EST Analysis of Ostreococcus lucimarinus, the Most Compact Eukaryotic Genome, Shows an Excess of Introns in Highly Expressed Genes
- Publication Date
- May 14, 2008
- Journal
- PLOS ONE
- Authors
- William Lanier, Ahmed Moustafa, Debashish Bhattacharya & Josep M. Comeron
- Volume
- 3
- Issue
- 5
- Pages
- e2171
- DOI
- https://dx.plos.org/10.1371/journal.pone.0002171
- Publisher URL
- http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0002171
- PubMed
- http://www.ncbi.nlm.nih.gov/pubmed/18478122
- PubMed Central
- http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2367439
- Europe PMC
- http://europepmc.org/abstract/MED/18478122
- Web of Science
- 000262172800036
- Scopus
- 48249153013
- Mendeley
- http://www.mendeley.com/research/est-analysis-ostreococcus-lucimarinus-most-compact-eukaryotic-genome-shows-excess-introns-highly-exp
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CiteULike | Further Information
- {"link"=>{"url"=>"http://www.citeulike.org/user/dandaman/article/6657495"}, "post_time"=>"2010-02-12 13:39:33", "tag"=>["algae", "ostreococcus", "prasinophyta"], "linkout"=>[{"type"=>"DOI", "url"=>"http://dx.doi.org/10.1371/journal.pone.0002171"}, {"type"=>"Pubmed", "url"=>"http://view.ncbi.nlm.nih.gov/pubmed/18478122"}, {"type"=>"Hubmed", "url"=>"http://www.hubmed.org/display.cgi?uids=18478122"}], "username"=>"dandaman", "article_id"=>"6657495"}
- {"link"=>{"url"=>"http://www.citeulike.org/user/jpetrie/article/3308390"}, "post_time"=>"2008-09-21 12:01:54", "tag"=>"microalgae", "linkout"=>[{"type"=>"URL", "url"=>"http://www.ncbi.nlm.nih.gov/pubmed/18478122"}, {"type"=>"DOI", "url"=>"http://dx.doi.org/10.1371/journal.pone.0002171"}], "username"=>"jpetrie", "article_id"=>"3308390"}
Mendeley | Further Information
{"title"=>"EST analysis of Ostreococcus lucimarinus, the most compact eukaryotic genome, shows an excess of introns in highly expressed genes", "type"=>"journal", "authors"=>[{"first_name"=>"William", "last_name"=>"Lanier", "scopus_author_id"=>"56212312100"}, {"first_name"=>"Ahmed", "last_name"=>"Moustafa", "scopus_author_id"=>"55251149600"}, {"first_name"=>"Debashish", "last_name"=>"Bhattacharya", "scopus_author_id"=>"7201931909"}, {"first_name"=>"Josep M.", "last_name"=>"Comeron", "scopus_author_id"=>"6701860658"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"18478122", "sgr"=>"48249153013", "scopus"=>"2-s2.0-48249153013", "isbn"=>"10.1371/journal.pone.0002171", "doi"=>"10.1371/journal.pone.0002171", "pui"=>"352068491", "issn"=>"19326203"}, "id"=>"748cf7b7-8b63-31dd-bd0c-c0e74d494641", "abstract"=>"Background: The genome of the pico-eukaryotic (bacterial-sized) prasinophyte green alga Ostreococcus lucimarinus has one of the highest gene densities known in eukaryotes, yet it contains many introns. Phylogenetic studies suggest this unusually compact genome (13.2 Mb) is an evolutionarily derived state among prasinophytes. The presence of introns in the highly reduced O. lucimarinus genome appears to be in opposition to simple explanations of genome evolution based on unidirectional tendencies, either neutral or selective. Therefore, patterns of intron retention in this species can potentially provide insights into the forces governing intron evolution. Methodology/Principal Findings: Here we studied intron features and levels of expression in O. lucimarinus using expressed sequence tags (ESTs) to annotate the current genome assembly. ESTs were assembled into unigene clusters that were mapped back to the O. lucimarinus Build 2.0 assembly using BLAST and the level of gene expression was inferred from the number of ESTs in each cluster. We find a positive correlation between expression levels and both intron number (R鈥?鈥?0.0893, p鈥?鈥?0.0005) and intron density (number of introns/kb of CDS; R鈥?鈥?0.0753, p鈥?鈥?0.005). Conclusions/Significance: In a species with a genome that has been recently subjected to a great reduction of non-coding DNA, these results imply the existence of selective/functional roles for introns that are principally detectable in highly expressed genes. In these cases, introns are likely maintained by balancing the selective forces favoring their maintenance with other mutational and/or selective forces acting on genome size.", "link"=>"http://www.mendeley.com/research/est-analysis-ostreococcus-lucimarinus-most-compact-eukaryotic-genome-shows-excess-introns-highly-exp", "reader_count"=>46, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>9, "Student > Doctoral Student"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>15, "Student > Master"=>3, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>9, "Student > Doctoral Student"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>15, "Student > Master"=>3, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>35, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>35}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1, "United States"=>1, "Egypt"=>1, "Brazil"=>1, "Chile"=>2, "France"=>1, "Portugal"=>1}, "group_count"=>2}CrossRef
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Scopus | Further Information
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Journal Comments | Further Information
