Divergent Evolution of CHD3 Proteins Resulted in MOM1 Refining Epigenetic Control in Vascular Plants
Identifieur interne : 001079 ( Pmc/Checkpoint ); précédent : 001078; suivant : 001080Divergent Evolution of CHD3 Proteins Resulted in MOM1 Refining Epigenetic Control in Vascular Plants
Auteurs : Marian Aikovski [Suisse] ; Chotika Yokthongwattana [Suisse] ; Yoshiki Habu [Japon] ; Taisuke Nishimura [Suisse, Japon] ; Olivier Mathieu [Suisse, France] ; Jerzy Paszkowski [Suisse]Source :
- PLoS Genetics [ 1553-7390 ] ; 2008.
Abstract
Url:
DOI: 10.1371/journal.pgen.1000165
PubMed: 18725928
PubMed Central: 2507757
Affiliations:
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<author><name sortKey="Yokthongwattana, Chotika" sort="Yokthongwattana, Chotika" uniqKey="Yokthongwattana C" first="Chotika" last="Yokthongwattana">Chotika Yokthongwattana</name>
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<author><name sortKey="Nishimura, Taisuke" sort="Nishimura, Taisuke" uniqKey="Nishimura T" first="Taisuke" last="Nishimura">Taisuke Nishimura</name>
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<author><name sortKey="Mathieu, Olivier" sort="Mathieu, Olivier" uniqKey="Mathieu O" first="Olivier" last="Mathieu">Olivier Mathieu</name>
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<front><div type="abstract" xml:lang="en"><p><italic>Arabidopsis</italic>
MOM1 is required for the heritable maintenance of transcriptional gene silencing (TGS). Unlike many other silencing factors, depletion of MOM1 evokes transcription at selected loci without major changes in DNA methylation or histone modification. These loci retain unusual, bivalent chromatin properties, intermediate to both euchromatin and heterochromatin. The structure of MOM1 previously suggested an integral nuclear membrane protein with chromatin-remodeling and actin-binding activities. Unexpected results presented here challenge these presumed MOM1 activities and demonstrate that less than 13% of MOM1 sequence is necessary and sufficient for TGS maintenance. This active sequence encompasses a novel <underline>C</underline>
onserved <underline>M</underline>
OM1 <underline>M</underline>
otif <underline>2</underline>
(CMM2). The high conservation suggests that CMM2 has been the subject of strong evolutionary pressure. The replacement of <italic>Arabidopsis</italic>
CMM2 by a poplar motif reveals its functional conservation. Interspecies comparison suggests that MOM1 proteins emerged at the origin of vascular plants through neo-functionalization of the ubiquitous eukaryotic CHD3 chromatin remodeling factors. Interestingly, despite the divergent evolution of CHD3 and MOM1, we observed functional cooperation in epigenetic control involving unrelated protein motifs and thus probably diverse mechanisms.</p>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Genet</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Genet</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosgen</journal-id>
<journal-title-group><journal-title>PLoS Genetics</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7390</issn>
<issn pub-type="epub">1553-7404</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">18725928</article-id>
<article-id pub-id-type="pmc">2507757</article-id>
<article-id pub-id-type="publisher-id">08-PLGE-RA-0559R2</article-id>
<article-id pub-id-type="doi">10.1371/journal.pgen.1000165</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline"><subject>Genetics and Genomics/Epigenetics</subject>
</subj-group>
</article-categories>
<title-group><article-title>Divergent Evolution of CHD3 Proteins Resulted in MOM1 Refining Epigenetic Control in Vascular Plants</article-title>
<alt-title alt-title-type="running-head">MOM1 Evolution</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Čaikovski</surname>
<given-names>Marian</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yokthongwattana</surname>
<given-names>Chotika</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>¤</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Habu</surname>
<given-names>Yoshiki</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nishimura</surname>
<given-names>Taisuke</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mathieu</surname>
<given-names>Olivier</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Paszkowski</surname>
<given-names>Jerzy</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Laboratory of Plant Genetics, University of Geneva, Geneva, Switzerland</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo, Japan</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Centre National de la Recherche Scientifique (CNRS), UMR6247 - INSERM U931 - GReD, Clermont Université, Aubière Cedex, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Kakutani</surname>
<given-names>Tetsuji</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">National Institute of Genetics, Japan</aff>
<author-notes><corresp id="cor1">* E-mail: <email>jerzy.paszkowski@bioveg.unige.ch</email>
</corresp>
<fn id="fn1" fn-type="current-aff"><p><bold>¤:</bold>
Current address: Department of Biochemistry, Faculty of Sciences, Kasetsart University, Chatuchak, Bangkok, Thailand</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: MČ CY YH TN OM JP. Performed the experiments: MČ CY YH TN OM. Analyzed the data: MČ CY YH TN OM JP. Wrote the paper: MČ TN OM JP.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>8</month>
