Mating of the Stichotrichous Ciliate Oxytricha trifallax Induces Production of a Class of 27 nt Small RNAs Derived from the Parental Macronucleus
Identifieur interne : 001071 ( Pmc/Curation ); précédent : 001070; suivant : 001072Mating of the Stichotrichous Ciliate Oxytricha trifallax Induces Production of a Class of 27 nt Small RNAs Derived from the Parental Macronucleus
Auteurs : Alan M. Zahler [États-Unis] ; Zachary T. Neeb [États-Unis] ; Athena Lin [États-Unis] ; Sol Katzman [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2012.
Abstract
Ciliated protozoans possess two types of nuclei; a transcriptionally silent micronucleus, which serves as the germ line nucleus, and a transcriptionally active macronucleus, which serves as the somatic nucleus. The macronucleus is derived from a new diploid micronucleus after mating, with epigenetic information contributed by the parental macronucleus serving to guide the formation of the new macronucleus. In the stichotrichous ciliate
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DOI: 10.1371/journal.pone.0042371
PubMed: 22900016
PubMed Central: 3416858
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Mating of the Stichotrichous Ciliate <italic>Oxytricha trifallax</italic> Induces Production of a Class of 27 nt Small RNAs Derived from the Parental Macronucleus</title><author><name sortKey="Zahler, Alan M" sort="Zahler, Alan M" uniqKey="Zahler A" first="Alan M." last="Zahler">Alan M. Zahler</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Neeb, Zachary T" sort="Neeb, Zachary T" uniqKey="Neeb Z" first="Zachary T." last="Neeb">Zachary T. Neeb</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Lin, Athena" sort="Lin, Athena" uniqKey="Lin A" first="Athena" last="Lin">Athena Lin</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Katzman, Sol" sort="Katzman, Sol" uniqKey="Katzman S" first="Sol" last="Katzman">Sol Katzman</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>The Center for Biomolecular Science and Engineering, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Center for Biomolecular Science and Engineering, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22900016</idno><idno type="pmc">3416858</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3416858</idno><idno type="RBID">PMC:3416858</idno><idno type="doi">10.1371/journal.pone.0042371</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">001071</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001071</idno><idno type="wicri:Area/Pmc/Curation">001071</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001071</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Mating of the Stichotrichous Ciliate <italic>Oxytricha trifallax</italic> Induces Production of a Class of 27 nt Small RNAs Derived from the Parental Macronucleus</title><author><name sortKey="Zahler, Alan M" sort="Zahler, Alan M" uniqKey="Zahler A" first="Alan M." last="Zahler">Alan M. Zahler</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Neeb, Zachary T" sort="Neeb, Zachary T" uniqKey="Neeb Z" first="Zachary T." last="Neeb">Zachary T. Neeb</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Lin, Athena" sort="Lin, Athena" uniqKey="Lin A" first="Athena" last="Lin">Athena Lin</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author><author><name sortKey="Katzman, Sol" sort="Katzman, Sol" uniqKey="Katzman S" first="Sol" last="Katzman">Sol Katzman</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>The Center for Biomolecular Science and Engineering, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Center for Biomolecular Science and Engineering, University of California Santa Cruz, Santa Cruz, California</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Ciliated protozoans possess two types of nuclei; a transcriptionally silent micronucleus, which serves as the germ line nucleus, and a transcriptionally active macronucleus, which serves as the somatic nucleus. The macronucleus is derived from a new diploid micronucleus after mating, with epigenetic information contributed by the parental macronucleus serving to guide the formation of the new macronucleus. In the stichotrichous ciliate <italic>Oxytricha trifallax</italic>, the macronuclear DNA is highly processed to yield gene-sized nanochromosomes with telomeres at each end. Here we report that soon after mating of <italic>Oxytricha trifallax</italic>, abundant 27 nt small RNAs are produced that are not present prior to mating. We performed next generation sequencing of <italic>Oxytricha</italic> small RNAs from vegetative and mating cells. Using sequence comparisons between macronuclear and micronuclear versions of genes, we found that the 27 nt RNA class derives from the parental macronucleus, not the developing macronucleus. These small RNAs are produced equally from both strands of macronuclear nanochromosomes, but in a highly non-uniform distribution along the length of the nanochromosome, and with a particular depletion in the 30 nt telomere-proximal positions. This production of small RNAs from the parental macronucleus during macronuclear development stands in contrast to the mechanism of epigenetic control in the distantly related ciliate <italic>Tetrahymena</italic>. In that species, 28–29 nt scanRNAs are produced from the micronucleus and these micronuclear-derived RNAs serve as epigenetic controllers of macronuclear development. Unlike the <italic>Tetrahymena</italic> scanRNAs, the <italic>Oxytricha</italic> macronuclear-derived 27 mers are not modified by 2′O-methylation at their 3′ ends. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22900016</article-id><article-id pub-id-type="pmc">3416858</article-id><article-id pub-id-type="publisher-id">PONE-D-12-10815</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0042371</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Genomics</subject><subj-group><subject>Genome Sequencing</subject></subj-group></subj-group><subj-group><subject>Molecular cell biology</subject><subj-group><subject>Chromosome Biology</subject><subj-group><subject>Telomeres</subject></subj-group></subj-group><subj-group><subject>Gene expression</subject><subj-group><subject>RNA interference</subject><subject>RNA processing</subject></subj-group></subj-group><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>RNA interference</subject><subject>RNA processing</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Mating of the Stichotrichous Ciliate <italic>Oxytricha trifallax</italic> Induces Production of a Class of 27 nt Small RNAs Derived from the Parental Macronucleus</article-title><alt-title alt-title-type="running-head">Mating-Specific 27 nt RNAs of <italic>Oxytricha</italic></alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zahler</surname><given-names>Alan M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Neeb</surname><given-names>Zachary T.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Athena</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Katzman</surname><given-names>Sol</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Department of Molecular, Cell and Developmental Biology and The Center for Molecular Biology of RNA, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></aff><aff id="aff2"><label>2</label><addr-line>The Center for Biomolecular Science and Engineering, University of California Santa Cruz, Santa Cruz, California, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Qu</surname><given-names>Liang-Hu</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Sun Yat-sen University, China</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>zahler@ucsc.edu</email></corresp><fn fn-type="COI-statement"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: AMZ SK. Performed the experiments: AMZ ZN AL SK. Analyzed the data: AMZ SK. Wrote the paper: AMZ.</p></fn></author-notes><pub-date pub-type="collection"><year>2012</year></pub-date><pub-date pub-type="epub"><day>10</day><month>8</month><year>2012</year></pub-date><volume>7</volume><issue>8</issue><elocation-id>e42371</elocation-id><history><date date-type="received"><day>16</day><month>4</month><year>2012</year></date><date date-type="accepted"><day>6</day><month>7</month><year>2012</year></date></history><permissions><copyright-statement>© 2012 Zahler et al</copyright-statement><copyright-year>2012</copyright-year><copyright-holder>Zahler et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><p>Ciliated protozoans possess two types of nuclei; a transcriptionally silent micronucleus, which serves as the germ line nucleus, and a transcriptionally active macronucleus, which serves as the somatic nucleus. The macronucleus is derived from a new diploid micronucleus after mating, with epigenetic information contributed by the parental macronucleus serving to guide the formation of the new macronucleus. In the stichotrichous ciliate <italic>Oxytricha trifallax</italic>, the macronuclear DNA is highly processed to yield gene-sized nanochromosomes with telomeres at each end. Here we report that soon after mating of <italic>Oxytricha trifallax</italic>, abundant 27 nt small RNAs are produced that are not present prior to mating. We performed next generation sequencing of <italic>Oxytricha</italic> small RNAs from vegetative and mating cells. Using sequence comparisons between macronuclear and micronuclear versions of genes, we found that the 27 nt RNA class derives from the parental macronucleus, not the developing macronucleus. These small RNAs are produced equally from both strands of macronuclear nanochromosomes, but in a highly non-uniform distribution along the length of the nanochromosome, and with a particular depletion in the 30 nt telomere-proximal positions. This production of small RNAs from the parental macronucleus during macronuclear development stands in contrast to the mechanism of epigenetic control in the distantly related ciliate <italic>Tetrahymena</italic>. In that species, 28–29 nt scanRNAs are produced from the micronucleus and these micronuclear-derived RNAs serve as epigenetic controllers of macronuclear development. Unlike the <italic>Tetrahymena</italic> scanRNAs, the <italic>Oxytricha</italic> macronuclear-derived 27 mers are not modified by 2′O-methylation at their 3′ ends. We propose models for the role of these “27macRNAs” in macronuclear development.</p></abstract><funding-group><funding-statement>This work was supported in part by a grant from the National Science Foundation (MCB-1121290) to AMZ. SK is supported in part by the University of California Institute for Quantitative Biology (QB3). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="19"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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