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/efbd9a81-aef9-4109-86b6-8051f11ec001", "title"=>"Referee Comments: Referee 1", "body"=>"Referee 1's Review:\n\n**********\nN.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication, the manuscript has been revised in light of these comments and to address other editorial requirements.\n*********\n\nThe data is novel and in an important field. However, as the average ESTs difference in expression between both groups (wit or without introns) is only of 1.39 ESTs (Fig. 2), it will be necessary to rule out a bias in the composition of the EST library towards longer transcripts if the length of the groups is different. I ask for the length of the transcripts of both groups becompared. \n\nThe R for the relationship of expression with length of transcripts is stronger than for the expression with introns. \n\nI am nearly an illiterate in statistics, so I did not evaluate the statistics of the manuscript. \n\nThe senior author has a previous report in which he found a positive correlation between introns and increased gene expression in humans, Ref 26. This report has not been confirmed yet in animals. Although in D. Melanogaster in Table 1 of the paper by Fahey and Higgins, J. Mol. Evol. 2007; 65:349-357; there is a positive correlation. \n\nIn plant it seems that highly expressed genes have more introns. I suggest including this information in the discussion. \n\nThe mechanism postulated in the discussion is an educated guess. \n\nPlease edit freely my commentsRemarks for the AuthorOstreococcus organisms, are the smallest known free-living eukaryotes. They have the most gene packed genomes among free-living taxa, in part due to extensive reduction of intergenic regions. It is assumed that these small nuclear genomes of Prasinophyta, a class of green algae where ostreococcus lucimarinus belongs, are evolutionarly derived rather than ancestral. \nOstreococcus is an interesting organism where to study questions on intron evolution. \nContrary to yeast S. cerevisiae compact genome in which a few intron-containing genes (4 %) produce nearly a third of the total mRNA transcripts, ostreococcus lucimarinus introns are present in an estimated 20-25% of transcripts. \n\nIn this study the authors have found a positive correlation between intron presence or intron density and increased gene expression in ostreococcus lucimarinus. \n\nThis positive correlation, in a species with a genome devoid of the majority of non coding DNA, suggests a non-random pattern for the distribution of introns with respect to gene expression. \n\nThis is an interesting paper providing useful data in the still unresolved mechanisms that govern splioceosomal intron evolution. Intron evolution is a matter of great interest in the study of genome evolution as a whole (Roy and Gilbert, Nature Reviews 2006). \n\nHowever, I would like to see more information for the statistical tests reported, and an extended discussion about highly expressed genes and introns in other organisms. \n\nGeneral\n\n1. The authors report a positive correlation between intron presence and increased expression (R= + 0.0984, p>0.0005) that was maintained, although with a higher p value, when intron number was replaced by intron density (R= + 0.0844, p<0.005), accounting for more introns being found in longer transcripts. \n\nTo replace intron number by intron density was important because a stronger positive correlation was found in all analysis between gene expression and both assembled cluster length (R= 0.4869, p<0.005) and corresponding longest open reading frame (R= 0,4835, p<0.0005). \n\nOn the other hand, as it is plausible that longer mRNA sequences are overrepresented in ESTs databases, as they take more time to decay. I would like the authors to provide information on the length of the assembled cluster length and longest open reading frame for both groups of clusters the cluster laking introns and for the cluster containing intron. \n\nIt has been suggested that length of transcripts should be accounted for when EST data are being used to estimate expression levels. (Munoz et al, 2004). The data correlation between high expression level and intron density will be strengthen if the length of the transcripts is taken into account for the estimation of expression levels. \n\n2. Ostreococcus lucimarinus introns are present in an estimated 20-25% of transcripts, but in Table 1, the percentage of clusters with introns is a little lover 16% (262 out of 1647). Please could you discuss. \n\n3. Please, it will be interesting to discuss the following published information in the context of your finding. \n\n- In plants (arabidopsis and oryza) highly expressed genes have more and longer introns (Ren et al, 2006). \n\n- The negative correlation between gene expression level and intron density in C. elegans and D. melanogaster (Fahey and Higgins, 2007). \n\n- The lack of correlation between intron density and gene expression in C. elegans and H. sapiens reported by Castillo-Davies et al, 2002) \n\n- The compactness of human housekeeping genes (Eisenberg and Levanon, 2003) \n\n- Your