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<title xml:lang="en">An Ancient Duplication of Apple MYB Transcription Factors Is Responsible for Novel Red Fruit-Flesh Phenotypes
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[W]</sup>
</xref>
</title>
<author>
<name sortKey="Chagne, David" sort="Chagne, David" uniqKey="Chagne D" first="David" last="Chagné">David Chagné</name>
</author>
<author>
<name sortKey="Lin Wang, Kui" sort="Lin Wang, Kui" uniqKey="Lin Wang K" first="Kui" last="Lin-Wang">Kui Lin-Wang</name>
</author>
<author>
<name sortKey="Espley, Richard V" sort="Espley, Richard V" uniqKey="Espley R" first="Richard V." last="Espley">Richard V. Espley</name>
</author>
<author>
<name sortKey="Volz, Richard K" sort="Volz, Richard K" uniqKey="Volz R" first="Richard K." last="Volz">Richard K. Volz</name>
</author>
<author>
<name sortKey="How, Natalie M" sort="How, Natalie M" uniqKey="How N" first="Natalie M." last="How">Natalie M. How</name>
</author>
<author>
<name sortKey="Rouse, Simon" sort="Rouse, Simon" uniqKey="Rouse S" first="Simon" last="Rouse">Simon Rouse</name>
</author>
<author>
<name sortKey="Brendolise, Cyril" sort="Brendolise, Cyril" uniqKey="Brendolise C" first="Cyril" last="Brendolise">Cyril Brendolise</name>
</author>
<author>
<name sortKey="Carlisle, Charmaine M" sort="Carlisle, Charmaine M" uniqKey="Carlisle C" first="Charmaine M." last="Carlisle">Charmaine M. Carlisle</name>
</author>
<author>
<name sortKey="Kumar, Satish" sort="Kumar, Satish" uniqKey="Kumar S" first="Satish" last="Kumar">Satish Kumar</name>
</author>
<author>
<name sortKey="De Silva, Nihal" sort="De Silva, Nihal" uniqKey="De Silva N" first="Nihal" last="De Silva">Nihal De Silva</name>
</author>
<author>
<name sortKey="Micheletti, Diego" sort="Micheletti, Diego" uniqKey="Micheletti D" first="Diego" last="Micheletti">Diego Micheletti</name>
</author>
<author>
<name sortKey="Mcghie, Tony" sort="Mcghie, Tony" uniqKey="Mcghie T" first="Tony" last="Mcghie">Tony Mcghie</name>
</author>
<author>
<name sortKey="Crowhurst, Ross N" sort="Crowhurst, Ross N" uniqKey="Crowhurst R" first="Ross N." last="Crowhurst">Ross N. Crowhurst</name>
</author>
<author>
<name sortKey="Storey, Roy D" sort="Storey, Roy D" uniqKey="Storey R" first="Roy D." last="Storey">Roy D. Storey</name>
</author>
<author>
<name sortKey="Velasco, Riccardo" sort="Velasco, Riccardo" uniqKey="Velasco R" first="Riccardo" last="Velasco">Riccardo Velasco</name>
</author>
<author>
<name sortKey="Hellens, Roger P" sort="Hellens, Roger P" uniqKey="Hellens R" first="Roger P." last="Hellens">Roger P. Hellens</name>
</author>
<author>
<name sortKey="Gardiner, Susan E" sort="Gardiner, Susan E" uniqKey="Gardiner S" first="Susan E." last="Gardiner">Susan E. Gardiner</name>
</author>
<author>
<name sortKey="Allan, Andrew C" sort="Allan, Andrew C" uniqKey="Allan A" first="Andrew C." last="Allan">Andrew C. Allan</name>
</author>
</titleStmt>
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<idno type="wicri:source">PMC</idno>
<idno type="pmid">23096157</idno>
<idno type="pmc">3532254</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3532254</idno>
<idno type="RBID">PMC:3532254</idno>
<idno type="doi">10.1104/pp.112.206771</idno>
<date when="2012">2012</date>
<idno type="wicri:Area/Pmc/Corpus">000D05</idno>
</publicationStmt>
<sourceDesc>
<biblStruct>
<analytic>
<title xml:lang="en" level="a" type="main">An Ancient Duplication of Apple MYB Transcription Factors Is Responsible for Novel Red Fruit-Flesh Phenotypes
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[W]</sup>
</xref>
</title>
<author>
<name sortKey="Chagne, David" sort="Chagne, David" uniqKey="Chagne D" first="David" last="Chagné">David Chagné</name>
</author>
<author>
<name sortKey="Lin Wang, Kui" sort="Lin Wang, Kui" uniqKey="Lin Wang K" first="Kui" last="Lin-Wang">Kui Lin-Wang</name>
</author>
<author>
<name sortKey="Espley, Richard V" sort="Espley, Richard V" uniqKey="Espley R" first="Richard V." last="Espley">Richard V. Espley</name>
</author>
<author>
