Physcomitrella patens DCL3 Is Required for 22–24 nt siRNA Accumulation, Suppression of Retrotransposon-Derived Transcripts, and Normal Development
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{"title"=>"Physcomitrella patens DCL3 is required for 22-24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development", "type"=>"journal", "authors"=>[{"first_name"=>"Hyun Cho", "last_name"=>"Sung", "scopus_author_id"=>"26661578800"}, {"first_name"=>"Charles", "last_name"=>"Addo-Quaye", "scopus_author_id"=>"11540967900"}, {"first_name"=>"Ceyda", "last_name"=>"Coruh", "scopus_author_id"=>"25931453100"}, {"first_name"=>"M. Asif", "last_name"=>"Arif", "scopus_author_id"=>"55994390800"}, {"first_name"=>"Zhaorong", "last_name"=>"Ma", "scopus_author_id"=>"55479129100"}, {"first_name"=>"Wolfgang", "last_name"=>"Frank", "scopus_author_id"=>"8640047500"}, {"first_name"=>"Michael J.", "last_name"=>"Axtell", "scopus_author_id"=>"6603457695"}], "year"=>2008, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"19096705", "sgr"=>"58149163280", "doi"=>"10.1371/journal.pgen.1000314", "scopus"=>"2-s2.0-58149163280", "pui"=>"354027903", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "issn"=>"15537390"}, "id"=>"c3f2ac2e-f87f-3e87-a938-e06ac3c12186", "abstract"=>"Endogenous 24 nt short interfering RNAs (siRNAs), derived mostly from intergenic and repetitive genomic regions, constitute a major class of endogenous small RNAs in flowering plants. Accumulation of Arabidopsis thaliana 24 nt siRNAs requires the Dicer family member DCL3, and clear homologs of DCL3 exist in both flowering and non-flowering plants. However, the absence of a conspicuous 24 nt peak in the total RNA populations of several non-flowering plants has raised the question of whether this class of siRNAs might, in contrast to the ancient 21 nt microRNAs (miRNAs) and 21-22 nt trans-acting siRNAs (tasiRNAs), be an angiosperm-specific innovation. Analysis of non-miRNA, non-tasiRNA hotspots of small RNA production within the genome of the moss Physcomitrella patens revealed multiple loci that consistently produced a mixture of 21-24 nt siRNAs with a peak at 23 nt. These Pp23SR loci were significantly enriched in transposon content, depleted in overlap with annotated genes, and typified by dense concentrations of the 5-methyl cytosine (5 mC) DNA modification. Deep sequencing of small RNAs from two independent Ppdcl3 mutants showed that the P. patens DCL3 homolog is required for the accumulation of 22-24 nt siRNAs, but not 21 nt siRNAs, at Pp23SR loci. The 21 nt component of Pp23SR-derived siRNAs was also unaffected by a mutation in the RNA-dependent RNA polymerase mutant Pprdr6. Transcriptome-wide, Ppdcl3 mutants failed to accumulate 22-24 nt small RNAs from repetitive regions while transcripts from two abundant families of long terminal repeat (LTR) retrotransposon-associated reverse transcriptases were up-regulated. Ppdcl3 mutants also displayed an acceleration of leafy gametophore production, suggesting that repetitive siRNAs may play a role in the development of P. patens. We conclude that intergenic/repeat-derived siRNAs are indeed a broadly conserved, distinct class of small regulatory RNAs within land plants.", "link"=>"http://www.mendeley.com/research/physcomitrella-patens-dcl3-required-2224-nt-sirna-accumulation-suppression-retrotransposonderived-tr", "reader_count"=>92, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>30, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>3, "Student > Master"=>12, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>30, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>3, "Student > Master"=>12, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>10, "Mathematics"=>1, "Agricultural and Biological Sciences"=>77, "Medicine and Dentistry"=>1, "Business, Management and Accounting"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>77}, "Computer Science"=>{"Computer Science"=>2}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Mathematics"=>{"Mathematics"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United States"=>4, "Norway"=>1, "Japan"=>1, "Brazil"=>1, "United Kingdom"=>2, "Switzerland"=>1, "Germany"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/451137", "https://ndownloader.figshare.com/files/451146", "https://ndownloader.figshare.com/files/451157", "https://ndownloader.figshare.com/files/451175", "https://ndownloader.figshare.com/files/451196", "https://ndownloader.figshare.com/files/451214", "https://ndownloader.figshare.com/files/451239", "https://ndownloader.figshare.com/files/451256", "https://ndownloader.figshare.com/files/451269"], "description"=>"<div><p>Endogenous 24 nt short interfering RNAs (siRNAs), derived mostly from intergenic and repetitive