finding of highly expressed genes have more introns in humans (Ref. 26) \n\nSpecific \n\nAbstract \n\n1. The p value (p= < 0.0001) of the correlation R= 0.0984 between expression levels and intron number in the abstract is different from the p value in the Results section and in table 2 (p< 0.0005). \n\n2. The p value (p= 0.0006) of the correlation R= 0.0844 between expression levels and intron density in the abstract is different from the p value in the Results section and in table 2 (p< 0.005). \n\nIntroduction \n\n1. Figure 1 provides no information related to the core of the study. Please considerer taking it out. \n\n2. Please provide a reference for the paragraph. \"the general positive relationship between introns and intergenic size, and ultimately genome size, observed across a broad range of eukaryotes. \n\nResults \nPercentage values have either one or two decimals. One decimal should suffice. \n\nFigure Legends \n\nAlthough it can be found in Table 1 please provide the n for the groups. \n\nTable 1. \n\n1. The ratio of unigene clusters mapped per genes predicted (Map/Predicted ) values will be better display as % of unigene clusters mapped per genes predicted (21,4 instead of 0.2135 in Chr. 1, etc.) as in the results section. \n\n2. \"Introns found in mapped clusters\" and \"introns found\" mining is not as clear as \"mapped cluster with introns\" and \"Clusters with introns\". \n\nReferences \nMunoz et al, BMC genomics. 2004; 5:30 \nRen et al, TRENDS in Genetics. 2006; 22:528-532 \nFahey and Higgins, J. Mol. Evol. 2007; 65:349-357 \nDavies et al, Nature Genetics, 2002; 31:415-418 \nEisenberg and Levanon, TRENDS in Genetics. 2003; 19:362-365 ", "isRemoved"=>false, "created"=>"2008-05-16T21:57:09Z", "lastModified"=>"2008-05-16T21:57:09Z", "creator"=>{"userId"=>"80539"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002171", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-05-16T21:57:09Z", "replies"=>[]}
- {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/eff5c592-f9c0-4cfd-bc48-80cc908025b7", "title"=>"good explanation for intron number, but how about the length", "body"=>"I am very exciting to see that the authors have connected the excess of introns in highly expressed Ostreococcus genes to the lower number of nuclear pores per nucleus. Although this takes only a few sentenses in their discussion, it is really an advance. It is much more reasonable than the assumption that introns may have undiscovered regulatory elements that may promote the expression of their host genes. As I see, this is a very hopeful explanation for the retention of introns in highly expressed genes in plants and microorganisms.\r\n\r\nHowever, the explanation for longer intron length in highly expressed genes is not so satisfactory. Splicing is enough for the attachment of export-related proteins to mRNA, I do not know any evidence for the necessity of longer length. And it is the same case for NMD. I am looking forwards to more detailed discussion on intron length if the authors know some related references.\r\n\r\nDeng-Ke Niu\r\nCollege of Life Sciences\r\nBeijing Normal University\r\nBeijing, 100875\r\nP. R. China\r\nhttp://cmb.bnu.edu.cn/teachers/niudk_files/niudk_e.htm\r\ndkniu@bnu.edu.cn, dengkeniu@hotmail.com, dengkeniu@sina.com", "isRemoved"=>false, "created"=>"2008-05-21T16:32:39Z", "lastModified"=>"2008-05-21T16:32:39Z", "creator"=>{"userId"=>"35529"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002171", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2008-05-21T16:32:39Z", "replies"=>[]}
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- {"month"=>"4", "year"=>"2013", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"5", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"29"}
- {"month"=>"6", "year"=>"2013", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"7", "year"=>"2013", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"8", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"9", "year"=>"2013", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"24"}
- {"month"=>"10", "year"=>"2013", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"24"}
- {"month"=>"11", "year"=>"2013", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"26"}
- {"month"=>"12", "year"=>"2013", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"1", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"2", "year"=>"2014", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"3", "year"=>"2014", "pdf_views"=>"0", "xml_views"=>"3", "html_views"=>"12"}
- {"month"=>"4", "year"=>"2014", "pdf_views"=>"3", "xml_views"=>"2", "html_views"=>"24"}
- {"month"=>"5", "year"=>"2014", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"20"}
- {"month"=>"6", "year"=>"2014", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"15"}
- {"month"=>"7", "year"=>"2014", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"33"}
- {"month"=>"8", "year"=>"2014", "pdf_views"=>"3", "xml_views"=>"2", "html_views"=>"20"}
- {"month"=>"9", "year"=>"2014", "pdf_views"=>"2", "xml_views"=>"1", "html_views"=>"14"}
- {"month"=>"10", "year"=>"2014", "pdf_views"=>"1", "xml_views"=>"1", "html_views"=>"64"}
