Role of Transposon-Derived Small RNAs in the Interplay between Genomes and Parasitic DNA in Rice
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{"title"=>"Role of Transposon-Derived Small RNAs in the Interplay between Genomes and Parasitic DNA in Rice", "type"=>"journal", "authors"=>[{"first_name"=>"Misuzu", "last_name"=>"Nosaka", "scopus_author_id"=>"22941536300"}, {"first_name"=>"Jun Ichi", "last_name"=>"Itoh", "scopus_author_id"=>"35884878700"}, {"first_name"=>"Yasuo", "last_name"=>"Nagato", "scopus_author_id"=>"7006054530"}, {"first_name"=>"Akemi", "last_name"=>"Ono", "scopus_author_id"=>"23493271100"}, {"first_name"=>"Aiko", "last_name"=>"Ishiwata", "scopus_author_id"=>"55370211300"}, {"first_name"=>"Yutaka", "last_name"=>"Sato", "scopus_author_id"=>"56517114500"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"365755991", "doi"=>"10.1371/journal.pgen.1002953", "issn"=>"15537390", "pmid"=>"23028360", "scopus"=>"2-s2.0-84866946845", "sgr"=>"84866946845"}, "id"=>"dc737b23-0f95-3c25-aca9-5a2a44a18abd", "abstract"=>"RNA silencing is a defense system against \"genomic parasites\" such as transposable elements (TE), which are potentially harmful to host genomes. In plants, transcripts from TEs induce production of double-stranded RNAs (dsRNAs) and are processed into small RNAs (small interfering RNAs, siRNAs) that suppress TEs by RNA-directed DNA methylation. Thus, the majority of TEs are epigenetically silenced. On the other hand, most of the eukaryotic genome is composed of TEs and their remnants, suggesting that TEs have evolved countermeasures against host-mediated silencing. Under some circumstances, TEs can become active and increase in copy number. Knowledge is accumulating on the mechanisms of TE silencing by the host; however, the mechanisms by which TEs counteract silencing are poorly understood. Here, we show that a class of TEs in rice produces a microRNA (miRNA) to suppress host silencing. Members of the microRNA820 (miR820) gene family are located within CACTA DNA transposons in rice and target a de novo DNA methyltransferase gene, OsDRM2, one of the components of epigenetic silencing. We confirmed that miR820 negatively regulates the expression of OsDRM2. In addition, we found that expression levels of various TEs are increased quite sensitively in response to decreased OsDRM2 expression and DNA methylation at TE loci. Furthermore, we found that the nucleotide sequence of miR820 and its recognition site within the target gene in some Oryza species have co-evolved to maintain their base-pairing ability. The co-evolution of these sequences provides evidence for the functionality of this regulation. Our results demonstrate how parasitic elements in the genome escape the host's defense machinery. Furthermore, our analysis of the regulation of OsDRM2 by miR820 sheds light on the action of transposon-derived small RNAs, not only as a defense mechanism for host genomes but also as a regulator of interactions between hosts and their parasitic elements.", "link"=>"http://www.mendeley.com/research/role-transposonderived-small-rnas-interplay-between-genomes-parasitic-dna-rice", "reader_count"=>93, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>30, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>30, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>22, "Student > Postgraduate"=>2, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>80, "Chemistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>80}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Canada"=>2, "Austria"=>1, "Czech Republic"=>1, "United States"=>4, "Norway"=>1, "Brazil"=>3, "United Kingdom"=>3, "Mexico"=>1, "France"=>2, "Paraguay"=>1, "Portugal"=>1, "Germany"=>2}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/567646"], "description"=>"<p>(A) The phylogenetic tree shows the evolutionary relationships between <i>Oryza</i> species (left). Boxes indicate the types of <i>miR820</i> sequences and <i>DRM2</i> target site sequences identified in each genome (right). Within each column, boxes of the same color indicate identical sequences. The genome origins of the sequences in the