genomic regions, constitute a major class of endogenous small RNAs in flowering plants. Accumulation of <em>Arabidopsis thaliana</em> 24 nt siRNAs requires the Dicer family member DCL3, and clear homologs of <em>DCL3</em> exist in both flowering and non-flowering plants. However, the absence of a conspicuous 24 nt peak in the total RNA populations of several non-flowering plants has raised the question of whether this class of siRNAs might, in contrast to the ancient 21 nt microRNAs (miRNAs) and 21–22 nt <em>trans</em>-acting siRNAs (tasiRNAs), be an angiosperm-specific innovation. Analysis of non-miRNA, non-tasiRNA hotspots of small RNA production within the genome of the moss <em>Physcomitrella patens</em> revealed multiple loci that consistently produced a mixture of 21–24 nt siRNAs with a peak at 23 nt. These <em>Pp23SR</em> loci were significantly enriched in transposon content, depleted in overlap with annotated genes, and typified by dense concentrations of the 5-methyl cytosine (5 mC) DNA modification. Deep sequencing of small RNAs from two independent <em>Ppdcl3</em> mutants showed that the <em>P. patens DCL3</em> homolog is required for the accumulation of 22–24 nt siRNAs, but not 21 nt siRNAs, at <em>Pp23SR</em> loci. The 21 nt component of <em>Pp23SR</em>-derived siRNAs was also unaffected by a mutation in the RNA-dependent RNA polymerase mutant <em>Pprdr6</em>. Transcriptome-wide, <em>Ppdcl3</em> mutants failed to accumulate 22–24 nt small RNAs from repetitive regions while transcripts from two abundant families of long terminal repeat (LTR) retrotransposon-associated reverse transcriptases were up-regulated. <em>Ppdcl3</em> mutants also displayed an acceleration of leafy gametophore production, suggesting that repetitive siRNAs may play a role in the development of <em>P. patens</em>. We conclude that intergenic/repeat-derived siRNAs are indeed a broadly conserved, distinct class of small regulatory RNAs within land plants.</p></div>", "links"=>[], "tags"=>["patens", "nt", "sirna", "suppression", "retrotransposon-derived"], "article_id"=>148909, "categories"=>["Genetics", "Cell Biology", "Medicine", "Cancer"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000314.s001", "https://dx.doi.org/10.1371/journal.pgen.1000314.s002", "https://dx.doi.org/10.1371/journal.pgen.1000314.s003", "https://dx.doi.org/10.1371/journal.pgen.1000314.s004", "https://dx.doi.org/10.1371/journal.pgen.1000314.s005", "https://dx.doi.org/10.1371/journal.pgen.1000314.s006", "https://dx.doi.org/10.1371/journal.pgen.1000314.s007", "https://dx.doi.org/10.1371/journal.pgen.1000314.s008", "https://dx.doi.org/10.1371/journal.pgen.1000314.s009"], "stats"=>{"downloads"=>18, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Physcomitrella_patens_DCL3_Is_Required_for_22_24_nt_siRNA_Accumulation_Suppression_of_Retrotransposon_Derived_Transcripts_and_Normal_Development/148909", "title"=>"<em>Physcomitrella patens DCL3</em> Is Required for 22–24 nt siRNA Accumulation, Suppression of Retrotransposon-Derived Transcripts, and Normal Development", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-12-19 02:28:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/912856"], "description"=>"<p>Details can be found in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000314#pgen.1000314.s007\" target=\"_blank\">Table S3</a>. (A) Schematic of small RNA accumulation at <i>Pp23SR1</i>. The normalized abundances of corresponding small RNAs between 21 and 24 nts in length were plotted relative to the genomic sequence as a function of the positions of their 5′ ends using a bin size of 100 nts. “+” indicates small RNAs matching the positive strand of the genome, and “−” indicates small RNAs matching the minus strand. Relative positions of sequence features are indicated. Percentages refer to identities between inverted repeat arms. Dashed lines connect predicted LTRs but do not indicate full-length, intact elements. Gray boxes show positions of PCR amplicons used for methylation analyses. (B) Schematic of <i>Pp23SR2</i>, displayed as in A. (C) Schematic of <i>Pp23SR23</i>, displayed as in A. (D) Schematic of <i>Pp23SR35</i>, displayed as in A, except using 50 nt bins.