<year>2008</year>
</pub-date>
<pub-date pub-type="epub"><day>22</day>
<month>8</month>
<year>2008</year>
</pub-date>
<volume>4</volume>
<issue>8</issue>
<elocation-id>e1000165</elocation-id>
<history><date date-type="received"><day>14</day>
<month>5</month>
<year>2008</year>
</date>
<date date-type="accepted"><day>15</day>
<month>7</month>
<year>2008</year>
</date>
</history>
<permissions><copyright-statement>Čaikovski et al.</copyright-statement>
<copyright-year>2008</copyright-year>
<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><italic>Arabidopsis</italic>
MOM1 is required for the heritable maintenance of transcriptional gene silencing (TGS). Unlike many other silencing factors, depletion of MOM1 evokes transcription at selected loci without major changes in DNA methylation or histone modification. These loci retain unusual, bivalent chromatin properties, intermediate to both euchromatin and heterochromatin. The structure of MOM1 previously suggested an integral nuclear membrane protein with chromatin-remodeling and actin-binding activities. Unexpected results presented here challenge these presumed MOM1 activities and demonstrate that less than 13% of MOM1 sequence is necessary and sufficient for TGS maintenance. This active sequence encompasses a novel <underline>C</underline>
onserved <underline>M</underline>
OM1 <underline>M</underline>
otif <underline>2</underline>
(CMM2). The high conservation suggests that CMM2 has been the subject of strong evolutionary pressure. The replacement of <italic>Arabidopsis</italic>
CMM2 by a poplar motif reveals its functional conservation. Interspecies comparison suggests that MOM1 proteins emerged at the origin of vascular plants through neo-functionalization of the ubiquitous eukaryotic CHD3 chromatin remodeling factors. Interestingly, despite the divergent evolution of CHD3 and MOM1, we observed functional cooperation in epigenetic control involving unrelated protein motifs and thus probably diverse mechanisms.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>Epigenetic regulation of transcription usually involves changes in histone modifications, as well as DNA methylation changes in plants and mammals. Previously, we found an exceptional epigenetic regulator in <italic>Arabidopsis</italic>
, MOM1, acting independently of these epigenetic marks. Interestingly, MOM1 controls loci associated with bivalent chromatin marks, intermediate to active euchromatin and silent heterochromatin. Such bivalent marks are often associated with newly inserted and/or potentially active transposons, silent transgenes, and certain chromosomal loci. Notably, bivalent chromatin seems to be characteristic for embryonic stem cells, where such loci change their activity and determination of epigenetic marks during cell differentiation. Here, we provide evidence that in vascular plants, the MOM1-like proteins evolved from the ubiquitous eukaryotic chromatin remodeling factor CHD3. The domains necessary for CHD3 function degenerated in MOM1, became dispensable for its gene silencing activity, and were replaced by a novel, unrelated domain providing silencing function. Therefore, MOM1-like proteins use a different silencing mechanism compared to the ancestral CHD3s. In spite of this divergent evolution, CHD3 and MOM1 seem to retain a functional cooperation in control of transcriptionally silent loci. Our results provide an unprecedented example of an evolutionary path for epigenetic components resulting in increased complexity of an epigenetic regulatory network characteristic for multicellular eukaryotes.</p>
</abstract>
<counts><page-count count="8"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
<li>Japon</li>
<li>Suisse</li>
</country>
<region><li>Canton de Genève</li>
</region>
<settlement><li>Genève</li>
</settlement>
<orgName><li>Université de Genève</li>
</orgName>
</list>
<tree><country name="Suisse"><region name="Canton de Genève"><name sortKey=" Aikovski, Marian" sort=" Aikovski, Marian" uniqKey=" Aikovski M" first="Marian" last=" Aikovski">Marian Aikovski</name>
</region>
<name sortKey="Mathieu, Olivier" sort="Mathieu, Olivier" uniqKey="Mathieu O" first="Olivier" last="Mathieu">Olivier Mathieu</name>
<name sortKey="Nishimura, Taisuke" sort="Nishimura, Taisuke" uniqKey="Nishimura T" first="Taisuke" last="Nishimura">Taisuke Nishimura</name>
<name sortKey="Paszkowski, Jerzy" sort="Paszkowski, Jerzy" uniqKey="Paszkowski J" first="Jerzy" last="Paszkowski">Jerzy Paszkowski</name>
<name sortKey="Yokthongwattana, Chotika" sort="Yokthongwattana, Chotika" uniqKey="Yokthongwattana C" first="Chotika" last="Yokthongwattana">Chotika Yokthongwattana</name>
</country>
<country name="Japon"><noRegion><name sortKey="Habu, Yoshiki" sort="Habu, Yoshiki" uniqKey="Habu Y" first="Yoshiki" last="Habu">Yoshiki Habu</name>
</noRegion>
<name sortKey="Nishimura, Taisuke" sort="Nishimura, Taisuke" uniqKey="Nishimura T" first="Taisuke" last="Nishimura">Taisuke Nishimura</name>
</country>
<country name="France"><noRegion><name sortKey="Mathieu, Olivier" sort="Mathieu, Olivier" uniqKey="Mathieu O" first="Olivier" last="Mathieu">Olivier Mathieu</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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