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MicroRNA390-Directed TAS3 Cleavage Leads to the Production of tasiRNA-ARF3/4 During Somatic Embryogenesis in Dimocarpus longan Lour

Identifieur interne : 000096 ( Pmc/Curation ); précédent : 000095; suivant : 000097

MicroRNA390-Directed TAS3 Cleavage Leads to the Production of tasiRNA-ARF3/4 During Somatic Embryogenesis in Dimocarpus longan Lour

Auteurs : Yuling Lin ; Lixia Lin ; Ruilian Lai ; Weihua Liu ; Yukun Chen ; Zihao Zhang ; Xu Xuhan ; Zhongxiong Lai

Source :

RBID : PMC:4680215

Abstract

Trans-acting short-interfering RNAs (tasiRNAs) originate from TAS3 families through microRNA (miRNA) 390-guided cleavage of primary transcripts and target auxin response factors (ARF3/-4), which are involved in the normal development of lateral roots and flowers in plants. However, their roles in embryo development are still unclear. Here, the pathway miR390-TAS3-ARF3/-4 was identified systematically for the first time during somatic embryo development in Dimocarpus longan. We identified the miR390 primary transcript and promoter. The promoter contained cis-acting elements responsive to stimuli such as light, salicylic acid, anaerobic induction, fungal elicitor, circadian control, and heat stress. The longan TAS3 transcript, containing two miR390-binding sites, was isolated; the miR390- guided cleavage site located near the 3′ end of the TAS3 transcript was verified. Eight TAS3-tasiRNAs with the 21-nucleotides phase were found among longan small RNA data, further confirming that miR390-directed TAS3 cleavage leads to the production of tasiRNA in longan. Among them, TAS3_5′D5+ and 5′D6+ tasiRNAs were highly abundant, and verified to target ARF3 and -4, implying that miR390-guided TAS3 cleavage with 21-nucleotides phase leading to the production of tasiRNA-ARF is conserved in plants. Pri-miR390 was highly expressed in friable-embryogenic callus (EC), and less expressed in incomplete compact pro-embryogenic cultures, while miR390 showed its lowest expression in EC and highest expression in torpedo-shaped embryos (TEs). DlTAS3 and DlARF4 both exhibited their lowest expressions in EC, and reached their peaks in the globular embryos stage, which were mainly inversely proportional to the expression of miR390, especially at the globular embryos to cotyledonary embryos (CEs) stages. While DlARF3 showed little variation from the EC to TEs stages, and exhibited its lowest expression in the CEs stage. There was a general lack of correlation between the expressions of DlARF3 and miR390. In addition, pri-miR390, DlTAS3, DlARF3 and -4 were up-regulated by 2,4-D in a concentration-dependent manner. They were also preferentially expressed in roots, pulp, and seeds of ‘Sijimi’ longan, implying their extended roles in the development of longan roots and fruit. This study provided insights into a possible role of miR390-tasiRNAs-ARF in plant somatic embryo development.


