Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3
Lateral root primordia (LRP) originate from pericycle stem cells located deep within parental root tissues. LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin-inducible auxin influx carrier LAX3 plays a key role co...
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Veröffentlicht in: | Development (Cambridge) 2016-09, Vol.143 (18), p.3340-3349 |
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creator | Porco, Silvana Larrieu, Antoine Du, Yujuan Gaudinier, Allison Goh, Tatsuaki Swarup, Kamal Swarup, Ranjan Kuempers, Britta Bishopp, Anthony Lavenus, Julien Casimiro, Ilda Hill, Kristine Benkova, Eva Fukaki, Hidehiro Brady, Siobhan M Scheres, Ben Péret, Benjamin Bennett, Malcolm J |
description | Lateral root primordia (LRP) originate from pericycle stem cells located deep within parental root tissues. LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin-inducible auxin influx carrier LAX3 plays a key role concentrating this signal in cells overlying LRP. Delimiting LAX3 expression to two adjacent cell files overlying new LRP is crucial to ensure that auxin-regulated cell separation occurs solely along their shared walls. Multiscale modeling has predicted that this highly focused pattern of expression requires auxin to sequentially induce auxin efflux and influx carriers PIN3 and LAX3, respectively. Consistent with model predictions, we report that auxin-inducible LAX3 expression is regulated indirectly by AUXIN RESPONSE FACTOR 7 (ARF7). Yeast one-hybrid screens revealed that the LAX3 promoter is bound by the transcription factor LBD29, which is a direct target for regulation by ARF7. Disrupting auxin-inducible LBD29 expression or expressing an LBD29-SRDX transcriptional repressor phenocopied the lax3 mutant, resulting in delayed lateral root emergence. We conclude that sequential LBD29 and LAX3 induction by auxin is required to coordinate cell separation and organ emergence. |
doi_str_mv | 10.1242/dev.136283 |
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LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin-inducible auxin influx carrier LAX3 plays a key role concentrating this signal in cells overlying LRP. Delimiting LAX3 expression to two adjacent cell files overlying new LRP is crucial to ensure that auxin-regulated cell separation occurs solely along their shared walls. Multiscale modeling has predicted that this highly focused pattern of expression requires auxin to sequentially induce auxin efflux and influx carriers PIN3 and LAX3, respectively. Consistent with model predictions, we report that auxin-inducible LAX3 expression is regulated indirectly by AUXIN RESPONSE FACTOR 7 (ARF7). Yeast one-hybrid screens revealed that the LAX3 promoter is bound by the transcription factor LBD29, which is a direct target for regulation by ARF7. Disrupting auxin-inducible LBD29 expression or expressing an LBD29-SRDX transcriptional repressor phenocopied the lax3 mutant, resulting in delayed lateral root emergence. We conclude that sequential LBD29 and LAX3 induction by auxin is required to coordinate cell separation and organ emergence.</description><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.136283</identifier><identifier>PMID: 27578783</identifier><language>eng</language><publisher>England</publisher><subject>Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Gene Expression Regulation, Plant - genetics ; Gene Expression Regulation, Plant - physiology ; Indoleacetic Acids - metabolism ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - metabolism ; Plant Roots - metabolism ; Plant Roots - physiology ; Signal Transduction - genetics ; Signal Transduction - physiology ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Development (Cambridge), 2016-09, Vol.143 (18), p.3340-3349</ispartof><rights>2016. Published by The Company of Biologists Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0003-0475-390X ; 