Identification of Novel Target Genes for Safer and More Specific Control of Root-Knot Nematodes from a Pan-Genome Mining
Publication Date
October 31, 2013
Journal
PLOS Pathogens
Authors
Etienne G. J. Danchin, Marie Jeanne Arguel, Amandine Campan Fournier, Laetitia Perfus Barbeoch, et al
Volume
9
Issue
10
Pages
e1003745
DOI
https://dx.plos.org/10.1371/journal.ppat.1003745
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1003745
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24204279
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3814813
Europe PMC
http://europepmc.org/abstract/MED/24204279
Web of Science
000330383800095
Scopus
84887297982
Mendeley
http://www.mendeley.com/research/identification-novel-target-genes-safer-more-specific-control-rootknot-nematodes-pangenome-mining
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Mendeley | Further Information

{"title"=>"Identification of Novel Target Genes for Safer and More Specific Control of Root-Knot Nematodes from a Pan-Genome Mining", "type"=>"journal", "authors"=>[{"first_name"=>"Etienne G.J.", "last_name"=>"Danchin", "scopus_author_id"=>"35304529700"}, {"first_name"=>"Marie Jeanne", "last_name"=>"Arguel", "scopus_author_id"=>"15838756400"}, {"first_name"=>"Amandine", "last_name"=>"Campan-Fournier", "scopus_author_id"=>"55343926000"}, {"first_name"=>"Laetitia", "last_name"=>"Perfus-Barbeoch", "scopus_author_id"=>"6507560999"}, {"first_name"=>"Marc", "last_name"=>"Magliano", "scopus_author_id"=>"8948982600"}, {"first_name"=>"Marie Noëlle", "last_name"=>"Rosso", "scopus_author_id"=>"7005224485"}, {"first_name"=>"Martine", "last_name"=>"Da Rocha", "scopus_author_id"=>"8053808400"}, {"first_name"=>"Corinne", "last_name"=>"Da Silva", "scopus_author_id"=>"35336572800"}, {"first_name"=>"Nicolas", "last_name"=>"Nottet", "scopus_author_id"=>"55921408400"}, {"first_name"=>"Karine", "last_name"=>"Labadie", "scopus_author_id"=>"9844786800"}, {"first_name"=>"Julie", "last_name"=>"Guy", "scopus_author_id"=>"55920995900"}, {"first_name"=>"François", "last_name"=>"Artiguenave", "scopus_author_id"=>"6602850294"}, {"first_name"=>"Pierre", "last_name"=>"Abad", "scopus_author_id"=>"55344098800"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-84887297982", "pui"=>"370218116", "pmid"=>"24204279", "issn"=>"15537366", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "doi"=>"10.1371/journal.ppat.1003745", "sgr"=>"84887297982"}, "id"=>"c049c0d1-b348-3233-b065-f68d797dfdac", "abstract"=>"Root-knot nematodes are globally the most aggressive and damaging plant-parasitic nematodes. Chemical nematicides have so far constituted the most efficient control measures against these agricultural pests. Because of their toxicity for the environment and danger for human health, these nematicides have now been banned from use. Consequently, new and more specific control means, safe for the environment and human health, are urgently needed to avoid worldwide proliferation of these devastating plant-parasites. Mining the genomes of root-knot nematodes through an evolutionary and comparative genomics approach, we identified and analyzed 15,952 nematode genes conserved in genomes of plant-damaging species but absent from non target genomes of chordates, plants, annelids, insect pollinators and mollusks. Functional annotation of the corresponding proteins revealed a relative abundance of putative transcription factors in this parasite-specific set compared to whole proteomes of root-knot nematodes. This may point to important and specific regulators of genes involved in parasitism. Because these nematodes are known to secrete effector proteins in planta, essential for parasitism, we searched and identified 993 such effector-like proteins absent from non-target species. Aiming at identifying novel targets for the development of future control methods, we biologically tested the effect of inactivation of the corresponding genes through RNA interference. A total of 15 novel effector-like proteins and one putative transcription factor compatible with the design of siRNAs were present as non-redundant genes and had transcriptional support in the model root-knot nematode Meloidogyne incognita. Infestation assays with siRNA-treated M. incognita on tomato plants showed significant and reproducible reduction of the infestation for 12 of the 16 tested genes compared to control nematodes. These 12 novel genes, showing efficient reduction of parasitism when silenced, constitute promising targets for the development of more specific and safer control means.", "link"=>"http://www.mendeley.com/research/identification-novel-target-genes-safer-more-specific-control-rootknot-nematodes-pangenome-mining", "reader_count"=>91, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>5, "Researcher"=>27, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>5, "Professor > Associate Professor"=>5, "Researcher"=>27, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>8, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>75, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>75}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>8}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "Brazil"=>5, "France"=>3, "Chile"=>1, "Spain"=>1, "India"=>2}, "group_count"=>3}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1263270"], "description"=>"<p>This Venn diagram represents the number of proteins that cumulate transcription-related terms in their Gene Ontology annotation in protein set 1. A total of 315 proteins have been assigned the term ‘Transcription’ in their Biological Process G.O. annotation. A total of 191 proteins have been assigned the term ‘Nucleus’ in their Cellular Component G.O. annotation. A total of 197 proteins have been assigned the term ‘Transcription factor activity” in their Molecular Function G.O. annotation. Overall, a total of 109 proteins in set 1 cumulate these three transcription factor-related G.O. terms.