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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Lineage-specific expansions of TET/JBP genes and a new class of DNA transposons shape fungal genomic and epigenetic landscapes</title>
<author><name sortKey="Iyer, Lakshminarayan M" sort="Iyer, Lakshminarayan M" uniqKey="Iyer L" first="Lakshminarayan M." last="Iyer">Lakshminarayan M. Iyer</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Dapeng" sort="Zhang, Dapeng" uniqKey="Zhang D" first="Dapeng" last="Zhang">Dapeng Zhang</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="De Souza, Robson F" sort="De Souza, Robson F" uniqKey="De Souza R" first="Robson F." last="De Souza">Robson F. De Souza</name>
<affiliation><nlm:aff id="aff2">Microbiology Department, Biomedical Sciences Institute,<institution>University of Sao Paulo</institution>
, 05508-900, Sao Paulo,<country>Brazil</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Pukkila, Patricia J" sort="Pukkila, Patricia J" uniqKey="Pukkila P" first="Patricia J." last="Pukkila">Patricia J. Pukkila</name>
<affiliation><nlm:aff wicri:cut="; and" id="aff3">Department of Biology,<institution>University of North Carolina at Chapel Hill</institution>
, Chapel Hill,<addr-line>NC</addr-line>
27599-3280</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Rao, Anjana" sort="Rao, Anjana" uniqKey="Rao A" first="Anjana" last="Rao">Anjana Rao</name>
<affiliation><nlm:aff id="aff4"><institution>Sanford Consortium for Regenerative Medicine and La Jolla Institute for Allergy and Immunology</institution>
, La Jolla,<addr-line>CA</addr-line>
92037</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Aravind, L" sort="Aravind, L" uniqKey="Aravind L" first="L." last="Aravind">L. Aravind</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
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<idno type="pmid">24398522</idno>
<idno type="pmc">3918813</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3918813</idno>
<idno type="RBID">PMC:3918813</idno>
<idno type="doi">10.1073/pnas.1321818111</idno>
<date when="2014">2014</date>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Lineage-specific expansions of TET/JBP genes and a new class of DNA transposons shape fungal genomic and epigenetic landscapes</title>
<author><name sortKey="Iyer, Lakshminarayan M" sort="Iyer, Lakshminarayan M" uniqKey="Iyer L" first="Lakshminarayan M." last="Iyer">Lakshminarayan M. Iyer</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Dapeng" sort="Zhang, Dapeng" uniqKey="Zhang D" first="Dapeng" last="Zhang">Dapeng Zhang</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="De Souza, Robson F" sort="De Souza, Robson F" uniqKey="De Souza R" first="Robson F." last="De Souza">Robson F. De Souza</name>
<affiliation><nlm:aff id="aff2">Microbiology Department, Biomedical Sciences Institute,<institution>University of Sao Paulo</institution>
, 05508-900, Sao Paulo,<country>Brazil</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Pukkila, Patricia J" sort="Pukkila, Patricia J" uniqKey="Pukkila P" first="Patricia J." last="Pukkila">Patricia J. Pukkila</name>
<affiliation><nlm:aff wicri:cut="; and" id="aff3">Department of Biology,<institution>University of North Carolina at Chapel Hill</institution>
, Chapel Hill,<addr-line>NC</addr-line>
27599-3280</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Rao, Anjana" sort="Rao, Anjana" uniqKey="Rao A" first="Anjana" last="Rao">Anjana Rao</name>
<affiliation><nlm:aff id="aff4"><institution>Sanford Consortium for Regenerative Medicine and La Jolla Institute for Allergy and Immunology</institution>
, La Jolla,<addr-line>CA</addr-line>
92037</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Aravind, L" sort="Aravind, L" uniqKey="Aravind L" first="L." last="Aravind">L. Aravind</name>
<affiliation><nlm:aff id="aff1">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>5-Methylcytosine in DNA of eukaryotes, such as humans, is an important epigenetic mark. The recently characterized TET/JBP enzymes generate oxidized derivatives of methylcytosine, such as hydroxy-, formyl-, and carboxymethylcytosine in mammals, which serve as further epigenetic marks or intermediates for demethylation. Unlike animals, which contain one to three TET genes, fungi, such as mushrooms and rusts, display lineage-specific expansions with numerous TET/JBP genes, which are often associated with a unique class of transposable elements. We present evidence that expansion and turnover of these elements and associated TET/JBP genes play important roles in genomic organization, epigenetics, and speciation of fungal lineages, especially basidiomycetes (mushrooms, rusts, and smuts). Domesticated versions of these transposons might also participate in genome rearrangements or repair in humans.</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="iso-abbrev">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">24398522</article-id>
<article-id pub-id-type="pmc">3918813</article-id>
<article-id pub-id-type="publisher-id">201321818</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1321818111</article-id>
<article-categories><subj-group subj-group-type="hwp-journal-coll"><subject>1</subject>
</subj-group>
<subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Evolution</subject>
</subj-group>
</subj-group>
<series-title>Inaugural Article</series-title>
</article-categories>
<title-group><article-title>Lineage-specific expansions of TET/JBP genes and a new class of DNA transposons shape fungal genomic and epigenetic landscapes</article-title>