<name sortKey="Volz, Richard K" sort="Volz, Richard K" uniqKey="Volz R" first="Richard K." last="Volz">Richard K. Volz</name>
</author>
<author>
<name sortKey="How, Natalie M" sort="How, Natalie M" uniqKey="How N" first="Natalie M." last="How">Natalie M. How</name>
</author>
<author>
<name sortKey="Rouse, Simon" sort="Rouse, Simon" uniqKey="Rouse S" first="Simon" last="Rouse">Simon Rouse</name>
</author>
<author>
<name sortKey="Brendolise, Cyril" sort="Brendolise, Cyril" uniqKey="Brendolise C" first="Cyril" last="Brendolise">Cyril Brendolise</name>
</author>
<author>
<name sortKey="Carlisle, Charmaine M" sort="Carlisle, Charmaine M" uniqKey="Carlisle C" first="Charmaine M." last="Carlisle">Charmaine M. Carlisle</name>
</author>
<author>
<name sortKey="Kumar, Satish" sort="Kumar, Satish" uniqKey="Kumar S" first="Satish" last="Kumar">Satish Kumar</name>
</author>
<author>
<name sortKey="De Silva, Nihal" sort="De Silva, Nihal" uniqKey="De Silva N" first="Nihal" last="De Silva">Nihal De Silva</name>
</author>
<author>
<name sortKey="Micheletti, Diego" sort="Micheletti, Diego" uniqKey="Micheletti D" first="Diego" last="Micheletti">Diego Micheletti</name>
</author>
<author>
<name sortKey="Mcghie, Tony" sort="Mcghie, Tony" uniqKey="Mcghie T" first="Tony" last="Mcghie">Tony Mcghie</name>
</author>
<author>
<name sortKey="Crowhurst, Ross N" sort="Crowhurst, Ross N" uniqKey="Crowhurst R" first="Ross N." last="Crowhurst">Ross N. Crowhurst</name>
</author>
<author>
<name sortKey="Storey, Roy D" sort="Storey, Roy D" uniqKey="Storey R" first="Roy D." last="Storey">Roy D. Storey</name>
</author>
<author>
<name sortKey="Velasco, Riccardo" sort="Velasco, Riccardo" uniqKey="Velasco R" first="Riccardo" last="Velasco">Riccardo Velasco</name>
</author>
<author>
<name sortKey="Hellens, Roger P" sort="Hellens, Roger P" uniqKey="Hellens R" first="Roger P." last="Hellens">Roger P. Hellens</name>
</author>
<author>
<name sortKey="Gardiner, Susan E" sort="Gardiner, Susan E" uniqKey="Gardiner S" first="Susan E." last="Gardiner">Susan E. Gardiner</name>
</author>
<author>
<name sortKey="Allan, Andrew C" sort="Allan, Andrew C" uniqKey="Allan A" first="Andrew C." last="Allan">Andrew C. Allan</name>
</author>
</analytic>
<series>
<title level="j">Plant Physiology</title>
<idno type="ISSN">0032-0889</idno>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
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<front>
<div type="abstract" xml:lang="en">
<p>Anthocyanin accumulation is coordinated in plants by a number of conserved transcription factors. In apple (
<italic>Malus</italic>
×
<italic>domestica</italic>
), an R2R3 MYB transcription factor has been shown to control fruit flesh and foliage anthocyanin pigmentation (
<italic>MYB10</italic>
) and fruit skin color (
<italic>MYB1</italic>
). However, the pattern of expression and allelic variation at these loci does not explain all anthocyanin-related apple phenotypes. One such example is an open-pollinated seedling of cv Sangrado that has green foliage and develops red flesh in the fruit cortex late in maturity. We used methods that combine plant breeding, molecular biology, and genomics to identify duplicated MYB transcription factors that could control this phenotype. We then demonstrated that the red-flesh cortex phenotype is associated with enhanced expression of
<italic>MYB110a</italic>
, a paralog of
<italic>MYB10</italic>
. Functional characterization of
<italic>MYB110a</italic>
showed that it was able to up-regulate anthocyanin biosynthesis in tobacco (
<italic>Nicotiana tabacum</italic>
). The chromosomal location of
<italic>MYB110a</italic>
is consistent with a whole-genome duplication event that occurred during the evolution of apple within the Maloideae family. Both
<italic>MYB10</italic>
and
<italic>MYB110a</italic>
have conserved function in some cultivars, but they differ in their expression pattern and response to fruit maturity.</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">Plant Physiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Plant Physiol</journal-id>
