Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis
Alternative splicing (AS) of pre-mRNA represents a major mechanism underlying increased transcriptome and proteome complexity. Here, we show that the nuclear speckle RNA-binding protein (NSR) and the AS competitor long noncoding RNA (or ASCO-lncRNA) constitute an AS regulatory module. AtNSR-GFP tran...
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Veröffentlicht in: | Developmental cell 2014-07, Vol.30 (2), p.166-176 |
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creator | Bardou, Florian Ariel, Federico Simpson, Craig G. Romero-Barrios, Natali Laporte, Philippe Balzergue, Sandrine Brown, John W.S. Crespi, Martin |
description | Alternative splicing (AS) of pre-mRNA represents a major mechanism underlying increased transcriptome and proteome complexity. Here, we show that the nuclear speckle RNA-binding protein (NSR) and the AS competitor long noncoding RNA (or ASCO-lncRNA) constitute an AS regulatory module. AtNSR-GFP translational fusions are expressed in primary and lateral root (LR) meristems. Double Atnsr mutants and ASCO overexpressors exhibit an altered ability to form LRs after auxin treatment. Interestingly, auxin induces a major change in AS patterns of many genes, a response largely dependent on NSRs. RNA immunoprecipitation assays demonstrate that AtNSRs interact not only with their alternatively spliced mRNA targets but also with the ASCO-RNA in vivo. The ASCO-RNA displaces an AS target from an NSR-containing complex in vitro. Expression of ASCO-RNA in Arabidopsis affects the splicing patterns of several NSR-regulated mRNA targets. Hence, lncRNA can hijack nuclear AS regulators to modulate AS patterns during development.
•NSRs are nuclear speckle localized RNA-binding proteins expressed in lateral roots•NSRs control alternative splicing patterns of gene expression in response to auxin•The ASCO long noncoding RNA interacts with NSRs and displaces mRNA targets in vitro•lncRNAs can hijack nuclear AS regulators to modulate AS patterns during development
Alternative splicing (AS) of pre-mRNA represents a major mechanism that underlies increased transcriptome and proteome complexity. Bardou et al. show in Arabidopsis that a long noncoding RNA interacts with splicing regulators nuclear speckle RNA-binding proteins to modulate AS patterns during the developmental transition of lateral root formation. |
doi_str_mv | 10.1016/j.devcel.2014.06.017 |
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•NSRs are nuclear speckle localized RNA-binding proteins expressed in lateral roots•NSRs control alternative splicing patterns of gene expression in response to auxin•The ASCO long noncoding RNA interacts with NSRs and displaces mRNA targets in vitro•lncRNAs can hijack nuclear AS regulators to modulate AS patterns during development
Alternative splicing (AS) of pre-mRNA represents a major mechanism that underlies increased transcriptome and proteome complexity. Bardou et al. show in Arabidopsis that a long noncoding RNA interacts with splicing regulators nuclear speckle RNA-binding proteins to modulate AS patterns during the developmental transition of lateral root formation.</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2014.06.017</identifier><identifier>PMID: 25073154</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Alternative Splicing ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Gene Expression Regulation, Plant ; Life Sciences ; Meristem - metabolism ; Plant Roots - growth & development ; Plant Roots - metabolism ; RNA, Long Noncoding - genetics ; RNA, Long Noncoding - metabolism ; Vegetal Biology</subject><ispartof>Developmental cell, 2014-07, Vol.30 (2), p.166-176</ispartof><rights>2014 Elsevier Inc.</rights><rights>Copyright © 2014 Elsevier Inc. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-a343485378a3a5a7c99490db01f84c69f64d6943a9af737cc9f2c1d69558453c3</citedby><cites>FETCH-LOGICAL-c442t-a343485378a3a5a7c99490db01f84c69f64d6943a9af737cc9f2c1d69558453c3</cites><orcidid>0000-0001-6823-0601 ; 0000-0002-5698-9482 ; 0000-0001-8478-8808</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1534580714004067$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25073154$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02639339$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bardou, Florian</creatorcontrib><creatorcontrib>Ariel, Federico</creatorcontrib><creatorcontrib>Simpson, Craig G.</creatorcontrib><creatorcontrib>Romero-Barrios, Natali</creatorcontrib><creatorcontrib>Laporte, Philippe</creatorcontrib><creatorcontrib>Balzergue, Sandrine</creatorcontrib><creatorcontrib>Brown, John W.S.</creatorcontrib><creatorcontrib>Crespi, Martin</creatorcontrib><title>Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis</title><title>Developmental cell</title><addtitle>Dev Cell</addtitle><description>Alternative splicing (AS) of pre-mRNA represents a major mechanism underlying increased transcriptome and proteome complexity. Here, we show that the nuclear speckle RNA-binding protein (NSR) and the AS competitor long noncoding RNA (or ASCO-lncRNA) constitute an AS regulatory module. AtNSR-GFP translational fusions are expressed in primary and lateral root (LR) meristems. Double Atnsr mutants and ASCO overexpressors exhibit an altered ability to form LRs after auxin treatment. Interestingly, auxin induces a major change in AS patterns of many genes, a response largely dependent on NSRs. RNA immunoprecipitation assays demonstrate that AtNSRs interact not only with their alternatively spliced mRNA targets but also with the ASCO-RNA in vivo. The ASCO-RNA displaces an AS target from an NSR-containing complex in vitro. Expression of ASCO-RNA in Arabidopsis affects the splicing patterns of several NSR-regulated mRNA targets. Hence, lncRNA can hijack nuclear AS regulators to modulate AS patterns during development.
•NSRs are nuclear speckle localized RNA-binding proteins expressed in lateral roots•NSRs control alternative splicing patterns of gene expression in response to auxin•The ASCO long noncoding RNA interacts with NSRs and displaces mRNA targets in vitro•lncRNAs can hijack nuclear AS regulators to modulate AS patterns during development
Alternative splicing (AS) of pre-mRNA represents a major mechanism that underlies increased transcriptome and proteome complexity. Bardou et al. show in Arabidopsis that a long noncoding RNA interacts with splicing regulators nuclear speckle RNA-binding proteins to modulate AS patterns during the developmental transition of lateral root formation.</description><subject>Alternative Splicing</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Life Sciences</subject><subject>Meristem - metabolism</subject><subject>Plant Roots - growth & development</subject><subject>Plant Roots - metabolism</subject><subject>RNA, Long Noncoding - genetics</subject><subject>RNA, Long Noncoding - metabolism</subject><subject>Vegetal Biology</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kMFOGzEQhq2qqAHKG1TVHsthl_HaXtuXSqsIStUAUoGz5dhe6mizTu1NJN6-DpvmyGlGM98_I30IfcFQYcDN1aqybmdcX9WAaQVNBZh_QKdYcFFixvDH3DNCSyaAz9BZSivIMSzgE5rVDDjBjJ6iX4swvBT3YTDB-tz9vm-Lu2C3vR5dKtp-dHHQo9-54nHTe_OGuJf9OsRU-KFoo156GzbJp8_opNN9cheHeo6eb66f5rfl4uHHz3m7KA2l9VhqQgkVjHChiWaaGympBLsE3AlqGtk11DaSEi11xwk3Rna1wXnEmKCMGHKOLqe7f3SvNtGvdXxVQXt12y7UfgZ1QyQhcocz-21iNzH83bo0qrVP2VqvBxe2SWVTAFzUGDJKJ9TEkFJ03fE2BrVXrlZqUq72yhU0KivPsa-HD9vl2tlj6L_jDHyfAJed7LyLKhnvBuOsj86Mygb__od_yAGR4g</recordid><startdate>20140728</startdate><enddate>20140728</enddate><creator>Bardou, Florian</creator><creator>Ariel, Federico</creator><creator>Simpson, Craig G.</creator><creator>Romero-Barrios, Natali</creator><creator>Laporte, Philippe</creator><creator>Balzergue, Sandrine</creator><creator>Brown, John W.S.