- {"month"=>"11", "year"=>"2014", "pdf_views"=>"2", "xml_views"=>"2", "html_views"=>"22"}
- {"month"=>"12", "year"=>"2014", "pdf_views"=>"7", "xml_views"=>"2", "html_views"=>"18"}
- {"month"=>"1", "year"=>"2015", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"2", "year"=>"2015", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"3", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"17"}
- {"month"=>"4", "year"=>"2015", "pdf_views"=>"2", "xml_views"=>"1", "html_views"=>"15"}
- {"month"=>"5", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"6", "year"=>"2015", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"7", "year"=>"2015", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"8", "year"=>"2015", "pdf_views"=>"1", "xml_views"=>"2", "html_views"=>"12"}
- {"month"=>"9", "year"=>"2015", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"65"}
- {"month"=>"10", "year"=>"2015", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"17"}
- {"month"=>"11", "year"=>"2015", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"8"}
- {"month"=>"12", "year"=>"2015", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"19"}
- {"month"=>"1", "year"=>"2016", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"16"}
- {"month"=>"2", "year"=>"2016", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"27"}
- {"month"=>"3", "year"=>"2016", "pdf_views"=>"5", "xml_views"=>"1", "html_views"=>"19"}
- {"month"=>"4", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"27"}
- {"month"=>"5", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"7"}
- {"month"=>"6", "year"=>"2016", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"7", "year"=>"2016", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"9"}
- {"month"=>"8", "year"=>"2016", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"20"}
- {"month"=>"9", "year"=>"2016", "pdf_views"=>"6", "xml_views"=>"0", "html_views"=>"37"}
- {"month"=>"10", "year"=>"2016", "pdf_views"=>"8", "xml_views"=>"0", "html_views"=>"13"}
- {"month"=>"11", "year"=>"2016", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"20"}
- {"month"=>"12", "year"=>"2016", "pdf_views"=>"7", "xml_views"=>"0", "html_views"=>"21"}
- {"month"=>"1", "year"=>"2017", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"14"}
- {"month"=>"2", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"27"}
- {"month"=>"3", "year"=>"2017", "pdf_views"=>"0", "xml_views"=>"1", "html_views"=>"20"}
- {"month"=>"4", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"18"}
- {"month"=>"5", "year"=>"2017", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"11"}
- {"month"=>"6", "year"=>"2017", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"28"}
- {"month"=>"7", "year"=>"2017", "pdf_views"=>"3", "xml_views"=>"1", "html_views"=>"14"}
- {"month"=>"8", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"9", "year"=>"2017", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"5"}
- {"month"=>"10", "year"=>"2017", "pdf_views"=>"6", "xml_views"=>"1", "html_views"=>"29"}
- {"month"=>"11", "year"=>"2017", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"17"}
- {"month"=>"12", "year"=>"2017", "pdf_views"=>"6", "xml_views"=>"1", "html_views"=>"18"}
- {"month"=>"1", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"10"}
- {"month"=>"2", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"3"}
- {"month"=>"3", "year"=>"2018", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"9"}
- {"month"=>"4", "year"=>"2018", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"7"}
- {"month"=>"5", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"7"}
- {"month"=>"6", "year"=>"2018", "pdf_views"=>"17", "xml_views"=>"1", "html_views"=>"3"}
- {"month"=>"7", "year"=>"2018", "pdf_views"=>"3", "xml_views"=>"3", "html_views"=>"10"}
- {"month"=>"8", "year"=>"2018", "pdf_views"=>"6", "xml_views"=>"1", "html_views"=>"7"}
- {"month"=>"9", "year"=>"2018", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"0"}
- {"month"=>"10", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"1", "html_views"=>"1"}
- {"month"=>"11", "year"=>"2018", "pdf_views"=>"0", "xml_views"=>"0", "html_views"=>"2"}
- {"month"=>"12", "year"=>"2018", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"0"}
- {"month"=>"1", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"2"}
- {"month"=>"2", "year"=>"2019", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"1"}
- {"month"=>"3", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"1"}
- {"month"=>"4", "year"=>"2019", "pdf_views"=>"4", "xml_views"=>"0", "html_views"=>"4"}
- {"month"=>"5", "year"=>"2019", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"1"}
- {"month"=>"6", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"4"}
- {"month"=>"7", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"3"}
- {"month"=>"8", "year"=>"2019", "pdf_views"=>"5", "xml_views"=>"0", "html_views"=>"5"}
- {"month"=>"9", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"0"}
- {"month"=>"10", "year"=>"2019", "pdf_views"=>"2", "xml_views"=>"0", "html_views"=>"0"}
- {"month"=>"11", "year"=>"2019", "pdf_views"=>"3", "xml_views"=>"0", "html_views"=>"1"}
- {"month"=>"12", "year"=>"2019", "pdf_views"=>"1", "xml_views"=>"0", "html_views"=>"0"}
