Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.
Identifieur interne : 000131 ( Main/Exploration ); précédent : 000130; suivant : 000132Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.
Auteurs : Sara I. Zandalinas [États-Unis] ; Luhua Song [États-Unis] ; Soham Sengupta [États-Unis] ; Samuel A. Mcinturf [États-Unis] ; Deana G. Grant [États-Unis] ; Henri-Baptiste Marjault [Israël] ; Norma A. Castro-Guerrero [États-Unis] ; David Burks [États-Unis] ; Rajeev K. Azad [États-Unis] ; David G. Mendoza-Cozatl [États-Unis] ; Rachel Nechushtai [Israël] ; Ron Mittler [États-Unis]Source :
- The Plant journal : for cell and molecular biology [ 1365-313X ] ; 2020.
Abstract
Iron-sulfur (Fe-S) clusters play an essential role in plants as protein cofactors mediating diverse electron transfer reactions. Because they can react with oxygen to form reactive oxygen species (ROS) and inflict cellular damage, the biogenesis of Fe-S clusters is highly regulated. A recently discovered group of 2Fe-2S proteins, termed NEET proteins, was proposed to coordinate Fe-S, Fe and ROS homeostasis in mammalian cells. Here we report that disrupting the function of AtNEET, the sole member of the NEET protein family in Arabidopsis thaliana, triggers leaf-associated Fe-S- and Fe-deficiency responses, elevated Fe content in chloroplasts (1.2-1.5-fold), chlorosis, structural damage to chloroplasts and a high seedling mortality rate. Our findings suggest that disrupting AtNEET function disrupts the transfer of 2Fe-2S clusters from the chloroplastic 2Fe-2S biogenesis pathway to different cytosolic and chloroplastic Fe-S proteins, as well as to the cytosolic Fe-S biogenesis system, and that uncoupling this process triggers leaf-associated Fe-S- and Fe-deficiency responses that result in Fe over-accumulation in chloroplasts and enhanced ROS accumulation. We further show that AtNEET transfers its 2Fe-2S clusters to DRE2, a key protein of the cytosolic Fe-S biogenesis system, and propose that the availability of 2Fe-2S clusters in the chloroplast and cytosol is linked to Fe homeostasis in plants.
DOI: 10.1111/tpj.14581
PubMed: 31642128
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.</title><author><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I" last="Zandalinas">Sara I. Zandalinas</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Song, Luhua" sort="Song, Luhua" uniqKey="Song L" first="Luhua" last="Song">Luhua Song</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Sengupta, Soham" sort="Sengupta, Soham" uniqKey="Sengupta S" first="Soham" last="Sengupta">Soham Sengupta</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Mcinturf, Samuel A" sort="Mcinturf, Samuel A" uniqKey="Mcinturf S" first="Samuel A" last="Mcinturf">Samuel A. Mcinturf</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Grant, Deana G" sort="Grant, Deana G" uniqKey="Grant D" first="Deana G" last="Grant">Deana G. Grant</name><affiliation wicri:level="1"><nlm:affiliation>Electron Microscopy Core Facility, University of Missouri, W136 Veterinary Medicine Building 1600 East Rollins Street, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Electron Microscopy Core Facility, University of Missouri, W136 Veterinary Medicine Building 1600 East Rollins Street, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Marjault, Henri Baptiste" sort="Marjault, Henri Baptiste" uniqKey="Marjault H" first="Henri-Baptiste" last="Marjault">Henri-Baptiste Marjault</name><affiliation wicri:level="1"><nlm:affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904</wicri:regionArea><wicri:noRegion>91904</wicri:noRegion></affiliation></author><author><name sortKey="Castro Guerrero, Norma A" sort="Castro Guerrero, Norma A" uniqKey="Castro Guerrero N" first="Norma A" last="Castro-Guerrero">Norma A. Castro-Guerrero</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Burks, David" sort="Burks, David" uniqKey="Burks D" first="David" last="Burks">David Burks</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Azad, Rajeev K" sort="Azad, Rajeev K" uniqKey="Azad R" first="Rajeev K" last="Azad">Rajeev K. Azad</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Mendoza Cozatl, David G" sort="Mendoza Cozatl, David G" uniqKey="Mendoza Cozatl D" first="David G" last="Mendoza-Cozatl">David