<journal-id journal-id-type="hwp">plantphysiol</journal-id>
<journal-id journal-id-type="publisher-id">aspb</journal-id>
<journal-title-group>
<journal-title>Plant Physiology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0032-0889</issn>
<issn pub-type="epub">1532-2548</issn>
<publisher>
<publisher-name>American Society of Plant Biologists</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">23096157</article-id>
<article-id pub-id-type="pmc">3532254</article-id>
<article-id pub-id-type="publisher-id">206771</article-id>
<article-id pub-id-type="doi">10.1104/pp.112.206771</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Genes, Development, and Evolution</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>An Ancient Duplication of Apple MYB Transcription Factors Is Responsible for Novel Red Fruit-Flesh Phenotypes
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[W]</sup>
</xref>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Chagné</surname>
<given-names>David</given-names>
</name>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lin-Wang</surname>
<given-names>Kui</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Espley</surname>
<given-names>Richard V.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Volz</surname>
<given-names>Richard K.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>How</surname>
<given-names>Natalie M.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rouse</surname>
<given-names>Simon</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brendolise</surname>
<given-names>Cyril</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Carlisle</surname>
<given-names>Charmaine M.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kumar</surname>
<given-names>Satish</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>De Silva</surname>
<given-names>Nihal</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Micheletti</surname>
<given-names>Diego</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>McGhie</surname>
<given-names>Tony</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Crowhurst</surname>
<given-names>Ross N.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Storey</surname>
<given-names>Roy D.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Velasco</surname>
<given-names>Riccardo</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hellens</surname>
<given-names>Roger P.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gardiner</surname>
<given-names>Susan E.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Allan</surname>
<given-names>Andrew C.</given-names>
</name>
</contrib>
<aff id="aff1">New Zealand Institute for Plant and Food Research Limited (Plant and Food Research), Palmerston North Research Centre, Palmerston North 4442, New Zealand (D.C., C.M.C., T.M., S.E.G.); Plant and Food Research, Mount Albert Research Centre, Auckland 1142, New Zealand (K.L.-W., R.V.E., S.R., C.B., N.D.S., R.N.C., R.D.S., R.P.H., A.C.A.); Plant and Food Research, Hawke’s Bay Research Centre, Havelock North 4157, New Zealand (R.K.V., N.M.H., S.K.); Istituto Agrario di San Michele All'Adige Research and Innovation Centre, Foundation Edmund Mach, San Michele all’Adige, Trento 38010, Italy (D.M., R.V.); and School of Biological Sciences, University of Auckland, Auckland 1020, New Zealand (A.C.A.)</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<label>*</label>
Corresponding author; e-mail
<email>david.chagne@plantandfood.co.nz</email>
.</corresp>
<fn id="fn1" fn-type="supported-by">
<label>1</label>
<p>This work was supported by the New Zealand Foundation for Research, Science, and Technology (contract no. PREV0401) and by Prevar Limited.</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="http://www.plantphysiol.org">www.plantphysiol.org</ext-link>
) is: David Chagné (
<email>david.chagne@plantandfood.co.nz</email>
).</p>
</fn>
<fn id="fn2">
<label>[C]</label>
<p>Some figures in this article are displayed in color online but in black and white in the print edition.</p>
</fn>
<fn id="fn3">
<label>[W]</label>
