Accelerated Growth Rate and Increased Drought Stress Resilience of the Model Grass Brachypodium distachyon Colonized by Bacillus subtilis B26
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{"title"=>"Accelerated growth rate and increased drought stress resilience of the model grass brachypodium distachyon colonized by bacillus subtilis B26", "type"=>"journal", "authors"=>[{"first_name"=>"François", "last_name"=>"Gagné-Bourque", "scopus_author_id"=>"56728613500"}, {"first_name"=>"Boris F.", "last_name"=>"Mayer", "scopus_author_id"=>"56061573300"}, {"first_name"=>"Jean Benoit", "last_name"=>"Charron", "scopus_author_id"=>"8313763000"}, {"first_name"=>"Hojatollah", "last_name"=>"Vali", "scopus_author_id"=>"7004175757"}, {"first_name"=>"Annick", "last_name"=>"Bertrand", "scopus_author_id"=>"7102204171"}, {"first_name"=>"Suha", "last_name"=>"Jabaji", "scopus_author_id"=>"6603956702"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"26103151", "scopus"=>"2-s2.0-84939195473", "pui"=>"605586190", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0130456", "sgr"=>"84939195473"}, "id"=>"4aa33ad8-9db8-3353-b547-75e100d6be93", "abstract"=>"Plant growth-promoting bacteria (PGB) induce positive effects in plants, for instance, increased growth and reduced abiotic stresses susceptibility. The mechanisms by which these bacteria impact the host plant are numerous, diverse and often specific. Here, we studied the agronomical, molecular and biochemical effects of the endophytic PGB Bacillus subtilis B26 on the full life cycle of Brachypodium distachyon Bd21, an established model species for functional genomics in cereal crops and temperate grasses. Inoculation of Brachypodium with B. subtilis strain B26 increased root and shoot weights, accelerated growth rate and seed yield as compared to control plants. B. subtilis strain B26 efficiently colonized the plant and was recovered from roots, stems and blades as well as seeds of Brachypodium, indicating that the bacterium is able to migrate, spread systemically inside the plant, establish itself in the aerial plant tissues and organs, and is vertically transmitted to seeds. The presence of B. subtilis strain B26 in the seed led to systemic colonization of the next generation of Brachypodium plants. Inoculated Brachypodium seedlings and mature plants exposed to acute and chronic drought stress minimized the phenotypic effect of drought compared to plants not harbouring the bacterium. Protection from the inhibitory effects of drought by the bacterium was linked to upregulation of the drought-response genes, DREB2B-like, DHN3-like and LEA-14-A-like and modulation of the DNA methylation genes, MET1B-like, CMT3-like and DRM2-like, that regulate the process. Additionally, total soluble sugars and starch contents increased in stressed inoculated plants, a biochemical indication of drought tolerance. In conclusion, we show a single inoculation of Brachypodium with a PGB affected the whole growth cycle of the plant, accelerating its growth rates, shortening its vegetative period, and alleviating drought stress effects. These effects are relevant to grasses and cereal crops.", "link"=>"http://www.mendeley.com/research/accelerated-growth-rate-increased-drought-stress-resilience-model-grass-brachypodium-distachyon-colo-1", "reader_count"=>69, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>12, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>17, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>12, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>17, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>5, "Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>41, "Medicine and Dentistry"=>1, "Chemistry"=>4, "Social Sciences"=>1, "Immunology and Microbiology"=>1, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>41}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>5}}, "reader_count_by_country"=>{"Argentina"=>1, "Norway"=>1}, "group_count"=>7}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2133563"], "description"=>"<p>Non-inoculated (left) and inoculated (right) <i>Brachypodium</i> plants (A) before or (B and C) after one and two hours of acute drought stress. Pictures of non-inoculated (left) and inoculated (right) <i>Brachypodium</i> plants were also taken at (D) 0 day, (E) 5 days and (F) 8 days after last watering.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460969, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g004", "stats"=>{"downloads"=>3, "page_views"=>87, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_drought_stress_on_non_inoculated_and_inoculated_Brachypodium_plants_/1460969", "title"=>"Effects of drought stress on non-inoculated and inoculated <i>Brachypodium</i> plants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133575"], "description"=>"<p>*Days post inoculation.</p><p>**Biologische Bundesantalt Bundessortenamt and CHemische industrie (BBCH) growth scale [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0130456#pone.0130456.ref024\" target=\"_blank\">24</a>].</p><p>Scale for phonological growth stages in <i>Brachypodium distachyon</i>.