Misregulation of AUXIN RESPONSE FACTOR 8 Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis
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{"title"=>"Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis", "type"=>"journal", "authors"=>[{"first_name"=>"Florence", "last_name"=>"Jay", "scopus_author_id"=>"24577289500"}, {"first_name"=>"Yu", "last_name"=>"Wang", "scopus_author_id"=>"12244754500"}, {"first_name"=>"Agnès", "last_name"=>"Yu", "scopus_author_id"=>"25926195400"}, {"first_name"=>"Ludivine", "last_name"=>"Taconnat", "scopus_author_id"=>"6603661268"}, {"first_name"=>"Sandra", "last_name"=>"Pelletier", "scopus_author_id"=>"7103284400"}, {"first_name"=>"Vincent", "last_name"=>"Colot", "scopus_author_id"=>"6701570802"}, {"first_name"=>"Jean Pierre", "last_name"=>"Renou", "scopus_author_id"=>"7005194295"}, {"first_name"=>"Olivier", "last_name"=>"Voinnet", "scopus_author_id"=>"6701861200"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-79958047255", "doi"=>"10.1371/journal.ppat.1002035", "sgr"=>"79958047255", "isbn"=>"1553-7374 (Electronic)\\n1553-7366 (Linking)", "pmid"=>"21589905", "issn"=>"15537366", "pui"=>"361895948"}, "id"=>"500f8cea-fc0f-3af7-986d-1288c1c6af3d", "abstract"=>"In Arabidopsis, micro (mi)RNAs and trans-acting (ta-si)RNAs synthesized directly or indirectly through the DICER-LIKE-1 (DCL1) ribonuclease have roles in patterning and hormonal responses, while DCL2,3,4-dependent small-interfering (si)RNAs are mainly involved in silencing of transposable elements and antiviral defense. Viral suppressors of RNA silencing (VSRs) produced by phytoviruses to counter plant defense may perturb plant developmental programs because of the collision of their inhibitory effects with the regulatory action of endogenous miRNAs and ta-siRNAs. This could explain the similar developmental aberrations displayed by Arabidopsis miRNA/ta-siRNA pathway mutants, including dcl1, and by some VSR-expressing plants. Nonetheless, the molecular bases for these morphological aberrations have remained mysterious, and their contribution to viral disease symptoms/virulence unexplored. The extent of VSR inhibitory actions to other types of endogenous small RNAs remains also unclear. Here, we present an in-depth analysis of transgenic Arabidopsis expressing constitutively HcPro, P19 and P15, three unrelated VSRs. We show that VSR expression has comparable, yet modest effects on known miRNA and ta-siRNA target RNA levels, similar to those observed using an hypomorphic dcl1 mutation. However, by combining results of transcriptome studies with deep-sequencing data from immuno-precipitated small RNAs, additional, novel endogenous targets of miRNA and ta-siRNA were identified, unraveling an unsuspected complexity in the origin and scope-of-action of these molecules. Other stringent analyses pinpointed misregulation of the miR167 target AUXIN RESPONSE FACTOR 8 (ARF8) as a major cause for the developmental aberrations exhibited by VSR transgenic plants, but also for the phenotypes induced during normal viral infection caused by the HcPro-encoding Turnip mosaic virus (TuMV). Neither RNA silencing, its suppression by VSRs, nor the virulence/accumulation of TuMV was altered by mutations in ARF8. These findings have important implications for our understanding of viral disease symptoms and small RNA-directed regulation of plant growth/development.", "link"=>"http://www.mendeley.com/research/misregulation-auxin-response-factor-8-underlies-developmental-abnormalities-caused-three-distinct-vi", "reader_count"=>122, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>12, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>35, "Student > Postgraduate"=>7, "Student > Master"=>14, "Other"=>2, "Student > Bachelor"=>6, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>12, "Student > Doctoral Student"=>8, "Researcher"=>35, "Student > Ph. D. Student"=>35, "Student > Postgraduate"=>7, "Student > Master"=>14, "Other"=>2, "Student > Bachelor"=>6, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>105, "Social Sciences"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>105}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Argentina"=>2, "Norway"=>1, "United States"=>1, "Japan"=>1, "United