Reactive oxygen species coordinate the transcriptional responses to iron availability in Arabidopsis
Abstract Reactive oxygen species play a central role in the regulation of plant responses to environmental stress. Under prolonged iron (Fe) deficiency, increased levels of hydrogen peroxide (H2O2) initiate signaling events, resulting in the attenuation of Fe acquisition through the inhibition of FE...
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Veröffentlicht in: | Journal of experimental botany 2021-03, Vol.72 (6), p.2181-2195 |
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creator | von der Mark, Claudia Ivanov, Rumen Eutebach, Monique Maurino, Veronica G Bauer, Petra Brumbarova, Tzvetina |
description | Abstract
Reactive oxygen species play a central role in the regulation of plant responses to environmental stress. Under prolonged iron (Fe) deficiency, increased levels of hydrogen peroxide (H2O2) initiate signaling events, resulting in the attenuation of Fe acquisition through the inhibition of FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT). As this H2O2 increase occurs in a FIT-dependent manner, our aim was to understand the processes involved in maintaining H2O2 levels under prolonged Fe deficiency and the role of FIT. We identified the CAT2 gene, encoding one of the three Arabidopsis catalase isoforms, as regulated by FIT. CAT2 loss-of-function plants displayed severe susceptibility to Fe deficiency and greatly increased H2O2 levels in roots. Analysis of the Fe homeostasis transcription cascade revealed that H2O2 influences the gene expression of downstream regulators FIT, BHLH genes of group Ib, and POPEYE (PYE); however, H2O2 did not affect their upstream regulators, such as BHLH104 and ILR3. Our data shows that FIT and CAT2 participate in a regulatory loop between H2O2 and prolonged Fe deficiency.
We demonstrate that CAT2 modulates root H2O2 levels and forms a regulatory loop with the central Fe acquisition transcription factor FIT to influence Arabidopsis response to prolonged Fe deficiency. |
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Reactive oxygen species play a central role in the regulation of plant responses to environmental stress. Under prolonged iron (Fe) deficiency, increased levels of hydrogen peroxide (H2O2) initiate signaling events, resulting in the attenuation of Fe acquisition through the inhibition of FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT). As this H2O2 increase occurs in a FIT-dependent manner, our aim was to understand the processes involved in maintaining H2O2 levels under prolonged Fe deficiency and the role of FIT. We identified the CAT2 gene, encoding one of the three Arabidopsis catalase isoforms, as regulated by FIT. CAT2 loss-of-function plants displayed severe susceptibility to Fe deficiency and greatly increased H2O2 levels in roots. Analysis of the Fe homeostasis transcription cascade revealed that H2O2 influences the gene expression of downstream regulators FIT, BHLH genes of group Ib, and POPEYE (PYE); however, H2O2 did not affect their upstream regulators, such as BHLH104 and ILR3. Our data shows that FIT and CAT2 participate in a regulatory loop between H2O2 and prolonged Fe deficiency.
We demonstrate that CAT2 modulates root H2O2 levels and forms a regulatory loop with the central Fe acquisition transcription factor FIT to influence Arabidopsis response to prolonged Fe deficiency.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/eraa522</identifier><identifier>PMID: 33159788</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins ; Basic Helix-Loop-Helix Leucine Zipper Transcription Factors ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Gene Expression Regulation, Plant ; Hydrogen Peroxide ; Iron - metabolism ; Plant Roots - metabolism ; Reactive Oxygen Species - metabolism ; Research Papers</subject><ispartof>Journal of experimental botany, 2021-03, Vol.72 (6), p.2181-2195</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-718907b6939078f54359fcc9aae1bc95f0b47279f8a6f4ddc2d18f92f54c4d453</citedby><cites>FETCH-LOGICAL-c412t-718907b6939078f54359fcc9aae1bc95f0b47279f8a6f4ddc2d18f92f54c4d453</cites><orcidid>0000-0002-0404-4532 ; 0000-0003-4338-5265 ; 0000-0002-3104-6795 ; 0000-0001-7909-4123</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33159788$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Foyer, Christine</contributor><creatorcontrib>von der Mark, Claudia</creatorcontrib><creatorcontrib>Ivanov, Rumen</creatorcontrib><creatorcontrib>Eutebach, Monique</creatorcontrib><creatorcontrib>Maurino, Veronica G</creatorcontrib><creatorcontrib>Bauer, Petra</creatorcontrib><creatorcontrib>Brumbarova, Tzvetina</creatorcontrib><title>Reactive oxygen species coordinate the transcriptional responses to iron availability in Arabidopsis</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Abstract
Reactive oxygen species play a central role in the regulation of plant responses to environmental stress. Under prolonged iron (Fe) deficiency, increased levels of hydrogen peroxide (H2O2) initiate signaling events, resulting in the attenuation of Fe acquisition through the inhibition of FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT). As this H2O2 increase occurs in a FIT-dependent manner, our aim was to understand the processes involved in maintaining H2O2 levels under prolonged Fe deficiency and the role of FIT. We identified the CAT2 gene, encoding one of the three Arabidopsis catalase isoforms, as regulated by FIT. CAT2 loss-of-function plants displayed severe susceptibility to Fe deficiency and greatly increased H2O2 levels in roots. Analysis of the Fe homeostasis transcription cascade revealed that H2O2 influences the gene expression of downstream regulators FIT, BHLH genes of group Ib, and POPEYE (PYE); however, H2O2 did not affect their upstream regulators, such as BHLH104 and ILR3. Our data shows that FIT and CAT2 participate in a regulatory loop between H2O2 and prolonged Fe deficiency.
