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{"title"=>"Expression patterns of genes involved in sugar metabolism and accumulation during apple fruit development", "type"=>"journal", "authors"=>[{"first_name"=>"Mingjun", "last_name"=>"Li", "scopus_author_id"=>"36514910400"}, {"first_name"=>"Fengjuan", "last_name"=>"Feng", "scopus_author_id"=>"35423657300"}, {"first_name"=>"Lailiang", "last_name"=>"Cheng", "scopus_author_id"=>"7403337037"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84863253119", "pui"=>"364373905", "doi"=>"10.1371/journal.pone.0033055", "isbn"=>"1932-6203", "sgr"=>"84863253119", "pmid"=>"22412983"}, "id"=>"584d028a-294f-32d4-868a-42967339b1ad", "abstract"=>"Both sorbitol and sucrose are imported into apple fruit from leaves. The metabolism of sorbitol and sucrose fuels fruit growth and development, and accumulation of sugars in fruit is central to the edible quality of apple. However, our understanding of the mechanisms controlling sugar metabolism and accumulation in apple remains quite limited. We identified members of various gene families encoding key enzymes or transporters involved in sugar metabolism and accumulation in apple fruit using homology searches and comparison of their expression patterns in different tissues, and analyzed the relationship of their transcripts with enzyme activities and sugar accumulation during fruit development. At the early stage of fruit development, the transcript levels of sorbitol dehydrogenase, cell wall invertase, neutral invertase, sucrose synthase, fructokinase and hexokinase are high, and the resulting high enzyme activities are responsible for the rapid utilization of the imported sorbitol and sucrose for fruit growth, with low levels of sugar accumulation. As the fruit continues to grow due to cell expansion, the transcript levels and activities of these enzymes are down-regulated, with concomitant accumulation of fructose and elevated transcript levels of tonoplast monosaccharide transporters (TMTs), MdTMT1 and MdTMT2; the excess carbon is converted into starch. At the late stage of fruit development, sucrose accumulation is enhanced, consistent with the elevated expression of sucrose-phosphate synthase (SPS), MdSPS5 and MdSPS6, and an increase in its total activity. Our data indicate that sugar metabolism and accumulation in apple fruit is developmentally regulated. This represents a comprehensive analysis of the genes involved in sugar metabolism and accumulation in apple, which will serve as a platform for further studies on the functions of these genes and subsequent manipulation of sugar metabolism and fruit quality traits related to carbohydrates.", "link"=>"http://www.mendeley.com/research/expression-patterns-genes-involved-sugar-metabolism-accumulation-during-apple-fruit-development-3", "reader_count"=>65, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>14, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>4, "Other"=>5, "Student > Master"=>12, "Student > Bachelor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>14, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>4, "Other"=>5, "Student > Master"=>12, "Student > Bachelor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>55, "Chemistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>55}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Belgium"=>2, "United States"=>1, "China"=>1, "Brazil"=>1}, "group_count"=>2}

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• {"id"=>"238591908996341761", "text"=>"#PLOS: Expression Patterns of Genes Involved in Sugar Metabolism and Accumulation during ... http://t.co/1t4CEj0C", "created_at"=>"2012-08-23T11:01:58Z", "user"=>"martinalzugaray", "user_name"=>"martín alzugaray", "user_profile_image"=>"http://a0.twimg.com/profile_images/1581710754/28_normal.jpg"}

