Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species
Identifieur interne : 000471 ( Ncbi/Merge ); précédent : 000470; suivant : 000472Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species
Auteurs : Amanda J. Waters ; Paul Bilinski ; Steven R. Eichten ; Matthew W. Vaughn ; Jeffrey Ross-Ibarra ; Mary Gehring ; Nathan M. SpringerSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2013.
Abstract
In many eukaryotes, reproduction involves contributions of genetic material from two parents. At some genes there are parent-of-origin differences in the expression of the maternal and paternal alleles of a gene and this is referred to as imprinting. The analysis of allele-specific expression in several maize hybrids allowed the comprehensive detection of imprinted genes. By comparing allelic expression patterns in multiple crosses, it was possible to observe allelic variation for imprinting in maize. The comparison of genes subject to imprinting in multiple plant species reveals limited conservation for imprinting. The subset of genes that exhibit conserved imprinting in maize and rice may play important, dosage-dependent roles in regulation of seed development.
Url:
DOI: 10.1073/pnas.1309182110
PubMed: 24218619
PubMed Central: 3845156
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<author><name sortKey="Waters, Amanda J" sort="Waters, Amanda J" uniqKey="Waters A" first="Amanda J." last="Waters">Amanda J. Waters</name>
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, St. Paul,<addr-line>MN</addr-line>
55108;</nlm:aff>
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<author><name sortKey="Eichten, Steven R" sort="Eichten, Steven R" uniqKey="Eichten S" first="Steven R." last="Eichten">Steven R. Eichten</name>
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<author><name sortKey="Ross Ibarra, Jeffrey" sort="Ross Ibarra, Jeffrey" uniqKey="Ross Ibarra J" first="Jeffrey" last="Ross-Ibarra">Jeffrey Ross-Ibarra</name>
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<affiliation><nlm:aff id="aff3">The Genome Center and Center for Population Biology,<institution>University of California, Davis</institution>
,<addr-line>CA</addr-line>
95616;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gehring, Mary" sort="Gehring, Mary" uniqKey="Gehring M" first="Mary" last="Gehring">Mary Gehring</name>
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<affiliation><nlm:aff id="aff6">Department of Biology,<institution>Massachusetts Institute of Technology</institution>
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<author><name sortKey="Springer, Nathan M" sort="Springer, Nathan M" uniqKey="Springer N" first="Nathan M." last="Springer">Nathan M. Springer</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species</title>
<author><name sortKey="Waters, Amanda J" sort="Waters, Amanda J" uniqKey="Waters A" first="Amanda J." last="Waters">Amanda J. Waters</name>
<affiliation><nlm:aff id="aff1">Microbial and Plant Genomics Institute and Department of Plant Biology,<institution>University of Minnesota</institution>
, St. Paul,<addr-line>MN</addr-line>
55108;</nlm:aff>
</affiliation>
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<author><name sortKey="Bilinski, Paul" sort="Bilinski, Paul" uniqKey="Bilinski P" first="Paul" last="Bilinski">Paul Bilinski</name>
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</affiliation>
</author>
<author><name sortKey="Eichten, Steven R" sort="Eichten, Steven R" uniqKey="Eichten S" first="Steven R." last="Eichten">Steven R. Eichten</name>
<affiliation><nlm:aff id="aff1">Microbial and Plant Genomics Institute and Department of Plant Biology,<institution>University of Minnesota</institution>
, St. Paul,<addr-line>MN</addr-line>
55108;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Vaughn, Matthew W" sort="Vaughn, Matthew W" uniqKey="Vaughn M" first="Matthew W." last="Vaughn">Matthew W. Vaughn</name>
<affiliation><nlm:aff id="aff4">Texas Advanced Computing Center,<institution>University of Texas–Austin</institution>
, Austin<addr-line>TX</addr-line>
78758;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ross Ibarra, Jeffrey" sort="Ross Ibarra, Jeffrey" uniqKey="Ross Ibarra J" first="Jeffrey" last="Ross-Ibarra">Jeffrey Ross-Ibarra</name>
