Distinct Roles of Jasmonates and Aldehydes in Plant-Defense Responses
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{"title"=>"Distinct roles of jasmonates and aldehydes in plant-defense responses", "type"=>"journal", "authors"=>[{"first_name"=>"E. Wassim", "last_name"=>"Chehab", "scopus_author_id"=>"14024172800"}, {"first_name"=>"Roy", "last_name"=>"Kaspi", "scopus_author_id"=>"7005238062"}, {"first_name"=>"Tatyana", "last_name"=>"Savchenko", "scopus_author_id"=>"56144589900"}, {"first_name"=>"Heather", "last_name"=>"Rowe", "scopus_author_id"=>"12769488000"}, {"first_name"=>"Florence", "last_name"=>"Negre-Zakharov", "scopus_author_id"=>"23994099900"}, {"first_name"=>"Dan", "last_name"=>"Kliebenstein", "scopus_author_id"=>"6602082706"}, {"first_name"=>"Katayoon", "last_name"=>"Dehesh", "scopus_author_id"=>"6701636328"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"18382679", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0001904", "pui"=>"351954390", "isbn"=>"1932-6203 (Electronic)", "scopus"=>"2-s2.0-44849137630", "sgr"=>"44849137630"}, "id"=>"a985bfbd-f7d4-3c1c-99a6-0e2b82cd4d0c", "abstract"=>"BACKGROUND: Many inducible plant-defense responses are activated by jasmonates (JAs), C(6)-aldehydes, and their corresponding derivatives, produced by the two main competing branches of the oxylipin pathway, the allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches, respectively. In addition to competition for substrates, these branch-pathway-derived metabolites have substantial overlap in regulation of gene expression. Past experiments to define the role of C(6)-aldehydes in plant defense responses were biased towards the exogenous application of the synthetic metabolites or the use of genetic manipulation of HPL expression levels in plant genotypes with intact ability to produce the competing AOS-derived metabolites. To uncouple the roles of the C(6)-aldehydes and jasmonates in mediating direct and indirect plant-defense responses, we generated Arabidopsis genotypes lacking either one or both of these metabolites. These genotypes were subsequently challenged with a phloem-feeding insect (aphids: Myzus persicae), an insect herbivore (leafminers: Liriomyza trifolii), and two different necrotrophic fungal pathogens (Botrytis cinerea and Alternaria brassicicola). We also characterized the volatiles emitted by these plants upon aphid infestation or mechanical wounding and identified hexenyl acetate as the predominant compound in these volatile blends. Subsequently, we examined the signaling role of this compound in attracting the parasitoid wasp (Aphidius colemani), a natural enemy of aphids. PRINCIPAL FINDINGS: This study conclusively establishes that jasmonates and C(6)-aldehydes play distinct roles in plant defense responses. The jasmonates are indispensable metabolites in mediating the activation of direct plant-defense responses, whereas the C(6)-aldehyes are not. On the other hand, hexenyl acetate, an acetylated C(6)-aldehyde, is the predominant wound-inducible volatile signal that mediates indirect defense responses by directing tritrophic (plant-herbivore-natural enemy) interactions. SIGNIFICANCE: The data suggest that jasmonates and hexenyl acetate play distinct roles in mediating direct and indirect plant-defense responses. The potential advantage of this \"division of labor\" is to ensure the most effective defense strategy that minimizes incurred damages at a reduced metabolic cost.", "link"=>"http://www.mendeley.com/research/distinct-roles-jasmonates-aldehydes-plantdefense-responses", "reader_count"=>125, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>37, "Student > Postgraduate"=>5, "Student > Master"=>13, "Other"=>7, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>37, "Student > Postgraduate"=>5, "Student > Master"=>13, "Other"=>7, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Engineering"=>1, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>99, "Chemistry"=>5, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>99}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>4}}, "reader_count_by_country"=>{"United States"=>4, "Spain"=>2, "New Zealand"=>1, "Canada"=>1, "Austria"=>1, "China"=>1, "Mexico"=>2, "South Africa"=>1, "Italy"=>1, "Uganda"=>1, "France"=>1, "Germany"=>2, "Nepal"=>1}, "group_count"=>5}