G. Mendoza-Cozatl</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Nechushtai, Rachel" sort="Nechushtai, Rachel" uniqKey="Nechushtai R" first="Rachel" last="Nechushtai">Rachel Nechushtai</name><affiliation wicri:level="1"><nlm:affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904</wicri:regionArea><wicri:noRegion>91904</wicri:noRegion></affiliation></author><author><name sortKey="Mittler, Ron" sort="Mittler, Ron" uniqKey="Mittler R" first="Ron" last="Mittler">Ron Mittler</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:31642128</idno><idno type="pmid">31642128</idno><idno type="doi">10.1111/tpj.14581</idno><idno type="wicri:Area/Main/Corpus">000209</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000209</idno><idno type="wicri:Area/Main/Curation">000209</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000209</idno><idno type="wicri:Area/Main/Exploration">000209</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.</title><author><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I" last="Zandalinas">Sara I. Zandalinas</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Song, Luhua" sort="Song, Luhua" uniqKey="Song L" first="Luhua" last="Song">Luhua Song</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Sengupta, Soham" sort="Sengupta, Soham" uniqKey="Sengupta S" first="Soham" last="Sengupta">Soham Sengupta</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Mcinturf, Samuel A" sort="Mcinturf, Samuel A" uniqKey="Mcinturf S" first="Samuel A" last="Mcinturf">Samuel A. Mcinturf</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Grant, Deana G" sort="Grant, Deana G" uniqKey="Grant D" first="Deana G" last="Grant">Deana G. Grant</name><affiliation wicri:level="1"><nlm:affiliation>Electron Microscopy Core Facility, University of Missouri, W136 Veterinary Medicine Building 1600 East Rollins Street, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Electron Microscopy Core Facility, University of Missouri, W136 Veterinary Medicine Building 1600 East Rollins Street, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Marjault, Henri Baptiste" sort="Marjault, Henri Baptiste" uniqKey="Marjault H" first="Henri-Baptiste" last="Marjault">Henri-Baptiste Marjault</name><affiliation wicri:level="1"><nlm:affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904</wicri:regionArea><wicri:noRegion>91904</wicri:noRegion></affiliation></author><author><name sortKey="Castro Guerrero, Norma A" sort="Castro Guerrero, Norma A" uniqKey="Castro Guerrero N" first="Norma A" last="Castro-Guerrero">Norma A. Castro-Guerrero</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Burks, David" sort="Burks, David" uniqKey="Burks D" first="David" last="Burks">David Burks</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Azad, Rajeev K" sort="Azad, Rajeev K" uniqKey="Azad R" first="Rajeev K" last="Azad">Rajeev K. Azad</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017</wicri:regionArea><wicri:noRegion>76203-5017</wicri:noRegion></affiliation></author><author><name sortKey="Mendoza Cozatl, David G" sort="Mendoza Cozatl, David G" uniqKey="Mendoza Cozatl D" first="David G" last="Mendoza-Cozatl">David G. Mendoza-Cozatl</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author><author><name sortKey="Nechushtai, Rachel" sort="Nechushtai, Rachel" uniqKey="Nechushtai R" first="Rachel" last="Nechushtai">Rachel Nechushtai</name><affiliation wicri:level="1"><nlm:affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904</wicri:regionArea><wicri:noRegion>91904</wicri:noRegion></affiliation></author><author><name sortKey="Mittler, Ron" sort="Mittler, Ron" uniqKey="Mittler R" first="Ron" last="Mittler">Ron Mittler</name><affiliation wicri:level="1"><nlm:affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of Missouri, 1201 Rollins St, Columbia, MO, 65211</wicri:regionArea><wicri:noRegion>65211</wicri:noRegion></affiliation></author></analytic><series><title level="j">The Plant journal : for cell and molecular biology</title><idno type="eISSN">1365-313X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Iron-sulfur (Fe-S) clusters play an essential role in plants as protein cofactors mediating diverse electron transfer reactions. Because they can react with oxygen to form reactive oxygen species (ROS) and inflict cellular damage, the biogenesis of Fe-S clusters is highly regulated. A recently discovered group of 