<alt-title alt-title-type="short">TET/JBP and transposons in fungi</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Iyer</surname>
<given-names>Lakshminarayan M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Dapeng</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Souza</surname>
<given-names>Robson F.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pukkila</surname>
<given-names>Patricia J.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rao</surname>
<given-names>Anjana</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Aravind</surname>
<given-names>L.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20894;</aff>
<aff id="aff2"><sup>b</sup>
Microbiology Department, Biomedical Sciences Institute,<institution>University of Sao Paulo</institution>
, 05508-900, Sao Paulo,<country>Brazil</country>
;</aff>
<aff id="aff3"><sup>c</sup>
Department of Biology,<institution>University of North Carolina at Chapel Hill</institution>
, Chapel Hill,<addr-line>NC</addr-line>
27599-3280; and</aff>
<aff id="aff4"><sup>d</sup>
<institution>Sanford Consortium for Regenerative Medicine and La Jolla Institute for Allergy and Immunology</institution>
, La Jolla,<addr-line>CA</addr-line>
92037</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>2</sup>
To whom correspondence may be addressed. E-mail: <email>arao@liai.org</email>
or <email>aravind@ncbi.nlm.nih.gov</email>
.</corresp>
<fn fn-type="edited-by"><p>This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2008.</p>
</fn>
<fn fn-type="edited-by"><p>Contributed by Anjana Rao, December 17, 2013 (sent for review September 20, 2013)</p>
</fn>
<fn fn-type="con"><p>Author contributions: L.M.I., D.Z., A.R., and L.A. designed research; L.M.I., D.Z., and L.A. performed research; L.M.I., D.Z., R.F.d.S., P.J.P., and A.R. contributed new reagents/analytic tools; L.M.I., D.Z., R.F.d.S., and L.A. analyzed data; and A.R. and L.A. wrote the paper.</p>
</fn>
<fn id="fn1" fn-type="equal"><p><sup>1</sup>
L.M.I. and D.Z. contributed equally to this work.</p>
</fn>
<fn fn-type="conflict"><p>The authors declare no conflict of interest.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>4</day>
<month>2</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>7</day>
<month>1</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>7</day>
<month>1</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>111</volume>
<issue>5</issue>
<fpage>1676</fpage>
<lpage>1683</lpage>
<permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201321818.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>5-Methylcytosine in DNA of eukaryotes, such as humans, is an important epigenetic mark. The recently characterized TET/JBP enzymes generate oxidized derivatives of methylcytosine, such as hydroxy-, formyl-, and carboxymethylcytosine in mammals, which serve as further epigenetic marks or intermediates for demethylation. Unlike animals, which contain one to three TET genes, fungi, such as mushrooms and rusts, display lineage-specific expansions with numerous TET/JBP genes, which are often associated with a unique class of transposable elements. We present evidence that expansion and turnover of these elements and associated TET/JBP genes play important roles in genomic organization, epigenetics, and speciation of fungal lineages, especially basidiomycetes (mushrooms, rusts, and smuts). Domesticated versions of these transposons might also participate in genome rearrangements or repair in humans.</p>
</abstract>
<abstract><p>TET/JBP dioxygenases oxidize methylpyrimidines in nucleic acids and are implicated in generation of epigenetic marks and potential intermediates for DNA demethylation. We show that TET/JBP genes are lineage-specifically expanded in all major clades of basidiomycete fungi, with the majority of copies predicted to encode catalytically active proteins. This pattern differs starkly from the situation in most other organisms that possess just a single or a few copies of the TET/JBP family. In most basidiomycetes, TET/JBP genes are frequently linked to a unique class of transposons, KDZ (Kyakuja, Dileera, and Zisupton) and appear to have dispersed across chromosomes along with them. Several of these elements typically encode additional proteins, including a divergent version of the HMG domain. Analysis of their transposases shows that they contain a previously uncharacterized version of the RNase H fold with multiple distinctive Zn-chelating motifs and a unique insert, which are predicted to play roles in structural stabilization and target sequence recognition, respectively. We reconstruct the complex evolutionary history of TET/JBPs and associated transposons as involving multiple rounds of expansion with concomitant lineage sorting and loss, along with several capture events of TET/JBP genes by different transposon clades. On a few occasions, these TET/JBP genes were also laterally transferred to certain Ascomycota, Glomeromycota, Viridiplantae, and Amoebozoa. One such is an inactive version, calnexin-independence factor 1 (Cif1), from <italic>Schizosaccharomyces pombe</italic>
, which has been implicated in inducing an epigenetically transmitted prion state. We argue that this unique transposon-TET/JBP association is likely to play important roles in speciation during evolution and epigenetic regulation.</p>
</abstract>
<kwd-group><kwd>methylcytosine</kwd>
<kwd>fungal evolution</kwd>
<kwd>DNA modification</kwd>
<kwd>genomic association</kwd>
</kwd-group>
<counts><page-count count="8"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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