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/343199", "https://ndownloader.figshare.com/files/343248", "https://ndownloader.figshare.com/files/343303", "https://ndownloader.figshare.com/files/343352", "https://ndownloader.figshare.com/files/343398", "https://ndownloader.figshare.com/files/343456", "https://ndownloader.figshare.com/files/343513", "https://ndownloader.figshare.com/files/343573"], "description"=>"<div><p>Both sorbitol and sucrose are imported into apple fruit from leaves. The metabolism of sorbitol and sucrose fuels fruit growth and development, and accumulation of sugars in fruit is central to the edible quality of apple. However, our understanding of the mechanisms controlling sugar metabolism and accumulation in apple remains quite limited. We identified members of various gene families encoding key enzymes or transporters involved in sugar metabolism and accumulation in apple fruit using homology searches and comparison of their expression patterns in different tissues, and analyzed the relationship of their transcripts with enzyme activities and sugar accumulation during fruit development. At the early stage of fruit development, the transcript levels of sorbitol dehydrogenase, cell wall invertase, neutral invertase, sucrose synthase, fructokinase and hexokinase are high, and the resulting high enzyme activities are responsible for the rapid utilization of the imported sorbitol and sucrose for fruit growth, with low levels of sugar accumulation. As the fruit continues to grow due to cell expansion, the transcript levels and activities of these enzymes are down-regulated, with concomitant accumulation of fructose and elevated transcript levels of tonoplast monosaccharide transporters (TMTs), <em>MdTMT1</em> and <em>MdTMT2</em>; the excess carbon is converted into starch. At the late stage of fruit development, sucrose accumulation is enhanced, consistent with the elevated expression of sucrose-phosphate synthase (SPS), <em>MdSPS5</em> and <em>MdSPS6</em>, and an increase in its total activity. Our data indicate that sugar metabolism and accumulation in apple fruit is developmentally regulated. This represents a comprehensive analysis of the genes involved in sugar metabolism and accumulation in apple, which will serve as a platform for further studies on the functions of these genes and subsequent manipulation of sugar metabolism and fruit quality traits related to carbohydrates.</p> </div>", "links"=>[], "tags"=>["patterns", "genes", "metabolism", "accumulation"], "article_id"=>127847, "categories"=>["Biochemistry", "Developmental Biology", "Cell Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.s001", "https://dx.doi.org/10.1371/journal.pone.0033055.s002", "https://dx.doi.org/10.1371/journal.pone.0033055.s003", "https://dx.doi.org/10.1371/journal.pone.0033055.s004", "https://dx.doi.org/10.1371/journal.pone.0033055.s005", "https://dx.doi.org/10.1371/journal.pone.0033055.s006", "https://dx.doi.org/10.1371/journal.pone.0033055.s007", "https://dx.doi.org/10.1371/journal.pone.0033055.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Expression_Patterns_of_Genes_Involved_in_Sugar_Metabolism_and_Accumulation_during_Apple_Fruit_Development/127847", "title"=>"Expression Patterns of Genes Involved in Sugar Metabolism and Accumulation during Apple Fruit Development", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-03-07 02:10:47"}
• {"files"=>["https://ndownloader.figshare.com/files/671272"], "description"=>"<p>Both sorbitol (Sor) and sucrose (Suc) are unloaded to the cell wall space between sieve element-companion cell complex (SE-CC) and parenchyma cells in fruit <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Zhang2\" target=\"_blank\">[14]</a>. Sor is taken up into parenchyma cells via sorbitol transporter (SOT). Suc is directly transported into parenchyma cells by plasma membrane-bound sucrose transporter (SUT), or converted to fructose (Fru) and glucose (Glc) in the cell wall space by cell wall invertase (CWINV), and then transported into the parenchyma cells by hexose transporter (HT). In the cytosol, Sor is converted to Fru by sorbitol dehydrogenase (SDH), while Suc can be converted to Fru and Glc by neutral invertase (NINV) or to Fru and