We demonstrate that CAT2 modulates root H2O2 levels and forms a regulatory loop with the central Fe acquisition transcription factor FIT to influence Arabidopsis response to prolonged Fe deficiency.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins</subject><subject>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Hydrogen Peroxide</subject><subject>Iron - metabolism</subject><subject>Plant Roots - metabolism</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Research Papers</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kc1LAzEQxYMotlZP3iUnEWRtkk12NxehFL-gIIieQzabbVO2yZrslva_N9Ja9OJhGIb58eYxD4BLjO4w4ul4uSnH2kvJCDkCQ0wzlBCa4mMwRIiQBHGWD8BZCEuEEEOMnYJBmmLG86IYgupNS9WZtYZus51rC0OrldEBKud8ZazsNOwWsby0QXnTdsZZ2UCvQ-tsiGDnoPHOQrmWppGlaUy3hcbCiY9D5dpgwjk4qWUT9MW-j8DH48P79DmZvT69TCezRFFMuiTHBUd5mfE0tqJmNGW8VopLqXGpOKtRSXOS87qQWU2rSpEKFzUnkVS0oiwdgfudbtuXK10pbaPtRrTerKTfCieN-LuxZiHmbi1ynmU83huBm72Ad5-9Dp1YmaB000irXR8EoazIUxrfGNHbHaq8C8Hr-nAGI_Gdi4i5iH0ukb767ezA_gQRgesd4Pr2X6Uvly2awQ</recordid><startdate>20210317</startdate><enddate>20210317</enddate><creator>von der Mark, Claudia</creator><creator>Ivanov, Rumen</creator><creator>Eutebach, Monique</creator><creator>Maurino, Veronica G</creator><creator>Bauer, Petra</creator><creator>Brumbarova, Tzvetina</creator><general>Oxford University Press</general><scope>TOX</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>5PM</scope><orcidid>https://orcid.org/0000-0002-0404-4532</orcidid><orcidid>https://orcid.org/0000-0003-4338-5265</orcidid><orcidid>https://orcid.org/0000-0002-3104-6795</orcidid><orcidid>https://orcid.org/0000-0001-7909-4123</orcidid></search><sort><creationdate>20210317</creationdate><title>Reactive oxygen species coordinate the transcriptional responses to iron availability in Arabidopsis</title><author>von der Mark, Claudia ; Ivanov, Rumen ; Eutebach, Monique ; Maurino, Veronica G ; Bauer, Petra ; Brumbarova, Tzvetina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-718907b6939078f54359fcc9aae1bc95f0b47279f8a6f4ddc2d18f92f54c4d453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins</topic><topic>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Hydrogen Peroxide</topic><topic>Iron - metabolism</topic><topic>Plant Roots - metabolism</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Research Papers</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>von der Mark, Claudia</creatorcontrib><creatorcontrib>Ivanov, Rumen</creatorcontrib><creatorcontrib>Eutebach, Monique</creatorcontrib><creatorcontrib>Maurino, Veronica G</creatorcontrib><creatorcontrib>Bauer, Petra</creatorcontrib><creatorcontrib>Brumbarova, Tzvetina</creatorcontrib><collection>Oxford Journals Open Access Collection</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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>von der Mark, Claudia</au><au>Ivanov, Rumen</au><au>Eutebach, Monique</au><au>Maurino, Veronica G</au><au>Bauer, Petra</au><au>Brumbarova, Tzvetina</au><au>Foyer, Christine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reactive oxygen species coordinate the transcriptional responses to iron availability in Arabidopsis</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2021-03-17</date><risdate>2021</risdate><volume>72</volume><issue>6</issue><spage>2181</spage><epage>2195</epage><pages>2181-2195</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Abstract
Reactive oxygen species play a central role in the regulation of plant responses to environmental stress. Under prolonged iron (Fe) deficiency, increased levels of hydrogen peroxide (H2O2) initiate signaling events, resulting in the attenuation of Fe acquisition through the inhibition of FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT). As this H2O2 increase occurs in a FIT-dependent manner, our aim was to understand the processes involved in maintaining H2O2 levels under prolonged Fe deficiency and the role of FIT. We identified the CAT2 gene, encoding one of the three Arabidopsis catalase isoforms, as regulated by FIT. CAT2 loss-of-function plants displayed severe susceptibility to Fe deficiency and greatly increased H2O2 levels in roots. Analysis of the Fe homeostasis transcription cascade revealed that H2O2 influences the gene expression of downstream regulators FIT, BHLH genes of group Ib, and POPEYE (PYE); however, H2O2 did not affect their upstream regulators, such as BHLH104 and ILR3. Our data shows that FIT and CAT2 participate in a regulatory loop between H2O2 and prolonged Fe deficiency.
We demonstrate that CAT2 modulates root H2O2 levels and forms a regulatory loop with the central Fe acquisition transcription factor FIT to influence Arabidopsis response to prolonged Fe deficiency.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>33159788</pmid><doi>10.1093/jxb/eraa522</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-0404-4532</orcidid><orcidid>https://orcid.org/0000-0003-4338-5265</orcidid><orcidid>https://orcid.org/0000-0002-3104-6795</orcidid><orcidid>https://orcid.org/0000-0001-7909-4123</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins Basic Helix-Loop-Helix Leucine Zipper Transcription Factors Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Gene Expression Regulation, Plant Hydrogen Peroxide Iron - metabolism Plant Roots - metabolism Reactive Oxygen Species - metabolism Research Papers |
title | Reactive oxygen species coordinate the transcriptional responses to iron availability in Arabidopsis |
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