A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication
Identifieur interne : 000479 ( Pmc/Curation ); précédent : 000478; suivant : 000480A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication
Auteurs : Yan Zhong [République populaire de Chine] ; Zong-Ming Max Cheng [République populaire de Chine, États-Unis]Source :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Duplication, lateral gene transfer, domain fusion/fission and
Url:
DOI: 10.1038/srep32923
PubMed: 27678195
PubMed Central: 5039405
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication</title><author><name sortKey="Zhong, Yan" sort="Zhong, Yan" uniqKey="Zhong Y" first="Yan" last="Zhong">Yan Zhong</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>College of Horticulture, Nanjing Agricultural University</institution>, Nanjing, 210095,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Cheng, Zong Ming Max" sort="Cheng, Zong Ming Max" uniqKey="Cheng Z" first="Zong-Ming Max" last="Cheng">Zong-Ming Max Cheng</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>College of Horticulture, Nanjing Agricultural University</institution>, Nanjing, 210095,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Plant Science, University of Tennessee</institution>, Knoxville, 37996,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27678195</idno><idno type="pmc">5039405</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5039405</idno><idno type="RBID">PMC:5039405</idno><idno type="doi">10.1038/srep32923</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000480</idno><idno type="wicri:Area/Pmc/Curation">000479</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication</title><author><name sortKey="Zhong, Yan" sort="Zhong, Yan" uniqKey="Zhong Y" first="Yan" last="Zhong">Yan Zhong</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>College of Horticulture, Nanjing Agricultural University</institution>, Nanjing, 210095,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Cheng, Zong Ming Max" sort="Cheng, Zong Ming Max" uniqKey="Cheng Z" first="Zong-Ming Max" last="Cheng">Zong-Ming Max Cheng</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>College of Horticulture, Nanjing Agricultural University</institution>, Nanjing, 210095,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Plant Science, University of Tennessee</institution>, Knoxville, 37996,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Duplication, lateral gene transfer, domain fusion/fission and <italic>de novo</italic> domain creation play a key role in formation of initial common ancestral protein. Abundant protein diversities are produced by domain rearrangements, including fusions, fissions, duplications, and terminal domain losses. In this report, we explored the origin of the RPW8 domain and examined the domain rearrangements that have driven the evolution of RPW8-encoding genes in land plants. The RPW8 domain first emerged in the early land plant, <italic>Physcomitrella patens</italic>, and it likely originated <italic>de novo</italic> from a non-coding sequence or domain divergence after duplication. It was then incorporated into the NBS-LRR protein to create a main sub-class of RPW8-encoding genes, the RPW8-NBS-encoding genes. They evolved by a series of genetic events of domain fissions, fusions, and duplications. Many species-specific duplication events and tandemly duplicated clusters clearly demonstrated that species-specific and tandem duplications played important roles in expansion of RPW8-encoding genes, especially in gymnosperms and species of the Rosaceae. RPW8 domains with greater <italic>Ka</italic>/<italic>Ks</italic> values than those of the NBS domains indicated that they evolved faster than the NBS domains in RPW8-NBSs.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Moore, A D" uniqKey="Moore A">A. D. Moore</name></author><author><name sortKey="Bjorklund, A K" uniqKey="Bjorklund A">A. K. Bjorklund</name></author><author><name sortKey="Ekrnan, D" uniqKey="Ekrnan D">D. Ekrnan</name></author><author><name sortKey="Bornberg Bauer, E" uniqKey="Bornberg Bauer E">E. Bornberg-Bauer</name></author><author><name sortKey="Elofsson, A" uniqKey="Elofsson A">A. Elofsson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Levitt, M" uniqKey="Levitt M">M. Levitt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Apic, G" uniqKey="Apic G">G. Apic</name></author><author><name sortKey="Gough, J" uniqKey="Gough J">J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27678195</article-id><article-id pub-id-type="pmc">5039405</article-id><article-id pub-id-type="pii">srep32923</article-id><article-id