Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3
Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency a...
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| Veröffentlicht in: | The New phytologist 2019-08, Vol.223 (3), p.1433-1446 |
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| creator | Tissot, Nicolas Robe, Kevin Gao, Fei Grant-Grant, Susana Boucherez, Jossia Bellegarde, Fanny Maghiaoui, Amel Marcelin, Romain Izquierdo, Esther Benhamed, Moussa Martin, Antoine Vignols, Florence Roschzttardtz, Hannetz Gaymard, Frédéric Briat, Jean-François Dubos, Christian |
| description | Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency and to excess is still to be determined.
In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess.
A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant’s response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity.
Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor. |
| doi_str_mv | 10.1111/nph.15753 |
| format | Article |
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In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess.
A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant’s response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity.
Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15753</identifier><identifier>PMID: 30773647</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Arabidopsis ; Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; basic helix−loop−helix ; bHLH105 ; E-Box Elements - genetics ; Ferritin ; ferritins ; Ferritins - genetics ; Ferritins - metabolism ; Gene expression ; Gene Expression Regulation, Plant - drug effects ; Genes ; Genes, Plant ; Helix-loop-helix proteins (basic) ; Homeostasis ; ILR3 ; Integrated control ; Iron ; Iron - pharmacology ; Iron deficiency ; Life Sciences ; Models, Biological ; Plant breeding ; Plant growth ; Plant Leaves - drug effects ; Plant Leaves - metabolism ; Plant Roots - drug effects ; Plant Roots - growth & development ; Post-transcription ; Promoter Regions, Genetic - genetics ; Protein Binding - drug effects ; PYE ; Seedlings - drug effects ; Seedlings - growth & development ; Transcription, Genetic - drug effects ; Vegetal Biology</subject><ispartof>The New phytologist, 2019-08, Vol.223 (3), p.1433-1446</ispartof><rights>2019 INRA © 2019 New Phytologist Trust</rights><rights>2019 INRA © 2019 New Phytologist Trust</rights><rights>2019 INRA New Phytologist © 2019 New Phytologist Trust.</rights><rights>Copyright © 2019 New Phytologist Trust</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-c5103-616d811eeb529835bb5399237cb9cd6b315a9fa50ae3aa5e08cd4f0ac96d85a53</citedby><cites>FETCH-LOGICAL-c5103-616d811eeb529835bb5399237cb9cd6b315a9fa50ae3aa5e08cd4f0ac96d85a53</cites><orcidid>0000-0001-5486-3643 ; 0000-0002-4347-8499 ; 0000-0001-7221-5033 ; 0000-0002-2031-0407 ; 0000-0003-0448-4447 ; 0000-0002-6956-2904 ; 0000-0002-2614-2504 ; 0000-0001-7825-2142 ; 0000-0002-2716-748X ; 0000-0002-4181-1702</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26759486$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26759486$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,1411,1427,27901,27902,45550,45551,46384,46808,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30773647$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02414006$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Tissot, Nicolas</creatorcontrib><creatorcontrib>Robe, Kevin</creatorcontrib><creatorcontrib>Gao, Fei</creatorcontrib><creatorcontrib>Grant-Grant, Susana</creatorcontrib><creatorcontrib>Boucherez, Jossia</creatorcontrib><creatorcontrib>Bellegarde, Fanny</creatorcontrib><creatorcontrib>Maghiaoui, Amel</creatorcontrib><creatorcontrib>Marcelin, Romain</creatorcontrib><creatorcontrib>Izquierdo, Esther</creatorcontrib><creatorcontrib>Benhamed, Moussa</creatorcontrib><creatorcontrib>Martin, Antoine</creatorcontrib><creatorcontrib>Vignols, Florence</creatorcontrib><creatorcontrib>Roschzttardtz, Hannetz</creatorcontrib><creatorcontrib>Gaymard, Frédéric</creatorcontrib><creatorcontrib>Briat, Jean-François</creatorcontrib><creatorcontrib>Dubos, Christian</creatorcontrib><title>Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency and to excess is still to be determined.
In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess.
A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant’s response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity.
Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor.</description><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>basic helix−loop−helix</subject><subject>bHLH105</subject><subject>E-Box Elements - genetics</subject><subject>Ferritin</subject><subject>ferritins</subject><subject>Ferritins - genetics</subject><subject>Ferritins - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Helix-loop-helix proteins (basic)</subject><subject>Homeostasis</subject><subject>ILR3</subject><subject>Integrated control</subject><subject>Iron</subject><subject>Iron - pharmacology</subject><subject>Iron deficiency</subject><subject>Life Sciences</subject><subject>Models, Biological</subject><subject>Plant breeding</subject><subject>Plant growth</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - growth & development</subject><subject>Post-transcription</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Protein Binding - drug effects</subject><subject>PYE</subject><subject>Seedlings - drug effects</subject><subject>Seedlings - growth & development</subject><subject>Transcription, Genetic - drug effects</subject><subject>Vegetal Biology</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kVFLHDEUhUNpqVvtgz-gJeBL-zCaTCaZyeMitiMMKqLQt3CTybhZZidjMqvsv2_W1S0IzUPCTb5zbrgHoWNKTmlaZ8O4OKW85OwDmtFCyKyirPyIZoTkVSYK8ecAfYlxSQiRXOSf0QEjZclEUc7Q4i7AEE1w4-T8AD12w2QfAmwr7Ds8LSwONo5-iDbiyWMX0gM8getBu95Nm6TA85CK1o_RRaw3LyJdNzXuwEw-4Mvmlh2hTx300X59PQ_R_a-Lu_M6a65_X57Pm8xwSlgmqGgrSq3VPJcV41pzJmXOSqOlaYVmlIPsgBOwDIBbUpm26AgYmXQcODtEP3e-C-jVGNwKwkZ5cKqeN2p7R_KCFoSIJ5rYHzt2DP5xbeOkVi4a2_cwWL-OKqcVo1Xay4SevEOXfh3SwBKVb0dPOWX_mpvgYwy22_-AErWNSqWo1EtUif3-6rjWK9vuybdsEnC2A55dbzf_d1JXN_Wb5bedYhnT2PeKXJRcFpVgfwEid6Xg</recordid><startdate>201908</startdate><enddate>201908</enddate><creator>Tissot, Nicolas</creator><creator>Robe, Kevin</creator><creator>Gao, Fei</creator><creator>Grant-Grant, Susana</creator><creator>Boucherez, Jossia</creator><creator>Bellegarde, Fanny</creator><creator>Maghiaoui, Amel</creator><creator>Marcelin, Romain</creator><creator>Izquierdo, Esther</creator><creator>Benhamed, Moussa</creator><creator>Martin, Antoine</creator><creator>Vignols, Florence</creator><creator>Roschzttardtz, Hannetz</creator><creator>Gaymard, Frédéric</creator><creator>Briat, Jean-François</creator><creator>Dubos, Christian</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-5486-3643</orcidid><orcidid>https://orcid.org/0000-0002-4347-8499</orcidid><orcidid>https://orcid.org/0000-0001-7221-5033</orcidid><orcidid>https://orcid.org/0000-0002-2031-0407</orcidid><orcidid>https://orcid.org/0000-0003-0448-4447</orcidid><orcidid>https://orcid.org/0000-0002-6956-2904</orcidid><orcidid>https://orcid.org/0000-0002-2614-2504</orcidid><orcidid>https://orcid.org/0000-0001-7825-2142</orcidid><orcidid>https://orcid.org/0000-0002-2716-748X</orcidid><orcidid>https://orcid.org/0000-0002-4181-1702</orcidid></search><sort><creationdate>201908</creationdate><title>Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3</title><author>Tissot, Nicolas ; Robe, Kevin ; Gao, Fei ; Grant-Grant, Susana ; Boucherez, Jossia ; Bellegarde, Fanny ; Maghiaoui, Amel ; Marcelin, Romain ; Izquierdo, Esther ; Benhamed, Moussa ; Martin, Antoine ; Vignols, Florence ; Roschzttardtz, Hannetz ; Gaymard, Frédéric ; Briat, Jean-François ; Dubos, Christian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5103-616d811eeb529835bb5399237cb9cd6b315a9fa50ae3aa5e08cd4f0ac96d85a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>basic helix−loop−helix</topic><topic>bHLH105</topic><topic>E-Box Elements - genetics</topic><topic>Ferritin</topic><topic>ferritins</topic><topic>Ferritins - genetics</topic><topic>Ferritins - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Helix-loop-helix proteins (basic)</topic><topic>Homeostasis</topic><topic>ILR3</topic><topic>Integrated control</topic><topic>Iron</topic><topic>Iron - pharmacology</topic><topic>Iron deficiency</topic><topic>Life Sciences</topic><topic>Models, Biological</topic><topic>Plant breeding</topic><topic>Plant growth</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - growth & development</topic><topic>Post-transcription</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Protein Binding - drug effects</topic><topic>PYE</topic><topic>Seedlings - drug effects</topic><topic>Seedlings - growth & development</topic><topic>Transcription, Genetic - drug