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The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis1

Identifieur interne : 000C82 ( Pmc/Checkpoint ); précédent : 000C81; suivant : 000C83

The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis1

Auteurs : Nawel Haïli ; Noelya Planchard ; Nadège Arnal ; Martine Quadrado ; Nathalie Vrielynck ; Jennifer Dahan ; Catherine Colas Des Francs-Small ; Hakim Mireau

Source :

RBID : PMC:4704600

Abstract

A mitochondria-targeted pentatricopeptide repeat protein specifically facilitates the translation of a respiratory chain transcript without inducing any cleavage in its upstream noncoding region.


Url:
DOI: 10.1104/pp.15.01591
PubMed: 26537562
PubMed Central: 4704600


Affiliations:


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PMC:4704600

Le document en format XML

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<title xml:lang="en">The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial
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mRNA in Arabidopsis
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<sup>1</sup>
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<author>
<name sortKey="Haili, Nawel" sort="Haili, Nawel" uniqKey="Haili N" first="Nawel" last="Haïli">Nawel Haïli</name>
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<name sortKey="Planchard, Noelya" sort="Planchard, Noelya" uniqKey="Planchard N" first="Noelya" last="Planchard">Noelya Planchard</name>
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<name sortKey="Arnal, Nadege" sort="Arnal, Nadege" uniqKey="Arnal N" first="Nadège" last="Arnal">Nadège Arnal</name>
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<name sortKey="Quadrado, Martine" sort="Quadrado, Martine" uniqKey="Quadrado M" first="Martine" last="Quadrado">Martine Quadrado</name>
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<author>
<name sortKey="Vrielynck, Nathalie" sort="Vrielynck, Nathalie" uniqKey="Vrielynck N" first="Nathalie" last="Vrielynck">Nathalie Vrielynck</name>
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<name sortKey="Dahan, Jennifer" sort="Dahan, Jennifer" uniqKey="Dahan J" first="Jennifer" last="Dahan">Jennifer Dahan</name>
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<author>
<name sortKey="Des Francs Small, Catherine Colas" sort="Des Francs Small, Catherine Colas" uniqKey="Des Francs Small C" first="Catherine Colas" last="Des Francs-Small">Catherine Colas Des Francs-Small</name>
</author>
<author>
<name sortKey="Mireau, Hakim" sort="Mireau, Hakim" uniqKey="Mireau H" first="Hakim" last="Mireau">Hakim Mireau</name>
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<title xml:lang="en" level="a" type="main">The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial
<italic>NADH DEHYDROGENASE SUBUNIT7</italic>
mRNA in Arabidopsis
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<name sortKey="Planchard, Noelya" sort="Planchard, Noelya" uniqKey="Planchard N" first="Noelya" last="Planchard">Noelya Planchard</name>
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<name sortKey="Arnal, Nadege" sort="Arnal, Nadege" uniqKey="Arnal N" first="Nadège" last="Arnal">Nadège Arnal</name>
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<author>
<name sortKey="Quadrado, Martine" sort="Quadrado, Martine" uniqKey="Quadrado M" first="Martine" last="Quadrado">Martine Quadrado</name>
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<author>
<name sortKey="Vrielynck, Nathalie" sort="Vrielynck, Nathalie" uniqKey="Vrielynck N" first="Nathalie" last="Vrielynck">Nathalie Vrielynck</name>
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<author>
<name sortKey="Dahan, Jennifer" sort="Dahan, Jennifer" uniqKey="Dahan J" first="Jennifer" last="Dahan">Jennifer Dahan</name>
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<author>
<name sortKey="Des Francs Small, Catherine Colas" sort="Des Francs Small, Catherine Colas" uniqKey="Des Francs Small C" first="Catherine Colas" last="Des Francs-Small">Catherine Colas Des Francs-Small</name>
</author>
<author>
<name sortKey="Mireau, Hakim" sort="Mireau, Hakim" uniqKey="Mireau H" first="Hakim" last="Mireau">Hakim Mireau</name>
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<series>
<title level="j">Plant Physiology</title>
<idno type="ISSN">0032-0889</idno>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2015">2015</date>
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<div type="abstract" xml:lang="en">