boxes are indicated by arrows. (B) Sequence alignments of <i>miR820</i> and its target site in <i>DRM2</i> in the AA (Nipponbare; blue box) and BB/BBCC genomes (pink box). Dots between nucleotides indicate the type of nucleotide pair: a double dot indicates an A-U or G-C pair, a single dot indicates a G-U pair, and no dot indicates a mismatch. The positions of G-U pairs and mismatches are shown with broken and solid arrows, respectively. The eight nucleotide substitutions found between AA and BB/BBCC <i>Oryza</i> species are highlighted in yellow. Blue lines above and below the sequence of <i>DRM2</i> indicate the codons. Letters above and below the lines indicate the amino acids encoded by <i>DRM2</i> in AA and BB/BBCC <i>Oryza</i> species, respectively. Phylogenetic tree in (A) adapted from Ge et al. (1999) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002953#pgen.1002953-Ge1\" target=\"_blank\">[24]</a>.</p>", "links"=>[], "tags"=>["conserved"], "article_id"=>238144, "categories"=>["Genetics", "Plant Biology"], "users"=>["Misuzu Nosaka", "Jun-Ichi Itoh", "Yasuo Nagato", "Akemi Ono", "Aiko Ishiwata", "Yutaka Sato"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002953.g003", "stats"=>{"downloads"=>4, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regulation_of_DRM2_by_miR820_is_conserved_among_Oryza_species_/238144", "title"=>"Regulation of <i>DRM2</i> by <i>miR820</i> is conserved among <i>Oryza</i> species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:15:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/567764"], "description"=>"<p>(A) Detection of CACTA TEs carrying <i>pre-miR820</i> by Southern blot analysis. Genomic DNA from AA, BB, BBCC, and CC <i>Oryza</i> species were digested with the enzymes indicated and probed with <i>pre-miR820</i>. Red triangles indicate the bands corresponding to the five copies of <i>pre-miR820</i> in Nipponbare. The number next to each triangle indicates the chromosome location of that copy. (B) Mapping of CACTA carrying <i>pre-miR820</i> in the rice genome. The genomic locations of CACTA carrying <i>pre-miR820</i> in AA and BB <i>Oryza</i> species are shown by gray arrows and black arrows, respectively. (C) Phylogenetic analysis of <i>miR820</i>-CACTA sequences. Bootstrap values (1000 replicates) are given for branch nodes. Black and red numbers in parentheses indicate the chromosome locations of <i>pre-miR820</i> sequences in the AA and BB genomes, respectively. Multiple copies on one branch, indicating that the identical sequence was found at multiple loci, are highlighted in blue. (D) A model for the regulation of <i>DRM2</i> by <i>miR820</i>. Active transposons behave as “selfish” genetic elements. This characteristic is counteracted by the host's silencing machinery (blue arrow), which acts to methylate and silence transposon loci. This action can be blocked by <i>miR820</i> (thin red line), which suppresses the host's silencing machinery and can drive host genome evolution (thick red arrow).</p>", "links"=>[], "tags"=>["cacta", "carrying"], "article_id"=>238256, "categories"=>["Genetics", "Plant Biology"], "users"=>["Misuzu Nosaka", "Jun-Ichi Itoh", "Yasuo Nagato", "Akemi Ono", "Aiko Ishiwata", "Yutaka Sato"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002953.g004", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_copy_number_of_CACTA_carrying_pre_miR820_in_the_BB_BBCC_genome_/238256", "title"=>"Increased copy number of CACTA carrying <i>pre-miR820</i> in the BB/BBCC genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/300232", "https://ndownloader.figshare.com/files/300274", "https://ndownloader.figshare.com/files/300337", "https://ndownloader.figshare.com/files/300377", "https://ndownloader.figshare.com/files/300442", "https://ndownloader.figshare.com/files/300493", "https://ndownloader.figshare.com/files/300525", "https://ndownloader.figshare.com/files/300582", "https://ndownloader.figshare.com/files/300649"], "description"=>"<div><p>RNA silencing is a defense system against “genomic parasites” such as transposable elements (TE), which are potentially harmful to host genomes. In plants, transcripts