MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum
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{"title"=>"MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum", "type"=>"journal", "authors"=>[{"first_name"=>"Shouqiang", "last_name"=>"Ouyang", "scopus_author_id"=>"55179970000"}, {"first_name"=>"Gyungsoon", "last_name"=>"Park", "scopus_author_id"=>"7403041953"}, {"first_name"=>"Hagop S.", "last_name"=>"Atamian", "scopus_author_id"=>"16314849300"}, {"first_name"=>"Cliff S.", "last_name"=>"Han", "scopus_author_id"=>"7403379551"}, {"first_name"=>"Jason E.", "last_name"=>"Stajich", "scopus_author_id"=>"7003427286"}, {"first_name"=>"Isgouhi", "last_name"=>"Kaloshian", "scopus_author_id"=>"6701824525"}, {"first_name"=>"Katherine A.", "last_name"=>"Borkovich", "scopus_author_id"=>"7003426303"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"600311142", "sgr"=>"84908351430", "issn"=>"15537374", "pmid"=>"25330340", "scopus"=>"2-s2.0-84908351430", "doi"=>"10.1371/journal.ppat.1004464", "isbn"=>"10.1371/journal.ppat.1004464"}, "id"=>"5c1a541b-fec0-3f00-bd8d-86aa35653c1e", "abstract"=>"MicroRNAs (miRNAs) suppress the transcriptional and post-transcriptional expression of genes in plants. Several miRNA families target genes encoding nucleotide-binding site-leucine-rich repeat (NB-LRR) plant innate immune receptors. The fungus Fusarium oxysporum f. sp. lycopersici causes vascular wilt disease in tomato. We explored a role for miRNAs in tomato defense against F. oxysporum using comparative miRNA profiling of susceptible (Moneymaker) and resistant (Motelle) tomato cultivars. slmiR482f and slmiR5300 were repressed during infection of Motelle with F. oxysporum. Two predicted mRNA targets each of slmiR482f and slmiR5300 exhibited increased expression in Motelle and the ability of these four targets to be regulated by the miRNAs was confirmed by co-expression in Nicotiana benthamiana. Silencing of the targets in the resistant Motelle cultivar revealed a role in fungal resistance for all four genes. All four targets encode proteins with full or partial nucleotide-binding (NB) domains. One slmiR5300 target corresponds to tm-2, a susceptible allele of the Tomato Mosaic Virus resistance gene, supporting functions in immunity to a fungal pathogen. The observation that none of the targets correspond to I-2, the only known resistance (R) gene for F. oxysporum in tomato, supports roles for additional R genes in the immune response. Taken together, our findings suggest that Moneymaker is highly susceptible because its potential resistance is insufficiently expressed due to the action of miRNAs.", "link"=>"http://www.mendeley.com/research/micrornas-suppress-nb-domain-genes-tomato-confer-resistance-fusarium-oxysporum", "reader_count"=>74, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>4, "Researcher"=>24, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>4, "Researcher"=>24, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>64}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>64}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>5}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>2, "Poland"=>1, "Mexico"=>1, "Slovenia"=>1, "France"=>1, "Germany"=>1, "India"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1720166"], "description"=>"<p>In total, four small RNA libraries were subjected to deep sequencing: susceptible tomato cultivar Moneymaker treated with water; Moneymaker treated with <i>Fusarium oxysporum f. sp. lycopersici</i> (<i>F. oxysporum</i>); resistant tomato cultivar Motelle treated with water and Motelle treated with <i>F. oxysporum</i>. The sequence length of small RNAs (<b>A</b>) for the combined data from the four libraries was determined as described in the <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004464#s4\" target=\"_blank\">Materials and Methods</a>. Relative expression levels of known miRNAs (<b>B</b>) were determined by dividing normalized reads for <i>F. oxysporum</i> treatment by those for water treatment for each cultivar. The red bracket indicates the miRNAs that were negatively regulated in Motelle, but not Moneymaker, after <i>F. oxysporum</i> infection. Putative roles/targets of miRNAs in various plant species (information from miRBase.org): miR156, miR156c, miR156kj and miR157d: Squamosa-promoter Binding Protein (SBP)-like transcription factors; miR166glmf: HD-Zip transcription factors, including Phabulosa (PHB) and Phavoluta (PHV) that regulate axillary meristem initiation and leaf development; miR167b, miR167d and miR167fijeghac: Auxin Response Factors (ARF transcription factors); miR396abcd: Growth Regulating Factor (GRF) transcription factors, rhodenase-like proteins, and kinesin-like protein B; miR394ab, F-box proteins; miR827abc: Unknown; miR403bdf: Virus defense; miR162 and miR162abc: Unknown; miR530: Unknown; miR398abc: copper superoxide dismutases and cytochrome C oxidase subunit V; miR482f: NB domain proteins; miR5300, Unknown.