Dihydroflavonol 4-Reductase Genes Encode Enzymes with Contrasting Substrate Specificity and Show Divergent Gene Expression Profiles in Fragaria Species
Identifieur interne : 000218 ( Pmc/Curation ); précédent : 000217; suivant : 000219Dihydroflavonol 4-Reductase Genes Encode Enzymes with Contrasting Substrate Specificity and Show Divergent Gene Expression Profiles in Fragaria Species
Auteurs : Silvija Miosic [Autriche] ; Jana Thill [Autriche] ; Malvina Milosevic [Autriche] ; Christian Gosch [Autriche] ; Sabrina Pober [Autriche] ; Christian Molitor [Autriche] ; Shaghef Ejaz [Pakistan] ; Annette Rompel [Autriche] ; Karl Stich [Autriche] ; Heidi Halbwirth [Autriche]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
During fruit ripening, strawberries show distinct changes in the flavonoid classes that accumulate, switching from the formation of flavan 3-ols and flavonols in unripe fruits to the accumulation of anthocyanins in the ripe fruits. In the common garden strawberry (
Url:
DOI: 10.1371/journal.pone.0112707
PubMed: 25393679
PubMed Central: 4231056
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Species</title>
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<author><name sortKey="Ejaz, Shaghef" sort="Ejaz, Shaghef" uniqKey="Ejaz S" first="Shaghef" last="Ejaz">Shaghef Ejaz</name>
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<author><name sortKey="Halbwirth, Heidi" sort="Halbwirth, Heidi" uniqKey="Halbwirth H" first="Heidi" last="Halbwirth">Heidi Halbwirth</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dihydroflavonol 4-Reductase Genes Encode Enzymes with Contrasting Substrate Specificity and Show Divergent Gene Expression Profiles in <italic>Fragaria</italic>
Species</title>
<author><name sortKey="Miosic, Silvija" sort="Miosic, Silvija" uniqKey="Miosic S" first="Silvija" last="Miosic">Silvija Miosic</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Thill, Jana" sort="Thill, Jana" uniqKey="Thill J" first="Jana" last="Thill">Jana Thill</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Milosevic, Malvina" sort="Milosevic, Malvina" uniqKey="Milosevic M" first="Malvina" last="Milosevic">Malvina Milosevic</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Gosch, Christian" sort="Gosch, Christian" uniqKey="Gosch C" first="Christian" last="Gosch">Christian Gosch</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Pober, Sabrina" sort="Pober, Sabrina" uniqKey="Pober S" first="Sabrina" last="Pober">Sabrina Pober</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
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<author><name sortKey="Molitor, Christian" sort="Molitor, Christian" uniqKey="Molitor C" first="Christian" last="Molitor">Christian Molitor</name>
<affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Institut für Biophysikalische Chemie, Fakultät für Chemie, Universität Wien, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Institut für Biophysikalische Chemie, Fakultät für Chemie, Universität Wien, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Ejaz, Shaghef" sort="Ejaz, Shaghef" uniqKey="Ejaz S" first="Shaghef" last="Ejaz">Shaghef Ejaz</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Bahauddin Zakariya University, Department of Horticulture, Multan, Pakistan</addr-line>
</nlm:aff>
<country xml:lang="fr">Pakistan</country>
<wicri:regionArea>Bahauddin Zakariya University, Department of Horticulture, Multan</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Rompel, Annette" sort="Rompel, Annette" uniqKey="Rompel A" first="Annette" last="Rompel">Annette Rompel</name>
<affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Institut für Biophysikalische Chemie, Fakultät für Chemie, Universität Wien, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Institut für Biophysikalische Chemie, Fakultät für Chemie, Universität Wien, Vienna</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Stich, Karl" sort="Stich, Karl" uniqKey="Stich K" first="Karl" last="Stich">Karl Stich</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
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<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
</affiliation>
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<author><name sortKey="Halbwirth, Heidi" sort="Halbwirth, Heidi" uniqKey="Halbwirth H" first="Heidi" last="Halbwirth">Heidi Halbwirth</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</nlm:aff>
<country xml:lang="fr">Autriche</country>