0000-0003-1336-0796</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27578783$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Porco, Silvana</creatorcontrib><creatorcontrib>Larrieu, Antoine</creatorcontrib><creatorcontrib>Du, Yujuan</creatorcontrib><creatorcontrib>Gaudinier, Allison</creatorcontrib><creatorcontrib>Goh, Tatsuaki</creatorcontrib><creatorcontrib>Swarup, Kamal</creatorcontrib><creatorcontrib>Swarup, Ranjan</creatorcontrib><creatorcontrib>Kuempers, Britta</creatorcontrib><creatorcontrib>Bishopp, Anthony</creatorcontrib><creatorcontrib>Lavenus, Julien</creatorcontrib><creatorcontrib>Casimiro, Ilda</creatorcontrib><creatorcontrib>Hill, Kristine</creatorcontrib><creatorcontrib>Benkova, Eva</creatorcontrib><creatorcontrib>Fukaki, Hidehiro</creatorcontrib><creatorcontrib>Brady, Siobhan M</creatorcontrib><creatorcontrib>Scheres, Ben</creatorcontrib><creatorcontrib>Péret, Benjamin</creatorcontrib><creatorcontrib>Bennett, Malcolm J</creatorcontrib><title>Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>Lateral root primordia (LRP) originate from pericycle stem cells located deep within parental root tissues. LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin-inducible auxin influx carrier LAX3 plays a key role concentrating this signal in cells overlying LRP. Delimiting LAX3 expression to two adjacent cell files overlying new LRP is crucial to ensure that auxin-regulated cell separation occurs solely along their shared walls. Multiscale modeling has predicted that this highly focused pattern of expression requires auxin to sequentially induce auxin efflux and influx carriers PIN3 and LAX3, respectively. Consistent with model predictions, we report that auxin-inducible LAX3 expression is regulated indirectly by AUXIN RESPONSE FACTOR 7 (ARF7). Yeast one-hybrid screens revealed that the LAX3 promoter is bound by the transcription factor LBD29, which is a direct target for regulation by ARF7. Disrupting auxin-inducible LBD29 expression or expressing an LBD29-SRDX transcriptional repressor phenocopied the lax3 mutant, resulting in delayed lateral root emergence. We conclude that sequential LBD29 and LAX3 induction by auxin is required to coordinate cell separation and organ emergence.</description><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - physiology</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo1kE1LxDAQhoMg7rp68QdIjl665mO3aY7r-gkFL3vwVqbNdIm0SU1SWf-9VVcYGOblmYdhCLnibMnFStwa_FxymYtCnpA5XymVaS70jJzH-M4Yk7lSZ2Qm1FoVqpBzcighYYCOBu8TxR7DHl2D1Dq6CVBb44doI53K4IDOoEvUO5oCuNgEOyQ7TS00yQda3t0LTQPuxw5-c99SGA-Tyrq2Gw-0gRAsTuDmTV6Q0xa6iJfHviC7x4fd9jkrX59etpsyGwTnKWs58FzWa6an2xupQDIuFc_RSCNWWrbI8tyAXgtRMGBaN1xqxnUhoNDT5oLc_GmH4D9GjKnqbWyw68ChH2PFC641mxw_6PURHeseTTUE20P4qv6fJb8BNthojg</recordid><startdate>20160915</startdate><enddate>20160915</enddate><creator>Porco, Silvana</creator><creator>Larrieu, Antoine</creator><creator>Du, Yujuan</creator><creator>Gaudinier, Allison</creator><creator>Goh, Tatsuaki</creator><creator>Swarup, Kamal</creator><creator>Swarup, Ranjan</creator><creator>Kuempers, Britta</creator><creator>Bishopp, Anthony</creator><creator>Lavenus, Julien</creator><creator>Casimiro, Ilda</creator><creator>Hill, Kristine</creator><creator>Benkova, Eva</creator><creator>Fukaki, Hidehiro</creator><creator>Brady, Siobhan M</creator><creator>Scheres, Ben</creator><creator>Péret, Benjamin</creator><creator>Bennett, Malcolm J</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-0475-390X</orcidid><orcidid>https://orcid.org/0000-0003-1336-0796</orcidid></search><sort><creationdate>20160915</creationdate><title>Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3</title><author>Porco, Silvana ; Larrieu, Antoine ; Du, Yujuan ; Gaudinier, Allison ; Goh, Tatsuaki ; Swarup, Kamal ; Swarup, Ranjan ; Kuempers, Britta ; Bishopp, Anthony ; Lavenus, Julien ; Casimiro, Ilda ; Hill, Kristine ; Benkova, Eva ; Fukaki, Hidehiro ; Brady, Siobhan M ; Scheres, Ben ; Péret, Benjamin ; Bennett, Malcolm