The Complex Intron Landscape and Massive Intron Invasion in a Picoeukaryote Provides Insights into Intron Evolution
Identifieur interne : 000260 ( Pmc/Checkpoint ); précédent : 000259; suivant : 000261The Complex Intron Landscape and Massive Intron Invasion in a Picoeukaryote Provides Insights into Intron Evolution
Auteurs : Bram Verhelst [Belgique] ; Yves Van De Peer [Belgique, Afrique du Sud] ; Pierre Rouzé [Belgique]Source :
- Genome Biology and Evolution [ 1759-6653 ] ; 2013.
Abstract
Genes in pieces and spliceosomal introns are a landmark of eukaryotes, with intron invasion usually assumed to have happened early on in evolution. Here, we analyze the intron landscape of
Url:
DOI: 10.1093/gbe/evt189
PubMed: 24273312
PubMed Central: 3879977
Affiliations:
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Complex Intron Landscape and Massive Intron Invasion in a Picoeukaryote Provides Insights into Intron Evolution</title>
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<author><name sortKey="Van De Peer, Yves" sort="Van De Peer, Yves" uniqKey="Van De Peer Y" first="Yves" last="Van De Peer">Yves Van De Peer</name>
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<front><div type="abstract" xml:lang="en"><p>Genes in pieces and spliceosomal introns are a landmark of eukaryotes, with intron invasion usually assumed to have happened early on in evolution. Here, we analyze the intron landscape of <italic>Micromonas</italic>
, a unicellular green alga in the Mamiellophyceae lineage, demonstrating the coexistence of several classes of introns and the occurrence of recent massive intron invasion. This study focuses on two strains, CCMP1545 and RCC299, and their related individuals from ocean samplings, showing that they not only harbor different classes of introns depending on their location in the genome, as for other Mamiellophyceae, but also uniquely carry several classes of repeat introns. These introns, dubbed introner elements (IEs), are found at novel positions in genes and have conserved sequences, contrary to canonical introns. This IE invasion has a huge impact on the genome, doubling the number of introns in the CCMP1545 strain. We hypothesize that each IE class originated from a single ancestral IE that has been colonizing the genome after strain divergence by inserting copies of itself into genes by intron transposition, likely involving reverse splicing. Along with similar cases recently observed in other organisms, our observations in <italic>Micromonas</italic>
strains shed a new light on the evolution of introns, suggesting that intron gain is more widespread than previously thought.</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">Genome Biol Evol</journal-id>
<journal-id journal-id-type="iso-abbrev">Genome Biol Evol</journal-id>
<journal-id journal-id-type="publisher-id">gbe</journal-id>
<journal-id journal-id-type="hwp">gbe</journal-id>
<journal-title-group><journal-title>Genome Biology and Evolution</journal-title>
</journal-title-group>
<issn pub-type="epub">1759-6653</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24273312</article-id>
<article-id pub-id-type="pmc">3879977</article-id>
<article-id pub-id-type="doi">10.1093/gbe/evt189</article-id>
<article-id pub-id-type="publisher-id">evt189</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Complex Intron Landscape and Massive Intron Invasion in a Picoeukaryote Provides Insights into Intron Evolution</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Verhelst</surname>
<given-names>Bram</given-names>
</name>
<xref ref-type="aff" rid="evt189-AFF1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="evt189-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Van de Peer</surname>
<given-names>Yves</given-names>
</name>
<xref ref-type="aff" rid="evt189-AFF1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="evt189-AFF2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="evt189-AFF3"><sup>3</sup>
</xref>
<xref ref-type="corresp" rid="evt189-COR1">*</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Rouzé</surname>
<given-names>Pierre</given-names>
</name>