UDP-glucose by sucrose synthase (SUSY). The resulting Glc and Fru can be phosphorylated to glucose 6-phsophate (G6P) and fructose 6-phosphate (F6P) by hexokinase (HK) and fructokinase (FK, specific for Fru). The conversions between F6P, G6P, G1P, and UDPG are catalyzed by phosphoglucoisomerase (PGI), phosphoglucomutase (PGM), and UDPG-pyrophosphorylase (UGP) in readily reversible reactions. The F6P produced in sugar metabolism enters glycolysis/TCA cycle to generate energy and intermediates for other processes. G1P is used for starch synthesis. UDPG can be used for cellulose synthesis or combined with F6P for re-synthesis of Suc via sucrose phosphate synthase (SPS) and sucrose-phosphatase (SPP). Most of the Fru, Glc and Suc that have not been metabolized are transported by special tonoplast transporters into vacuole for storage. Inside the vacuole, Suc can be also converted to Glc and Fru by vacuolar acid invertase (vAINV).</p>", "links"=>[], "tags"=>["metabolism", "accumulation"], "article_id"=>341763, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sugar_metabolism_and_accumulation_in_apple_fruit_1_14_/341763", "title"=>"Sugar metabolism and accumulation in apple fruit [1], [14].", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:29:23"}
• {"files"=>["https://ndownloader.figshare.com/files/671420"], "description"=>"<p>The tree was produced using MUSCLE and PhyML with the JTT amino acid substitution model, a discrete gamma model with 4 categories and an estimated shape parameter of 1.0. Bootstrapping was performed with 100 replicates. A, cell wall invertase (CWINV); B, neutral invertases (NINV), α and β type NINV according to Nonis et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Nonis1\" target=\"_blank\">[37]</a>; C, vacuolar acid invertase (vAINV); D; sucrose synthase (SUSY), different types according to Bieniawska et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Bieniawska1\" target=\"_blank\">[38]</a>; E, fructokinase (FK), cytosolic and plastid fructokinases in tomato according to Granot <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Granot1\" target=\"_blank\">[19]</a>; F, hexokinase (HK), different groups according to Karve et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Karve1\" target=\"_blank\">[39]</a>; G, Sucrose phosphate synthases (SPS), <i>Arabidopsis</i> types according to Lutfiyya et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Lutfiyya1\" target=\"_blank\">[40]</a>; H, Sucrose transporter (SUT), different groups according to Braun & Slewinski <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0033055#pone.0033055-Braun1\" target=\"_blank\">[41]</a>; I, tonoplast monosaccharide transporter (TMT); J, vacuolar glucose transporter (vGT).</p>", "links"=>[], "tags"=>["phylogeny", "genes", "encoding", "enzymes", "transporters", "metabolism", "accumulation", "lycopersicon"], "article_id"=>341901, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maximum_likelihood_phylogeny_of_Malus_genes_encoding_enzymes_and_transporters_involved_in_sugar_metabolism_and_accumulation_with_those_from_Arabidopsis_or_Lycopersicon_esculentum_/341901", "title"=>"Maximum likelihood phylogeny of <i>Malus</i> genes encoding enzymes and transporters involved in sugar metabolism and accumulation with those from <i>Arabidopsis or Lycopersicon esculentum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:31:41"}
• {"files"=>["https://ndownloader.figshare.com/files/671525"], "description"=>"<p>Quantitative RT-PCR was performed with gene-specific primers, except for <i>MdSDH2</i>-9 where a pair of universal primer was designed from the conserved cDNA region of <i>MdSDH2</i> to <i>MdSDH9</i>. For each sample, transcript levels were normalized with those of <i>Actin</i>, and the relative expression levels of each gene were obtained using the ddCT method while expression in 40-DAB-fruit was designated as ‘10’. Values are means of three replicates of the reverse transcribed RNA sample pooled from 5 biological replicates ± SD.