2Fe-2S proteins, termed NEET proteins, was proposed to coordinate Fe-S, Fe and ROS homeostasis in mammalian cells. Here we report that disrupting the function of AtNEET, the sole member of the NEET protein family in Arabidopsis thaliana, triggers leaf-associated Fe-S- and Fe-deficiency responses, elevated Fe content in chloroplasts (1.2-1.5-fold), chlorosis, structural damage to chloroplasts and a high seedling mortality rate. Our findings suggest that disrupting AtNEET function disrupts the transfer of 2Fe-2S clusters from the chloroplastic 2Fe-2S biogenesis pathway to different cytosolic and chloroplastic Fe-S proteins, as well as to the cytosolic Fe-S biogenesis system, and that uncoupling this process triggers leaf-associated Fe-S- and Fe-deficiency responses that result in Fe over-accumulation in chloroplasts and enhanced ROS accumulation. We further show that AtNEET transfers its 2Fe-2S clusters to DRE2, a key protein of the cytosolic Fe-S biogenesis system, and propose that the availability of 2Fe-2S clusters in the chloroplast and cytosol is linked to Fe homeostasis in plants.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31642128</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>29</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1365-313X</ISSN><JournalIssue CitedMedium="Internet"><Volume>101</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>03</Month></PubDate></JournalIssue><Title>The Plant journal : for cell and molecular biology</Title><ISOAbbreviation>Plant J</ISOAbbreviation></Journal><ArticleTitle>Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.</ArticleTitle><Pagination><MedlinePgn>1152-1169</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.14581</ELocationID><Abstract><AbstractText>Iron-sulfur (Fe-S) clusters play an essential role in plants as protein cofactors mediating diverse electron transfer reactions. Because they can react with oxygen to form reactive oxygen species (ROS) and inflict cellular damage, the biogenesis of Fe-S clusters is highly regulated. A recently discovered group of 2Fe-2S proteins, termed NEET proteins, was proposed to coordinate Fe-S, Fe and ROS homeostasis in mammalian cells. Here we report that disrupting the function of AtNEET, the sole member of the NEET protein family in Arabidopsis thaliana, triggers leaf-associated Fe-S- and Fe-deficiency responses, elevated Fe content in chloroplasts (1.2-1.5-fold), chlorosis, structural damage to chloroplasts and a high seedling mortality rate. Our findings suggest that disrupting AtNEET function disrupts the transfer of 2Fe-2S clusters from the chloroplastic 2Fe-2S biogenesis pathway to different cytosolic and chloroplastic Fe-S proteins, as well as to the cytosolic Fe-S biogenesis system, and that uncoupling this process triggers leaf-associated Fe-S- and Fe-deficiency responses that result in Fe over-accumulation in chloroplasts and enhanced ROS accumulation. We further show that AtNEET transfers its 2Fe-2S clusters to DRE2, a key protein of the cytosolic Fe-S biogenesis system, and propose that the availability of 2Fe-2S clusters in the chloroplast and cytosol is linked to Fe homeostasis in plants.</AbstractText><CopyrightInformation>© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zandalinas</LastName><ForeName>Sara I</ForeName><Initials>SI</Initials><Identifier Source="ORCID">0000-0002-1256-9371</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Song</LastName><ForeName>Luhua</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sengupta</LastName><ForeName>Soham</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-5013-1506</Identifier><AffiliationInfo><Affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>McInturf</LastName><ForeName>Samuel A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grant</LastName><ForeName>DeAna G</ForeName><Initials>DG</Initials><AffiliationInfo><Affiliation>Electron Microscopy Core Facility, University of Missouri, W136 Veterinary Medicine Building 1600 East Rollins Street, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Marjault</LastName><ForeName>Henri-Baptiste</ForeName><Initials>HB</Initials><AffiliationInfo><Affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Castro-Guerrero</LastName><ForeName>Norma