Url:
DOI: 10.3389/fpls.2015.01119
PubMed: 26734029
PubMed Central: 4680215

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<title xml:lang="en">MicroRNA390-Directed
<italic>TAS3</italic>
Cleavage Leads to the Production of tasiRNA-
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During Somatic Embryogenesis in
<italic>Dimocarpus longan</italic>
Lour</title>
<author>
<name sortKey="Lin, Yuling" sort="Lin, Yuling" uniqKey="Lin Y" first="Yuling" last="Lin">Yuling Lin</name>
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<name sortKey="Lin, Lixia" sort="Lin, Lixia" uniqKey="Lin L" first="Lixia" last="Lin">Lixia Lin</name>
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<name sortKey="Lai, Ruilian" sort="Lai, Ruilian" uniqKey="Lai R" first="Ruilian" last="Lai">Ruilian Lai</name>
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<name sortKey="Liu, Weihua" sort="Liu, Weihua" uniqKey="Liu W" first="Weihua" last="Liu">Weihua Liu</name>
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<name sortKey="Chen, Yukun" sort="Chen, Yukun" uniqKey="Chen Y" first="Yukun" last="Chen">Yukun Chen</name>
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<name sortKey="Zhang, Zihao" sort="Zhang, Zihao" uniqKey="Zhang Z" first="Zihao" last="Zhang">Zihao Zhang</name>
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<name sortKey="Xuhan, Xu" sort="Xuhan, Xu" uniqKey="Xuhan X" first="Xu" last="Xuhan">Xu Xuhan</name>
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<name sortKey="Lai, Zhongxiong" sort="Lai, Zhongxiong" uniqKey="Lai Z" first="Zhongxiong" last="Lai">Zhongxiong Lai</name>
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<title xml:lang="en" level="a" type="main">MicroRNA390-Directed
<italic>TAS3</italic>
Cleavage Leads to the Production of tasiRNA-
<italic>ARF3/4</italic>
During Somatic Embryogenesis in
<italic>Dimocarpus longan</italic>
Lour</title>
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<name sortKey="Lin, Yuling" sort="Lin, Yuling" uniqKey="Lin Y" first="Yuling" last="Lin">Yuling Lin</name>
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<name sortKey="Lin, Lixia" sort="Lin, Lixia" uniqKey="Lin L" first="Lixia" last="Lin">Lixia Lin</name>
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<name sortKey="Lai, Ruilian" sort="Lai, Ruilian" uniqKey="Lai R" first="Ruilian" last="Lai">Ruilian Lai</name>
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<author>
<name sortKey="Liu, Weihua" sort="Liu, Weihua" uniqKey="Liu W" first="Weihua" last="Liu">Weihua Liu</name>
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<name sortKey="Chen, Yukun" sort="Chen, Yukun" uniqKey="Chen Y" first="Yukun" last="Chen">Yukun Chen</name>
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<name sortKey="Zhang, Zihao" sort="Zhang, Zihao" uniqKey="Zhang Z" first="Zihao" last="Zhang">Zihao Zhang</name>
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<name sortKey="Xuhan, Xu" sort="Xuhan, Xu" uniqKey="Xuhan X" first="Xu" last="Xuhan">Xu Xuhan</name>
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<name sortKey="Lai, Zhongxiong" sort="Lai, Zhongxiong" uniqKey="Lai Z" first="Zhongxiong" last="Lai">Zhongxiong Lai</name>
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<title level="j">Frontiers in Plant Science</title>
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<p>
<italic>Trans</italic>
-acting short-interfering RNAs (tasiRNAs) originate from
<italic>TAS3</italic>
families through microRNA (miRNA) 390-guided cleavage of primary transcripts and target auxin response factors (ARF3/-4), which are involved in the normal development of lateral roots and flowers in plants. However, their roles in embryo development are still unclear. Here, the pathway miR390-
<italic>TAS3</italic>
-
<italic>ARF3</italic>
/
<italic>-4</italic>
was identified systematically for the first time during somatic embryo development in
<italic>Dimocarpus longan</italic>
. We identified the miR390 primary transcript and promoter. The promoter contained
<italic>cis</italic>
-acting elements responsive to stimuli such as light, salicylic acid, anaerobic induction, fungal elicitor, circadian control, and heat stress. The longan
<italic>TAS3</italic>
transcript, containing two miR390-binding sites, was isolated; the miR390- guided cleavage site located near the 3′ end of the
<italic>TAS3</italic>
transcript was verified. Eight
<italic>TAS3</italic>
-tasiRNAs with the 21-nucleotides phase were found among longan small RNA data, further confirming that miR390-directed
<italic>TAS3</italic>
cleavage leads to the production of tasiRNA in longan. Among them, TAS3_5′D5+ and 5′D6+ tasiRNAs were highly abundant, and verified to target
<italic>ARF3</italic>
and
<italic>-4</italic>
, implying that miR390-guided
<italic>TAS3</italic>
cleavage with 21-nucleotides phase leading to the production of tasiRNA-ARF is conserved in plants. Pri-miR390 was highly expressed in friable-embryogenic callus (EC), and less expressed in incomplete compact pro-embryogenic cultures, while miR390 showed its lowest expression in EC and highest expression in torpedo-shaped embryos (TEs).
<italic>DlTAS3</italic>
and
<italic>DlARF4</italic>
both exhibited their lowest expressions in EC, and reached their peaks in the globular embryos stage, which were mainly inversely proportional to the expression of miR390, especially at the globular embryos to cotyledonary embryos (CEs) stages. While
<italic>DlARF3</italic>
showed little variation from the EC to TEs stages, and exhibited its lowest expression in the CEs stage. There was a general lack of correlation between the expressions of
<italic>DlARF3</italic>
and miR390. In addition, pri-miR390,
<italic>DlTAS3</italic>
,
<italic>DlARF3</italic>
and
<italic>-4</italic>
were up-regulated by 2,4-
<sc>D</sc>
in a concentration-dependent manner. They were also preferentially expressed in roots, pulp, and seeds of ‘Sijimi’ longan, implying their extended roles in the development of longan roots and fruit. This study provided insights into a possible role of miR390-tasiRNAs-ARF in plant somatic embryo development.</p>