</p>", "links"=>[], "tags"=>["genetics and genomics/epigenetics", "genetics and genomics/plant genetics and gene expression", "genetics and genomics/plant genomes and evolution", "plant biology", "plant biology/plant genetics and gene expression", "plant biology/plant genomes and evolution"], "article_id"=>583303, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g003", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_Pp23SR_loci_/583303", "title"=>"Examples of <i>Pp23SR</i> loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 00:55:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/912784"], "description"=>"<p>(A) The percentage of nucleotides with high similarity to <i>Helitron</i> rolling circle DNA transposons (left) and LTR-retrotransposons (right) is shown for the <i>P. patens</i> genome as a whole (black), the 52 <i>Pp21SR</i> loci (blue-filled), and the 48 <i>Pp23SR</i> loci (red-filled). The averages and standard deviations for ten cohorts of <i>Pp21SR</i> loci (blue-hollow) and <i>Pp23SR</i> (red-hollow) with randomized positions in the genome are also shown. (B) The fraction of <i>Pp21SR</i> (blue) and <i>Pp23SR</i> (red) loci which had at least some overlap with sequences similar to LTR-retrotransposons (filled), <i>Helitrons</i> (hollow), or both (vertical stripes) is shown.</p>", "links"=>[], "tags"=>["loci", "enriched", "transposon-derived"], "article_id"=>583236, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pp23SR_loci_are_enriched_in_transposon_derived_sequences_/583236", "title"=>"<i>Pp23SR</i> loci are enriched in transposon-derived sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 00:53:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/913288"], "description"=>"<p>(A) Amplification of the indicated loci from genomic DNA pre-treated with (+) or without (−) the 5-methyl cytosine specific endonuclease <i>Mcr</i>BC. WT: Wild Type. (B) The fraction of methylated cytosines in the symmetric CG context within the indicated loci was estimated by sequencing PCR products derived from bisulfite-converted genomic DNA. 5 mC: 5-methyl cytosine. Error bars indicate standard deviation. (C) As in B for cytosines in the symmetric CHG context. (D) As in B for cytosines in the asymmetric CHH context. Details of bisulfite sequencing data are given in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000314#pgen.1000314.s009\" target=\"_blank\">Table S5</a>. For all panels, where present, letters indicate distinct PCR products from different regions of a locus.</p>", "links"=>[], "tags"=>["5-methyl", "cytosine", "modification", "loci", "unaffected", "deletion"], "article_id"=>583732, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g007", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dense_5_methyl_cytosine_modification_at_Pp23SR_loci_is_largely_unaffected_by_deletion_of_PpDCL3_/583732", "title"=>"Dense 5-methyl cytosine modification at <i>Pp23SR</i> loci is largely unaffected by deletion of <i>PpDCL3</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 01:02:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/913180"], "description"=>"<p>(A) Size distribution of sequenced small RNAs, counted by abundance (number of reads). (B) Size distribution of sequenced small RNAs, counted by uniquely obtained sequences, regardless of their apparent abundance. (C) Histogram displaying median number of genome matches for sequenced small RNAs from the indicated samples. Replicates are shown as two identically colored bars.</p>", "links"=>[], "tags"=>["deletion", "nt", "rna"], "article_id"=>583630, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g006", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcriptome_wide_effects_of_PpDCL3_deletion_on_23_24_nt_RNA_accumulation_/583630", "title"=>"Transcriptome-wide effects of <i>PpDCL3</i> deletion on 23–24 nt RNA accumulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 01:00:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/913427"], "description"=>"<p>New <i>P. patens</i> small RNA libraries (NCBI GEO GSE12468).</p>", "links"=>[], "tags"=>["rna", "libraries", "geo"], "article_id"=>583882, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.t001", "stats"=>{"downloads"=>6, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_New_P_patens_small_RNA_libraries_NCBI_GEO_GSE12468_/583882", "title"=>"New <i>P. patens</i> small RNA libraries (NCBI GEO GSE12468).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-12-19 01:04:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/913091"], "description"=>"<p>(A) Abundance of sequenced small RNAs matching annotated small RNA loci from the indicated samples. NRPM: Normalized reads per million. (B) The ratio of the mean NRPM from the <i>Ppdcl3</i> samples over the mean of the two wild type replicates is plotted for the indicated loci as a function of mean abundance in the wild type. (C) Small RNA abundance from <i>Pp23SR</i> loci binned by small RNA length.</p>", "links"=>[], "tags"=>["accumulation", "nt", "sirnas"], "article_id"=>583544, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PpDCL3_is_required_for_the_accumulation_of_22_24_nt_siRNAs_from_Pp23SR_loci_/583544", "title"=>"<i>PpDCL3</i> is required for the accumulation of 22–24 nt siRNAs from <i>Pp23SR</i> loci.