<p>A mitochondria-targeted pentatricopeptide repeat protein specifically facilitates the translation of a respiratory chain transcript without inducing any cleavage in its upstream noncoding region.</p>
</div>
</front>
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<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Plant Physiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Plant Physiol</journal-id>
<journal-id journal-id-type="hwp">plantphysiol</journal-id>
<journal-id journal-id-type="publisher-id">aspb</journal-id>
<journal-title-group>
<journal-title>Plant Physiology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0032-0889</issn>
<issn pub-type="epub">1532-2548</issn>
<publisher>
<publisher-name>American Society of Plant Biologists</publisher-name>
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<article-id pub-id-type="pmid">26537562</article-id>
<article-id pub-id-type="pmc">4704600</article-id>
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<article-categories>
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<subject>Articles</subject>
<subj-group subj-group-type="heading">
<subject>Genes, Development and Evolution</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial
<italic>NADH DEHYDROGENASE SUBUNIT7</italic>
mRNA in Arabidopsis
<xref ref-type="fn" rid="fn1">
<sup>1</sup>
</xref>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Haïli</surname>
<given-names>Nawel</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Planchard</surname>
<given-names>Noelya</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Arnal</surname>
<given-names>Nadège</given-names>
</name>
<xref ref-type="author-notes" rid="afn1">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Quadrado</surname>
<given-names>Martine</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Vrielynck</surname>
<given-names>Nathalie</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dahan</surname>
<given-names>Jennifer</given-names>
</name>
<xref ref-type="author-notes" rid="afn2">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-6386-5672</contrib-id>
<name>
<surname>des Francs-Small</surname>
<given-names>Catherine Colas</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-2299-5139</contrib-id>
<name>
<surname>Mireau</surname>
<given-names>Hakim</given-names>
</name>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<aff id="aff1">Institut Jean-Pierre Bourgin, Institut National de la Recherche Agronomique, AgroParisTech, Centre National de la Recherche Scientifique, Université Paris-Saclay, 78026 Versailles cedex, France (N.H., N.P., N.A., M.Q., N.V., J.D., H.M.);</aff>
<aff id="aff2">Université Paris-Sud, Université Paris-Saclay, 91405 Orsay cedex, France (N.H., N.P.); and</aff>
<aff id="aff3">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia (C.C.d.F.-S.)</aff>
</contrib-group>
<author-notes>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="http://www.plantphysiol.org/cgi/doi/10.1104/pp.15.01591">www.plantphysiol.org/cgi/doi/10.1104/pp.15.01591</ext-link>
</p>
</fn>
<fn id="afn1" fn-type="present-address">
<label>2</label>
<p>Present address: Institut National de la Recherche Agronomique, Centre National de Ressources Génomiques Végétales, 31326 Castanet Tolosan, France.</p>
</fn>
<fn id="afn2" fn-type="present-address">
<label>3</label>
<p>Present address: Department of Plant, Soil, and Entomological Sciences, University of Idaho, Moscow, ID 83844.</p>
</fn>
<corresp id="cor1">
<label>*</label>
Address correspondence to
<email>hakim.mireau@versailles.inra.fr</email>
.</corresp>
<fn id="afn3">
<p>The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (
<ext-link ext-link-type="uri" xlink:href="http://www.plantphysiol.org">www.plantphysiol.org</ext-link>
) is: Hakim Mireau (
<email>hakim.mireau@versailles.inra.fr</email>
).</p>
</fn>
<fn id="afn4">
<p>N.H. performed most of the experiments; N.P. performed part of the experiments; J.D. performed part of the experiments; C.C.d.F.-S. performed part of the experiments; N.A. provided technical assistance to N.H. and J.D.; M.Q. provided technical assistance to N.H., J.D., and N.P.; H.M. conceived the project, supervised the experiments, and wrote the article with contributions of all the authors.</p>
</fn>
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<pmc-comment>Fake ppub date generated by PMC from publisher pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub">
<month>1</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub">
<day>4</day>
<month>11</month>
<year>2015</year>
</pub-date>
<volume>170</volume>
<issue>1</issue>
<fpage>354</fpage>
<lpage>366</lpage>
<history>
<date date-type="received">