<wicri:regionArea>Vienna University of Technology, Institute of Chemical Engineering, Vienna</wicri:regionArea>
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<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2014">2014</date>
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<front><div type="abstract" xml:lang="en"><p>During fruit ripening, strawberries show distinct changes in the flavonoid classes that accumulate, switching from the formation of flavan 3-ols and flavonols in unripe fruits to the accumulation of anthocyanins in the ripe fruits. In the common garden strawberry (<italic>Fragaria</italic>
×<italic>ananassa</italic>
) this is accompanied by a distinct switch in the pattern of hydroxylation demonstrated by the almost exclusive accumulation of pelargonidin based pigments. In <italic>Fragaria vesca</italic>
the proportion of anthocyanins showing one (pelargonidin) and two (cyanidin) hydroxyl groups within the B-ring is almost equal. We isolated two dihydroflavonol 4-reductase (DFR) cDNA clones from strawberry fruits, which show 82% sequence similarity. The encoded enzymes revealed a high variability in substrate specificity. One enzyme variant did not accept DHK (with one hydroxyl group present in the <italic>B-</italic>
ring), whereas the other strongly preferred DHK as a substrate. This appears to be an uncharacterized DFR variant with novel substrate specificity. Both <italic>DFR</italic>
s were expressed in the receptacle and the achenes of both <italic>Fragaria</italic>
species and the <italic>DFR2</italic>
expression profile showed a pronounced dependence on fruit development, whereas <italic>DFR1</italic>
expression remained relatively stable. There were, however, significant differences in their relative rates of expression. The <italic>DFR1/DFR2</italic>
expression ratio was much higher in the <italic>Fragaria</italic>
×<italic>ananassa</italic>
and enzyme preparations from <italic>F.</italic>
×<italic>ananassa</italic>
receptacles showed higher capability to convert DHK than preparations from <italic>F. vesca</italic>
. Anthocyanin concentrations in the <italic>F.</italic>
×<italic>ananassa</italic>
cultivar were more than twofold higher and the cyanidin:pelargonidin ratio was only 0.05 compared to 0.51 in the <italic>F. ve</italic>
sca cultivar. The differences in the fruit colour of the two <italic>Fragaria</italic>
species can be explained by the higher expression of <italic>DFR1</italic>
in <italic>F.</italic>
×<italic>ananassa</italic>
as compared to <italic>F. vesca</italic>
, a higher enzyme efficiency (<italic>K</italic>
<sub>cat</sub>
/<italic>K</italic>
<sub>m</sub>
values) of DFR1 combined with the loss of F3’H activity late in fruit development of <italic>F.</italic>
×<italic>ananassa</italic>
.</p>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25393679</article-id>
<article-id pub-id-type="pmc">4231056</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-21042</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0112707</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Agriculture</subject>
</subj-group>
<subj-group><subject>Biochemistry</subject>
</subj-group>
<subj-group><subject>Biotechnology</subject>
</subj-group>
<subj-group><subject>Molecular Biology</subject>
</subj-group>
<subj-group><subject>Plant Science</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Dihydroflavonol 4-Reductase Genes Encode Enzymes with Contrasting Substrate Specificity and Show Divergent Gene Expression Profiles in <italic>Fragaria</italic>
Species</article-title>
<alt-title alt-title-type="running-head">Dihydroflavonol 4-Reductase from <italic>Fragaria</italic>
Species</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Miosic</surname>
<given-names>Silvija</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thill</surname>
<given-names>Jana</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Milosevic</surname>
<given-names>Malvina</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gosch</surname>
<given-names>Christian</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pober</surname>
<given-names>Sabrina</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Molitor</surname>
<given-names>Christian</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ejaz</surname>
<given-names>Shaghef</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rompel</surname>
<given-names>Annette</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stich</surname>
