Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements
Identifieur interne : 002030 ( Ncbi/Merge ); précédent : 002029; suivant : 002031Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements
Auteurs : Zoé Joly-Lopez [Canada] ; Douglas R. Hoen [Canada] ; Mathieu Blanchette [Canada] ; Thomas E. Bureau [Canada]Source :
- Molecular Biology and Evolution [ 0737-4038 ] ; 2016.
Abstract
Once perceived as merely selfish, transposable elements (TEs) are now recognized as potent agents of adaptation. One way TEs contribute to evolution is through TE exaptation, a process whereby TEs, which persist by replicating in the genome, transform into novel host genes, which persist by conferring phenotypic benefits. Known exapted TEs (ETEs) contribute diverse and vital functions, and may facilitate punctuated equilibrium, yet little is known about this process. To better understand TE exaptation, we designed an approach to resolve the phylogenetic context and timing of exaptation events and subsequent patterns of ETE diversification. Starting with known ETEs, we search in diverse genomes for basal ETEs and closely related TEs, carefully curate the numerous candidate sequences, and infer detailed phylogenies. To distinguish TEs from ETEs, we also weigh several key genomic characteristics including repetitiveness, terminal repeats, pseudogenic features, and conserved domains. Applying this approach to the well-characterized plant ETEs
Url:
DOI: 10.1093/molbev/msw067
PubMed: 27189548
PubMed Central: 4948706
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<series><title level="j">Molecular Biology and Evolution</title>
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<front><div type="abstract" xml:lang="en"><p>Once perceived as merely selfish, transposable elements (TEs) are now recognized as potent agents of adaptation. One way TEs contribute to evolution is through TE exaptation, a process whereby TEs, which persist by replicating in the genome, transform into novel host genes, which persist by conferring phenotypic benefits. Known exapted TEs (ETEs) contribute diverse and vital functions, and may facilitate punctuated equilibrium, yet little is known about this process. To better understand TE exaptation, we designed an approach to resolve the phylogenetic context and timing of exaptation events and subsequent patterns of ETE diversification. Starting with known ETEs, we search in diverse genomes for basal ETEs and closely related TEs, carefully curate the numerous candidate sequences, and infer detailed phylogenies. To distinguish TEs from ETEs, we also weigh several key genomic characteristics including repetitiveness, terminal repeats, pseudogenic features, and conserved domains. Applying this approach to the well-characterized plant ETEs <italic>MUG</italic>
and <italic>FHY3</italic>
, we show that each group is paraphyletic and we argue that this pattern demonstrates that each originated in not one but multiple exaptation events. These exaptations and subsequent ETE diversification occurred throughout angiosperm evolution including the crown group expansion, the angiosperm radiation, and the primitive evolution of angiosperms. In addition, we detect evidence of several putative novel ETE families. Our findings support the hypothesis that TE exaptation generates novel genes more frequently than is currently thought, often coinciding with key periods of evolution.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Biol Evol</journal-id>
<journal-id journal-id-type="iso-abbrev">Mol. Biol. Evol</journal-id>
<journal-id journal-id-type="publisher-id">molbev</journal-id>
<journal-id journal-id-type="hwp">molbiolevol</journal-id>
<journal-title-group><journal-title>Molecular Biology and Evolution</journal-title>
</journal-title-group>
<issn pub-type="ppub">0737-4038</issn>
<issn pub-type="epub">1537-1719</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27189548</article-id>
<article-id pub-id-type="pmc">4948706</article-id>
<article-id pub-id-type="doi">10.1093/molbev/msw067</article-id>
<article-id pub-id-type="publisher-id">msw067</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Discoveries</subject>
</subj-group>
</article-categories>
<title-group><article-title>Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Joly-Lopez</surname>
<given-names>Zoé</given-names>
</name>
<xref ref-type="author-notes" rid="msw067-FM1"><sup>†</sup>
</xref>
<xref ref-type="author-notes" rid="msw067-FM2"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="msw067-aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hoen</surname>
<given-names>Douglas R.</given-names>
</name>
<xref ref-type="author-notes" rid="msw067-FM1"><sup>†</sup>
</xref>
<xref ref-type="aff" rid="msw067-aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Blanchette</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="msw067-aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bureau</surname>