Kingdom"=>2, "Slovenia"=>1, "Portugal"=>1}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/389303", "https://ndownloader.figshare.com/files/389333", "https://ndownloader.figshare.com/files/389338", "https://ndownloader.figshare.com/files/389348", "https://ndownloader.figshare.com/files/389355", "https://ndownloader.figshare.com/files/389360", "https://ndownloader.figshare.com/files/389368", "https://ndownloader.figshare.com/files/389374", "https://ndownloader.figshare.com/files/389414", "https://ndownloader.figshare.com/files/389428", "https://ndownloader.figshare.com/files/389441", "https://ndownloader.figshare.com/files/389453", "https://ndownloader.figshare.com/files/389461", "https://ndownloader.figshare.com/files/389470", "https://ndownloader.figshare.com/files/389477", "https://ndownloader.figshare.com/files/389483", "https://ndownloader.figshare.com/files/389528", "https://ndownloader.figshare.com/files/389553"], "description"=>"<div><p>In Arabidopsis, micro (mi)RNAs and <em>trans</em>-acting (ta-si)RNAs synthesized directly or indirectly through the DICER-LIKE-1 (DCL1) ribonuclease have roles in patterning and hormonal responses, while DCL2,3,4-dependent small-interfering (si)RNAs are mainly involved in silencing of transposable elements and antiviral defense. Viral suppressors of RNA silencing (VSRs) produced by phytoviruses to counter plant defense may perturb plant developmental programs because of the collision of their inhibitory effects with the regulatory action of endogenous miRNAs and ta-siRNAs. This could explain the similar developmental aberrations displayed by Arabidopsis miRNA/ta-siRNA pathway mutants, including <em>dcl1</em>, and by some VSR-expressing plants. Nonetheless, the molecular bases for these morphological aberrations have remained mysterious, and their contribution to viral disease symptoms/virulence unexplored. The extent of VSR inhibitory actions to other types of endogenous small RNAs remains also unclear. Here, we present an in-depth analysis of transgenic Arabidopsis expressing constitutively HcPro, P19 and P15, three unrelated VSRs. We show that VSR expression has comparable, yet modest effects on known miRNA and ta-siRNA target RNA levels, similar to those observed using an hypomorphic <em>dcl1</em> mutation. However, by combining results of transcriptome studies with deep-sequencing data from immuno-precipitated small RNAs, additional, novel endogenous targets of miRNA and ta-siRNA were identified, unraveling an unsuspected complexity in the origin and scope-of-action of these molecules. Other stringent analyses pinpointed misregulation of the miR167 target AUXIN RESPONSE FACTOR 8 (ARF8) as a major cause for the developmental aberrations exhibited by VSR transgenic plants, but also for the phenotypes induced during normal viral infection caused by the HcPro-encoding <em>Turnip mosaic virus</em> (TuMV). Neither RNA silencing, its suppression by VSRs, nor the virulence/accumulation of TuMV was altered by mutations in <em>ARF8</em>. These findings have important implications for our understanding of viral disease symptoms and small RNA-directed regulation of plant growth/development.</p> </div>", "links"=>[], "tags"=>["misregulation", "underlies", "abnormalities", "caused", "viral", "suppressors", "arabidopsis"], "article_id"=>136876, "categories"=>["Cell Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.s001", "https://dx.doi.org/10.1371/journal.ppat.1002035.s002", "https://dx.doi.org/10.1371/journal.ppat.1002035.s003", "https://dx.doi.org/10.1371/journal.ppat.1002035.s004", "https://dx.doi.org/10.1371/journal.ppat.1002035.s005", "https://dx.doi.org/10.1371/journal.ppat.1002035.s006", "https://dx.doi.org/10.1371/journal.ppat.1002035.s007", "https://dx.doi.org/10.1371/journal.ppat.1002035.s008", "https://dx.doi.org/10.1371/journal.ppat.1002035.s009", "https://dx.doi.org/10.1371/journal.ppat.1002035.s010", "https://dx.doi.org/10.1371/journal.ppat.1002035.s011", "https://dx.doi.org/10.1371/journal.ppat.1002035.s012", "https://dx.doi.org/10.1371/journal.ppat.1002035.s013", "https://dx.doi.org/10.1371/journal.ppat.1002035.s014", "https://dx.doi.org/10.1371/journal.ppat.1002035.s015", "https://dx.doi.org/10.1371/journal.ppat.1002035.s016", "https://dx.doi.org/10.1371/journal.ppat.1002035.s017", "https://dx.doi.org/10.1371/journal.ppat.1002035.s018"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Misregulation_of_AUXIN_RESPONSE_FACTOR_8_Underlies_the_Developmental_Abnormalities_Caused_by_Three_Distinct_Viral_Silencing_Suppressors_in_Arabidopsis/136876", "title"=>"Misregulation of <em>AUXIN RESPONSE FACTOR 8</em> Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-05-12 