</p>", "links"=>[], "tags"=>["ontology", "annotation", "putative", "transcription"], "article_id"=>838636, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_Ontology_annotation_of_putative_transcription_factors_/838636", "title"=>"Gene Ontology annotation of putative transcription factors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263268"], "description"=>"<p>The relative phylogenetic position and simplified taxonomy of the 25 species included in the OrthoMCL comparison of whole proteomes. The topology is according to the NCBI's taxonomy, except within the nematode and insecta lineages which are according to ref <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003745#ppat.1003745-vanMegen1\" target=\"_blank\">[45]</a> and to ref <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003745#ppat.1003745-Trautwein1\" target=\"_blank\">[46]</a>, respectively. Species that are known plant-parasites plant-pathogens or phytophagous are highlighted in green and with a plant symbol. The animal-parasitic nematode <i>B. malayi</i> is highlighted in red and with a dog symbol. All the other species, in black, with a “wrong way” sign, are blacklisted.</p>", "links"=>[], "tags"=>["orthomcl"], "article_id"=>838633, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g002", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_tree_of_selected_species_for_OrthoMCL_comparison_/838633", "title"=>"Phylogenetic tree of selected species for OrthoMCL comparison.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263267"], "description"=>"<p>Pipeline illustrating the main filtering steps, from the two RKN whole protein sets, that allowed identification of novel and non-redundant targets for the development of specific and safer control methods.</p>", "links"=>[], "tags"=>["rkn", "proteomes", "filtering", "pipeline"], "article_id"=>838631, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Whole_RKN_proteomes_filtering_pipeline_for_identification_of_novel_targets_/838631", "title"=>"Whole RKN proteomes filtering pipeline for identification of novel targets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263273"], "description"=>"*<p>statistically significant and reproducible reduction.</p>", "links"=>[], "tags"=>[], "article_id"=>838641, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.t002", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_infestation_qPCR_and_in_situ_hybridization_/838641", "title"=>"Results of infestation, qPCR, and <i>in-situ</i> hybridization.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263271"], "description"=>"<p>siRNAs induced significant change in the targeted transcripts expression level. Transcript level for each of the targeted gene was measured by qPCR 24<i>M. incognita</i> genome (siRNA random).</p>", "links"=>[], "tags"=>["abundance", "sirna", "soaked", "j2s"], "article_id"=>838639, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g005", "stats"=>{"downloads"=>1, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcript_abundance_percentage_change_in_siRNA_soaked_J2s_relative_to_control_/838639", "title"=>"Transcript abundance percentage change in siRNA soaked J2s relative to control.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263272"], "description"=>"<p>Controls are J2 larvae soaked with siRNA targeting no sequence in the <i>M. incognita</i> genome, accession numbers indicate M. incognita genes targeted by siRNAs. Infection tests were performed in duplicate represented as dark color bars for the first replicate and light color bars for the second replicate. Variations of number of galls and of numbers of egg masses, measured six weeks after inoculation, are represented in the top panels in green and in the bottom panel in red/orange, respectively. Error bars were calculated by standard error of the mean (SEM). P-Value above each bar indicates measures statistically different from controls. A significant change between the two duplicates is represented by p-values above a line spanning duplicates. P-value signification codes are as follows: 0.0001 ‘***’, 0.001 ‘**’, 0.01 ‘*’, 0.05 ‘.’.</p>", "links"=>[], "tags"=>["sirna", "nematode"], "article_id"=>838640, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_siRNA_on_nematode_infestation_/838640", "title"=>"Effect of siRNA on nematode infestation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263269"], "description"=>"<p>Kiviat diagram representing, the relative abundance of Gene Ontology (GO) terms, in percent for the whole <i>M. incognita</i> and <i>M. hapla</i> proteomes (in blue and red, respectively) as well as for the proteins that passed the OrthoMCL and BLAST filters (protein set 1 in green). (A) Relative abundance of GO terms assigned to whole RKN proteomes and protein set 1in the Biological Process category. (B) Relative abundance of GO terms assigned to whole RKN proteomes and protein set 1 in the Molecular Function category. (C) Relative abundance of GO terms assigned to whole RKN proteomes and protein set 1 in the Cellular Component category. In the three categories, the ten GO terms that presented the most different relative abundance (in percent) in protein set 1 compared to the whole RKN proteomes are presented.</p>", "links"=>[], "tags"=>["ontology", "abundance", "targets", "compared"], "article_id"=>838635, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_Ontology_terms_relative_abundance_in_candidate_targets_compared_to_whole_proteomes_/838635", "title"=>"Gene Ontology terms relative abundance in candidate targets compared to whole proteomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263275", "https://ndownloader.figshare.com/files/1263276", "https://ndownloader.figshare.com/files/1263277", "https://ndownloader.figshare.com/files/1263278", "https://ndownloader.figshare.com/files/1263279", "https://ndownloader.figshare.com/files/1263280", "https://ndownloader.figshare.com/files/1263281", "https://ndownloader.figshare.com/files/1263282", "https://ndownloader.figshare.com/files/1263283"], "description"=>"<div><p>Root-knot nematodes are globally the most aggressive and damaging plant-parasitic nematodes. Chemical