pub-id-type="doi">10.1038/srep32923</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zhong</surname><given-names>Yan</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Cheng</surname><given-names>Zong-Ming (Max)</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="corresp" rid="c2">b</xref><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref></contrib><aff id="a1"><label>1</label><institution>College of Horticulture, Nanjing Agricultural University</institution>, Nanjing, 210095,<country>China</country></aff><aff id="a2"><label>2</label><institution>Department of Plant Science, University of Tennessee</institution>, Knoxville, 37996,<country>USA</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>zmc@njau.edu.cn</email></corresp><corresp id="c2"><label>b</label><email>zcheng@utk.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>28</day><month>09</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>32923</elocation-id><history><date date-type="received"><day>18</day><month>12</month><year>2015</year></date><date date-type="accepted"><day>16</day><month>08</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016, The Author(s)</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Duplication, lateral gene transfer, domain fusion/fission and <italic>de novo</italic> domain creation play a key role in formation of initial common ancestral protein. Abundant protein diversities are produced by domain rearrangements, including fusions, fissions, duplications, and terminal domain losses. In this report, we explored the origin of the RPW8 domain and examined the domain rearrangements that have driven the evolution of RPW8-encoding genes in land plants. The RPW8 domain first emerged in the early land plant, <italic>Physcomitrella patens</italic>, and it likely originated <italic>de novo</italic> from a non-coding sequence or domain divergence after duplication. It was then incorporated into the NBS-LRR protein to create a main sub-class of RPW8-encoding genes, the RPW8-NBS-encoding genes. They evolved by a series of genetic events of domain fissions, fusions, and duplications. Many species-specific duplication events and tandemly duplicated clusters clearly demonstrated that species-specific and tandem duplications played important roles in expansion of RPW8-encoding genes, especially in gymnosperms and species of the Rosaceae. RPW8 domains with greater <italic>Ka</italic>/<italic>Ks</italic> values than those of the NBS domains indicated that they evolved faster than the NBS domains in RPW8-NBSs.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Identification of RPW8-encoding genes across plant genomes.</title><p>The species tree on the left was obtained from Common Taxonomy Tree of NCBI (<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi">http://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi</ext-link>).</p></caption><graphic xlink:href="srep32923-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Domain organization of RPW8-encoding genes across plant genomes.</title><p>The Figure shows a list of the top 19 domains in all species. The “ + ” means presence of the corresponding domain in the specie, and “−” represents absence of the domain in the genome.</p></caption><graphic xlink:href="srep32923-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Two types of domain organization of RPW8-containing proteins.</title><p>The type 1 contains RPW8-NBSs, and the type 2 contains RPW8-non-NBSs, including RPW8-domain only and RPW8-X proteins. Most of RPW8-containing proteins have only one RPW8 domain, but RPW8-RPW8 (mrna11212.1), RPW8-RPW8-RPW8-Peptidase_C48 (mrna29374.1) and RNL-RNL (mrna24122.1) encode more than one RPW8 domains or NBS domains. “X” means domain other than RPW8 and NBS. “LRR” in the dashed box means present or absence of LRR in the related genes.</p></caption><graphic xlink:href="srep32923-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Genetic events of the RPW8 domain and other domains during the evolutionary history.</title><p>Dashed line represents non-coding region; dashed box means presence or absence of LRR domain in RPW8-encoding genes. (<bold>A</bold>,<bold>E</bold>): two hypotheses of domain emergence, <italic>de novo</italic> origination (<bold>A</bold>) and duplication-divergence (<bold>E</bold>) mechanism; (<bold>B</bold>): domain loss; (<bold>C</bold>): domain fission; (<bold>D</bold>): domain fusion; (<bold>F</bold>): duplication.</p></caption><graphic xlink:href="srep32923-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Genetic events of RPW8-encoding genes in the evolutionary tree of plants. Dashed line represents no RPW8-encoding gene in algae.