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206701, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g001", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Properties_of_miRNAs_expressed_in_resistant_and_susceptible_tomato_cultivars_treated_with_water_or_the_fungal_pathogen_Fusarium_oxysporum_/1206701", "title"=>"Properties of miRNAs expressed in resistant and susceptible tomato cultivars treated with water or the fungal pathogen <i>Fusarium oxysporum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720173"], "description"=>"<p>All control and VIGS plants were cultivated together in the same growth chamber. Similar results were obtained in three biological replicates. Errors are expressed as standard error. *** indicate significant differences when compared to the corresponding control plants in the same treatments at p<0.001. A. <b>Phenotype of control plants infected by </b><b><i>Fusarium oxysporum</i></b><b>.</b> Two-week-old seedlings of the indicated cultivars were treated with water or <i>F. oxysporum</i> and photographed four weeks later. Cultivars were Moneymaker (left panel), Motelle (center panel) and Motelle infected with TRV empty vector (right panel). B. <b>The relative level of </b><b><i>F. oxysporum</i></b><b> in control plants.</b> Leaves were collected from water or <i>F. oxysporum</i>-treated plants and genomic DNA isolated. qPCR of the Intergenic Spacer region (IGS) of <i>F. oxysporum</i> was used to measure relative fungal cell loads <i>in planta</i>. Note the different y-axis scale for Moneymaker (left graph) vs. Motelle (center and right graphs). C. <b>Phenotypes of VIGS plants after infection with </b><b><i>F. oxysporum</i></b><b>.</b> Motelle tomato plants were infiltrated with constructs carrying vectors that would lead to VIGS of a predicted target gene. Results for the two targets of slmiR482f are shown to the left, while the two for slmiR5300 are shown to the right. Four weeks after initiation of VIGS, roots of tomato plants were infected with <i>F. oxysporum</i> or with water (controls). Phenotypes were scored four weeks later. A water-treated control VIGS plant or a leaf is shown on the left of each panel, with three plants or leaves from <i>F. oxysporum</i>-infected VIGS plants to the right. D. <b>qPCR to determine relative levels of </b><b><i>F. oxysporum</i></b><b> cells in leaves of VIGS plants.</b> qPCR of the <i>F. oxysporum</i> rRNA intergenic spacer region was performed on genomic DNA isolated from leaves of water or <i>F. oxysporum</i>- infected plants as described in (B).</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206708, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g007", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Targets_of_slmiR482f_and_slmiR5300_are_required_for_F_oxysporum_defense_in_tomato_/1206708", "title"=>"Targets of slmiR482f and slmiR5300 are required for <i>F. oxysporum</i> defense in tomato.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720170"], "description"=>"<p>Total tomato root RNA was used for qRT-PCR with gene-specific primers. Errors are expressed as the standard error. * and *** indicate significant differences when compared to the corresponding control plants in the same treatments at p<0.05 and p<0.001, respectively. A. <b>Transcript levels of </b><b><i>Mi-1</i></b><b>, </b><b><i>I-2</i></b><b> and four </b><b><i>I-2</i></b><b> homologs.</b> Motelle and Moneymaker have different alleles of <i>Mi-1</i><a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004464#ppat.1004464-Laterrot1\" target=\"_blank\">[89]</a>, while Moneymaker appears to lack <i>I-2</i>. The prefix “Mot” signifies that the indicated <i>I-2</i> homolog has been previously identified in Motelle <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004464#ppat.1004464-Simons1\" target=\"_blank\">[28]</a>, while “Sol” indicates that the homolog was found during BLAST searches of the Sol database. B. <b>Expression of the four predicted target genes.</b> Solyc08g075630 and Solyc08g076000 are predicted targets of slmiR482f, while Solyc05g008650 and Solyc08g018220 are predicted targets of slmiR5300.