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Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common1[W][OA]

Identifieur interne : 000471 ( Ncbi/Merge ); précédent : 000470; suivant : 000472

Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common1[W][OA]

Auteurs : Adam Wawrzynski ; Tom Ashfield ; Nicolas W. G. Chen ; Jafar Mammadov ; Ashley Nguyen ; Ram Podicheti ; Steven B. Cannon ; Vincent Thareau ; Carine Ameline-Torregrosa ; Ethalinda Cannon ; Ben Chacko ; Arnaud Couloux ; Anita Dalwani ; Roxanne Denny ; Shweta Deshpande ; Ashley N. Egan ; Natasha Glover ; Stacy Howell ; Dan Ilut ; Hongshing Lai ; Sara Martin Del Campo ; Michelle Metcalf ; Majesta O'Bleness ; Bernard E. Pfeil ; Milind B. Ratnaparkhe ; Sylvie Samain ; Iryna Sanders ; Béatrice Ségurens ; Mireille Sévignac ; Sue Sherman-Broyles ; Dominic M. Tucker ; Jing Yi ; Jeff J. Doyle ; Valérie Geffroy ; Bruce A. Roe ; M. A. Saghai Maroof ; Nevin D. Young ; Roger W. Innes

Source :

RBID : PMC:2593652

Abstract

Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (Zea mays) and rice (Oryza sativa), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (Glycine max). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from Glycine tomentella, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from Phaseolus vulgaris (common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in Glycine and Phaseolus. The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.