</div>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Plant Science</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26734029</article-id>
<article-id pub-id-type="pmc">4680215</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2015.01119</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>MicroRNA390-Directed
<italic>TAS3</italic>
Cleavage Leads to the Production of tasiRNA-
<italic>ARF3/4</italic>
During Somatic Embryogenesis in
<italic>Dimocarpus longan</italic>
Lour</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Lin</surname>
<given-names>Yuling</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lin</surname>
<given-names>Lixia</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lai</surname>
<given-names>Ruilian</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Liu</surname>
<given-names>Weihua</given-names>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Chen</surname>
<given-names>Yukun</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Zihao</given-names>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>XuHan</surname>
<given-names>Xu</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lai</surname>
<given-names>Zhongxiong</given-names>
</name>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/262941/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<institution>Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University</institution>
<country>Fuzhou, China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by:
<italic>Agnieszka Ludwików, Adam Mickiewicz University in Poznań, Poland</italic>
</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by:
<italic>Andrzej Miroslaw Pacak, Adam Mickiewicz University in Poznań, Poland; Antonio Ferrante, Università degli Studi di Milano, Italy</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence:
<italic>Zhongxiong Lai,
<email xlink:type="simple">laizx01@163.com</email>
</italic>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Plant Biotechnology, a section of the journal Frontiers in Plant Science</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>16</day>
<month>12</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>6</volume>
<elocation-id>1119</elocation-id>
<history>
<date date-type="received">
<day>22</day>
<month>9</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>11</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2015 Lin, Lin, Lai, Liu, Chen, Zhang, XuHan and Lai.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>Lin, Lin, Lai, Liu, Chen, Zhang, XuHan and Lai</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 Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>
<italic>Trans</italic>
-acting short-interfering RNAs (tasiRNAs) originate from
<italic>TAS3</italic>
families through microRNA (miRNA) 390-guided cleavage of primary transcripts and target auxin response factors (ARF3/-4), which are involved in the normal development of lateral roots and flowers in plants. However, their roles in embryo development are still unclear. Here, the pathway miR390-
<italic>TAS3</italic>
-
<italic>ARF3</italic>
/
<italic>-4</italic>
was identified systematically for the first time during somatic embryo development in
<italic>Dimocarpus longan</italic>
. We identified the miR390 primary transcript and promoter. The promoter contained
<italic>cis</italic>
-acting elements responsive to stimuli such as light, salicylic acid, anaerobic induction, fungal elicitor, circadian control, and heat stress. The longan
<italic>TAS3</italic>
transcript, containing two miR390-binding sites, was isolated; the miR390- guided cleavage site located near the 3′ end of the
<italic>TAS3</italic>
transcript was verified. Eight
<italic>TAS3</italic>
-tasiRNAs with the 21-nucleotides phase were found among longan small RNA data, further confirming that miR390-directed
<italic>TAS3</italic>
cleavage leads to the production of tasiRNA in longan. Among them, TAS3_5′D5+ and 5′D6+ tasiRNAs were highly abundant, and verified to target
<italic>ARF3</italic>
and
<italic>-4</italic>
, implying that miR390-guided
<italic>TAS3</italic>
cleavage with 21-nucleotides phase leading to the production of tasiRNA-ARF is conserved in plants. Pri-miR390 was highly expressed in friable-embryogenic callus (EC), and less expressed in incomplete compact pro-embryogenic cultures, while miR390 showed its lowest expression in EC and highest expression in torpedo-shaped embryos (TEs).
<italic>DlTAS3</italic>
and
<italic>DlARF4</italic>
both exhibited their lowest expressions in EC, and reached their peaks in the globular embryos stage, which were mainly inversely proportional to the expression of miR390, especially at the globular embryos to cotyledonary embryos (CEs) stages. While
<italic>DlARF3</italic>
showed little variation from the EC to TEs stages, and exhibited its lowest expression in the CEs stage. There was a general lack of correlation between the expressions of
<italic>DlARF3</italic>
and miR390. In addition, pri-miR390,
<italic>DlTAS3</italic>
,
<italic>DlARF3</italic>
and
<italic>-4</italic>
were up-regulated by 2,4-
<sc>D</sc>
in a concentration-dependent manner. They were also preferentially expressed in roots, pulp, and seeds of ‘Sijimi’ longan, implying their extended roles in the development of longan roots and fruit. This study provided insights into a possible role of miR390-tasiRNAs-ARF in plant somatic embryo development.</p>
</abstract>
<kwd-group>
<kwd>
<italic>Dimocarpus longan</italic>
</kwd>
<kwd>somatic embryo</kwd>
<kwd>microRNA390</kwd>
<kwd>
<italic>TAS3</italic>
-tasiRNA</kwd>
<kwd>auxin response factors</kwd>
<kwd>gene regulation</kwd>
</kwd-group>
<counts>
<fig-count count="5"></fig-count>
<table-count count="4"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="60"></ref-count>
<page-count count="15"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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