from TEs induce production of double-stranded RNAs (dsRNAs) and are processed into small RNAs (small interfering RNAs, siRNAs) that suppress TEs by RNA–directed DNA methylation. Thus, the majority of TEs are epigenetically silenced. On the other hand, most of the eukaryotic genome is composed of TEs and their remnants, suggesting that TEs have evolved countermeasures against host-mediated silencing. Under some circumstances, TEs can become active and increase in copy number. Knowledge is accumulating on the mechanisms of TE silencing by the host; however, the mechanisms by which TEs counteract silencing are poorly understood. Here, we show that a class of TEs in rice produces a microRNA (miRNA) to suppress host silencing. Members of the <em>microRNA820</em> (<em>miR820</em>) gene family are located within CACTA DNA transposons in rice and target a <em>de novo</em> DNA methyltransferase gene, <em>OsDRM2</em>, one of the components of epigenetic silencing. We confirmed that <em>miR820</em> negatively regulates the expression of <em>OsDRM2</em>. In addition, we found that expression levels of various TEs are increased quite sensitively in response to decreased <em>OsDRM2</em> expression and DNA methylation at TE loci. Furthermore, we found that the nucleotide sequence of <em>miR820</em> and its recognition site within the target gene in some <em>Oryza</em> species have co-evolved to maintain their base-pairing ability. The co-evolution of these sequences provides evidence for the functionality of this regulation. Our results demonstrate how parasitic elements in the genome escape the host's defense machinery. Furthermore, our analysis of the regulation of <em>OsDRM2</em> by <em>miR820</em> sheds light on the action of transposon-derived small RNAs, not only as a defense mechanism for host genomes but also as a regulator of interactions between hosts and their parasitic elements.</p> </div>", "links"=>[], "tags"=>["transposon-derived", "rnas", "interplay", "genomes", "parasitic", "dna"], "article_id"=>119201, "categories"=>["Genetics", "Cell Biology"], "users"=>["Misuzu Nosaka", "Jun-Ichi Itoh", "Yasuo Nagato", "Akemi Ono", "Aiko Ishiwata", "Yutaka Sato"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002953.s001", "https://dx.doi.org/10.1371/journal.pgen.1002953.s002", "https://dx.doi.org/10.1371/journal.pgen.1002953.s003", "https://dx.doi.org/10.1371/journal.pgen.1002953.s004", "https://dx.doi.org/10.1371/journal.pgen.1002953.s005", "https://dx.doi.org/10.1371/journal.pgen.1002953.s006", "https://dx.doi.org/10.1371/journal.pgen.1002953.s007", "https://dx.doi.org/10.1371/journal.pgen.1002953.s008", "https://dx.doi.org/10.1371/journal.pgen.1002953.s009"], "stats"=>{"downloads"=>29, "page_views"=>69, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Role_of_Transposon_Derived_Small_RNAs_in_the_Interplay_between_Genomes_and_Parasitic_DNA_in_Rice/119201", "title"=>"Role of Transposon-Derived Small RNAs in the Interplay between Genomes and Parasitic DNA in Rice", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-09-27 02:33:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/567412"], "description"=>"<p>(A) The location of <i>miR820</i> within the CACTA DNA transposon is shown in the first row. The second and third rows indicate the similarity between the sequences of the <i>miR820</i> precursor (<i>pre-miR820</i>) and <i>Os03g0110800</i> (<i>OsDRM2</i>). The numbers beside the lines indicate the nucleotide identities between the regions. The red triangle indicates the location of <i>miR820</i> within the stem-loop region. (B) Northern blot analysis of <i>miR820</i> expression in the wild-type (WT) and in <i>waf1</i> mutants. (C) Detection of <i>miR820</i>-cleaved <i>OsDRM2</i> mRNA by RNA ligation–mediated 5′ RACE (upper panel). The same cDNA templates were used for PCR to amplify <i>OsDRM2</i> (middle panel) and <i>OsActin</i> (bottom panel) as controls for <i>OsDRM2</i> expression and RNA integrity. (D) qRT-PCR analysis measuring the expression level of <i>OsDRM2</i> in <i>waf1-1</i>, <i>waf1-2</i>, and WT. The expression level of the WT was set as 1. Values are means, with bars showing standard errors. Significance was assessed by a two-tailed Student’s t-test; (**) significant at the 1% level; (*) significant at the 5% level. The n value represents the number of mutant or wild-type individuals.