A</ForeName><Initials>NA</Initials><AffiliationInfo><Affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Burks</LastName><ForeName>David</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Azad</LastName><ForeName>Rajeev K</ForeName><Initials>RK</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, College of Science, University of North Texas, 1155 Union Circle #305220, Denton, TX, 76203-5017, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mendoza-Cozatl</LastName><ForeName>David G</ForeName><Initials>DG</Initials><Identifier Source="ORCID">0000-0002-9616-0791</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nechushtai</LastName><ForeName>Rachel</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>The Alexander Silberman Institute of Life Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus at Givat Ram, Jerusalem, 91904, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mittler</LastName><ForeName>Ron</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0003-3192-7450</Identifier><AffiliationInfo><Affiliation>Division of Plant Sciences, College of Agriculture Food and Natural Resources and Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Surgery, University of Missouri School of Medicine, Christopher S. Bond Life Sciences Center University of Missouri, 1201 Rollins St, Columbia, MO, 65211, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>12</Month><Day>09</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Plant J</MedlineTA><NlmUniqueID>9207397</NlmUniqueID><ISSNLinking>0960-7412</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Arabidopsis thaliana
</Keyword><Keyword MajorTopicYN="Y">AtNEET</Keyword><Keyword MajorTopicYN="Y">DRE2</Keyword><Keyword MajorTopicYN="Y">iron</Keyword><Keyword MajorTopicYN="Y">iron-sulfur cluster</Keyword><Keyword MajorTopicYN="Y">reactive oxygen species</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>04</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>10</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>10</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31642128</ArticleId><ArticleId IdType="doi">10.1111/tpj.14581</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Ahmad, A.S., Mendes, M., Hernandez, D. and Doré, S. (2017) Efficacy of laropiprant in minimizing brain injury following experimental intracerebral hemorrhage. Sci. Rep. 7, 9489.</Citation></Reference><Reference><Citation>Andreini, C., Rosato, A. and Banci, L. (2017) The relationship between environmental dioxygen and iron-sulfur proteins explored at the genome level. PLoS One, 12, e0171279.</Citation></Reference><Reference><Citation>Andrews, S. (2010) FastQC: a quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.</Citation></Reference><Reference><Citation>Armas, A.M., Balparda, M., Turowski, V.R., Busi, M.V., Pagani, M.A. and Gomez-Casati, D.F. (2019) Altered levels of mitochondrial NFS1 affect cellular Fe and S contents in plants. Plant Cell, Rep. 38, 981-990.</Citation></Reference><Reference><Citation>Balk, J. and Pilon, M. (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci. 16, 218-226.</Citation></Reference><Reference><Citation>Balk, J. and Schaedler, T.A. (2014) Iron cofactor assembly in plants. Annu. Rev. Plant Biol. 65, 125-153.</Citation></Reference><Reference><Citation>Bernard, D.G., Netz, D.J.A., Lagny, T.J., Pierik, A.J. and Balk, J. (2013) Requirements of the cytosolic iron-sulfur cluster assembly pathway in Arabidopsis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120259.</Citation></Reference><Reference><Citation>Boyd, E.S., Thomas, K.M., Dai, Y., Boyd, J.M. and Outten, F.W. (2014) Interplay between oxygen and Fe-S cluster biogenesis: insights from the Suf pathway. Biochemistry, 53, 5834-5847.</Citation></Reference><Reference><Citation>Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.</Citation></Reference><Reference><Citation>Brumbarova, T., Bauer, P. and Ivanov, R. (2015) Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci. 20, 124-133.</Citation></Reference><Reference><Citation>Dahal, D., Newton, K.J. and Mooney, B.P. (2016) Quantitative proteomics of Zea mays hybrids exhibiting different levels of heterosis. J. Proteome Res. 15, 2445-2454.</Citation></Reference><Reference><Citation>Darash-Yahana, M., Pozniak, Y., Lu, M. et al. (2016) Breast cancer tumorigenicity is dependent on high expression levels of NAF-1 and the lability of its Fe-S clusters. Proc. Natl. Acad. Sci. USA, 113, 10890-10895.