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206705, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g004", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Determination_of_mRNA_levels_for_control_genes_and_predicted_targets_in_tomato_cultivars_using_qRT_PCR_/1206705", "title"=>"Determination of mRNA levels for control genes and predicted targets in tomato cultivars using qRT-PCR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720168"], "description"=>"<p>Oligonucleotide probes were used to quantitate levels of several miRNAs identified during deep sequencing using northern blot analysis. Root total RNA samples (40 µg each) were from Moneymaker treated with water (MM-H<sub>2</sub>O), Moneymaker infected with <i>F. oxysporum</i> (MM-Foxy), Motelle treated with water (Mot-H<sub>2</sub>O) and Motelle infected with <i>F. oxysporum</i> (Mot-Foxy). U6 RNA served as a loading control for each blot. Blots were imaged using a Phosphorimager and miRNA species quantitated using Imagequant software, with normalization to the amount of U6 RNA. The numbers below each blot indicate the amount of miRNA in each sample relative to the corresponding water-treated control. Note that due to significant sequence homology, slmiR482 subfamily members cannot be quantitatively distinguished from one another using northern analysis.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206703, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g002", "stats"=>{"downloads"=>4, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Northern_blot_analysis_of_miRNAs_/1206703", "title"=>"Northern blot analysis of miRNAs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720169"], "description"=>"<p>A. <b>Predicted mRNA target sequences.</b> Targets for slmiR482f and slmiR5300 were identified using the Sol Genomics website (<a href=\"http://solgenomics.net\" target=\"_blank\">http://solgenomics.net</a>). Alignments were made using ClustalW2. The nucleotides shown in red in each mRNA target are mismatches with the corresponding miRNA. B. <b>Protein domains.</b> Analysis was performed using Interpro (<a href=\"http://www.ebi.ac.uk/interpro/\" target=\"_blank\">http://www.ebi.ac.uk/interpro/</a>). NB: A signaling motif shared by plant resistance gene products and regulators of cell death in animals. CC: Coiled-Coil domain. LRR: Leucine-rich repeats. DUF3542: Protein domain of unknown function found in eukaryotes and viruses. The NB domain in Solyc05g008650 is truncated at the C-terminus. The red arrow indicates the miRNA binding site in the P-loop region of the NBS-ARC domain.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206704, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g003", "stats"=>{"downloads"=>2, "page_views"=>85, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alignment_of_slmiRNA_sequences_with_predicted_mRNA_targets_and_protein_domain_analysis_/1206704", "title"=>"Alignment of slmiRNA sequences with predicted mRNA targets and protein domain analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720176", "https://ndownloader.figshare.com/files/1720177", "https://ndownloader.figshare.com/files/1720178", "https://ndownloader.figshare.com/files/1720179", "https://ndownloader.figshare.com/files/1720180", "https://ndownloader.figshare.com/files/1720181", "https://ndownloader.figshare.com/files/1720182", "https://ndownloader.figshare.com/files/1720183", "https://ndownloader.figshare.com/files/1720184"], "description"=>"<div><p>MicroRNAs (miRNAs) suppress the transcriptional and post-transcriptional expression of genes in plants. Several miRNA families target genes encoding nucleotide-binding site–leucine-rich repeat (NB-LRR) plant innate immune receptors. The fungus <i>Fusarium oxysporum</i> f. sp. <i>lycopersici</i> causes vascular wilt disease in tomato. We explored a role for miRNAs in tomato defense against <i>F. oxysporum</i> using comparative miRNA profiling of susceptible (Moneymaker) and resistant (Motelle) tomato cultivars. slmiR482f and slmiR5300 were repressed during infection of Motelle with <i>F. oxysporum</i>. Two predicted mRNA targets each of slmiR482f and slmiR5300 exhibited increased expression in Motelle and the ability of these four targets to be regulated by the miRNAs was confirmed by co-expression in <i>Nicotiana benthamiana</i>. Silencing of the targets in the resistant Motelle cultivar revealed a role in fungal resistance for all four genes. All four targets encode proteins with full or partial nucleotide-binding (NB) domains. One slmiR5300 target corresponds to <i>tm-2</i>, a susceptible allele of the <i>Tomato Mosaic Virus</i> resistance gene, supporting functions in immunity to a fungal pathogen. The observation that none of the targets correspond to <i>I-2</i>, the only known resistance (<i>R</i>) gene for <i>F. oxysporum</i> in tomato, supports roles for additional <i>R</i> genes in the immune response. Taken together, our findings suggest that Moneymaker is highly susceptible because its potential resistance is insufficiently expressed due to the action of miRNAs.