Url:
DOI: 10.1104/pp.108.127910
PubMed: 18952860
PubMed Central: 2593652

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PMC:2593652

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<title xml:lang="en" level="a" type="main">Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common
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<name sortKey="Metcalf, Michelle" sort="Metcalf, Michelle" uniqKey="Metcalf M" first="Michelle" last="Metcalf">Michelle Metcalf</name>
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<div type="abstract" xml:lang="en">
<p>Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (
<italic>Zea mays</italic>
) and rice (
<italic>Oryza sativa</italic>
), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (
<italic>Glycine max</italic>
). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from
<italic>Glycine tomentella</italic>
, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from
<italic>Phaseolus vulgaris</italic>
(common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in
<italic>Glycine</italic>
and
<italic>Phaseolus</italic>
. The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.</p>
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<subject>Genome Analysis</subject>
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<title-group>
<article-title>Replication of Nonautonomous Retroelements in Soybean Appears to Be Both Recent and Common
<xref ref-type="fn" rid="fn1">1</xref>
<xref ref-type="fn" rid="fn3">[W]</xref>
<xref ref-type="fn" rid="fn4">[OA]</xref>
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<contrib contrib-type="author">
<name>
<surname>Wawrzynski</surname>
<given-names>Adam</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ashfield</surname>
<given-names>Tom</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chen</surname>
<given-names>Nicolas W.G.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mammadov</surname>
<given-names>Jafar</given-names>
</name>
<xref ref-type="fn" rid="fn2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nguyen</surname>
<given-names>Ashley</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Podicheti</surname>
<given-names>Ram</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cannon</surname>
<given-names>Steven B.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Thareau</surname>
<given-names>Vincent</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ameline-Torregrosa</surname>
<given-names>Carine</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cannon</surname>
<given-names>Ethalinda</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chacko</surname>
<given-names>Ben</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Couloux</surname>
<given-names>Arnaud</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dalwani</surname>
<given-names>Anita</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Denny</surname>
<given-names>Roxanne</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Deshpande</surname>
<given-names>Shweta</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Egan</surname>
<given-names>Ashley N.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Glover</surname>
<given-names>Natasha</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Howell</surname>
<given-names>Stacy</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ilut</surname>
<given-names>Dan</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lai</surname>
<given-names>Hongshing</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>del Campo</surname>
<given-names>Sara Martin</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Metcalf</surname>
<given-names>Michelle</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>O'Bleness</surname>
<given-names>Majesta</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pfeil</surname>
<given-names>Bernard E.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ratnaparkhe</surname>
<given-names>Milind B.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Samain</surname>
<given-names>Sylvie</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sanders</surname>
<given-names>Iryna</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ségurens</surname>
<given-names>Béatrice</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sévignac</surname>
<given-names>Mireille</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sherman-Broyles</surname>
<given-names>Sue</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tucker</surname>
<given-names>Dominic M.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Yi</surname>
<given-names>Jing</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Doyle</surname>
<given-names>Jeff J.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Geffroy</surname>
<given-names>Valérie</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Roe</surname>
<given-names>Bruce A.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Maroof</surname>
<given-names>M.A. Saghai</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Young</surname>