</Citation></Reference><Reference><Citation>Davletova, S., Schlauch, K., Coutu, J. and Mittler, R. (2005) The zinc-finger Protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847-856.</Citation></Reference><Reference><Citation>Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M. and Gingeras, T.R. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.</Citation></Reference><Reference><Citation>Duy, D., Stube, R., Wanner, G. and Philippar, K. (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol. 155, 1709-1722.</Citation></Reference><Reference><Citation>Gao, H., Subramanian, S., Couturier, J. et al. (2013) Arabidopsis thaliana Nfu2 accommodates [2Fe-2S] or [4Fe-4S] clusters and is competent for in vitro maturation of chloroplast [2Fe-2S] and [4Fe-4S] cluster-containing proteins. Biochemistry, 52, 6633-6645.</Citation></Reference><Reference><Citation>Gapinske, M., Luu, A., Winter, J., Woods, W.S., Kostan, K.A., Shiva, N., Song, J.S. and Perez-Pinera, P. (2018) CRISPR-SKIP: programmable gene splicing with single base editors. Genome Biol. 19, 107.</Citation></Reference><Reference><Citation>Grishchuk, Y., Pena, K.A., Coblentz, J., King, V.E., Humphrey, D.M., Wang, S.L., Kiselyov, K.I. and Slaugenhaupt, S.A. (2015) Impaired myelination and reduced brain ferric iron in the mouse model of mucolipidosis IV. Dis. Model. Mech. 8, 1591-1601.</Citation></Reference><Reference><Citation>Hantzis, L.J., Kroh, G.E., Jahn, C.E., Cantrell, M., Peers, G., Pilon, M. and Ravet, K. (2018) A program for iron economy during deficiency targets specific Fe proteins. Plant Physiol. 176, 596-610.</Citation></Reference><Reference><Citation>Hindt, M.N., Akmakjian, G.Z., Pivarski, K.L., Punshon, T., Baxter, I., Salt, D.E. and Guerinot, M.Lou (2017) BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. Metallomics, 9, 876-890.</Citation></Reference><Reference><Citation>Hu, X., Kato, Y., Sumida, A., Tanaka, A. and Tanaka, R. (2017) The SUFBC 2 D complex is required for the biogenesis of all major classes of plastid Fe-S proteins. Plant J. 90, 235-248.</Citation></Reference><Reference><Citation>Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.</Citation></Reference><Reference><Citation>Jeong, J., Merkovich, A., Clyne, M. and Connolly, E.L. (2017) Directing iron transport in dicots: regulation of iron acquisition and translocation. Curr. Opin. Plant Biol. 39, 106-113.</Citation></Reference><Reference><Citation>Khalaf, S., Ahmad, A.S., Chamara, K.V.D.R. and Doré, S. (2019) Unique properties associated with the brain penetrant iron chelator HBED reveal remarkable beneficial effects after brain trauma. J. Neurotrauma, 36, 43-53.</Citation></Reference><Reference><Citation>Khan, M.A., Castro-Guerrero, N.A., McInturf, S.A. et al. (2018) Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots. Plant. Cell Environ. 41, 2263-2276.</Citation></Reference><Reference><Citation>Kobayashi, T., Nozoye, T. and Nishizawa, N.K. (2019) Iron transport and its regulation in plants. Free Radic. Biol. Med. 133, 11-20.</Citation></Reference><Reference><Citation>Lalonde, S., Stone, O.A., Lessard, S., Lavertu, A., Desjardins, J., Beaudoin, M., Rivas, M., Stainier, D.Y.R. and Lettre, G. (2017) Frameshift indels introduced by genome editing can lead to in-frame exon skipping. PLoS One, 12, e0178700.</Citation></Reference><Reference><Citation>Le, C.T.T., Brumbarova, T., Ivanov, R., Stoof, C., Weber, E., Mohrbacher, J., Fink-Straube, C. and Bauer, P. (2016) ZINC FINGER OF ARABIDOPSIS THALIANA12 (ZAT12) interacts with FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT) linking iron deficiency and oxidative stress responses. Plant Physiol. 170, 540-557.</Citation></Reference><Reference><Citation>Leclerc, J.L., Lampert, A.S., Diller, M.A., Immergluck, J.B. and Doré, S. (2015) Prostaglandin E2 EP2 receptor deletion attenuates intracerebral hemorrhage-induced brain injury and improves functional recovery. ASN Neuro, 7, 175909141557871.</Citation></Reference><Reference><Citation>Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature, 460, 831-838.</Citation></Reference><Reference><Citation>Lipper, C.H., Paddock, M.L., Onuchic, J.N., Mittler, R., Nechushtai, R. and Jennings, P.A. (2015) Cancer-related NEET proteins transfer 2Fe-2S clusters to anamorsin, a protein required for cytosolic iron-sulfur cluster biogenesis. PLoS One, 10, e0139699.