<day>08</day>
<month>10</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>03</day>
<month>11</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>© 2016 American Society of Plant Biologists. All Rights Reserved.</copyright-statement>
<copyright-year>2016</copyright-year>
</permissions>
<self-uri xlink:role="icon" xlink:href="PP_PP201501591DR1_ic1.gif"></self-uri>
<abstract abstract-type="precis">
<p>A mitochondria-targeted pentatricopeptide repeat protein specifically facilitates the translation of a respiratory chain transcript without inducing any cleavage in its upstream noncoding region.</p>
</abstract>
<abstract>
<p>Mitochondrial translation involves a complex interplay of ancient bacteria-like features and host-derived functionalities. Although the basic components of the mitochondrial translation apparatus have been recognized, very few protein factors aiding in recruiting ribosomes on mitochondria-encoded messenger RNA (mRNAs) have been identified in higher plants. In this study, we describe the identification of the Arabidopsis (
<italic>Arabidopsis thaliana</italic>
) MITOCHONDRIAL TRANSLATION FACTOR1 (MTL1) protein, a new member of the Pentatricopeptide Repeat family, and show that it is essential for the translation of the mitochondrial
<italic>NADH dehydrogenase subunit7</italic>
(
<italic>nad7</italic>
) mRNA. We demonstrate that
<italic>mtl1</italic>
mutant plants fail to accumulate the Nad7 protein, even though the
<italic>nad7</italic>
mature mRNA is produced and bears the same 5′ and 3′ extremities as in wild-type plants. We next observed that polysome association of
<italic>nad7</italic>
mature mRNA is specifically disrupted in
<italic>mtl1</italic>
mutants, indicating that the absence of Nad7 results from a lack of translation of
<italic>nad7</italic>
mRNA. These findings illustrate that mitochondrial translation requires the intervention of gene-specific nucleus-encoded PPR trans-factors and that their action does not necessarily involve the 5′ processing of their target mRNA, as observed previously. Interestingly, a partial decrease in
<italic>nad7</italic>
intron 2 splicing was also detected in
<italic>mtl1</italic>
mutants, suggesting that MTL1 is also involved in group II intron splicing. However, this second function appears to be less essential for
<italic>nad7</italic>
expression than its role in translation. MTL1 will be instrumental to understand the multifunctionality of PPR proteins and the mechanisms governing mRNA translation and intron splicing in plant mitochondria.</p>
</abstract>
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<meta-name> DJS Export </meta-name>
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<notes>
<glossary>
<title>Glossary</title>
<def-list>
<def-item>
<term id="term1">SD</term>
<def id="def1">
<p>Shine and Dalgarno</p>
</def>
</def-item>
<def-item>
<term id="term2">T-DNA</term>
<def id="def2">
<p>transfer DNA</p>
</def>
</def-item>
<def-item>
<term id="term3">RT</term>
<def id="def3">
<p>reverse transcription</p>
</def>
</def-item>
<def-item>
<term id="term4">Col-0</term>
<def id="def4">
<p>Columbia-0</p>
</def>
</def-item>
<def-item>
<term id="term5">cDNA</term>
<def id="def5">
<p>complementary DNA</p>
</def>
</def-item>
</def-list>
</glossary>
</notes>
</front>
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<list></list>
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<name sortKey="Arnal, Nadege" sort="Arnal, Nadege" uniqKey="Arnal N" first="Nadège" last="Arnal">Nadège Arnal</name>
<name sortKey="Dahan, Jennifer" sort="Dahan, Jennifer" uniqKey="Dahan J" first="Jennifer" last="Dahan">Jennifer Dahan</name>
<name sortKey="Des Francs Small, Catherine Colas" sort="Des Francs Small, Catherine Colas" uniqKey="Des Francs Small C" first="Catherine Colas" last="Des Francs-Small">Catherine Colas Des Francs-Small</name>
<name sortKey="Haili, Nawel" sort="Haili, Nawel" uniqKey="Haili N" first="Nawel" last="Haïli">Nawel Haïli</name>
<name sortKey="Mireau, Hakim" sort="Mireau, Hakim" uniqKey="Mireau H" first="Hakim" last="Mireau">Hakim Mireau</name>
<name sortKey="Planchard, Noelya" sort="Planchard, Noelya" uniqKey="Planchard N" first="Noelya" last="Planchard">Noelya Planchard</name>
<name sortKey="Quadrado, Martine" sort="Quadrado, Martine" uniqKey="Quadrado M" first="Martine" last="Quadrado">Martine Quadrado</name>
<name sortKey="Vrielynck, Nathalie" sort="Vrielynck, Nathalie" uniqKey="Vrielynck N" first="Nathalie" last="Vrielynck">Nathalie Vrielynck</name>
</noCountry>
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