01:54:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/775692"], "description"=>"<p>(<b>A</b>) CATMA gene chip analysis of the ranges in expression changes of known miRNA and ta-siRNA target transcripts that are up-regulated in leaves of transgenic VSR plants and <i>dcl1-9</i> mutant, as compared to WT plants. Data for other organs are available in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat.1002035.s003\" target=\"_blank\">Figure S3</a>-<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat.1002035.s005\" target=\"_blank\">S5</a>. nb: number. (<b>B</b>) Diagram summarizing the strategy used in this study for <i>de novo</i> RNA silencing target identification through AGO1-IP small RNA deep sequencing data. (<b>C</b>) Proportions of the total number of genes expressed in each organ analyzed, which were found up-regulated by at least 1.5 fold in at least one VSR transgenic background compared to non-transgenic Arabidopsis. Also indicated is the fraction of up-regulated genes with at least one matching AGO1-IP small RNA read, as assessed by computer-based prediction (see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#s4\" target=\"_blank\">methods</a>).</p>", "links"=>[], "tags"=>["incur", "changes", "mirna", "ta-sirna", "transcripts"], "article_id"=>446054, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_VSRs_incur_modest_yet_consistent_expression_changes_to_known_miRNA_and_ta_siRNA_target_transcripts_in_Arabidopsis_/446054", "title"=>"VSRs incur modest yet consistent expression changes to known miRNA and ta-siRNA target transcripts in Arabidopsis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:40:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/775842"], "description"=>"<p>(<b>A-E</b>) Left panels provide ASRP genome browser views of the small RNA loci of origin. Colored arrows indicate the position and length of the small RNA. Blue, green and red labels indicate 21nt-long, 22nt-long and 24nt-long siRNA species, respectively. A black color signifies small RNAs with length diverging from the above. The right panels depict predicted target sites alongside the small RNA identification number (as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat.1002035-Mi1\" target=\"_blank\">[30]</a>), AGO1-IP read value (underlined in red) and number of loci of origin (hit). The gene identification number of the predicted target is underlined in red. (<b>A–C</b>) Inverted-repeat (IR)-derived siRNAs and their predicted targets, At1g12320 (in leaves; A), At4g08390 (in stems and leaves; B) and At4g28490 (in stems and leaves; C). (<b>D</b>) Predicted secondary structure of the transposon-derived <i>IR6735</i>. (<b>E</b>) A 21nt-long siRNA derived from the <i>TAS3</i> locus predicted to target the At2g38120 transcript in leaves. For each example, statistically significant up-regulation of gene expression was validated in two independent qRT-PCR analyses of total RNA extracted from the indicated tissues.</p>", "links"=>[], "tags"=>["ago1-ip", "conjunction", "vsr", "microarray", "uncovers", "sirna", "transcripts", "altered", "accumulation"], "article_id"=>446199, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Using_the_AGO1_IP_read_filter_in_conjunction_with_VSR_microarray_data_uncovers_possibly_novel_IR_and_TAS_derived_siRNA_target_transcripts_with_altered_accumulation_by_VSRs_/446199", "title"=>"Using the AGO1-IP read filter in conjunction with VSR microarray data uncovers possibly novel <i>IR</i>- and<i>TAS</i>-derived siRNA target transcripts with altered accumulation by VSRs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:43:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/776018"], "description"=>"<p>As in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat-1002035-g003\" target=\"_blank\">Figure 3</a>, the upper panels in A–C provide ASRP genome browser views of the small RNA loci of origin. (<b>A-B</b>) Abundantly AGO1-loaded miRNA passenger strands (miR*) for miR159b and miR408, alongside their predicted targets, At3g58780 (stems and leaves; A) and At2g47020 (flowers; B). The blue panels show the predicted stem-loop structures of the corresponding miRNA precursors, in which the miRNA* sequence is boxed in blue. (<b>C</b>) The sulfate transporter At5g13550 transcript is a putative target for the Arabidopsis-specific miR843 in stems. For each example, statistically significant up-regulation of gene expression was validated in two independent qRT-PCR analyses of total RNA extracted from the indicated tissues.