</Citation></Reference><Reference><Citation>Love, M.I., Huber, W. and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.</Citation></Reference><Reference><Citation>Lu, Y. (2018) Assembly and transfer of iron-sulfur clusters in the plastid. Front. Plant Sci. 9, 336.</Citation></Reference><Reference><Citation>Mena, N.P., Urrutia, P.J., Lourido, F., Carrasco, C.M. and Núñez, M.T. (2015) Mitochondrial iron homeostasis and its dysfunctions in neurodegenerative disorders. Mitochondrion, 21, 92-105.</Citation></Reference><Reference><Citation>Mittler, R., Darash-Yahana, M., Sohn, Y.S., Bai, F., Song, L., Cabantchik, I.Z., Jennings, P.A., Onuchic, J.N. and Nechushtai, R. (2018) NEET proteins: a new link between iron metabolism, reactive oxygen species, and cancer. Antioxid. Redox Signal. 30, 1083-1095.</Citation></Reference><Reference><Citation>Moran, R. (1982) Formulae for determination of chlorophyllous pigments extracted with n, n-dimethylformamide. Plant Physiol. 69, 1376-1381.</Citation></Reference><Reference><Citation>Mou, H., Smith, J.L., Peng, L. et al. (2017) CRISPR/Cas9-mediated genome editing induces exon skipping by alternative splicing or exon deletion. Genome Biol. 18, 108.</Citation></Reference><Reference><Citation>Nechushtai, R., Conlan, A.R., Harir, Y. et al. (2012) Characterization of Arabidopsis NEET reveals an ancient role for NEET proteins in iron metabolism. Plant Cell, 24, 2139-2154.</Citation></Reference><Reference><Citation>Ohama, N., Sato, H., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 22, 53-65.</Citation></Reference><Reference><Citation>Przybyla-Toscano, J., Roland, M., Gaymard, F., Couturier, J. and Rouhier, N. (2018) Roles and maturation of iron-sulfur proteins in plastids. JBIC J. Biol. Inorg. Chem. 23, 545-566.</Citation></Reference><Reference><Citation>Rey, P., Becuwe, N., Tourrette, S. and Rouhier, N. (2017) Involvement of Arabidopsis glutaredoxin S14 in the maintenance of chlorophyll content. Plant. Cell Environ. 40, 2319-2332.</Citation></Reference><Reference><Citation>Saha, K., Webb, M.E., Rigby, S.E.J., Leech, H.K., Warren, M.J. and Smith, A.G. (2012) Characterization of the evolutionarily conserved iron-sulfur cluster of sirohydrochlorin ferrochelatase from Arabidopsis thaliana. Biochem. J. 444, 227-237.</Citation></Reference><Reference><Citation>Schuler, M., Rellán-Álvarez, R., Fink-Straube, C., Abadía, J. and Bauer, P. (2012) Nicotianamine functions in the Phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell, 24, 2380-2400.</Citation></Reference><Reference><Citation>Selote, D., Samira, R., Matthiadis, A., Gillikin, J.W. and Long, T.A. (2015) Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol. 167, 273-286.</Citation></Reference><Reference><Citation>Sengupta, S., Nechushtai, R., Jennings, P.A., Onuchic, J.N., Padilla, P.A., Azad, R.K. and Mittler, R. (2018) Phylogenetic analysis of the CDGSH iron-sulfur binding domain reveals its ancient origin. Sci. Rep. 8, 4840.</Citation></Reference><Reference><Citation>Smith, J.L., Mou, H. and Xue, W. (2018) Understanding and repurposing CRISPR-mediated alternative splicing. Genome Biol. 19, 184.</Citation></Reference><Reference><Citation>Su, L.W., Chang, S.H., Li, M.Y., Huang, H.Y., Jane, W.N. and Yang, J.Y. (2013) Purification and biochemical characterization of Arabidopsis At-NEET, an ancient iron-sulfur protein, reveals a conserved cleavage motif for subcellular localization. Plant Sci. 213, 46-54.</Citation></Reference><Reference><Citation>Sui, T., Song, Y., Liu, Z., Chen, M., Deng, J., Xu, Y., Lai, L. and Li, Z. (2018) CRISPR-induced exon skipping is dependent on premature termination codon mutations. Genome Biol. 19, 164.</Citation></Reference><Reference><Citation>Suzuki, N., Miller, G., Salazar, C. et al. (2013) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell, 25, 3553-3569.</Citation></Reference><Reference><Citation>Tamir, S., Eisenberg-Domovich, Y., Conlan, A.R. et al. (2014) A point mutation in the [2Fe-2S] cluster binding region of the NAF-1 protein (H114C) dramatically hinders the cluster donor properties. Acta Crystallogr. Sect. D Biol. Crystallogr. 70, 1572-1578.