<given-names>Thomas E.</given-names>
</name>
<xref ref-type="corresp" rid="msw067-cor1">*</xref>
<xref ref-type="aff" rid="msw067-aff1"><sup>1</sup>
</xref>
</contrib>
<aff id="msw067-aff1"><sup>1</sup>
Department of Biology, McGill University, Montréal, QC, Canada</aff>
<aff id="msw067-aff2"><sup>2</sup>
School of Computer Science, McGill University, Montréal, QC, Canada</aff>
</contrib-group>
<author-notes><fn id="msw067-FM1"><p><sup>†</sup>
These authors contributed equally to this work.</p>
</fn>
<fn id="msw067-FM2"><p><sup>‡</sup>
Present address: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY, USA.</p>
</fn>
<corresp id="msw067-cor1">*<bold>Corresponding author:</bold>
E-mail: <email>thomas.bureau@mcgill.ca</email>
.</corresp>
<fn id="msw067-FM3"><p><bold>Associate editor:</bold>
Brandon Gaut</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>8</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>28</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>28</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>33</volume>
<issue>8</issue>
<fpage>1937</fpage>
<lpage>1956</lpage>
<permissions><copyright-statement>© The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</copyright-statement>
<copyright-year>2016</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by-nc/4.0/" license-type="creative-commons"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/">http://creativecommons.org/licenses/by-nc/4.0/</ext-link>
), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com</license-p>
</license>
</permissions>
<abstract><p>Once perceived as merely selfish, transposable elements (TEs) are now recognized as potent agents of adaptation. One way TEs contribute to evolution is through TE exaptation, a process whereby TEs, which persist by replicating in the genome, transform into novel host genes, which persist by conferring phenotypic benefits. Known exapted TEs (ETEs) contribute diverse and vital functions, and may facilitate punctuated equilibrium, yet little is known about this process. To better understand TE exaptation, we designed an approach to resolve the phylogenetic context and timing of exaptation events and subsequent patterns of ETE diversification. Starting with known ETEs, we search in diverse genomes for basal ETEs and closely related TEs, carefully curate the numerous candidate sequences, and infer detailed phylogenies. To distinguish TEs from ETEs, we also weigh several key genomic characteristics including repetitiveness, terminal repeats, pseudogenic features, and conserved domains. Applying this approach to the well-characterized plant ETEs <italic>MUG</italic>
and <italic>FHY3</italic>
, we show that each group is paraphyletic and we argue that this pattern demonstrates that each originated in not one but multiple exaptation events. These exaptations and subsequent ETE diversification occurred throughout angiosperm evolution including the crown group expansion, the angiosperm radiation, and the primitive evolution of angiosperms. In addition, we detect evidence of several putative novel ETE families. Our findings support the hypothesis that TE exaptation generates novel genes more frequently than is currently thought, often coinciding with key periods of evolution.</p>
</abstract>
<kwd-group kwd-group-type="author"><kwd><italic>MUSTANG</italic>
</kwd>
<kwd><italic>FAR1</italic>
</kwd>
<kwd><italic>FHY3</italic>
</kwd>
<kwd><italic>FRS</italic>
</kwd>
<kwd>transposable elements</kwd>
<kwd>exaptation</kwd>
<kwd>molecular domestication</kwd>
<kwd>phylogeny</kwd>
<kwd>evolution</kwd>
<kwd>mutator</kwd>
<kwd>MULE</kwd>
<kwd>Phox/Bem1p</kwd>
<kwd>PB1</kwd>
<kwd>Peptidase C48</kwd>
<kwd>angiosperm radiation</kwd>
<kwd>adaptation</kwd>
<kwd>transposon</kwd>
<kwd>co-option</kwd>
<kwd>selective constraint.</kwd>
</kwd-group>
<counts><page-count count="20"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Canada</li>
</country>
<region><li>Québec</li>
</region>
<settlement><li>Montréal</li>
</settlement>
<orgName><li>Université McGill</li>
</orgName>
</list>
<tree><country name="Canada"><region name="Québec"><name sortKey="Joly Lopez, Zoe" sort="Joly Lopez, Zoe" uniqKey="Joly Lopez Z" first="Zoé" last="Joly-Lopez">Zoé Joly-Lopez</name>
</region>
<name sortKey="Blanchette, Mathieu" sort="Blanchette, Mathieu" uniqKey="Blanchette M" first="Mathieu" last="Blanchette">Mathieu Blanchette</name>
<name sortKey="Bureau, Thomas E" sort="Bureau, Thomas E" uniqKey="Bureau T" first="Thomas E." last="Bureau">Thomas E. Bureau</name>
<name sortKey="Hoen, Douglas R" sort="Hoen, Douglas R" uniqKey="Hoen D" first="Douglas R." last="Hoen">Douglas R. Hoen</name>
</country>
</tree>
</affiliations>
</record>
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