<affiliation><nlm:aff wicri:cut=" and" id="aff2">Department of Plant Sciences</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff3">The Genome Center and Center for Population Biology,<institution>University of California, Davis</institution>
,<addr-line>CA</addr-line>
95616;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gehring, Mary" sort="Gehring, Mary" uniqKey="Gehring M" first="Mary" last="Gehring">Mary Gehring</name>
<affiliation><nlm:aff wicri:cut="; and" id="aff5"><institution>Whitehead Institute for Biomedical Research</institution>
, Cambridge,<addr-line>MA</addr-line>
02142</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff6">Department of Biology,<institution>Massachusetts Institute of Technology</institution>
, Cambridge,<addr-line>MA</addr-line>
02139</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Springer, Nathan M" sort="Springer, Nathan M" uniqKey="Springer N" first="Nathan M." last="Springer">Nathan M. Springer</name>
<affiliation><nlm:aff id="aff1">Microbial and Plant Genomics Institute and Department of Plant Biology,<institution>University of Minnesota</institution>
, St. Paul,<addr-line>MN</addr-line>
55108;</nlm:aff>
</affiliation>
</author>
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<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>In many eukaryotes, reproduction involves contributions of genetic material from two parents. At some genes there are parent-of-origin differences in the expression of the maternal and paternal alleles of a gene and this is referred to as imprinting. The analysis of allele-specific expression in several maize hybrids allowed the comprehensive detection of imprinted genes. By comparing allelic expression patterns in multiple crosses, it was possible to observe allelic variation for imprinting in maize. The comparison of genes subject to imprinting in multiple plant species reveals limited conservation for imprinting. The subset of genes that exhibit conserved imprinting in maize and rice may play important, dosage-dependent roles in regulation of seed development.</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">24218619</article-id>
<article-id pub-id-type="pmc">3845156</article-id>
<article-id pub-id-type="publisher-id">201309182</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1309182110</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Plant Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species</article-title>
<alt-title alt-title-type="short">Comprehensive analysis of imprinting in maize</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Waters</surname>
<given-names>Amanda J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bilinski</surname>
<given-names>Paul</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Eichten</surname>
<given-names>Steven R.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vaughn</surname>
<given-names>Matthew W.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ross-Ibarra</surname>
<given-names>Jeffrey</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gehring</surname>
<given-names>Mary</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Springer</surname>
<given-names>Nathan M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
Microbial and Plant Genomics Institute and Department of Plant Biology,<institution>University of Minnesota</institution>
, St. Paul,<addr-line>MN</addr-line>
55108;</aff>
<aff id="aff2"><sup>b</sup>
Department of Plant Sciences and</aff>
<aff id="aff3"><sup>d</sup>
The Genome Center and Center for Population Biology,<institution>University of California, Davis</institution>
,<addr-line>CA</addr-line>
95616;</aff>
<aff id="aff4"><sup>c</sup>
Texas Advanced Computing Center,<institution>University of Texas–Austin</institution>
, Austin<addr-line>TX</addr-line>
78758;</aff>
<aff id="aff5"><sup>e</sup>
<institution>Whitehead Institute for Biomedical Research</institution>
, Cambridge,<addr-line>MA</addr-line>
02142; and</aff>
<aff id="aff6"><sup>f</sup>
Department of Biology,<institution>Massachusetts Institute of Technology</institution>
, Cambridge,<addr-line>MA</addr-line>
02139</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. E-mail: <email>springer@umn.edu</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Steven E. Jacobsen, University of California, Los Angeles, CA, and approved October 18, 2013 (received for review May 17, 2013)</p>