<xref ref-type="aff" rid="evt189-AFF1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="evt189-AFF2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="evt189-AFF1">*</xref>
</contrib>
</contrib-group>
<aff id="evt189-AFF1"><sup>1</sup>
Department of Plant Biotechnology and Bioinformatics, Ghent University, Belgium</aff>
<aff id="evt189-AFF2"><sup>2</sup>
Department of Plant Systems Biology, VIB, Ghent, Belgium</aff>
<aff id="evt189-AFF3"><sup>3</sup>
Department of Genetics, Genomics Research Institute, University of Pretoria, South Africa</aff>
<author-notes><corresp id="evt189-COR1">*Corresponding author: E-mail: <email>yves.vandepeer@psb.ugent.be</email>
; <email>pierre.rouze@psb.ugent.be</email>
.</corresp>
<fn><p><bold>Associate editor:</bold>
Bill Martin</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>20</day>
<month>11</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection"><month>12</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>20</day>
<month>11</month>
<year>2013</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>5</volume>
<issue>12</issue>
<fpage>2393</fpage>
<lpage>2401</lpage>
<history><date date-type="accepted"><day>18</day>
<month>11</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>
), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Genes in pieces and spliceosomal introns are a landmark of eukaryotes, with intron invasion usually assumed to have happened early on in evolution. Here, we analyze the intron landscape of <italic>Micromonas</italic>
, a unicellular green alga in the Mamiellophyceae lineage, demonstrating the coexistence of several classes of introns and the occurrence of recent massive intron invasion. This study focuses on two strains, CCMP1545 and RCC299, and their related individuals from ocean samplings, showing that they not only harbor different classes of introns depending on their location in the genome, as for other Mamiellophyceae, but also uniquely carry several classes of repeat introns. These introns, dubbed introner elements (IEs), are found at novel positions in genes and have conserved sequences, contrary to canonical introns. This IE invasion has a huge impact on the genome, doubling the number of introns in the CCMP1545 strain. We hypothesize that each IE class originated from a single ancestral IE that has been colonizing the genome after strain divergence by inserting copies of itself into genes by intron transposition, likely involving reverse splicing. Along with similar cases recently observed in other organisms, our observations in <italic>Micromonas</italic>
strains shed a new light on the evolution of introns, suggesting that intron gain is more widespread than previously thought.</p>
</abstract>
<kwd-group><kwd>intron evolution</kwd>
<kwd>intron gain</kwd>
<kwd>Mamiellophyceae</kwd>
<kwd><italic>Micromonas</italic>
</kwd>
<kwd>introner elements</kwd>
</kwd-group>
<counts><page-count count="9"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Afrique du Sud</li>
<li>Belgique</li>
</country>
</list>
<tree><country name="Belgique"><noRegion><name sortKey="Verhelst, Bram" sort="Verhelst, Bram" uniqKey="Verhelst B" first="Bram" last="Verhelst">Bram Verhelst</name>
</noRegion>
<name sortKey="Rouze, Pierre" sort="Rouze, Pierre" uniqKey="Rouze P" first="Pierre" last="Rouzé">Pierre Rouzé</name>
<name sortKey="Rouze, Pierre" sort="Rouze, Pierre" uniqKey="Rouze P" first="Pierre" last="Rouzé">Pierre Rouzé</name>
<name sortKey="Van De Peer, Yves" sort="Van De Peer, Yves" uniqKey="Van De Peer Y" first="Yves" last="Van De Peer">Yves Van De Peer</name>
<name sortKey="Van De Peer, Yves" sort="Van De Peer, Yves" uniqKey="Van De Peer Y" first="Yves" last="Van De Peer">Yves Van De Peer</name>
<name sortKey="Verhelst, Bram" sort="Verhelst, Bram" uniqKey="Verhelst B" first="Bram" last="Verhelst">Bram Verhelst</name>
</country>
<country name="Afrique du Sud"><noRegion><name sortKey="Van De Peer, Yves" sort="Van De Peer, Yves" uniqKey="Van De Peer Y" first="Yves" last="Van De Peer">Yves Van De Peer</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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