</Citation></Reference><Reference><Citation>Tamir, S., Paddock, M.L., Darash-Yahana-Baram, M. et al. (2015) Structure-function analysis of NEET proteins uncovers their role as key regulators of iron and ROS homeostasis in health and disease. Biochim. Biophys. Acta, 1853, 1294-1315.</Citation></Reference><Reference><Citation>Thomine, S. and Vert, G. (2013) Iron transport in plants: better be safe than sorry. Curr. Opin. Plant Biol. 16, 322-327.</Citation></Reference><Reference><Citation>Tissot, N., Robe, K., Gao, F. et al. (2019) Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3. New Phytol. 223, 1433-1446.</Citation></Reference><Reference><Citation>Viana, V.E., Busanello, C., da Maia, L.C., Pegoraro, C. and Costa de Oliveira, A. (2018) Activation of rice WRKY transcription factors: an army of stress fighting soldiers? Curr. Opin. Plant Biol. 45, 268-275.</Citation></Reference><Reference><Citation>Xing, H.L., Dong, L., Wang, Z.P., Zhang, H.Y., Han, C.Y., Liu, B., Wang, X.C. and Chen, Q.J. (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.</Citation></Reference><Reference><Citation>Zandalinas, S.I., Sengupta, S., Burks, D., Azad, R.K. and Mittler, R. (2019) Identification and characterization of a core set of ROS wave-associated transcripts involved in the systemic acquired acclimation response of Arabidopsis to excess light. Plant J. 98, 126-141.</Citation></Reference><Reference><Citation>Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W. and Chua, N.H. (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646.</Citation></Reference><Reference><Citation>Zumbrennen-Bullough, K.B., Becker, L., Garrett, L. et al. (2014) Abnormal brain iron metabolism in Irp2 deficient mice is associated with mild neurological and behavioral impairments. PLoS One, 9, e98072.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>Israël</li><li>États-Unis</li></country></list><tree><country name="États-Unis"><noRegion><name sortKey="Zandalinas, Sara I" sort="Zandalinas, Sara I" uniqKey="Zandalinas S" first="Sara I" last="Zandalinas">Sara I. Zandalinas</name></noRegion><name sortKey="Azad, Rajeev K" sort="Azad, Rajeev K" uniqKey="Azad R" first="Rajeev K" last="Azad">Rajeev K. Azad</name><name sortKey="Burks, David" sort="Burks, David" uniqKey="Burks D" first="David" last="Burks">David Burks</name><name sortKey="Castro Guerrero, Norma A" sort="Castro Guerrero, Norma A" uniqKey="Castro Guerrero N" first="Norma A" last="Castro-Guerrero">Norma A. Castro-Guerrero</name><name sortKey="Grant, Deana G" sort="Grant, Deana G" uniqKey="Grant D" first="Deana G" last="Grant">Deana G. Grant</name><name sortKey="Mcinturf, Samuel A" sort="Mcinturf, Samuel A" uniqKey="Mcinturf S" first="Samuel A" last="Mcinturf">Samuel A. Mcinturf</name><name sortKey="Mendoza Cozatl, David G" sort="Mendoza Cozatl, David G" uniqKey="Mendoza Cozatl D" first="David G" last="Mendoza-Cozatl">David G. Mendoza-Cozatl</name><name sortKey="Mittler, Ron" sort="Mittler, Ron" uniqKey="Mittler R" first="Ron" last="Mittler">Ron Mittler</name><name sortKey="Mittler, Ron" sort="Mittler, Ron" uniqKey="Mittler R" first="Ron" last="Mittler">Ron Mittler</name><name sortKey="Sengupta, Soham" sort="Sengupta, Soham" uniqKey="Sengupta S" first="Soham" last="Sengupta">Soham Sengupta</name><name sortKey="Song, Luhua" sort="Song, Luhua" uniqKey="Song L" first="Luhua" last="Song">Luhua Song</name></country><country name="Israël"><noRegion><name sortKey="Marjault, Henri Baptiste" sort="Marjault, Henri Baptiste" uniqKey="Marjault H" first="Henri-Baptiste" last="Marjault">Henri-Baptiste Marjault</name></noRegion><name sortKey="Nechushtai, Rachel" sort="Nechushtai, Rachel" uniqKey="Nechushtai R" first="Rachel" last="Nechushtai">Rachel Nechushtai</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Bois/explor/IronSulferCluV1/Data/Main/Exploration
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000131 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd -nk 000131 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Bois
|area= IronSulferCluV1
|flux= Main
|étape= Exploration
|type= RBID
|clé= pubmed:31642128
|texte= Expression of a dominant-negative AtNEET-H89C protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis.
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Main/Exploration/RBID.i -Sk "pubmed:31642128" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd \
| NlmPubMed2Wicri -a IronSulferCluV1
| This area was generated with Dilib version V0.6.38. |  |