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Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development
The plant hormone auxin is a fundamental regulator of organ patterning and development that regulates gene expression via the canonical AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) combinatorial system. ARF and Aux/IAA factors interact, but at high auxin concentrations, the A...
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Published in: | Current biology 2021-02, Vol.31 (4), p.892-899.e3 |
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creator | Cucinotta, Mara Cavalleri, Alex Guazzotti, Andrea Astori, Chiara Manrique, Silvia Bombarely, Aureliano Oliveto, Stefania Biffo, Stefano Weijers, Dolf Kater, Martin M. Colombo, Lucia |
description | The plant hormone auxin is a fundamental regulator of organ patterning and development that regulates gene expression via the canonical AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) combinatorial system. ARF and Aux/IAA factors interact, but at high auxin concentrations, the Aux/IAA transcriptional repressor is degraded, allowing ARF-containing complexes to activate gene expression. ARF5/MONOPTEROS (MP) is an important integrator of auxin signaling in Arabidopsis development and activates gene transcription in cells with elevated auxin levels. Here, we show that in ovules, MP is expressed in cells with low levels of auxin and can activate the expression of direct target genes. We identified and characterized a splice variant of MP that encodes a biologically functional isoform that lacks the Aux/IAA interaction domain. This MP11ir isoform was able to complement inflorescence, floral, and ovule developmental defects in mp mutants, suggesting that it was fully functional. Our findings describe a novel scenario in which ARF post-transcriptional regulation controls the formation of an isoform that can function as a transcriptional activator in regions of subthreshold auxin concentration.
•In ovules, MP localizes and activates its targets in cells with auxin minima•The MP11ir splicing variant seems to function independently of the AUX/IAAs•Canonical MP and MP11ir complement mp mutants during reproductive development
Cucinotta et al. report that MONOPTEROS in ovules is a transcriptional activator in auxin minima regions. This auxin response factor is functioning independently of auxin regulation during reproductive development as evidenced by the observation that an alternative splicing isoform, uncoupled from auxin regulation, was able to rescue mp mutants. |
doi_str_mv | 10.1016/j.cub.2020.11.026 |
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•In ovules, MP localizes and activates its targets in cells with auxin minima•The MP11ir splicing variant seems to function independently of the AUX/IAAs•Canonical MP and MP11ir complement mp mutants during reproductive development
Cucinotta et al. report that MONOPTEROS in ovules is a transcriptional activator in auxin minima regions. This auxin response factor is functioning independently of auxin regulation during reproductive development as evidenced by the observation that an alternative splicing isoform, uncoupled from auxin regulation, was able to rescue mp mutants.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2020.11.026</identifier><identifier>PMID: 33275890</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Alternative Splicing ; arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; arf5 ; auxin ; auxin signalling ; auxin-responce factor ; DNA-Binding Proteins - metabolism ; Gene Expression Regulation, Plant ; Indoleacetic Acids ; monopteros ; ovule ; Ovule - genetics ; Ovule - metabolism ; ovule development ; plant development ; Protein Isoforms ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Current biology, 2021-02, Vol.31 (4), p.892-899.e3</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c396t-950d825c9e7bbf3c76353049a0db8b25a7b12a3b200feecf22b14a06964314793</citedby><cites>FETCH-LOGICAL-c396t-950d825c9e7bbf3c76353049a0db8b25a7b12a3b200feecf22b14a06964314793</cites><orcidid>0000-0003-4378-141X ; 0000-0003-1155-2575 ; 0000-0001-6257-8914 ; 0000-0001-6241-4143</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33275890$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cucinotta, Mara</creatorcontrib><creatorcontrib>Cavalleri, Alex</creatorcontrib><creatorcontrib>Guazzotti, Andrea</creatorcontrib><creatorcontrib>Astori, Chiara</creatorcontrib><creatorcontrib>Manrique, Silvia</creatorcontrib><creatorcontrib>Bombarely, Aureliano</creatorcontrib><creatorcontrib>Oliveto, Stefania</creatorcontrib><creatorcontrib>Biffo, Stefano</creatorcontrib><creatorcontrib>Weijers, Dolf</creatorcontrib><creatorcontrib>Kater, Martin M.</creatorcontrib><creatorcontrib>Colombo, Lucia</creatorcontrib><title>Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>The plant hormone auxin is a fundamental regulator of organ patterning and development that regulates gene expression via the canonical AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) combinatorial system. ARF and Aux/IAA factors interact, but at high auxin concentrations, the Aux/IAA transcriptional repressor is degraded, allowing ARF-containing complexes to activate gene expression. ARF5/MONOPTEROS (MP) is an important integrator of auxin signaling in Arabidopsis development and activates gene transcription in cells with elevated auxin levels. Here, we show that in ovules, MP is expressed in cells with low levels of auxin and can activate the expression of direct target genes. We identified and characterized a splice variant of MP that encodes a biologically functional isoform that lacks the Aux/IAA interaction domain. This MP11ir isoform was able to complement inflorescence, floral, and ovule developmental defects in mp mutants, suggesting that it was fully functional. Our findings describe a novel scenario in which ARF post-transcriptional regulation controls the formation of an isoform that can function as a transcriptional activator in regions of subthreshold auxin concentration.