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 00:59:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/912713"], "description"=>"<p>(A) Distribution of small RNA lengths within the 52 of the 100 most prolific, uncharacterized small RNA producing loci dominated by 21 nt small RNAs. Each line represents the small RNA size distribution within a single locus. These are referred to as the <i>Pp21SR</i> loci. (B) As in A for the 48 of the 100 most prolific small RNA producing loci which were typified by a collection of 21–24 nt small RNAs. These are referred to as the <i>Pp23SR</i> loci. (C) Scatterplot depicting the normalized small RNA abundances vs. the sizes of the small RNA producing loci. Blue triangles, <i>Pp21SR</i> loci; red circles, <i>Pp23SR</i> loci. (D) The fraction of the normalized small RNA abundance emanating from the most abundant genomic strand is categorized for <i>Pp23SR</i> loci (red) and <i>Pp21SR</i> loci (blue). The subset of the <i>Pp21SR</i> loci where more than 50% of the abundance stemmed from small RNA dyads (where the same small RNA mapped to both genomic strands within a locus) are indicated by hollow blue bars, while solid blue bars indicate <i>Pp21SR</i> loci with less than 50% dyad abundances. None of the <i>Pp23SR</i> loci had a majority of small RNA abundance derived from such dyads. (E) Fractions of the genome (black), <i>Pp21SR</i> loci (blue), <i>Pp23SR</i> loci (red) and randomized controls (hollow bars) overlapping annotated <i>P. patens</i> genes. (F) Percent identity of inverted repeat arms vs. the percent of <i>Pp21SR</i> (blue) and <i>Pp23SR</i> (red) loci which those arms overlap. Black indicates percentage of the <i>P. patens</i> genome which overlaps inverted repeats, with error bars indicating the first quartile, median, and third quartiles of genome-wide inverted repeat identities. (G) Normalized small RNA abundance within inverted repeat stems vs. the total normalized abundance for <i>Pp21SR</i> (blue) and <i>Pp23SR</i> (red) loci. For loci which overlapped multiple inverted repeats, the one with the maximum abundance is shown. The position corresponding to <i>Pp23SR1</i> is highlighted.</p>", "links"=>[], "tags"=>["classes", "rna", "producing", "loci", "moss"], "article_id"=>583158, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_classes_of_small_RNA_producing_loci_in_the_moss_P_patens_/583158", "title"=>"Two classes of small RNA producing loci in the moss <i>P. patens</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 00:52:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/913359"], "description"=>"<p>(A) RT-PCR for the indicated reverse transcriptase families was performed using cDNA from the indicated strains. Templates prepared without addition of reverse transcriptase (-RT) were used as a control for DNA contamination. <i>PpActin</i> was used as a positive control. (B) Total small RNA abundance from the 452 genomic sites corresponding to the potential <i>PpRT3</i> amplicons, binned by length. NRPM: Normalized reads per million. (C) As in B for the 426 potential <i>PpRT6</i> amplicons.</p>", "links"=>[], "tags"=>["suppresses", "ltr", "retrotrasnsposon-associated"], "article_id"=>583812, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PpDCL3_suppresses_LTR_retrotrasnsposon_associated_reverse_transcriptases_/583812", "title"=>"<i>PpDCL3</i> suppresses LTR retrotrasnsposon-associated reverse transcriptases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 01:03:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/912970"], "description"=>"<p>Two-day old protonemata (1–2 mm in diameter) from the indicated strains were inoculated onto media with (A) or without (B) ammonium supplementation and scored for gametophore number every other day. Error bars indicate standard deviation (n = 9). (C) Representative colony morphologies after 12 days of growth. Bars indicate 1 mm. (D) RNA gel blot analysis for the indicated small RNAs. U6 snRNA was used as a loading control.</p>", "links"=>[], "tags"=>["accelerates", "gametophore"], "article_id"=>583423, "categories"=>["Genetics", "Medicine", "Plant Biology", "Infectious Diseases"], "users"=>["Sung Hyun Cho", "Charles Addo-Quaye", "Ceyda Coruh", "M. Asif Arif", "Zhaorong Ma", "Wolfgang Frank", "Michael J. Axtell"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000314.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_PpDCL3_accelerates_gametophore_production_/583423", "title"=>"Deletion of <i>PpDCL3</i> accelerates gametophore production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-12-19 00:57:03"}

PMC Usage Stats | Further Information

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Relative Metric

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