<given-names>Nevin D.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Innes</surname>
<given-names>Roger W.</given-names>
</name>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
</contrib-group>
<aff id="N0x1d83860N0x3bb2010">Department of Biology, Indiana University, Bloomington, Indiana 47405 (A.W., T.A., R.P., A.D., S.H., S.M.d.C., M.M., R.W.I.); Institut de Biotechnologie des Plantes, UMR CNRS 8618, INRA, Université Paris Sud, 91 405 Orsay, France (N.W.G.C., V.T., M.S., V.G.); Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, Virginia 24061 (J.M., A.N., N.G., M.B.R., D.M.T., M.A.S.M.); Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108 (S.B.C., C.A.-T., E.C., B.C., R.D., N.D.Y.); U.S. Department of Agriculture-Agricultural Research Service and Department of Agronomy (S.B.C.), and Virtual Reality Application Center (E.C.), Iowa State University, Ames, Iowa 50011; Genoscope/CEA-Centre National de Séquençage, 91 057 Evry, France (A.C., S.S., B.S.); Department of Chemistry and Biochemistry, University of Oklahoma, Norman, Oklahoma 73019 (S.D., H.L., M.O., I.S., J.Y., B.A.R.); L.H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York 14853 (A.N.E., D.I., B.E.P., S.S.-B., J.J.D.); CSIRO Plant Industry, Canberra, Australian Capital Territory 2601, Australia (B.E.P.); and Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211 (M.B.R.)</aff>
<author-notes>
<fn id="cor1">
<label>*</label>
<p>Corresponding author; e-mail
<email>rinnes@indiana.edu</email>
.</p>
</fn>
<fn id="fn2">
<label>2</label>
<p>Present address: Trait Genetics and Technology, Dow AgroSciences LLC, Indianapolis, IN 46268.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<month>12</month>
<year>2008</year>
</pub-date>
<volume>148</volume>
<issue>4</issue>
<fpage>1760</fpage>
<lpage>1771</lpage>
<history>
<date date-type="received">
<day>10</day>
<month>8</month>
<year>2008</year>
</date>
<date date-type="accepted">
<day>22</day>
<month>10</month>
<year>2008</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2008, American Society of Plant Biologists</copyright-statement>
</permissions>
<abstract>
<p>Retrotransposons and their remnants often constitute more than 50% of higher plant genomes. Although extensively studied in monocot crops such as maize (
<italic>Zea mays</italic>
) and rice (
<italic>Oryza sativa</italic>
), the impact of retrotransposons on dicot crop genomes is not well documented. Here, we present an analysis of retrotransposons in soybean (
<italic>Glycine max</italic>
). Analysis of approximately 3.7 megabases (Mb) of genomic sequence, including 0.87 Mb of pericentromeric sequence, uncovered 45 intact long terminal repeat (LTR)-retrotransposons. The ratio of intact elements to solo LTRs was 8:1, one of the highest reported to date in plants, suggesting that removal of retrotransposons by homologous recombination between LTRs is occurring more slowly in soybean than in previously characterized plant species. Analysis of paired LTR sequences uncovered a low frequency of deletions relative to base substitutions, indicating that removal of retrotransposon sequences by illegitimate recombination is also operating more slowly. Significantly, we identified three subfamilies of nonautonomous elements that have replicated in the recent past, suggesting that retrotransposition can be catalyzed in trans by autonomous elements elsewhere in the genome. Analysis of 1.6 Mb of sequence from
<italic>Glycine tomentella</italic>
, a wild perennial relative of soybean, uncovered 23 intact retroelements, two of which had accumulated no mutations in their LTRs, indicating very recent insertion. A similar pattern was found in 0.94 Mb of sequence from
<italic>Phaseolus vulgaris</italic>
(common bean). Thus, autonomous and nonautonomous retrotransposons appear to be both abundant and active in
<italic>Glycine</italic>
and
<italic>Phaseolus</italic>
. The impact of nonautonomous retrotransposon replication on genome size appears to be much greater than previously appreciated.</p>
</abstract>
</article-meta>
<notes>
<fn-group>
<fn id="fn1">
<label>1</label>
<p>This work was supported by the National Science Foundation (Plant Genome Research Program grant no. DBI–0321664 to R.W.I., M.A.S.M., N.D.Y., B.A.R., and J.J.D. and Systematics award no. DEB–0516673 to A.N.E.) and by Genoscope/CEA-Centre National de Séquençage (grant to V.G.).</p>
</fn>
<fn>
<p>The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (
<ext-link ext-link-type="uri" xlink:href="www.plantphysiol.org">www.plantphysiol.org</ext-link>
) is: Roger W. Innes (
<email>rinnes@indiana.edu</email>
).</p>
</fn>
<fn id="fn3">
<label>[W]</label>
<p>The online version of this article contains Web-only data.</p>
</fn>
<fn id="fn4">
<label>[OA]</label>
<p>Open access articles can be viewed online without a subscription.</p>
</fn>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="www.plantphysiol.org/cgi/doi/10.1104/pp.108.127910">www.plantphysiol.org/cgi/doi/10.1104/pp.108.127910</ext-link>
</p>
</fn>
</fn-group>
</notes>
</front>
</pmc>
<affiliations>