</p>", "links"=>[], "tags"=>["members", "located", "cacta", "transposons", "dna", "methyltransferase"], "article_id"=>237890, "categories"=>["Genetics", "Plant Biology"], "users"=>["Misuzu Nosaka", "Jun-Ichi Itoh", "Yasuo Nagato", "Akemi Ono", "Aiko Ishiwata", "Yutaka Sato"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002953.g001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_miR820_family_members_are_located_within_CACTA_transposons_and_target_the_DNA_methyltransferase_gene_OsDRM2_/237890", "title"=>"<i>miR820</i> family members are located within CACTA transposons and target the DNA methyltransferase gene <i>OsDRM2</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:11:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/567531"], "description"=>"<p>(A) The general structure of the <i>OsDRM2::GFP</i> fusion constructs is shown at the bottom, and the sequences of <i>miR820a/b/c</i> and the target sites in the <i>35S:OsDRM2 intact:GFP</i>, <i>35S:OsDRM2 mutation1:GFP</i>, and <i>35S:OsDRM2 mutation2:GFP</i> constructs are shown at the top. The changed nucleotides in the mutant genes are shown in red letters. (B) The panels on the left show GFP fluorescence and white-light observations of longitudinal sections of shoots of transgenic plants transformed with the constructs in (A). The graph at the right shows relative expression levels of <i>GFP</i> mRNA in the corresponding transgenic lines as measured by quantitative RT-PCR. The expression level of <i>OsDRM2</i>-intact lines was set as 1. (C) Relative expression levels of <i>OsDRM2</i> and TEs in <i>OsDRM2</i> RNAi transgenic callus (black bars) measured by qRT-PCR. The expression level of empty-vector lines was set as 1. (D) <i>McrBC</i>-PCR analysis of genomic DNA from callus of WT and two independent transgenic lines of <i>OsDRM2</i> RNAi. Two of the six <i>OsDRM2</i> RNAi transgenic lines analyzed in (C) were used. In (B) and (C), values are means, with bars showing standard errors. Significance was assessed by a two-tailed Student's <i>t</i>-test; (**) significant at the 1% level; (*) significant at the 5% level. The n value represents the number of independent transformants.</p>", "links"=>[], "tags"=>["negatively", "regulated"], "article_id"=>238023, "categories"=>["Genetics", "Plant Biology"], "users"=>["Misuzu Nosaka", "Jun-Ichi Itoh", "Yasuo Nagato", "Akemi Ono", "Aiko Ishiwata", "Yutaka Sato"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002953.g002", "stats"=>{"downloads"=>4, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_OsDRM2_is_negatively_regulated_by_miR820_/238023", "title"=>"<i>OsDRM2</i> is negatively regulated by <i>miR820</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:13:43"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}

Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Agriculture", "average_usage"=>[323, 536, 657, 751, 847, 939, 1032, 1114, 1201, 1279, 1355, 1431, 1516, 1582, 1656, 1719, 1791, 1848, 1919, 2000, 2068, 2127, 2208, 2281, 2359]}, {"subject_area"=>"/Biology and life sciences/Biotechnology", "average_usage"=>[320, 560, 691, 804, 916, 1011, 1117, 1228, 1328, 1420, 1506, 1584, 1651, 1749, 1836, 1909, 1982, 2053, 2131, 2188, 2276, 2372, 2441, 2540, 2627]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[366, 574, 695, 795, 885, 973, 1063, 1148, 1233, 1319, 1389, 1459, 1533, 1611, 1685, 1754, 1820, 1882, 1937, 2001, 2071, 2129, 2219, 2273, 2335]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[331, 557, 677, 777, 868, 960, 1050, 1136, 1223, 1307, 1390, 1466, 1536, 1603, 1673, 1741, 1814, 1889, 1954, 2028, 2096, 2164, 2233, 2305, 2362]}, {"subject_area"=>"/Biology and life sciences/Plant science", "average_usage"=>[329, 543, 667, 773, 865, 963, 1066, 1149, 1233, 1323, 1411, 1500, 1588, 1661, 1732, 1803, 1887, 1978, 2057, 2138, 2203, 2283, 2363, 2419, 2493]}]}

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