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460981, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.t001", "stats"=>{"downloads"=>2, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scale_for_phonological_growth_stages_in_Brachypodium_distachyon_/1460981", "title"=>"Scale for phonological growth stages in <i>Brachypodium distachyon</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133574"], "description"=>"<p>(A, B) Relative mRNA abundance of <i>Methyltransferase 1</i> (<i>MET1</i>), (C, D) <i>Chromomethylase 3</i> (<i>CMT3</i>), and (E, F) <i>Domains-RearrangedMethyltransferase 2</i> (<i>DRM2</i>) before and one hour after uprooting non-inoculated and inoculated plants (A, C, E) or before and after 5 and 8 days following the last watering of non-inoculated and inoculated plants (B, D, F). * Represents a statistically significant difference.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460980, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g008", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_transcript_accumulation_of_DNA_methyltransferases_in_inoculated_and_non_inoculated_Brachypodium_plants_under_control_and_water_deficit_conditions_/1460980", "title"=>"Relative transcript accumulation of DNA methyltransferases in inoculated and non-inoculated <i>Brachypodium</i> plants under control and water deficit conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133554"], "description"=>"<p>(A) Cross section of root xylem with numerous bacterial cells present inside the vessel elements (arrows). (B, C) Leaf mesophyll cells and bundle sheath (inset) with bacterial cells (arrows). (D) Vessel elements of xylem stem tissue showing B26 inside and outside the vessel elements. (E) Cross section of seed with B26 cells. (F) Cross section of chloroplast of a leaf bundle sheath cell from a colonized leaf. Notice the abundance of starch granules and the integrity of the thylakoids. (G) <i>B</i>. <i>subtilis</i> B26 cells grown in pure culture.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460962, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g003", "stats"=>{"downloads"=>3, "page_views"=>56, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transmission_electron_microscopy_TEM_micrographs_of_colonized_Brachypodium_tissues_with_B_subtilis_B26_/1460962", "title"=>"Transmission electron microscopy (TEM) micrographs of colonized <i>Brachypodium</i> tissues with <i>B</i>. <i>subtilis</i> B26.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133530"], "description"=>"<p>Effects of the inoculation of <i>Brachypodium</i> plants with strain B26 on: (A) plant height (B) shoot dry weight (C) root dry weight (D) number of leaves (E) number of seed, and (F) picture of non-inoculated and inoculated plants. * Represents a statistically significant difference.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460943, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g001", "stats"=>{"downloads"=>5, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenotypic_effects_of_the_endophytic_bacteria_Bacillus_subtilis_B26_on_the_life_cycle_of_Brachypodium_/1460943", "title"=>"Phenotypic effects of the endophytic <i>bacteria Bacillus subtilis</i> B26 on the life cycle of <i>Brachypodium</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133570"], "description"=>"<p>(A) 5 days and (B) 8 days post watering. * Represents a statistically significant difference.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460976, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g006", "stats"=>{"downloads"=>3, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Soluble_sugars_and_starch_content_of_inoculated_and_non_inoculated_plants_under_water_deficit_conditions_/1460976", "title"=>"Soluble sugars and starch content of inoculated and non-inoculated plants under water deficit conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133567"], "description"=>"<p>Relative mRNA abundance of (A, B) <i>Dehydration-Responsive Element-Binding protein 2B-like</i> (<i>DREB2B-like</i>); (C, D) <i>Dehydrin 3-like</i> (<i>DHN3-like</i>); and (E, F), <i>Desiccation-related protein LEA-14-A-like</i> in non-inoculated and inoculated plants before and one hour after uprooting (A, C, E) or before and after 5 and 8 days of chronic drought stress (B, D, F). * Represents a statistically significant difference.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460974, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g005", "stats"=>{"downloads"=>5, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_transcript_accumulation_of_drought_responsive_genes_/1460974", "title"=>"Relative transcript accumulation of drought-responsive genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133582", "https://ndownloader.figshare.com/files/2133583", "https://ndownloader.figshare.com/files/2133584", "https://ndownloader.figshare.com/files/2133585", "https://ndownloader.figshare.com/files/2133586"], "description"=>"<div><p>Plant growth-promoting bacteria (PGB) induce positive effects in plants, for instance, increased growth and reduced abiotic stresses susceptibility. The mechanisms by which these bacteria impact the host plant are numerous, diverse and often