PMC Usage Stats | Further Information
- {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"12", "unique-ip"=>"9", "pdf"=>"4", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"11", "year"=>"2010", "pdf"=>"4", "unique-ip"=>"10", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"12", "unique-ip"=>"11", "pdf"=>"4", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2010", "pdf"=>"0", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"6", "unique-ip"=>"7", "pdf"=>"2", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "year"=>"2010", "pdf"=>"2", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"2", "unique-ip"=>"6", "pdf"=>"4", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2010", "pdf"=>"5", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"3", "unique-ip"=>"3", "pdf"=>"1", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"2", "year"=>"2010", "pdf"=>"1", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"2", "pdf"=>"0", "year"=>"2010", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2010", "pdf"=>"1", "unique-ip"=>"4", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "unique-ip"=>"6", "pdf"=>"1", "year"=>"2011", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"2"}
- {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"3", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"6", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"1"}
- {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"1", "unique-ip"=>"2", "pdf"=>"1", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2011", "pdf"=>"1", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"3", "unique-ip"=>"6", "pdf"=>"2", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"1", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"2", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"1", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2011", "pdf"=>"2", "unique-ip"=>"2", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"3", "pdf"=>"3", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"3", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"2", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"3", "pdf"=>"2", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"2", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "unique-ip"=>"4", "pdf"=>"0", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2012", "pdf"=>"1", "unique-ip"=>"2", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "unique-ip"=>"6", "pdf"=>"0", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2012", "pdf"=>"2", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "unique-ip"=>"3", "pdf"=>"2", "year"=>"2012", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"13", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "year"=>"2008", "pdf"=>"2", "unique-ip"=>"0", "figure"=>"39", "scanned-summary"=>"24", "supp-data"=>"24"}
- {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"24", "unique-ip"=>"24", "pdf"=>"12", "year"=>"2008", "figure"=>"7", "scanned-summary"=>"0", "supp-data"=>"2"}
- {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"21", "year"=>"2008", "pdf"=>"12", "unique-ip"=>"19", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"10", "month"=>"8", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"4", "unique-ip"=>"0", "pdf"=>"2", "year"=>"2008", "figure"=>"32", "scanned-summary"=>"16", "supp-data"=>"20"}
- {"month"=>"9", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"4", "year"=>"2008", "pdf"=>"5", "unique-ip"=>"8", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"10", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "unique-ip"=>"12", "pdf"=>"6", "year"=>"2008", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"11", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"14", "year"=>"2008", "pdf"=>"5", "unique-ip"=>"13", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"12", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"8", "unique-ip"=>"8", "pdf"=>"3", "year"=>"2008", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"1", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"9", "year"=>"2009", "pdf"=>"7", "unique-ip"=>"13", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"2", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"14", "unique-ip"=>"17", "pdf"=>"3", "year"=>"2009", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"2"}
- {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"9", "year"=>"2009", "pdf"=>"6", "unique-ip"=>"8", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"14", "unique-ip"=>"14", "pdf"=>"4", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"7", "year"=>"2009", "pdf"=>"3", "unique-ip"=>"8", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
- {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"8", "unique-ip"=>"11", "pdf"=>"7", "year"=>"2009", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"1"}
- {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"17", "year"=>"2009", "pdf"=>"6", "unique-ip"=>"19", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
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Relative Metric
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