</title></caption><graphic xlink:href="srep32923-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Phylogenetic analysis of RPW8-encoding genes in 20 plant species.</title><p>The tree was constructed by neighbor-joining (NJ) method from an alignment of amino acid sequences of 185 RPW8-encoding genes. Blue branch indicates RPW8-NBS-encoding genes, and pink branch shows RPW8-non-NBS-encoding genes.</p></caption><graphic xlink:href="srep32923-f6"></graphic></fig><fig id="f7"><label>Figure 7</label><caption><title>Phylogenetic tree of the RPW8 domains in 20 species.</title><p>The tree was constructed by NJ method with 1,000 replicates from an alignment of RPW8 domains from 185 RPW8-encoding genes.</p></caption><graphic xlink:href="srep32923-f7"></graphic></fig><fig id="f8"><label>Figure 8</label><caption><title>Linear analysis of <italic>Ka</italic>/<italic>Ks</italic> ratios between the RPW8 domains and the NBS domains.</title><p>The black line represents the trend line of dots and the red line means trend lines with slope = 1. The linear fitting was processed between RPW8 region and NBS region from RPW8-NBS-encoding genes in seven species, with linear fitting equation and an R<sup>2</sup> value.</p></caption><graphic xlink:href="srep32923-f8"></graphic></fig><fig id="f9"><label>Figure 9</label><caption><title>Distribution of <italic>Ka</italic> and <italic>Ka</italic>/<italic>Ks</italic> values in plant species with more RPW8-encoding genes.</title><p>The red triangle shows the RPW8 domain of RPW8-NBS-encoding gene, and the blue triangle indicates the NBS domain of RPW8-NBS-encoding gene.</p></caption><graphic xlink:href="srep32923-f9"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title><italic>Ks</italic> distribution of RPW8-encoding genes in ten plant species.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Ks range</th><th align="center" valign="top" charoff="50">A. thaliana</th><th align="center" valign="top" charoff="50">C.sinensis</th><th align="center" valign="top" charoff="50">C. sativus</th><th align="center" valign="top" charoff="50">F. vesca</th><th align="center" valign="top" charoff="50">G. raimondii</th><th align="center" valign="top" charoff="50">M. truncatula</th><th align="center" valign="top" charoff="50">P. abies</th><th align="center" valign="top" charoff="50">P. teada</th><th align="center" valign="top" charoff="50">P. trichocarpa</th><th align="center" valign="top" charoff="50">V. vinifera</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">0–0.1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">2</td></tr><tr><td align="left" valign="top" charoff="50">0.1–0.2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td></tr><tr><td align="left" valign="top" charoff="50">0.2–0.3</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">4</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">4</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.3–0.4</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">5</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.4–0.5</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">4</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.5–0.6</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td></tr><tr><td align="left" valign="top" charoff="50">0.6–0.7</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.7–0.8</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.8–0.9</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">0.9–1.0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">>1.0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">9</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">Total<xref ref-type="fn" rid="t1-fn1">a</xref></td><td align="center" valign="top" charoff="50">5</td><td align="center" valign="top" charoff="50">5</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">35</td><td align="center" valign="top" charoff="50">2</td><td align="center" valign="top" charoff="50">9</td><td align="center" valign="top" charoff="50">14</td><td align="center" valign="top" charoff="50">20<xref ref-type="fn" rid="t1-fn2">b</xref></td><td align="center" valign="top" charoff="50">3</td><td align="center" valign="top" charoff="50">4</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p><sup>a</sup>Total numbers of duplication times of RPW8-domain containing genes in each species based on the phylogenetic tree.</p></fn><fn id="t1-fn2"><p><sup>b</sup>There are 20 duplication events of RPW8-domain-containing genes of <italic>P. teada</italic>, but two duplication events had no <italic>Ks</italic> value (“n/c”).</p></fn></table-wrap-foot></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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