</p>", "links"=>[], "tags"=>["mrna", "genes", "encoding", "enzymes", "metabolism"], "article_id"=>342014, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_mRNA_expression_for_genes_encoding_enzymes_involved_in_sugar_metabolism_including_MdSDHs_MdCWINVs_MdNINVs_MdvAINVs_MdSUSYs_MdFKs_MdHKs_MdSPSs_during_apple_fruit_development_/342014", "title"=>"Relative mRNA expression for genes encoding enzymes involved in sugar metabolism (including <i>MdSDHs</i>, <i>MdCWINVs</i>, <i>MdNINVs</i>, <i>MdvAINVs</i>, <i>MdSUSYs</i>, <i>MdFKs</i>, <i>MdHKs</i>, <i>MdSPSs</i>) during apple fruit development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:33:34"}
• {"files"=>["https://ndownloader.figshare.com/files/671683"], "description"=>"<p>Quantitative RT-PCR was performed with gene-specific primers. For each sample, transcript levels were normalized with those of <i>Actin</i>, and the relative expression levels of each gene were obtained using the ddCT method while expression in 40-DAB-fruit was designated as ‘10’. Values are means of three technical replicates of the reverse transcribed RNA sample pooled from 5 biological replicates ± SD.</p>", "links"=>[], "tags"=>["mrna", "genes", "encoding", "transporters"], "article_id"=>342172, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_mRNA_expression_for_genes_encoding_sugar_transporters_including_MdSOTs_MdSUTs_MdTMTs_and_MdvGTs_during_apple_fruit_development_/342172", "title"=>"Relative mRNA expression for genes encoding sugar transporters (including <i>MdSOTs</i>, <i>MdSUTs</i>, <i>MdTMTs</i> and <i>MdvGTs</i>) during apple fruit development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:36:12"}
• {"files"=>["https://ndownloader.figshare.com/files/671803"], "description"=>"<p>SDH: Sorbitol dehydrogenase; CWINV: Cell wall invertase; NINV: Neutral invertase; vAINV: Vacuolar acid invertase; SUSY: Sucrose synthase; FK: Fructokinase; HK: Hexokinase; SPS: Sucrose-phosphate synthase. Values are means of five replicates ± SD.</p>", "links"=>[], "tags"=>["enzymes", "metabolism"], "article_id"=>342296, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activities_of_key_enzymes_involved_in_sugar_metabolism_during_apple_fruit_development_/342296", "title"=>"Activities of key enzymes involved in sugar metabolism during apple fruit development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:38:16"}
• {"files"=>["https://ndownloader.figshare.com/files/671868"], "description"=>"<p>Values are means of five replicates ± SD.</p>", "links"=>[], "tags"=>["sorbitol", "sucrose", "fructose", "glucose", "6-phosphate"], "article_id"=>342357, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Concentrations_of_sorbitol_Sor_sucrose_Suc_fructose_Fru_glucose_Glc_fructose_6_phosphate_F6P_and_glucose_6_phosphate_G6P_during_apple_fruit_development_/342357", "title"=>"Concentrations of sorbitol (Sor), sucrose (Suc), fructose (Fru), glucose (Glc), fructose 6-phosphate (F6P) and glucose 6-phosphate (G6P) during apple fruit development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:39:17"}
• {"files"=>["https://ndownloader.figshare.com/files/671926"], "description"=>"<p>Values are means of five replicates ± SD.</p>", "links"=>[], "tags"=>["concentrations"], "article_id"=>342420, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Starch_concentrations_during_apple_fruit_development_/342420", "title"=>"Starch concentrations during apple fruit development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-07 00:40:20"}