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  • {"files"=>["https://ndownloader.figshare.com/files/934233"], "description"=>"<p>Lesion development was monitored and compared between leaves from <i>aos-hpl</i> vs. <i>aos-HPL-OE</i> plants at 72h post inoculation (hpi) with conidia from either <i>B. cinerea</i> or from <i>A. brassicicola.</i> Each bar represents average lesion diameter±SD of 24 replicates for each genotype.</p>", "links"=>[], "tags"=>["necrotrophic", "fungi", "cinerea", "alternaria"], "article_id"=>604672, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g005", "stats"=>{"downloads"=>4, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Function_of_C_6_aldehydes_in_plant_protection_against_necrotrophic_fungi_Botrytis_cinerea_and_Alternaria_brassicicola_/604672", "title"=>"Function of C<sub>6</sub>-aldehydes in plant protection against necrotrophic fungi <i>Botrytis cinerea and Alternaria brassicicola</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:44:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/934094"], "description"=>"<p>Attraction of two-day old female leafminers to <i>aos-HPL-OE</i> versus <i>aos</i>-<i>hpl</i> plants was tested using glass Y-tube olfactometer. Each leafminer was introduced individually into the base of the Y-tube and its choice was recorded. The bar graph represents the numbers of herbivores examined and shows that they are equally attracted to the <i>aos</i>-<i>HPL-OE</i> and to the <i>aos-hpl</i> plants. One-tailed binomial tests were performed to determine the significance. (<i>P</i> = 0.443).</p>", "links"=>[], "tags"=>["leafminer"], "article_id"=>604539, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g003", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Choice_test_with_the_leafminer_Liriomyza_trifolii_/604539", "title"=>"Choice test with the leafminer (<i>Liriomyza trifolii)</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:43:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/934349"], "description"=>"<p>(A) Characterization and quantification of GLVs by adsorptive headspace collection and GC-MS analyses performed on three repeats of five independent biological replicates from intact and aphid infested <i>aos-hpl</i> and <i>aos-HPL-OE</i> genotypes show that hexenyl acetate is the predominant volatile produced in aphid infested plants with a functional <i>HPL</i>. (B) Volatile bioassays using glass Y-tube olfactometer was employed to determine the response of <i>A. colemani</i> to the volatile blend produced from mechanically wounded <i>aos-hpl</i> and <i>aos-HPL-OE</i> plant genotypes. The bar graph represents the number of parasitoids examined and shows that they are significantly attracted more to the wounded <i>aos</i>-<i>HPL-OE</i> than to the <i>aos-hpl</i> plants (<i>P</i> = 0.016). (C) Volatile bioassays using glass Y-tube olfactometer was employed to determine the response of <i>A. colemani</i> to the presence or absence of synthetic hexenyl acetate in chambers containing wounded <i>aos-hpl</i> plant genotype. The bar graph represents the number of parasitoids examined and shows that they are significantly attracted towards the chamber of wounded <i>aos-hpl</i> plants with hexenyl acetate-spotted filters as compared to the plant chamber containing the same plant genotype but with hexane-spotted filters as the control (<i>P</i> = 0.034). One-tailed binomial tests were used to determine significance.</p>", "links"=>[], "tags"=>["parasitoid", "wound-induced", "chemically", "synthesized", "hexenyl"], "article_id"=>604789, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g006", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Attraction_of_parasitoid_wasp_Aphidius_colemani_to_the_in_vivo_wound_induced_or_chemically_synthesized_hexenyl_acetate_/604789", "title"=>"Attraction of parasitoid wasp, <i>Aphidius colemani,</i> to the <i>in vivo</i> wound-induced or chemically synthesized hexenyl acetate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:44:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/934165"], "description"=>"<p>Lesion development was monitored and compared between leaves isolated from (A) <i>HPL-OE</i> vs. Col, (B) <i>aos</i>-<i>hpl</i> vs. <i>aos-HPL-OE</i>, (C) <i>gl-1</i> vs. <i>aos-hpl</i>, at 48, 72 or 96 hours post inoculation (hpi) with <i>B. cinerea</i> conidia. Each bar graph represents average lesion diameter±SD of 24 inoculated leaves. All leaves lacking jasmonates (<i>aos-hpl</i>, <i>aos-HPL-OE)</i> show larger lesions as compared to those with a functional AOS (Col, <i>HPL-OE</i>, <i>gl-1</i>). The lesion sizes were not affected by the presence or absence of HPL-derived metabolites. For comparison, representative photographs of each genotype 72 hpi is shown. Graphs are the means±SD of 24 replicates for each genotype. Bar = 1 cm. (D) Analyses of camalexin accumulation levels for leaves collected at 72 hpi (<i>gl-1</i>, <i>aos-hpl</i> and <i>aos-HPL-OE</i>) or 96 hpi (Col and <i>HPL-OE</i>) show negligible levels of camalexin in all plant genotypes with dysfunctional <i>AOS.</i> The <i>HPL-OE</i> lines contain 30% less camalexin than that in Col lines, potentially because of the reduced JA levels in these plants. Graphs are the means±SD of 24 replicates for each genotype. Within any given treatment, bars with different letters indicate significant differences (<i>P</i><0.005, Tukey's test).