</p></div>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206711, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004464.s001", "https://dx.doi.org/10.1371/journal.ppat.1004464.s002", "https://dx.doi.org/10.1371/journal.ppat.1004464.s003", "https://dx.doi.org/10.1371/journal.ppat.1004464.s004", "https://dx.doi.org/10.1371/journal.ppat.1004464.s005", "https://dx.doi.org/10.1371/journal.ppat.1004464.s006", "https://dx.doi.org/10.1371/journal.ppat.1004464.s007", "https://dx.doi.org/10.1371/journal.ppat.1004464.s008", "https://dx.doi.org/10.1371/journal.ppat.1004464.s009"], "stats"=>{"downloads"=>39, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MicroRNAs_Suppress_NB_Domain_Genes_in_Tomato_That_Confer_Resistance_to_Fusarium_oxysporum_/1206711", "title"=>"MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to <i>Fusarium oxysporum</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720172"], "description"=>"<p>Leaflets were harvested four weeks after VIGS and prior to infection with <i>F. oxysporum</i>. Total RNA was isolated and subjected to qRT-PCR to evaluate expression of the four predicted miRNA target genes, along with <i>Mi-1</i> and Mot-<i>I-2</i> controls. The silenced gene is indicated in the title for each horizontal panel, while the gene transcript being measured is shown under the y-axis at the bottom of the figure. Plants treated with water or the TRV empty vector are included as negative controls. mRNA levels are expressed relative to the Motelle plant not treated with TRV for each VIGS construct. Values were normalized using tomato 18S rRNA. Errors are expressed as the standard error. Significant differences are indicated by asterisks. Among all of the VIGS plants, only VIGS Solyc08g075630 Plant#2 exhibits evidence of an off-target reduction in Mot-<i>I-2</i> transcript levels relative to the water-treated control. * and *** indicate significant differences when compared to the corresponding control plants in the same treatments at p<0.05 and p<0.001, respectively.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206707, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g006", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qRT_PCR_to_assess_the_degree_of_gene_silencing_and_to_determine_possible_off_target_effects_in_VIGS_plants_/1206707", "title"=>"qRT-PCR to assess the degree of gene silencing and to determine possible off-target effects in VIGS plants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1720171"], "description"=>"<p><b>A. Levels of target mRNAs.</b> qRT-PCR was used to determine relative levels of predicted tomato mRNAs in <i>N. benthamiana</i> leaves expressing only empty vector; target mRNA and a control miRNA (slmiR166); target mRNA and the appropriate miRNA (slmiR482f or slmiR5300); or target mRNA and empty vector. Values were normalized to <i>N. benthamiana</i> actin. Errors are expressed as the standard error. *** indicates significant differences when compared to the corresponding control plants in the same treatments at p<0.001. B. <b>Target protein levels.</b> Total protein isolated from the samples in (A) was electrophoresed on SDS-PAGE gels and blotted onto nitrocellulose membranes. A FLAG antiserum was used to detect the tagged target proteins during western analysis as described in the <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004464#s4\" target=\"_blank\">Materials and Methods</a> (top panels). A duplicate gel was Coomassie-stained and used as a loading control (bottom panels). Similar results were obtained for two biological replicates. C. <b>Diagrammatic representation of target mRNA cleavage sites determined using 5′RACE.</b> Thick black lines represent open reading frames (nucleotide numbering begins at the start codon indicated by the black arrow), and the putative miRNA interaction site is shown as a gray box, with the nucleotide position within the ORF indicated. The nucleotides shown in red in each mRNA target are mismatches with the corresponding miRNA. The number of sequenced 5′RACE clones corresponding to each site is indicated by vertical arrowheads.</p>", "links"=>[], "tags"=>["targets encode proteins", "Motelle", "slmiR 5300", "role", "MicroRNAs Suppress NB Domain Genes", "Fusarium oxysporum MicroRNAs", "Tomato Mosaic Virus resistance gene", "mirna", "slmiR 482f", "fungus Fusarium oxysporum f", "slmiR 5300 target"], "article_id"=>1206706, "categories"=>["Biological Sciences"], "users"=>["Shouqiang Ouyang", "Gyungsoon Park", "Hagop S. Atamian", "Cliff S. Han", "Jason E. Stajich", "Isgouhi Kaloshian", "Katherine A. Borkovich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004464.g005", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_expression_of_slmiRNAs_and_predicted_targets_in_Nicotiana_benthamiana_leaves_/1206706", "title"=>"Co-expression of slmiRNAs and predicted targets in <i>Nicotiana benthamiana</i> leaves.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-16 03:19:18"}

PMC Usage Stats | Further Information

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