</p>", "links"=>[], "tags"=>["ago1-ip", "conjunction", "vsr", "microarray", "uncovers", "orphan", "mirna", "transcripts", "accumulation", "altered"], "article_id"=>446378, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Using_the_AGO1_IP_read_filter_in_conjunction_with_VSR_microarray_data_uncovers_possibly_novel_miRNA_and_orphan_miRNA_target_transcripts_whose_accumulation_is_altered_by_VSRs_/446378", "title"=>"Using the AGO1-IP read filter in conjunction with VSR microarray data uncovers possibly novel miRNA* and orphan miRNA target transcripts whose accumulation is altered by VSRs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:46:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/776202"], "description"=>"<p>(<b>A</b>) The Venn diagram on the left shows that only a modest number of transcripts are up-regulated in common in leaves of the three VSR transgenics. The table shows that refining the analysis with additional filters based on transcripts up-regulated in <i>dcl1-9</i> (pale grey) and <i>hen1-1</i> (dark grey) backgrounds singularizes ARF4 and ARF8, respectively direct targets of miR390 and miR167, as strong candidates for the underlying developmental defects seen in VSR transgenics. (<b>B–C</b>) Strong reduction of leaf and inflorescence defects (inlays) caused by HcPro in F1 progenies of crosses between <i>arf8</i> mutants and HcPro transgenics carrying the <i>CHS</i> RNAi transgene (B). The Northern blot in (C) shows comparable accumulation of HcPro transcripts in the various backgrounds involved in the crosses. (<b>D–E</b>) same as (B–C) for P15 transgenics with the <i>CHS</i> RNAi background. (<b>F–G</b>) Same as (B–C) for P19 transgenics with the <i>CHS</i> RNAi background. Arrows indicate the presence of slight leaf serration in F1 progeny plants. (<b>H–I</b>) Complete alleviation of developmental defects and sterility of P19 transgenic plants (<i>CHS</i> RNAi background) in the homozygous <i>arf8</i> mutant background. Northern analysis in (I) confirms comparable P19 levels in the various backgrounds indicated. Plants #1 and #2 where retrieved through independent genotyping in populations of P19 plants with homozygous or heterozygous <i>arf8</i> mutant genotype. rRNA: ethidium bromide staining of ribosomal RNA provides a control for equal RNA loading.</p>", "links"=>[], "tags"=>["homozygous", "mutant", "backgrounds", "attenuate", "alleviate", "phenotypes", "incurred"], "article_id"=>446567, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heterozygous_and_homozygous_arf8_mutant_backgrounds_respectively_attenuate_and_alleviate_the_developmental_phenotypes_incurred_by_VSRs_/446567", "title"=>"Heterozygous and homozygous <i>arf8</i> mutant backgrounds respectively attenuate and alleviate the developmental phenotypes incurred by VSRs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:49:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/776348"], "description"=>"<p>(<b>A</b>) Western analysis of DCL1 and AGO1 accumulation in <i>arf8</i> homozygous seedlings compared to WT seedlings. Negative controls were plants with the <i>dcl1–9</i> genotype, which accumulate a truncated form of the DCL1 protein, and null <i>ago1–36</i> mutants. Load: coomassie staining provides a control for equal loading of total proteins. (<b>B</b>) Northern analysis of various endogenous miRNAs in Col-0 or homozygous <i>arf8</i> mutant seedlings. (<b>C</b>) qRT-PCR analysis of transcript levels from various targets of the miRNAs studied in (B), showing intact miRNA-mediated repression in <i>arf8</i> mutants as compared to WT plants. (<b>D</b>) RNAi of <i>CHS</i>, diagnosed by a loss-of-seed pigmentation (inlays), remains unaltered in plants with the <i>arf8</i><sup>-/-</sup> genotype. (<b>E</b>) Northern analysis of CHS siRNAs and endogenous miRNA accumulation in VSR transgenics with the heterozygous <i>arf8</i> mutant background (as depicted in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat-1002035-g005\" target=\"_blank\">Figure 5B-I</a>). Note the strong decrease in siRNA levels caused by HcPro and P15 as well as the slight shift in electrophoretic migration and enhanced accumulation incurred to miRNAs by P19 and HcPro, respectively. The inlays at the bottom show that RNAi of <i>CHS</i> remains suppressed by the three VSRs in the <i>arf8</i> mutant background, as diagnosed by the dark-brown seed coloration. (<b>F</b>) qRT-PCR analysis of transcript levels from various targets of the miRNAs