</p>", "links"=>[], "tags"=>["jas", "necrotrophic"], "article_id"=>604610, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g004", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Function_of_JAs_and_C_6_aldehydes_in_plant_protection_against_necrotrophic_fungus_Botrytis_cinerea_/604610", "title"=>"Function of JAs and C<sub>6</sub>-aldehydes in plant protection against necrotrophic fungus, <i>Botrytis cinerea.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:43:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/933998"], "description"=>"<p>(A) Choice bioassays performed on pairs of plant genotypes where a single <i>M. persicae</i> alate female was released in each cage containing the most comparable pair of genotypes. The initial nymph deposition preference was determined within 2 days of aphid release. Bar graphs represent the actual numbers of alates. One-tailed binomial tests were used to determine significance (<i>P</i><0.05). (B) Population increase of aphids (fecundity) upon the release of a newly deposited nymph on a single plant of indicated genotype during 15 days of reproduction. The graphs indicate the mean numbers of aphids per plant±SE. Each of the above-described tests was performed on ∼30 individual plants per genotype.</p>", "links"=>[], "tags"=>["peach", "aphid"], "article_id"=>604439, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g002", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Choice_and_no_choice_tests_with_the_green_peach_aphid_Myzus_persicae_/604439", "title"=>"Choice and no choice tests with the green peach aphid (<i>Myzus persicae</i>).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:42:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/933838"], "description"=>"<p>(A) Levels of C<sub>6</sub>-aldehydes, (B) JAs (JA+MeJA), and (C) 12-OPDA determined in non wounded (grey bar), or wounded leaves 2 hours after mechanical damage (black bar). Each measurement is derived from the mean±standard deviation (SD) of three independent biological replicates. (D) Characterization and quantification of GLVs by adsorptive headspace collection and GC-MS analyses performed on three repeats of three independent biological replicates from wounded and non wounded <i>Arabidopsis</i> genotypes show that hexenyl acetate is the predominant volatile produced in wounded leaves of plants with a functional <i>HPL</i>. Double-headed arrow represents a scale for signal intensity. (E) Analyses of the emission rate of hexenyl acetate in non wounded (grey bar) or mechanically wounded (black bar) <i>aos-HPL-OE</i> plants, performed three times on three independent biological replicates show that emission of hexenyl acetate is wound-inducible and transient.</p>", "links"=>[], "tags"=>["hpl-", "aos-branch", "pathways"], "article_id"=>604280, "categories"=>["Medicine", "Virology", "Biotechnology"], "users"=>["E. Wassim Chehab", "Roy Kaspi", "Tatyana Savchenko", "Heather Rowe", "Florence Negre-Zakharov", "Dan Kliebenstein", "Katayoon Dehesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0001904.g001", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Profiling_of_the_HPL_and_AOS_branch_pathways_metabolites_/604280", "title"=>"Profiling of the HPL- and AOS-branch pathways metabolites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 10:41:45"}

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  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
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  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
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  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"6", "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"=>"10", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
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  • {"unique-ip"=>"16", "full-text"=>"15", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"11", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"11", "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"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"6", "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"=>"11", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"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"=>"12"}
  • {"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"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"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"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"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"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"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"=>"2017", "month"=>"12"}
  • {"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"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}

Relative Metric

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