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Neofunctionalization of Chromoplast Specific Lycopene Beta Cyclase Gene (CYC-B) in Tomato Clade

Identifieur interne : 001F90 ( Ncbi/Merge ); précédent : 001F89; suivant : 001F91

Neofunctionalization of Chromoplast Specific Lycopene Beta Cyclase Gene (CYC-B) in Tomato Clade

Auteurs : Vijee Mohan ; Arun Pandey ; Yellamaraju Sreelakshmi ; Rameshwar Sharma

Source :

RBID : PMC:4829152

Abstract

The ancestor of tomato underwent whole genome triplication ca. 71 Myr ago followed by widespread gene loss. However, few of the triplicated genes are retained in modern day tomato including lycopene beta cyclase that mediates conversion of lycopene to β-carotene. The fruit specific β-carotene formation is mediated by a chromoplast-specific paralog of lycopene beta cyclase (CYC-B) gene. Presently limited information is available about how the variations in CYC-B gene contributed to its neofunctionalization. CYC-B gene in tomato clade contained several SNPs and In-Dels in the coding sequence (33 haplotypes) and promoter region (44 haplotypes). The CYC-B gene coding sequence in tomato appeared to undergo purifying selection. The transit peptide sequence of CYC-B protein was predicted to have a stronger plastid targeting signal than its chloroplast specific paralog indicating a possible neofunctionalization. In promoter of two Bog (Beta old gold) mutants, a NUPT (nuclear plastid) DNA fragment of 256 bp, likely derived from a S. chilense accession, was present. In transient expression assay, this promoter was more efficient than the “Beta type” promoter. CARGATCONSENSUS box sequences are required for the binding of the MADS-box regulatory protein RIPENING INHIBITOR (RIN). The loss of CARGATCONSENSUS box sequence from CYC-B promoter in tomato may be related to attenuation of its efficiency to promote higher accumulation of β-carotene than lycopene during fruit ripening.


