Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis
Identifieur interne : 000537 ( Pmc/Curation ); précédent : 000536; suivant : 000538Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis
Auteurs : Peter Brodersen [France] ; Lali Sakvarelidze-Achard [France] ; Hubert Schaller [France] ; Mehdi Khafif [France] ; Grégory Schott [Suisse] ; Abdelhafid Bendahmane [France] ; Olivier Voinnet [France, Suisse]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2012.
Abstract
Plant and metazoan microRNAs (miRNAs) guide ARGONAUTE (AGO) protein complexes to regulate expression of complementary RNAs via base pairing. In the plant
Url:
DOI: 10.1073/pnas.1112500109
PubMed: 22247288
PubMed Central: 3277166
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<author><name sortKey="Sakvarelidze Achard, Lali" sort="Sakvarelidze Achard, Lali" uniqKey="Sakvarelidze Achard L" first="Lali" last="Sakvarelidze-Achard">Lali Sakvarelidze-Achard</name>
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<country xml:lang="fr">France</country>
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, Unité Propre de Recherche 2357, 67084 Strasbourg Cedex,<country>France</country>
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<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
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<front><div type="abstract" xml:lang="en"><p>Plant and metazoan microRNAs (miRNAs) guide ARGONAUTE (AGO) protein complexes to regulate expression of complementary RNAs via base pairing. In the plant <italic>Arabidopsis thaliana</italic>
, the main miRNA effector is AGO1, but few other factors required for miRNA activity are known. Here, we isolate the genes defined by the previously described <italic>miRNA action deficient</italic>
(<italic>mad</italic>
) mutants, <italic>mad3</italic>
and <italic>mad4</italic>
. Both genes encode enzymes involved in isoprenoid biosynthesis. <italic>MAD3</italic>
encodes 3-hydroxy-3-methylglutaryl CoA reductase (HMG1), which functions in the initial C<sub>5</sub>
building block biogenesis that precedes isoprenoid metabolism. HMG1 is a key regulatory enzyme that controls the amounts of isoprenoid end products. <italic>MAD4</italic>
encodes sterol C-8 isomerase (HYDRA1) that acts downstream in dedicated sterol biosynthesis. Using yeast complementation assays and <italic>in planta</italic>
application of lovastatin, a competitive inhibitor of HMG1, we show that defects in HMG1 catalytic activity are sufficient to inhibit miRNA activity. Many isoprenoid derivatives are indispensable structural and signaling components, and especially sterols are essential membrane constituents. Accordingly, we provide evidence that AGO1 is a peripheral membrane protein. Moreover, specific hypomorphic mutant alleles of <italic>AGO1</italic>
display compromised membrane association and AGO1-membrane interaction is reduced upon knockdown of HMG1/MAD3. These results suggest a possible basis for the requirement of isoprenoid biosynthesis for the activity of plant miRNAs, and unravel mechanistic features shared with their metazoan counterparts.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><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">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher><publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22247288</article-id>
<article-id pub-id-type="pmc">3277166</article-id>
<article-id pub-id-type="publisher-id">201112500</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1112500109</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Plant Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in <italic>Arabidopsis</italic>
</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Brodersen</surname>
<given-names>Peter</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn2"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sakvarelidze-Achard</surname>
<given-names>Lali</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Schaller</surname>
<given-names>Hubert</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Khafif</surname>
<given-names>Mehdi</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="fn3"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Schott</surname>
<given-names>Grégory</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bendahmane</surname>
<given-names>Abdelhafid</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Voinnet</surname>
<given-names>Olivier</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>3</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
Institut de Biologie Moléculaire des Plantes du<institution>Centre National de la Recherche Scientifique</institution>
, Unité Propre de Recherche 2357, 67084 Strasbourg Cedex,<country>France</country>
;</aff>
<aff id="aff2"><sup>b</sup>
<institution>Unité de Recherche en Génomique Végétale,</institution>
CP 57008 Evry Cedex,<country>France</country>
; and</aff>
<aff id="aff3"><sup>c</sup>
<institution>Swiss Federal Institute of Technology (ETH-Z), Department of Biology</institution>
, Zürich 8092,<country>Switzerland</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>3</sup>
To whom correspondence should be addressed. E-mail: <email>voinneto@ethz.ch</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited<xref ref-type="fn" rid="fn1">*</xref>
by James C. Carrington, Donald Danforth Plant Science Center, St. Louis, MO, and approved December 16, 2011 (received for review July 30, 2011)</p>
</fn>
<fn fn-type="con"><p>Author contributions: P.B. and O.V. designed research; P.B., L.S.-A., H.S., M.K., and G.S. performed research; H.S. contributed new reagents/analytic tools; P.B., H.S., A.B., and O.V. analyzed data; and P.B. and O.V. wrote the paper.</p>
</fn>
<fn id="fn2" fn-type="present-address"><p><sup>1</sup>
Present address: Copenhagen University, Department of Biology, Ole Maaløes Vej 5, 2200 Copenhagen N, Denmark.</p>
</fn>
<fn id="fn3" fn-type="present-address"><p><sup>2</sup>
Present address: Institut National de la Recherche Agronomique, Laboratoires des Interactions Plantes-Microorganismes, Unité Mixte de Recherche 441, 31326 Castanet-Tolosan, France.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>31</day>
<month>1</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>12</day>
<month>1</month>
<year>2012</year>
</pub-date>
<volume>109</volume>
<issue>5</issue>
<fpage>1778</fpage>
<lpage>1783</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201112500.pdf"></self-uri>
<abstract><p>Plant and metazoan microRNAs (miRNAs) guide ARGONAUTE (AGO) protein complexes to regulate expression of complementary RNAs via base pairing. In the plant <italic>Arabidopsis thaliana</italic>
, the main miRNA effector is AGO1, but few other factors required for miRNA activity are known. Here, we isolate the genes defined by the previously described <italic>miRNA action deficient</italic>
(<italic>mad</italic>
) mutants, <italic>mad3</italic>
and <italic>mad4</italic>
. Both genes encode enzymes involved in isoprenoid biosynthesis. <italic>MAD3</italic>
encodes 3-hydroxy-3-methylglutaryl CoA reductase (HMG1), which functions in the initial C<sub>5</sub>
building block biogenesis that precedes isoprenoid metabolism. HMG1 is a key regulatory enzyme that controls the amounts of isoprenoid end products. <italic>MAD4</italic>
encodes sterol C-8 isomerase (HYDRA1) that acts downstream in dedicated sterol biosynthesis. Using yeast complementation assays and <italic>in planta</italic>
application of lovastatin, a competitive inhibitor of HMG1, we show that defects in HMG1 catalytic activity are sufficient to inhibit miRNA activity. Many isoprenoid derivatives are indispensable structural and signaling components, and especially sterols are essential membrane constituents. Accordingly, we provide evidence that AGO1 is a peripheral membrane protein. Moreover, specific hypomorphic mutant alleles of <italic>AGO1</italic>
display compromised membrane association and AGO1-membrane interaction is reduced upon knockdown of HMG1/MAD3. These results suggest a possible basis for the requirement of isoprenoid biosynthesis for the activity of plant miRNAs, and unravel mechanistic features shared with their metazoan counterparts.</p>
</abstract>
<kwd-group><kwd>statins</kwd>
<kwd>forward genetics</kwd>
<kwd>miRNA sensor</kwd>
<kwd>GFP</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>
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