</fn>
<fn fn-type="con"><p>Author contributions: A.J.W., M.G., and N.M.S. designed research; A.J.W. and S.R.E. performed research; M.W.V. contributed new reagents/analytic tools; A.J.W., P.B., S.R.E., J.R.-I., M.G., and N.M.S. analyzed data; and A.J.W. and N.M.S. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>26</day>
<month>11</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>11</day>
<month>11</month>
<year>2013</year>
</pub-date>
<volume>110</volume>
<issue>48</issue>
<fpage>19639</fpage>
<lpage>19644</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201309182.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>In many eukaryotes, reproduction involves contributions of genetic material from two parents. At some genes there are parent-of-origin differences in the expression of the maternal and paternal alleles of a gene and this is referred to as imprinting. The analysis of allele-specific expression in several maize hybrids allowed the comprehensive detection of imprinted genes. By comparing allelic expression patterns in multiple crosses, it was possible to observe allelic variation for imprinting in maize. The comparison of genes subject to imprinting in multiple plant species reveals limited conservation for imprinting. The subset of genes that exhibit conserved imprinting in maize and rice may play important, dosage-dependent roles in regulation of seed development.</p>
</abstract>
<abstract><p>In plants, a subset of genes exhibit imprinting in endosperm tissue such that expression is primarily from the maternal or paternal allele. Imprinting may arise as a consequence of mechanisms for silencing of transposons during reproduction, and in some cases imprinted expression of particular genes may provide a selective advantage such that it is conserved across species. Separate mechanisms for the origin of imprinted expression patterns and maintenance of these patterns may result in substantial variation in the targets of imprinting in different species. Here we present deep sequencing of RNAs isolated from reciprocal crosses of four diverse maize genotypes, providing a comprehensive analysis that allows evaluation of imprinting at more than 95% of endosperm-expressed genes. We find that over 500 genes exhibit statistically significant parent-of-origin effects in maize endosperm tissue, but focused our analyses on a subset of these genes that had >90% expression from the maternal allele (69 genes) or from the paternal allele (108 genes) in at least one reciprocal cross. Over 10% of imprinted genes show evidence of allelic variation for imprinting. A comparison of imprinting in maize and rice reveals that 13% of genes with syntenic orthologs in both species exhibit conserved imprinting. Genes that exhibit conserved imprinting between maize and rice have elevated nonsynonymous to synonymous substitution ratios compared with other imprinted genes, suggesting a history of more rapid evolution. Together, these data suggest that imprinting only has functional relevance at a subset of loci that currently exhibit imprinting in maize.</p>
</abstract>
<counts><page-count count="6"></page-count>
</counts>
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</front>
</pmc>
<affiliations><list></list>
<tree><noCountry><name sortKey="Bilinski, Paul" sort="Bilinski, Paul" uniqKey="Bilinski P" first="Paul" last="Bilinski">Paul Bilinski</name>
<name sortKey="Eichten, Steven R" sort="Eichten, Steven R" uniqKey="Eichten S" first="Steven R." last="Eichten">Steven R. Eichten</name>
<name sortKey="Gehring, Mary" sort="Gehring, Mary" uniqKey="Gehring M" first="Mary" last="Gehring">Mary Gehring</name>
<name sortKey="Ross Ibarra, Jeffrey" sort="Ross Ibarra, Jeffrey" uniqKey="Ross Ibarra J" first="Jeffrey" last="Ross-Ibarra">Jeffrey Ross-Ibarra</name>
<name sortKey="Springer, Nathan M" sort="Springer, Nathan M" uniqKey="Springer N" first="Nathan M." last="Springer">Nathan M. Springer</name>
<name sortKey="Vaughn, Matthew W" sort="Vaughn, Matthew W" uniqKey="Vaughn M" first="Matthew W." last="Vaughn">Matthew W. Vaughn</name>
<name sortKey="Waters, Amanda J" sort="Waters, Amanda J" uniqKey="Waters A" first="Amanda J." last="Waters">Amanda J. Waters</name>
</noCountry>
</tree>
</affiliations>
</record>
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