specific. Here, we studied the agronomical, molecular and biochemical effects of the endophytic PGB <i>Bacillus subtilis</i> B26 on the full life cycle of <i>Brachypodium distachyon</i> Bd21, an established model species for functional genomics in cereal crops and temperate grasses. Inoculation of <i>Brachypodium</i> with <i>B</i>. <i>subtilis</i> strain B26 increased root and shoot weights, accelerated growth rate and seed yield as compared to control plants. <i>B</i>. <i>subtilis</i> strain B26 efficiently colonized the plant and was recovered from roots, stems and blades as well as seeds of <i>Brachypodium</i>, indicating that the bacterium is able to migrate, spread systemically inside the plant, establish itself in the aerial plant tissues and organs, and is vertically transmitted to seeds. The presence of <i>B</i>. <i>subtilis</i> strain B26 in the seed led to systemic colonization of the next generation of <i>Brachypodium</i> plants. Inoculated <i>Brachypodium</i> seedlings and mature plants exposed to acute and chronic drought stress minimized the phenotypic effect of drought compared to plants not harbouring the bacterium. Protection from the inhibitory effects of drought by the bacterium was linked to upregulation of the drought-response genes, <i>DREB2B-like</i>, <i>DHN3-like</i> and <i>LEA-14-A-like</i> and modulation of the DNA methylation genes, <i>MET1B-like</i>, <i>CMT3-like</i> and <i>DRM2-like</i>, that regulate the process. Additionally, total soluble sugars and starch contents increased in stressed inoculated plants, a biochemical indication of drought tolerance. In conclusion, we show a single inoculation of <i>Brachypodium</i> with a PGB affected the whole growth cycle of the plant, accelerating its growth rates, shortening its vegetative period, and alleviating drought stress effects. These effects are relevant to grasses and cereal crops.</p></div>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460988, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0130456.s001", "https://dx.doi.org/10.1371/journal.pone.0130456.s002", "https://dx.doi.org/10.1371/journal.pone.0130456.s003", "https://dx.doi.org/10.1371/journal.pone.0130456.s004", "https://dx.doi.org/10.1371/journal.pone.0130456.s005"], "stats"=>{"downloads"=>6, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Accelerated_Growth_Rate_and_Increased_Drought_Stress_Resilience_of_the_Model_Grass_Brachypodium_distachyon_Colonized_by_Bacillus_subtilis_B26/1460988", "title"=>"Accelerated Growth Rate and Increased Drought Stress Resilience of the Model Grass <i>Brachypodium distachyon</i> Colonized by <i>Bacillus subtilis</i> B26", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133536"], "description"=>"<p>(A) CFU and DNA copy number of <i>B</i>. <i>subtilis</i> B26 in roots, shoots, seeds and rhizosphere soil. Upper case letters represent differences in between time points of the same tissue/soil, and lower case letters represent differences between different tissues at the same time point. (B) PCR detection of <i>B</i>. <i>subtilis</i> B26 in different tissues using species-specific primers. Lane 1, pure <i>B</i>. <i>subtilis</i> B26 DNA; Lane 2, no template; Lanes 3 to 5, non-inoculated plant tissues of root, shoot and seed at D63; Lanes 6 to 8, inoculated plant tissues of root, shoot, seed at D63; Lanes 9 and 10, root and shoot tissues of second generation plant at D28.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460949, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g002", "stats"=>{"downloads"=>2, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_B_subtilis_B26_in_the_host_plant_/1460949", "title"=>"Dynamics of <i>B</i>. <i>subtilis</i> B26 in the host plant.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/2133572"], "description"=>"<p>(A) Before and after one hour of acute drought stress. (B) Before and after 5 and 8 days of chronic drought stress. * Represents a statistically significant difference.</p>", "links"=>[], "tags"=>["drm", "DREB", "subtilis strain B 26", "Model Grass Brachypodium distachyon Colonized", "2b", "DNA methylation genes", "Inoculated Brachypodium seedlings", "dhn", "cmt", "abiotic stresses susceptibility", "drought stress effects", "1b", "Drought Stress Resilience", "lea", "Cereal crops", "endophytic PGB Bacillus subtilis B 26"], "article_id"=>1460978, "categories"=>["Uncategorised"], "users"=>["François Gagné-Bourque", "Boris F. Mayer", "Jean-Benoit Charron", "Hojatollah Vali", "Annick Bertrand", "Suha Jabaji"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0130456.g007", "stats"=>{"downloads"=>3, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variation_of_global_DNA_methylation_in_inoculated_and_non_inoculated_Brachypodium_plants_under_control_and_water_deficit_conditions_/1460978", "title"=>"Variation of global DNA methylation in inoculated and non-inoculated <i>Brachypodium</i> plants under control and water deficit conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-23 02:47:01"}

PMC Usage Stats | Further Information

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

Relative Metric

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