nematicides have so far constituted the most efficient control measures against these agricultural pests. Because of their toxicity for the environment and danger for human health, these nematicides have now been banned from use. Consequently, new and more specific control means, safe for the environment and human health, are urgently needed to avoid worldwide proliferation of these devastating plant-parasites. Mining the genomes of root-knot nematodes through an evolutionary and comparative genomics approach, we identified and analyzed 15,952 nematode genes conserved in genomes of plant-damaging species but absent from non target genomes of chordates, plants, annelids, insect pollinators and mollusks. Functional annotation of the corresponding proteins revealed a relative abundance of putative transcription factors in this parasite-specific set compared to whole proteomes of root-knot nematodes. This may point to important and specific regulators of genes involved in parasitism. Because these nematodes are known to secrete effector proteins <i>in planta</i>, essential for parasitism, we searched and identified 993 such effector-like proteins absent from non-target species. Aiming at identifying novel targets for the development of future control methods, we biologically tested the effect of inactivation of the corresponding genes through RNA interference. A total of 15 novel effector-like proteins and one putative transcription factor compatible with the design of siRNAs were present as non-redundant genes and had transcriptional support in the model root-knot nematode <i>Meloidogyne incognita</i>. Infestation assays with siRNA-treated <i>M. incognita</i> on tomato plants showed significant and reproducible reduction of the infestation for 12 of the 16 tested genes compared to control nematodes. These 12 novel genes, showing efficient reduction of parasitism when silenced, constitute promising targets for the development of more specific and safer control means.</p></div>", "links"=>[], "tags"=>["genes", "safer", "root-knot", "nematodes", "pan-genome"], "article_id"=>838648, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003745.s001", "https://dx.doi.org/10.1371/journal.ppat.1003745.s002", "https://dx.doi.org/10.1371/journal.ppat.1003745.s003", "https://dx.doi.org/10.1371/journal.ppat.1003745.s004", "https://dx.doi.org/10.1371/journal.ppat.1003745.s005", "https://dx.doi.org/10.1371/journal.ppat.1003745.s006", "https://dx.doi.org/10.1371/journal.ppat.1003745.s007", "https://dx.doi.org/10.1371/journal.ppat.1003745.s008", "https://dx.doi.org/10.1371/journal.ppat.1003745.s009"], "stats"=>{"downloads"=>12, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_Novel_Target_Genes_for_Safer_and_More_Specific_Control_of_Root_Knot_Nematodes_from_a_Pan_Genome_Mining_/838648", "title"=>"Identification of Novel Target Genes for Safer and More Specific Control of Root-Knot Nematodes from a Pan-Genome Mining", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-10-31 03:15:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1263274"], "description"=>"*<p>after trimming, collapsing and cleaning as described in methods.</p>", "links"=>[], "tags"=>["rna-seq"], "article_id"=>838642, "categories"=>["Biological Sciences"], "users"=>["Etienne G. J. Danchin", "Marie-Jeanne Arguel", "Amandine Campan-Fournier", "Laetitia Perfus-Barbeoch", "Marc Magliano", "Marie-Noëlle Rosso", "Martine Da Rocha", "Corinne Da Silva", "Nicolas Nottet", "Karine Labadie", "Julie Guy", "François Artiguenave", "Pierre Abad"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003745.t001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Samples_used_for_RNA_seq_and_resulting_contigs_/838642", "title"=>"Samples used for RNA-seq and resulting contigs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-31 03:15:26"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"30", "full-text"=>"31", "pdf"=>"10", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"18", "full-text"=>"20", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"5", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"23", "full-text"=>"109", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"10", "pdf"=>"41", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"35", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"22", "full-text"=>"21", "pdf"=>"36", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"21", "full-text"=>"19", "pdf"=>"32", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"39", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"16", "full-text"=>"12", "pdf"=>"21", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"2", "cited-by"=>"1", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"17", "full-text"=>"22", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"21", "full-text"=>"26", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"11", "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"=>"17", "full-text"=>"18", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"20", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"17", "full-text"=>"17", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
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  • {"unique-ip"=>"19", "full-text"=>"18", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"19", "full-text"=>"18", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"21", "full-text"=>"18", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"20", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"16", "full-text"=>"19", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"11", "full-text"=>"25", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"14", "full-text"=>"24", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"17", "full-text"=>"25", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "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"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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Relative Metric

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