<given-names>Karl</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Halbwirth</surname>
<given-names>Heidi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Vienna University of Technology, Institute of Chemical Engineering, Vienna, Austria</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Institut für Biophysikalische Chemie, Fakultät für Chemie, Universität Wien, Vienna, Austria</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Bahauddin Zakariya University, Department of Horticulture, Multan, Pakistan</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Strack</surname>
<given-names>Stefan</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Iowa, United States of America</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>hhalb@mail.zserv.tuwien.ac.at</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: HH KS AR. Performed the experiments: SM MM SP CM SE CG. Analyzed the data: CM JT HH CG. Contributed to the writing of the manuscript: HH KS SM.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>13</day>
<month>11</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>11</issue>
<elocation-id>e112707</elocation-id>
<history><date date-type="received"><day>11</day>
<month>5</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>14</day>
<month>10</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-year>2014</copyright-year>
<copyright-holder>Miosic et al</copyright-holder>
<license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract><p>During fruit ripening, strawberries show distinct changes in the flavonoid classes that accumulate, switching from the formation of flavan 3-ols and flavonols in unripe fruits to the accumulation of anthocyanins in the ripe fruits. In the common garden strawberry (<italic>Fragaria</italic>
×<italic>ananassa</italic>
) this is accompanied by a distinct switch in the pattern of hydroxylation demonstrated by the almost exclusive accumulation of pelargonidin based pigments. In <italic>Fragaria vesca</italic>
the proportion of anthocyanins showing one (pelargonidin) and two (cyanidin) hydroxyl groups within the B-ring is almost equal. We isolated two dihydroflavonol 4-reductase (DFR) cDNA clones from strawberry fruits, which show 82% sequence similarity. The encoded enzymes revealed a high variability in substrate specificity. One enzyme variant did not accept DHK (with one hydroxyl group present in the <italic>B-</italic>
ring), whereas the other strongly preferred DHK as a substrate. This appears to be an uncharacterized DFR variant with novel substrate specificity. Both <italic>DFR</italic>
s were expressed in the receptacle and the achenes of both <italic>Fragaria</italic>
species and the <italic>DFR2</italic>
expression profile showed a pronounced dependence on fruit development, whereas <italic>DFR1</italic>
expression remained relatively stable. There were, however, significant differences in their relative rates of expression. The <italic>DFR1/DFR2</italic>
expression ratio was much higher in the <italic>Fragaria</italic>
×<italic>ananassa</italic>
and enzyme preparations from <italic>F.</italic>
×<italic>ananassa</italic>
receptacles showed higher capability to convert DHK than preparations from <italic>F. vesca</italic>
. Anthocyanin concentrations in the <italic>F.</italic>
×<italic>ananassa</italic>
cultivar were more than twofold higher and the cyanidin:pelargonidin ratio was only 0.05 compared to 0.51 in the <italic>F. ve</italic>
sca cultivar. The differences in the fruit colour of the two <italic>Fragaria</italic>
species can be explained by the higher expression of <italic>DFR1</italic>
in <italic>F.</italic>
×<italic>ananassa</italic>
as compared to <italic>F. vesca</italic>
, a higher enzyme efficiency (<italic>K</italic>
<sub>cat</sub>
/<italic>K</italic>
<sub>m</sub>
values) of DFR1 combined with the loss of F3’H activity late in fruit development of <italic>F.</italic>
×<italic>ananassa</italic>
.</p>
</abstract>
<funding-group><funding-statement>Investigations were supported by a grant from the Austrian Science Fund (FWF, <ext-link ext-link-type="uri" xlink:href="http://www.fwf.ac.at">www.fwf.ac.at</ext-link>
): [Projects V18-B03 and P24331-B16]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="10"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the Supporting Information files.</p>
</notes>
</front>
</pmc>
</record>
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