J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p211t-f1a163b509036c37a3013716ed3d2493fe066da952280a099c13901982a89163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Membrane Transport Proteins - genetics</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>Plant Roots - metabolism</topic><topic>Plant Roots - physiology</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - physiology</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Porco, Silvana</creatorcontrib><creatorcontrib>Larrieu, Antoine</creatorcontrib><creatorcontrib>Du, Yujuan</creatorcontrib><creatorcontrib>Gaudinier, Allison</creatorcontrib><creatorcontrib>Goh, Tatsuaki</creatorcontrib><creatorcontrib>Swarup, Kamal</creatorcontrib><creatorcontrib>Swarup, Ranjan</creatorcontrib><creatorcontrib>Kuempers, Britta</creatorcontrib><creatorcontrib>Bishopp, Anthony</creatorcontrib><creatorcontrib>Lavenus, Julien</creatorcontrib><creatorcontrib>Casimiro, Ilda</creatorcontrib><creatorcontrib>Hill, Kristine</creatorcontrib><creatorcontrib>Benkova, Eva</creatorcontrib><creatorcontrib>Fukaki, Hidehiro</creatorcontrib><creatorcontrib>Brady, Siobhan M</creatorcontrib><creatorcontrib>Scheres, Ben</creatorcontrib><creatorcontrib>Péret, Benjamin</creatorcontrib><creatorcontrib>Bennett, Malcolm J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>MEDLINE - Academic</collection><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Porco, Silvana</au><au>Larrieu, Antoine</au><au>Du, Yujuan</au><au>Gaudinier, Allison</au><au>Goh, Tatsuaki</au><au>Swarup, Kamal</au><au>Swarup, Ranjan</au><au>Kuempers, Britta</au><au>Bishopp, Anthony</au><au>Lavenus, Julien</au><au>Casimiro, Ilda</au><au>Hill, Kristine</au><au>Benkova, Eva</au><au>Fukaki, Hidehiro</au><au>Brady, Siobhan M</au><au>Scheres, Ben</au><au>Péret, Benjamin</au><au>Bennett, Malcolm J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2016-09-15</date><risdate>2016</risdate><volume>143</volume><issue>18</issue><spage>3340</spage><epage>3349</epage><pages>3340-3349</pages><eissn>1477-9129</eissn><abstract>Lateral root primordia (LRP) originate from pericycle stem cells located deep within parental root tissues. LRP emerge through overlying root tissues by inducing auxin-dependent cell separation and hydraulic changes in adjacent cells. The auxin-inducible auxin influx carrier LAX3 plays a key role concentrating this signal in cells overlying LRP. Delimiting LAX3 expression to two adjacent cell files overlying new LRP is crucial to ensure that auxin-regulated cell separation occurs solely along their shared walls. Multiscale modeling has predicted that this highly focused pattern of expression requires auxin to sequentially induce auxin efflux and influx carriers PIN3 and LAX3, respectively. Consistent with model predictions, we report that auxin-inducible LAX3 expression is regulated indirectly by AUXIN RESPONSE FACTOR 7 (ARF7). Yeast one-hybrid screens revealed that the LAX3 promoter is bound by the transcription factor LBD29, which is a direct target for regulation by ARF7. Disrupting auxin-inducible LBD29 expression or expressing an LBD29-SRDX transcriptional repressor phenocopied the lax3 mutant, resulting in delayed lateral root emergence. We conclude that sequential LBD29 and LAX3 induction by auxin is required to coordinate cell separation and organ emergence.</abstract><cop>England</cop><pmid>27578783</pmid><doi>10.1242/dev.136283</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-0475-390X</orcidid><orcidid>https://orcid.org/0000-0003-1336-0796</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Gene Expression Regulation, Plant - genetics Gene Expression Regulation, Plant - physiology Indoleacetic Acids - metabolism Membrane Transport Proteins - genetics Membrane Transport Proteins - metabolism Plant Roots - metabolism Plant Roots - physiology Signal Transduction - genetics Signal Transduction - physiology Transcription Factors - genetics Transcription Factors - metabolism |
title | Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3 |
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