effects</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tissot, Nicolas</creatorcontrib><creatorcontrib>Robe, Kevin</creatorcontrib><creatorcontrib>Gao, Fei</creatorcontrib><creatorcontrib>Grant-Grant, Susana</creatorcontrib><creatorcontrib>Boucherez, Jossia</creatorcontrib><creatorcontrib>Bellegarde, Fanny</creatorcontrib><creatorcontrib>Maghiaoui, Amel</creatorcontrib><creatorcontrib>Marcelin, Romain</creatorcontrib><creatorcontrib>Izquierdo, Esther</creatorcontrib><creatorcontrib>Benhamed, Moussa</creatorcontrib><creatorcontrib>Martin, Antoine</creatorcontrib><creatorcontrib>Vignols, Florence</creatorcontrib><creatorcontrib>Roschzttardtz, Hannetz</creatorcontrib><creatorcontrib>Gaymard, Frédéric</creatorcontrib><creatorcontrib>Briat, Jean-François</creatorcontrib><creatorcontrib>Dubos, Christian</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tissot, Nicolas</au><au>Robe, Kevin</au><au>Gao, Fei</au><au>Grant-Grant, Susana</au><au>Boucherez, Jossia</au><au>Bellegarde, Fanny</au><au>Maghiaoui, Amel</au><au>Marcelin, Romain</au><au>Izquierdo, Esther</au><au>Benhamed, Moussa</au><au>Martin, Antoine</au><au>Vignols, Florence</au><au>Roschzttardtz, Hannetz</au><au>Gaymard, Frédéric</au><au>Briat, Jean-François</au><au>Dubos, Christian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2019-08</date><risdate>2019</risdate><volume>223</volume><issue>3</issue><spage>1433</spage><epage>1446</epage><pages>1433-1446</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Iron (Fe) homeostasis is crucial for all living organisms. In mammals, an integrated posttranscriptional mechanism couples the regulation of both Fe deficiency and Fe excess responses. Whether in plants an integrated control mechanism involving common players regulates responses both to deficiency and to excess is still to be determined.
In this study, molecular, genetic and biochemical approaches were used to investigate transcriptional responses to both Fe deficiency and excess.
A transcriptional activator of responses to Fe shortage in Arabidopsis, called bHLH105/ILR3, was found to also negatively regulate the expression of ferritin genes, which are markers of the plant’s response to Fe excess. Further investigations revealed that ILR3 repressed the expression of several structural genes that function in the control of Fe homeostasis. ILR3 interacts directly with the promoter of its target genes, and repressive activity was conferred by its dimerisation with bHLH47/PYE. Last, this study highlighted that important facets of plant growth in response to Fe deficiency or excess rely on ILR3 activity.
Altogether, the data presented herein support that ILR3 is at the centre of the transcriptional regulatory network that controls Fe homeostasis in Arabidopsis, in which it acts as both transcriptional activator and repressor.</abstract><cop>England</cop><pub>Wiley</pub><pmid>30773647</pmid><doi>10.1111/nph.15753</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-5486-3643</orcidid><orcidid>https://orcid.org/0000-0002-4347-8499</orcidid><orcidid>https://orcid.org/0000-0001-7221-5033</orcidid><orcidid>https://orcid.org/0000-0002-2031-0407</orcidid><orcidid>https://orcid.org/0000-0003-0448-4447</orcidid><orcidid>https://orcid.org/0000-0002-6956-2904</orcidid><orcidid>https://orcid.org/0000-0002-2614-2504</orcidid><orcidid>https://orcid.org/0000-0001-7825-2142</orcidid><orcidid>https://orcid.org/0000-0002-2716-748X</orcidid><orcidid>https://orcid.org/0000-0002-4181-1702</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The New phytologist, 2019-08, Vol.223 (3), p.1433-1446 |
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| source | Jstor Complete Legacy; MEDLINE; Wiley Online Library Journals Frontfile Complete; Wiley Online Library Free Content; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Arabidopsis Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Basic Helix-Loop-Helix Transcription Factors - metabolism basic helix−loop−helix bHLH105 E-Box Elements - genetics Ferritin ferritins Ferritins - genetics Ferritins - metabolism Gene expression Gene Expression Regulation, Plant - drug effects Genes Genes, Plant Helix-loop-helix proteins (basic) Homeostasis ILR3 Integrated control Iron Iron - pharmacology Iron deficiency Life Sciences Models, Biological Plant breeding Plant growth Plant Leaves - drug effects Plant Leaves - metabolism Plant Roots - drug effects Plant Roots - growth & development Post-transcription Promoter Regions, Genetic - genetics Protein Binding - drug effects PYE Seedlings - drug effects Seedlings - growth & development Transcription, Genetic - drug effects Vegetal Biology |
| title | Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3 |
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