Url:
DOI: 10.1371/journal.pone.0153333
PubMed: 27070417
PubMed Central: 4829152

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PMC:4829152

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<p>The ancestor of tomato underwent whole genome triplication ca. 71 Myr ago followed by widespread gene loss. However, few of the triplicated genes are retained in modern day tomato including lycopene beta cyclase that mediates conversion of lycopene to
<italic>β</italic>
-carotene. The fruit specific
<italic>β</italic>
-carotene formation is mediated by a chromoplast-specific paralog of lycopene beta cyclase (
<italic>CYC-B)</italic>
gene. Presently limited information is available about how the variations in
<italic>CYC-B</italic>
gene contributed to its neofunctionalization.
<italic>CYC-B</italic>
gene in tomato clade contained several SNPs and In-Dels in the coding sequence (33 haplotypes) and promoter region (44 haplotypes). The
<italic>CYC-B</italic>
gene coding sequence in tomato appeared to undergo purifying selection. The transit peptide sequence of CYC-B protein was predicted to have a stronger plastid targeting signal than its chloroplast specific paralog indicating a possible neofunctionalization. In promoter of two
<italic>B</italic>
<sup>
<italic>og</italic>
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(
<italic>Beta old gold</italic>
) mutants, a NUPT (nuclear plastid) DNA fragment of 256 bp, likely derived from a
<italic>S</italic>
.
<italic>chilense</italic>
accession, was present. In transient expression assay, this promoter was more efficient than the “
<italic>Beta</italic>
type” promoter. CARGATCONSENSUS box sequences are required for the binding of the MADS-box regulatory protein RIPENING INHIBITOR (RIN). The loss of CARGATCONSENSUS box sequence from
<italic>CYC-B</italic>
promoter in tomato may be related to attenuation of its efficiency to promote higher accumulation of
<italic>β</italic>
-carotene than lycopene during fruit ripening.</p>
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<article-id pub-id-type="pmc">4829152</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0153333</article-id>
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<subject>DNA</subject>
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<subject>Promoter Regions</subject>
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<subject>Biology and Life Sciences</subject>
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<article-title>Neofunctionalization of Chromoplast Specific Lycopene Beta Cyclase Gene (
<italic>CYC-B</italic>
) in Tomato Clade</article-title>
<alt-title alt-title-type="running-head">Neofunctionalization of
<italic>CYC-B</italic>
in Tomato Clade</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Mohan</surname>
<given-names>Vijee</given-names>
</name>
<xref ref-type="author-notes" rid="currentaff001">
<sup>¤</sup>
</xref>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pandey</surname>
<given-names>Arun</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sreelakshmi</surname>
<given-names>Yellamaraju</given-names>
</name>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sharma</surname>
<given-names>Rameshwar</given-names>
</name>
<xref ref-type="corresp" rid="cor001">*</xref>
<xref ref-type="aff" rid="aff001"></xref>
</contrib>
</contrib-group>
<aff id="aff001">
<addr-line>Repository of Tomato Genomics Resources, Department of Plant Sciences, University of Hyderabad, Hyderabad, India</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Ezura</surname>
<given-names>Hiroshi</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>University of Tsukuba, JAPAN</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: VM YS RS. Performed the experiments: VM. Analyzed the data: VM YS RS. Contributed reagents/materials/analysis tools: VM AP YS RS. Wrote the paper: VM YS RS.</p>
</fn>
<fn fn-type="current-aff" id="currentaff001">
<label>¤</label>
<p>Current address: Institute of Plant Sciences, Agricultural Research Organization - The Volcani Center, Bet Dagan, Israel</p>
</fn>
<corresp id="cor001">* E-mail:
<email>rameshwar.sharma@gmail.com</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>12</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>11</volume>
<issue>4</issue>
<elocation-id>e0153333</elocation-id>
<history>
<date date-type="received">
<day>20</day>
<month>12</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>28</day>
<month>3</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© 2016 Mohan et al</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Mohan et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<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>
<self-uri content-type="pdf" xlink:href="pone.0153333.pdf"></self-uri>
<abstract>
<p>The ancestor of tomato underwent whole genome triplication ca. 71 Myr ago followed by widespread gene loss. However, few of the triplicated genes are retained in modern day tomato including lycopene beta cyclase that mediates conversion of lycopene to
<italic>β</italic>
-carotene. The fruit specific
<italic>β</italic>
-carotene formation is mediated by a chromoplast-specific paralog of lycopene beta cyclase (
<italic>CYC-B)</italic>
gene. Presently limited information is available about how the variations in
<italic>CYC-B</italic>
gene contributed to its neofunctionalization.
<italic>CYC-B</italic>
gene in tomato clade contained several SNPs and In-Dels in the coding sequence (33 haplotypes) and promoter region (44 haplotypes). The
<italic>CYC-B</italic>
gene coding sequence in tomato appeared to undergo purifying selection. The transit peptide sequence of CYC-B protein was predicted to have a stronger plastid targeting signal than its chloroplast specific paralog indicating a possible neofunctionalization. In promoter of two
<italic>B</italic>
<sup>
<italic>og</italic>
</sup>
(
<italic>Beta old gold</italic>
) mutants, a NUPT (nuclear plastid) DNA fragment of 256 bp, likely derived from a
<italic>S</italic>
.
<italic>chilense</italic>
accession, was present. In transient expression assay, this promoter was more efficient than the “
<italic>Beta</italic>
type” promoter. CARGATCONSENSUS box sequences are required for the binding of the MADS-box regulatory protein RIPENING INHIBITOR (RIN). The loss of CARGATCONSENSUS box sequence from
<italic>CYC-B</italic>
promoter in tomato may be related to attenuation of its efficiency to promote higher accumulation of
<italic>β</italic>
-carotene than lycopene during fruit ripening.</p>
</abstract>
<funding-group>
<award-group id="award001">
<funding-source>
<institution>Department of Biotechnology, India</institution>
</funding-source>
<award-id>BT/PR/5275/AGR/16/465/2004</award-id>
<principal-award-recipient>
<name>
<surname>Sharma</surname>
<given-names>Rameshwar</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award002">
<funding-source>
<institution>Department of Biotechnology, India</institution>
</funding-source>
<award-id>BT/PR/5275/AGR/16/465/2004</award-id>
<principal-award-recipient>
<name>
<surname>Sreelakshmi</surname>
<given-names>Yellamaraju</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award003">
<funding-source>
<institution>International Atomic Energy Agency, Vienna</institution>
</funding-source>
<principal-award-recipient>
<name>
<surname>Sreelakshmi</surname>
<given-names>Yellamaraju</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award004">
<funding-source>
<institution>Council of Scientific and Industrial Research, India</institution>
</funding-source>
<principal-award-recipient>
<name>
<surname>Mohan</surname>
<given-names>Vijee</given-names>
</name>
</principal-award-recipient>
</award-group>
<funding-statement>This work was supported by the Department of Biotechnology, India (grant no. BT/PR/5275/AGR/16/465/2004;) to RS and YS, International Atomic Energy Agency, Vienna to YS and Council of Scientific and Industrial Research, India (research fellowship to VM). 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>
<fig-count count="7"></fig-count>
<table-count count="2"></table-count>
<page-count count="22"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
<affiliations>
<list></list>
<tree>
<noCountry>
<name sortKey="Mohan, Vijee" sort="Mohan, Vijee" uniqKey="Mohan V" first="Vijee" last="Mohan">Vijee Mohan</name>
<name sortKey="Pandey, Arun" sort="Pandey, Arun" uniqKey="Pandey A" first="Arun" last="Pandey">Arun Pandey</name>
<name sortKey="Sharma, Rameshwar" sort="Sharma, Rameshwar" uniqKey="Sharma R" first="Rameshwar" last="Sharma">Rameshwar Sharma</name>
<name sortKey="Sreelakshmi, Yellamaraju" sort="Sreelakshmi, Yellamaraju" uniqKey="Sreelakshmi Y" first="Yellamaraju" last="Sreelakshmi">Yellamaraju Sreelakshmi</name>
</noCountry>
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