<list></list>
<tree>
<noCountry>
<name sortKey="Ameline Torregrosa, Carine" sort="Ameline Torregrosa, Carine" uniqKey="Ameline Torregrosa C" first="Carine" last="Ameline-Torregrosa">Carine Ameline-Torregrosa</name>
<name sortKey="Ashfield, Tom" sort="Ashfield, Tom" uniqKey="Ashfield T" first="Tom" last="Ashfield">Tom Ashfield</name>
<name sortKey="Cannon, Ethalinda" sort="Cannon, Ethalinda" uniqKey="Cannon E" first="Ethalinda" last="Cannon">Ethalinda Cannon</name>
<name sortKey="Cannon, Steven B" sort="Cannon, Steven B" uniqKey="Cannon S" first="Steven B." last="Cannon">Steven B. Cannon</name>
<name sortKey="Chacko, Ben" sort="Chacko, Ben" uniqKey="Chacko B" first="Ben" last="Chacko">Ben Chacko</name>
<name sortKey="Chen, Nicolas W G" sort="Chen, Nicolas W G" uniqKey="Chen N" first="Nicolas W. G." last="Chen">Nicolas W. G. Chen</name>
<name sortKey="Couloux, Arnaud" sort="Couloux, Arnaud" uniqKey="Couloux A" first="Arnaud" last="Couloux">Arnaud Couloux</name>
<name sortKey="Dalwani, Anita" sort="Dalwani, Anita" uniqKey="Dalwani A" first="Anita" last="Dalwani">Anita Dalwani</name>
<name sortKey="Del Campo, Sara Martin" sort="Del Campo, Sara Martin" uniqKey="Del Campo S" first="Sara Martin" last="Del Campo">Sara Martin Del Campo</name>
<name sortKey="Denny, Roxanne" sort="Denny, Roxanne" uniqKey="Denny R" first="Roxanne" last="Denny">Roxanne Denny</name>
<name sortKey="Deshpande, Shweta" sort="Deshpande, Shweta" uniqKey="Deshpande S" first="Shweta" last="Deshpande">Shweta Deshpande</name>
<name sortKey="Doyle, Jeff J" sort="Doyle, Jeff J" uniqKey="Doyle J" first="Jeff J." last="Doyle">Jeff J. Doyle</name>
<name sortKey="Egan, Ashley N" sort="Egan, Ashley N" uniqKey="Egan A" first="Ashley N." last="Egan">Ashley N. Egan</name>
<name sortKey="Geffroy, Valerie" sort="Geffroy, Valerie" uniqKey="Geffroy V" first="Valérie" last="Geffroy">Valérie Geffroy</name>
<name sortKey="Glover, Natasha" sort="Glover, Natasha" uniqKey="Glover N" first="Natasha" last="Glover">Natasha Glover</name>
<name sortKey="Howell, Stacy" sort="Howell, Stacy" uniqKey="Howell S" first="Stacy" last="Howell">Stacy Howell</name>
<name sortKey="Ilut, Dan" sort="Ilut, Dan" uniqKey="Ilut D" first="Dan" last="Ilut">Dan Ilut</name>
<name sortKey="Innes, Roger W" sort="Innes, Roger W" uniqKey="Innes R" first="Roger W." last="Innes">Roger W. Innes</name>
<name sortKey="Lai, Hongshing" sort="Lai, Hongshing" uniqKey="Lai H" first="Hongshing" last="Lai">Hongshing Lai</name>
<name sortKey="Mammadov, Jafar" sort="Mammadov, Jafar" uniqKey="Mammadov J" first="Jafar" last="Mammadov">Jafar Mammadov</name>
<name sortKey="Maroof, M A Saghai" sort="Maroof, M A Saghai" uniqKey="Maroof M" first="M. A. Saghai" last="Maroof">M. A. Saghai Maroof</name>
<name sortKey="Metcalf, Michelle" sort="Metcalf, Michelle" uniqKey="Metcalf M" first="Michelle" last="Metcalf">Michelle Metcalf</name>
<name sortKey="Nguyen, Ashley" sort="Nguyen, Ashley" uniqKey="Nguyen A" first="Ashley" last="Nguyen">Ashley Nguyen</name>
<name sortKey="O Bleness, Majesta" sort="O Bleness, Majesta" uniqKey="O Bleness M" first="Majesta" last="O'Bleness">Majesta O'Bleness</name>
<name sortKey="Pfeil, Bernard E" sort="Pfeil, Bernard E" uniqKey="Pfeil B" first="Bernard E." last="Pfeil">Bernard E. Pfeil</name>
<name sortKey="Podicheti, Ram" sort="Podicheti, Ram" uniqKey="Podicheti R" first="Ram" last="Podicheti">Ram Podicheti</name>
<name sortKey="Ratnaparkhe, Milind B" sort="Ratnaparkhe, Milind B" uniqKey="Ratnaparkhe M" first="Milind B." last="Ratnaparkhe">Milind B. Ratnaparkhe</name>
<name sortKey="Roe, Bruce A" sort="Roe, Bruce A" uniqKey="Roe B" first="Bruce A." last="Roe">Bruce A. Roe</name>
<name sortKey="Samain, Sylvie" sort="Samain, Sylvie" uniqKey="Samain S" first="Sylvie" last="Samain">Sylvie Samain</name>
<name sortKey="Sanders, Iryna" sort="Sanders, Iryna" uniqKey="Sanders I" first="Iryna" last="Sanders">Iryna Sanders</name>
<name sortKey="Segurens, Beatrice" sort="Segurens, Beatrice" uniqKey="Segurens B" first="Béatrice" last="Ségurens">Béatrice Ségurens</name>
<name sortKey="Sevignac, Mireille" sort="Sevignac, Mireille" uniqKey="Sevignac M" first="Mireille" last="Sévignac">Mireille Sévignac</name>
<name sortKey="Sherman Broyles, Sue" sort="Sherman Broyles, Sue" uniqKey="Sherman Broyles S" first="Sue" last="Sherman-Broyles">Sue Sherman-Broyles</name>
<name sortKey="Thareau, Vincent" sort="Thareau, Vincent" uniqKey="Thareau V" first="Vincent" last="Thareau">Vincent Thareau</name>
<name sortKey="Tucker, Dominic M" sort="Tucker, Dominic M" uniqKey="Tucker D" first="Dominic M." last="Tucker">Dominic M. Tucker</name>
<name sortKey="Wawrzynski, Adam" sort="Wawrzynski, Adam" uniqKey="Wawrzynski A" first="Adam" last="Wawrzynski">Adam Wawrzynski</name>
<name sortKey="Yi, Jing" sort="Yi, Jing" uniqKey="Yi J" first="Jing" last="Yi">Jing Yi</name>
<name sortKey="Young, Nevin D" sort="Young, Nevin D" uniqKey="Young N" first="Nevin D." last="Young">Nevin D. Young</name>
</noCountry>
</tree>
</affiliations>
</record>

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