•In ovules, MP localizes and activates its targets in cells with auxin minima•The MP11ir splicing variant seems to function independently of the AUX/IAAs•Canonical MP and MP11ir complement mp mutants during reproductive development
Cucinotta et al. report that MONOPTEROS in ovules is a transcriptional activator in auxin minima regions. This auxin response factor is functioning independently of auxin regulation during reproductive development as evidenced by the observation that an alternative splicing isoform, uncoupled from auxin regulation, was able to rescue mp mutants.</description><subject>Alternative Splicing</subject><subject>arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>arf5</subject><subject>auxin</subject><subject>auxin signalling</subject><subject>auxin-responce factor</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Indoleacetic Acids</subject><subject>monopteros</subject><subject>ovule</subject><subject>Ovule - genetics</subject><subject>Ovule - metabolism</subject><subject>ovule development</subject><subject>plant development</subject><subject>Protein Isoforms</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kEtr3DAUhUVpSaZJfkA3RctuPL2SbNmiqzB5dCCtyyRZC0m-Lhr8mJHsgfz7KMy0y6wuB75z4H6EfGGwZMDk9-3SzXbJgafMlsDlB7JgVakyyPPiI1mAkpCpivNz8jnGLQDjlZJn5FwIXhaVggXZXHcThsFM_oD0cdd554e_9B4HDGbCSA39Vf-u_zzdbupHuo5jO4aebnA_-4ANTYnWh7lDeoMH7MZdj8N0ST61pot4dboX5Pnu9mn1M3uo79er64fMCSWnTBXQVLxwCktrW-FKKQoBuTLQ2MrywpSWcSMsB2gRXcu5ZbkBqWQuWF4qcUG-HXd3YdzPGCfd--iw68yA4xw1z2UpmSryMqHsiLowxhiw1bvgexNeNAP9plJvdVKp31RqxnRSmTpfT_Oz7bH53_jnLgE_jgCmJw8eg47O4-CwSW7cpJvRvzP_Cob7guc</recordid><startdate>20210222</startdate><enddate>20210222</enddate><creator>Cucinotta, Mara</creator><creator>Cavalleri, Alex</creator><creator>Guazzotti, Andrea</creator><creator>Astori, Chiara</creator><creator>Manrique, Silvia</creator><creator>Bombarely, Aureliano</creator><creator>Oliveto, Stefania</creator><creator>Biffo, Stefano</creator><creator>Weijers, Dolf</creator><creator>Kater, Martin M.</creator><creator>Colombo, Lucia</creator><general>Elsevier Inc</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><orcidid>https://orcid.org/0000-0003-4378-141X</orcidid><orcidid>https://orcid.org/0000-0003-1155-2575</orcidid><orcidid>https://orcid.org/0000-0001-6257-8914</orcidid><orcidid>https://orcid.org/0000-0001-6241-4143</orcidid></search><sort><creationdate>20210222</creationdate><title>Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development</title><author>Cucinotta, Mara ; Cavalleri, Alex ; Guazzotti, Andrea ; Astori, Chiara ; Manrique, Silvia ; Bombarely, Aureliano ; Oliveto, Stefania ; Biffo, Stefano ; Weijers, Dolf ; Kater, Martin M. ; Colombo, Lucia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c396t-950d825c9e7bbf3c76353049a0db8b25a7b12a3b200feecf22b14a06964314793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Alternative Splicing</topic><topic>arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>arf5</topic><topic>auxin</topic><topic>auxin signalling</topic><topic>auxin-responce factor</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Indoleacetic Acids</topic><topic>monopteros</topic><topic>ovule</topic><topic>Ovule - genetics</topic><topic>Ovule - metabolism</topic><topic>ovule development</topic><topic>plant development</topic><topic>Protein Isoforms</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cucinotta, Mara</creatorcontrib><creatorcontrib>Cavalleri, Alex</creatorcontrib><creatorcontrib>Guazzotti, Andrea</creatorcontrib><creatorcontrib>Astori, Chiara</creatorcontrib><creatorcontrib>Manrique, Silvia</creatorcontrib><creatorcontrib>Bombarely, Aureliano</creatorcontrib><creatorcontrib>Oliveto, Stefania</creatorcontrib><creatorcontrib>Biffo, Stefano</creatorcontrib><creatorcontrib>Weijers, Dolf</creatorcontrib><creatorcontrib>Kater, Martin M.