</creator><creator>Crespi, Martin</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-6823-0601</orcidid><orcidid>https://orcid.org/0000-0002-5698-9482</orcidid><orcidid>https://orcid.org/0000-0001-8478-8808</orcidid></search><sort><creationdate>20140728</creationdate><title>Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis</title><author>Bardou, Florian ; Ariel, Federico ; Simpson, Craig G. ; Romero-Barrios, Natali ; Laporte, Philippe ; Balzergue, Sandrine ; Brown, John W.S. ; Crespi, Martin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-a343485378a3a5a7c99490db01f84c69f64d6943a9af737cc9f2c1d69558453c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Alternative Splicing</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Life Sciences</topic><topic>Meristem - metabolism</topic><topic>Plant Roots - growth & development</topic><topic>Plant Roots - metabolism</topic><topic>RNA, Long Noncoding - genetics</topic><topic>RNA, Long Noncoding - metabolism</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bardou, Florian</creatorcontrib><creatorcontrib>Ariel, Federico</creatorcontrib><creatorcontrib>Simpson, Craig G.</creatorcontrib><creatorcontrib>Romero-Barrios, Natali</creatorcontrib><creatorcontrib>Laporte, Philippe</creatorcontrib><creatorcontrib>Balzergue, Sandrine</creatorcontrib><creatorcontrib>Brown, John W.S.</creatorcontrib><creatorcontrib>Crespi, Martin</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bardou, Florian</au><au>Ariel, Federico</au><au>Simpson, Craig G.</au><au>Romero-Barrios, Natali</au><au>Laporte, Philippe</au><au>Balzergue, Sandrine</au><au>Brown, John W.S.</au><au>Crespi, Martin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2014-07-28</date><risdate>2014</risdate><volume>30</volume><issue>2</issue><spage>166</spage><epage>176</epage><pages>166-176</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><abstract>Alternative splicing (AS) of pre-mRNA represents a major mechanism underlying increased transcriptome and proteome complexity. Here, we show that the nuclear speckle RNA-binding protein (NSR) and the AS competitor long noncoding RNA (or ASCO-lncRNA) constitute an AS regulatory module. AtNSR-GFP translational fusions are expressed in primary and lateral root (LR) meristems. Double Atnsr mutants and ASCO overexpressors exhibit an altered ability to form LRs after auxin treatment. Interestingly, auxin induces a major change in AS patterns of many genes, a response largely dependent on NSRs. RNA immunoprecipitation assays demonstrate that AtNSRs interact not only with their alternatively spliced mRNA targets but also with the ASCO-RNA in vivo. The ASCO-RNA displaces an AS target from an NSR-containing complex in vitro. Expression of ASCO-RNA in Arabidopsis affects the splicing patterns of several NSR-regulated mRNA targets. Hence, lncRNA can hijack nuclear AS regulators to modulate AS patterns during development.
•NSRs are nuclear speckle localized RNA-binding proteins expressed in lateral roots•NSRs control alternative splicing patterns of gene expression in response to auxin•The ASCO long noncoding RNA interacts with NSRs and displaces mRNA targets in vitro•lncRNAs can hijack nuclear AS regulators to modulate AS patterns during development
Alternative splicing (AS) of pre-mRNA represents a major mechanism that underlies increased transcriptome and proteome complexity. Bardou et al. show in Arabidopsis that a long noncoding RNA interacts with splicing regulators nuclear speckle RNA-binding proteins to modulate AS patterns during the developmental transition of lateral root formation.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25073154</pmid><doi>10.1016/j.devcel.2014.06.017</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-6823-0601</orcidid><orcidid>https://orcid.org/0000-0002-5698-9482</orcidid><orcidid>https://orcid.org/0000-0001-8478-8808</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alternative Splicing Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Gene Expression Regulation, Plant Life Sciences Meristem - metabolism Plant Roots - growth & development Plant Roots - metabolism RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism Vegetal Biology |
title | Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis |
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