<p>The online version of this article contains Web-only data.</p>
</fn>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="http://www.plantphysiol.org/cgi/doi/10.1104/pp.112.206771">www.plantphysiol.org/cgi/doi/10.1104/pp.112.206771</ext-link>
</p>
</fn>
</author-notes>
<pmc-comment>Fake ppub date generated by PMC from publisher pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub">
<month>1</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>24</day>
<month>10</month>
<year>2012</year>
</pub-date>
<volume>161</volume>
<issue>1</issue>
<fpage>225</fpage>
<lpage>239</lpage>
<history>
<date date-type="received">
<day>03</day>
<month>9</month>
<year>2012</year>
</date>
<date date-type="accepted">
<day>23</day>
<month>10</month>
<year>2012</year>
</date>
</history>
<permissions>
<copyright-statement>© 2013 American Society of Plant Biologists. All Rights Reserved.</copyright-statement>
<copyright-year>2013</copyright-year>
</permissions>
<self-uri xlink:role="icon" xlink:type="simple" xlink:href="PP_206771_ic1.gif"></self-uri>
<abstract>
<p>Anthocyanin accumulation is coordinated in plants by a number of conserved transcription factors. In apple (
<italic>Malus</italic>
×
<italic>domestica</italic>
), an R2R3 MYB transcription factor has been shown to control fruit flesh and foliage anthocyanin pigmentation (
<italic>MYB10</italic>
) and fruit skin color (
<italic>MYB1</italic>
). However, the pattern of expression and allelic variation at these loci does not explain all anthocyanin-related apple phenotypes. One such example is an open-pollinated seedling of cv Sangrado that has green foliage and develops red flesh in the fruit cortex late in maturity. We used methods that combine plant breeding, molecular biology, and genomics to identify duplicated MYB transcription factors that could control this phenotype. We then demonstrated that the red-flesh cortex phenotype is associated with enhanced expression of
<italic>MYB110a</italic>
, a paralog of
<italic>MYB10</italic>
. Functional characterization of
<italic>MYB110a</italic>
showed that it was able to up-regulate anthocyanin biosynthesis in tobacco (
<italic>Nicotiana tabacum</italic>
). The chromosomal location of
<italic>MYB110a</italic>
is consistent with a whole-genome duplication event that occurred during the evolution of apple within the Maloideae family. Both
<italic>MYB10</italic>
and
<italic>MYB110a</italic>
have conserved function in some cultivars, but they differ in their expression pattern and response to fruit maturity.</p>
</abstract>
</article-meta>
<notes>
<glossary>
<title>Glossary</title>
<def-list>
<def-item>
<term id="term1">TF</term>
<def id="def1">
<p>transcription factor</p>
</def>
</def-item>
<def-item>
<term id="term2">bHLH</term>
<def id="def2">
<p>basic helix-loop-helix</p>
</def>
</def-item>
<def-item>
<term id="term3">QTL</term>
<def id="def3">
<p>quantitative trait locus</p>
</def>
</def-item>
<def-item>
<term id="term4">LG</term>
<def id="def4">
<p>linkage group</p>
</def>
</def-item>
<def-item>
<term id="term5">OP</term>
<def id="def5">
<p>open pollinated</p>
</def>
</def-item>
<def-item>
<term id="term6">WCI</term>
<def id="def6">
<p>weighted cortex intensity</p>
</def>
</def-item>
<def-item>
<term id="term7">SNP</term>
<def id="def7">
<p>single-nucleotide polymorphism</p>
</def>
</def-item>
<def-item>
<term id="term8">LOD</term>
<def id="def8">
<p>log of the odds</p>
</def>
</def-item>
<def-item>
<term id="term9">HRM</term>
<def id="def9">
<p>high-resolution melting</p>
</def>
</def-item>
<def-item>
<term id="term10">qPCR</term>
<def id="def10">
<p>quantitative PCR</p>
</def>
</def-item>
<def-item>
<term id="term11">UTR</term>
<def id="def11">
<p>untranslated region</p>
</def>
</def-item>
<def-item>
<term id="term12">MBW</term>
<def id="def12">
<p>MYB-bHLH-WD40</p>
</def>
</def-item>
<def-item>
<term id="term13">DAFB</term>
<def id="def13">
<p>days after full bloom</p>
</def>
</def-item>
</def-list>
</glossary>
</notes>
</front>
</pmc>
</record>

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