studied in (B) in the P19 transgenics carrying the homozygous <i>arf8</i> mutation (<i>CHS</i> RNAi background), as depicted in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat-1002035-g005\" target=\"_blank\">Figure 5H</a>. Reference plants used in the analysis were line <i>CHS</i> RNAi and its P19 transgenic derivative (P19 <i>CHS</i> RNAi) with a wild type background. Off-scale values for ARF17 and At4g22470 (a novel small target shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002035#ppat-1002035-g004\" target=\"_blank\">Figure 4A</a>) are indicated by double-dashed lines. U6: oligonucleotide hybridization of the ubiquitous U6 small nucleolar RNA provides a control for equal RNA loading.</p>", "links"=>[], "tags"=>["mirna-mediated", "compromised"], "article_id"=>446713, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RNAi_and_miRNA_mediated_gene_silencing_are_not_compromised_by_the_arf8_mutation_/446713", "title"=>"RNAi and miRNA-mediated gene silencing are not compromised by the <i>arf8</i> mutation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:51:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/776467"], "description"=>"<p>(<b>A–B</b>) F1 progenies of crosses between <i>arf8–4</i> mutant and P6 transgenic plants (ecotype Ler) exhibit the typical dwarfism, chlorosis and pointy leaf phenotype incurred by P6 expression. The Northern analysis in (B) shows comparable accumulation of P6 transcripts in the various backgrounds involved in these crosses. (<b>C</b>) The leaf serrations caused by TuMV infection of Col-0 plants (upper panel) are strongly reduced in plants with the <i>arf8–6</i><sup>-/-</sup> mutant background. Note the persistence of chlorosis in both cases. (<b>D</b>) Comparative Northern analysis of TuMV RNA accumulation in Col-0 versus <i>arf8–6</i><sup>-/-</sup> mutant plants. The tracks contain RNA isolated in two independent infections. i: infected; ni: non-infected. rRNA: ethidium bromide staining of ribosomal RNA provides a control for equal RNA loading.</p>", "links"=>[], "tags"=>["mutation", "phenotypes", "caused", "p6", "vsr", "mosaic", "incurred"], "article_id"=>446827, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_arf8_mutation_does_not_alter_the_developmental_phenotypes_caused_by_the_P6_VSR_of_Cauliflower_mosaic_virus_but_strongly_reduces_those_incurred_by_Turnip_mosaic_virus_infection_/446827", "title"=>"The <i>arf8</i> mutation does not alter the developmental phenotypes caused by the P6 VSR of <i>Cauliflower mosaic virus</i> but strongly reduces those incurred by<i>Turnip mosaic virus</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-12 01:53:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/776558"], "description"=>"<p>Primer sequences used in this study.</p>", "links"=>[], "tags"=>["sequences"], "article_id"=>446924, "categories"=>["Plant Biology"], "users"=>["Florence Jay", "Yu Wang", "Agnès Yu", "Ludivine Taconnat", "Sandra Pelletier", "Vincent Colot", "Jean-Pierre Renou", "Olivier Voinnet"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002035.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sequences_used_in_this_study_/446924", "title"=>"Primer sequences used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-12 01:55:24"}

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  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"19", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"16", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}

Relative Metric

{"start_date"=>"2011-01-01T00:00:00Z", "end_date"=>"2011-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[304, 568, 702, 818, 927, 1027, 1118, 1206, 1285, 1357, 1427, 1500, 1564, 1636, 1705, 1773, 1840, 1909, 1974, 2039, 2106, 2170, 2234, 2296, 2358, 2423, 2484, 2546, 2606, 2673, 2734, 2795, 2857, 2921, 2984, 3046, 3100]}, {"subject_area"=>"/Biology and life sciences/Agriculture", "average_usage"=>[308, 573, 694, 810, 910, 993, 1084, 1153, 1231, 1302, 1368, 1447, 1509, 1581, 1659, 1737, 1803, 1867, 1937, 2011, 2067, 2142, 2196, 2260, 2318, 2376, 2413, 2492, 2584, 2650, 2729, 2803, 2868, 2929, 3006, 3082, 3146]}, {"subject_area"=>"/Biology and life sciences/Plant science", "average_usage"=>[310, 524, 653, 750, 838, 945, 1028, 1110, 1190, 1259, 1339, 1411, 1473, 1551, 1623, 1697, 1767, 1830, 1910, 1986, 2055, 2117, 2178, 2236, 2299, 2364, 2418, 2501, 2550, 2615, 2673, 2736, 2828, 2895, 2972, 3070, 3118]}]}

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