</creatorcontrib><creatorcontrib>Colombo, Lucia</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><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cucinotta, Mara</au><au>Cavalleri, Alex</au><au>Guazzotti, Andrea</au><au>Astori, Chiara</au><au>Manrique, Silvia</au><au>Bombarely, Aureliano</au><au>Oliveto, Stefania</au><au>Biffo, Stefano</au><au>Weijers, Dolf</au><au>Kater, Martin M.</au><au>Colombo, Lucia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2021-02-22</date><risdate>2021</risdate><volume>31</volume><issue>4</issue><spage>892</spage><epage>899.e3</epage><pages>892-899.e3</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>The plant hormone auxin is a fundamental regulator of organ patterning and development that regulates gene expression via the canonical AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) combinatorial system. ARF and Aux/IAA factors interact, but at high auxin concentrations, the Aux/IAA transcriptional repressor is degraded, allowing ARF-containing complexes to activate gene expression. ARF5/MONOPTEROS (MP) is an important integrator of auxin signaling in Arabidopsis development and activates gene transcription in cells with elevated auxin levels. Here, we show that in ovules, MP is expressed in cells with low levels of auxin and can activate the expression of direct target genes. We identified and characterized a splice variant of MP that encodes a biologically functional isoform that lacks the Aux/IAA interaction domain. This MP11ir isoform was able to complement inflorescence, floral, and ovule developmental defects in mp mutants, suggesting that it was fully functional. Our findings describe a novel scenario in which ARF post-transcriptional regulation controls the formation of an isoform that can function as a transcriptional activator in regions of subthreshold auxin concentration.
•In ovules, MP localizes and activates its targets in cells with auxin minima•The MP11ir splicing variant seems to function independently of the AUX/IAAs•Canonical MP and MP11ir complement mp mutants during reproductive development
Cucinotta et al. report that MONOPTEROS in ovules is a transcriptional activator in auxin minima regions. This auxin response factor is functioning independently of auxin regulation during reproductive development as evidenced by the observation that an alternative splicing isoform, uncoupled from auxin regulation, was able to rescue mp mutants.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>33275890</pmid><doi>10.1016/j.cub.2020.11.026</doi><orcidid>https://orcid.org/0000-0003-4378-141X</orcidid><orcidid>https://orcid.org/0000-0003-1155-2575</orcidid><orcidid>https://orcid.org/0000-0001-6257-8914</orcidid><orcidid>https://orcid.org/0000-0001-6241-4143</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alternative Splicing arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism arf5 auxin auxin signalling auxin-responce factor DNA-Binding Proteins - metabolism Gene Expression Regulation, Plant Indoleacetic Acids monopteros ovule Ovule - genetics Ovule - metabolism ovule development plant development Protein Isoforms Transcription Factors - genetics Transcription Factors - metabolism |
title | Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development |
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