• {"files"=>["https://ndownloader.figshare.com/files/671981"], "description"=>"<p>Values are means of three technical replicates of the reverse transcribed RNA sample pooled from 5 biological replicates ± SD. n/d means no expression was detected.</p><p>qRT-PCR was performed with gene-specific primers, except that a pair of universal primers was designed from the conserved cDNA region of <i>MdSDH2</i> to <i>MdSDH9</i> for the expression of <i>MdSDH2</i>-9. For each sample, transcript levels were normalized with those of <i>Actin</i>, and the relative expression levels of each gene were obtained using the ddCT method while expression in mature leaves was designated as ‘1’.</p>", "links"=>[], "tags"=>["mrna", "genes", "encoding", "enzymes", "metabolism", "mature"], "article_id"=>342466, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_relative_mRNA_expression_for_genes_encoding_enzymes_involved_in_sugar_metabolism_including_MdSDHs_MdCWINVs_MdNINVs_MdvAINVs_MdSUSYs_MdFKs_MdHKs_and_MdSPSs_among_mature_leaves_shoot_tips_young_fruit_40_DAB_and_mature_fruit_135_DAB_of_apple_/342466", "title"=>"Comparison of relative mRNA expression for genes encoding enzymes involved in sugar metabolism (including <i>MdSDHs</i>, <i>MdCWINVs</i>, <i>MdNINVs</i>, <i>MdvAINVs</i>, <i>MdSUSYs</i>, <i>MdFKs</i>, <i>MdHKs</i>, and <i>MdSPSs</i>) among mature leaves, shoot tips, young fruit (40 DAB) and mature fruit (135 DAB) of apple.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-07 00:41:06"}
• {"files"=>["https://ndownloader.figshare.com/files/672030"], "description"=>"<p>Values are means of three technical replicates of the reverse transcribed RNA sample pooled from 5 biological replicates ± SD.</p><p>qRT-PCR was performed with gene-specific primers. For each sample, transcript levels were normalized with those of <i>Actin</i>, and the relative expression levels of each gene were obtained using the ddCT method while expression in mature leaves was designated as ‘1.’</p>", "links"=>[], "tags"=>["mrna", "genes", "encoding", "sorbitol", "transporter", "sucrose", "tonoplast", "monosaccharide", "vacuolar", "glucose", "mature"], "article_id"=>342506, "categories"=>["Biochemistry", "Developmental Biology", "Plant Biology"], "users"=>["Mingjun Li", "Fengjuan Feng", "Lailiang Cheng"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033055.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_relative_mRNA_expression_for_genes_encoding_sorbitol_transporter_SOT_sucrose_transporter_SUT_tonoplast_monosaccharide_transporter_TMT_and_vacuolar_glucose_transporter_vGT_among_mature_leaves_shoot_tips_young_fruit_40_DAB_and_mature_fruit_13/342506", "title"=>"Comparison of relative mRNA expression for genes encoding sorbitol transporter (SOT), sucrose transporter (SUT), tonoplast monosaccharide transporter (TMT), and vacuolar glucose transporter (vGT) among mature leaves, shoot tips, young fruit (40 DAB) and mature fruit (135 DAB) of apple.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-07 00:41:46"}

PMC Usage Stats | Further Information

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• {"unique-ip"=>"16", "full-text"=>"22", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
• {"unique-ip"=>"21", "full-text"=>"20", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
• {"unique-ip"=>"14", "full-text"=>"16", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
• {"unique-ip"=>"22", "full-text"=>"21", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"10"}
• {"unique-ip"=>"17", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
• {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
• {"unique-ip"=>"23", "full-text"=>"24", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}

Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[322, 550, 671, 773, 864, 955, 1048, 1135, 1223, 1308, 1387, 1465, 1534, 1602, 1673, 1744, 1813, 1885, 1955, 2026, 2093, 2160, 2228, 2290, 2349]}, {"subject_area"=>"/Biology and life sciences/Agriculture", "average_usage"=>[323, 536, 657, 751, 847, 939, 1032, 1114, 1201, 1279, 1355, 1431, 1516, 1582, 1656, 1719, 1791, 1848, 1919, 2000, 2068, 2127, 2208, 2281, 2359]}, {"subject_area"=>"/Biology and life sciences/Plant science", "average_usage"=>[329, 543, 667, 773, 865, 963, 1066, 1149, 1233, 1323, 1411, 1500, 1588, 1661, 1732, 1803, 1887, 1978, 2057, 2138, 2203, 2283, 2363, 2419, 2493]}, {"subject_area"=>"/Physical sciences/Physics", "average_usage"=>[298, 476, 578, 665, 743, 821, 891, 962, 1036, 1108, 1174, 1240, 1312, 1371, 1430, 1494, 1551, 1609, 1673, 1736, 1795, 1857, 1913, 1976, 2035]}]}

F1000Prime