinal cord. (<b>C–D</b>) GFP fluorescence in the rostral hindbrain in stage 26 transient transgenic lamprey embryos generated by meganuclease-mediated transgenesis with the pm3299 (<b>C</b>) and dr3299 (<b>D</b>) enhancers. GFP expression driven by pm3285 (<b>E</b>) and dr3285 (<b>F</b>) in 54hpf F1 transgenic zebrafish embryos, created by Tol2 transgenesis. Expression in the cranial ganglia is seen for the elements from both zebrafish and lamprey (arrowheads). Expression is also seen in primary neurons of the hindbrain and spinal cord. (<b>G–H</b>) 54hpf F1 transgenic zebrafish embryos showing GFP expression driven by the pm3299 (<b>G</b>) and dr3299 enhancers (<b>H</b>). GFP expression in the hindbrain is driven by both elements, whilst only the zebrafish element up-regulates GFP in the neural crest. (<b>I–J</b>) Expression of <i>Meis1/2a</i> (<b>I</b>) and <i>b</i> (<b>J</b>) genes in stage 25 lamprey embryos, revealed by <i>in-situ</i> hybridisation. Arrowheads highlight expression in cranial ganglia. Abbreviations: glV2,3, trigeminal ganglion; gldIX, epibranchial ganglion of the glossopharyngeal nerve; gldX1, epibranchial ganglion of the vagus nerve; glf, facial ganglion; hb, hindbrain; nc, neural crest; ov, otic vesicle; ph, pharynx; pllg, posterior lateral line ganglion; sc, spinal cord.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary developmental biology", "morphogenesis", "Pattern formation", "Evolutionary biology", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Functional genomics", "Genome evolution", "systems biology", "driven", "cnes", "3285", "3299", "lamprey", "zebrafish"], "article_id"=>898654, "categories"=>["Biological Sciences"], "users"=>["Hugo J. Parker", "Tatjana Sauka-Spengler", "Marianne Bronner", "Greg Elgar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085492.g002", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reporter_expression_driven_by_CNEs_3285_and_3299_in_lamprey_and_zebrafish_embryos_/898654", "title"=>"Reporter expression driven by CNEs 3285 and 3299 in lamprey and zebrafish embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-09 03:36:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1344233"], "description"=>"<p>(<b>A–C</b>) Transient transgenic lamprey generated through injection of the linearised pm3285_cfos_EGFP plasmid showing mosaic GFP expression in the ectoderm and in neurons of the spinal cord at stage 23 (<b>A</b>), stage 25 (<b>B</b>) and at the ammocoete larval stage (<b>C</b>). (<b>D–F</b>) Lamprey embryo with GFP expression in the hindbrain and spinal cord at stage 23 (<b>D</b>), stage 24 (<b>E</b>) and stage 25 (<b>F</b>), obtained using the meganuclease assay with the pm3285 enhancer. (<b>G–J</b>) ‘Background’ GFP expression in the ectoderm of lamprey embryos at stage 19 (<b>G</b>), 21 (<b>H</b>), 23 (<b>I</b>) and 25 (<b>J</b>), driven by the cfos_IsceI_EFGP plasmid with no enhancer using the meganuclease method (embryos shown are different individuals). Abbreviations: ec, ectoderm; hb, hindbrain; ph, pharynx; sc, spinal cord.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary developmental biology", "morphogenesis", "Pattern formation", "Evolutionary biology", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Functional genomics", "Genome evolution", "systems biology", "meganuclease-mediated", "transgenesis", "lamprey"], "article_id"=>898651, "categories"=>["Biological Sciences"], "users"=>["Hugo J. Parker", "Tatjana Sauka-Spengler", "Marianne Bronner", "Greg Elgar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085492.g001", "stats"=>{"downloads"=>6, "page_views"=>52, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_I_sceI_meganuclease_mediated_transgenesis_in_lamprey_embryos_/898651", "title"=>"I-sceI meganuclease-mediated transgenesis in lamprey embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-09 03:36:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1344239"], "description"=>"<p>(<b>A–B</b>) Lateral (<b>A</b>) and dorsal (<b>B</b>) views of stage 26 transient transgenic lamprey embryos, showing reporter expression in the anterior hindbrain driven by different minimal promoters in conjunction with the pm3299 enhancer using the I-SceI meganuclease approach. (<b>C</b>) Lateral views of stage 23 lamprey embryos injected with the same constructs as those in <b>A</b> and <b>B</b>, showing early expression in ectoderm and yolk, similar to the background expression driven by the control cfos_I-SceI_EGFP construct (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085492#pone-0085492-g001\" target=\"_blank\">Figure 1I</a>). The identity of the minimal promoter used in each case is indicated above the top panel. Abbreviations: ec, ectoderm; hb, hindbrain; ph, pharynx; y, yolk.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary developmental biology", "morphogenesis", "Pattern formation", "Evolutionary biology", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Functional genomics", "Genome evolution", "systems biology", "promoters"], "article_id"=>898657, "categories"=>["Biological Sciences"], "users"=>["Hugo J. Parker", "Tatjana Sauka-Spengler", "Marianne Bronner", "Greg Elgar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085492.g003", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identifying_minimal_promoters_that_are_functional_in_lamprey_/898657", "title"=>"Identifying minimal promoters that are functional in lamprey.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-09 03:36:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1344240"], "description"=>"<p>Results are shown for linearised plasmid injection and meganuclease-mediated transgenesis. Ectodermal background expression was not counted for the injections of pm3285 and pm3299 with the meganuclease method, but the proportion of embryos with this background expression was in keeping with that found for the cfos_I-SceI_EGFP construct.</p>", "links"=>[], "tags"=>["developmental biology", "Evolutionary developmental biology", "morphogenesis", "Pattern formation", "Evolutionary biology", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Functional genomics", "Genome evolution", "systems biology", "lamprey", "transgenesis"], "article_id"=>898658, "categories"=>["Biological Sciences"], "users"=>["Hugo J. Parker", "Tatjana Sauka-Spengler", "Marianne Bronner", "Greg Elgar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085492.t001", "stats"=>{"downloads"=>4, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_comparison_of_lamprey_transgenesis_methods_/898658", "title"=>"A comparison of lamprey transgenesis methods.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-09 03:36:25"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"19", "full-text"=>"19", "pdf"=>"13", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"0", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"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"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"9", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"1", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"18", "full-text"=>"14", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"7", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"5", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"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"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"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"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"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"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"3", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"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"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Anatomy", "average_usage"=>[267]}, {"subject_area"=>"/Biology and life sciences/Computational biology", "average_usage"=>[341, 529]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[285]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[333]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[292, 461]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[310]}]}
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