di-Cysteine motifs in the C-terminus of plant HMA4 proteins confer nanomolar affinity for zinc and are essential for HMA4 function in vivo.
Identifieur interne : 000050 ( Main/Corpus ); précédent : 000049; suivant : 000051di-Cysteine motifs in the C-terminus of plant HMA4 proteins confer nanomolar affinity for zinc and are essential for HMA4 function in vivo.
Auteurs : Gilles Lekeux ; Clémentine Laurent ; Marine Joris ; Alice Jadoul ; Dan Jiang ; Bernard Bosman ; Monique Carnol ; Patrick Motte ; Zhiguang Xiao ; Moreno Galleni ; Marc HanikenneSource :
- Journal of experimental botany [ 1460-2431 ] ; 2018.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Adenosine Triphosphatases, Arabidopsis Proteins.
- chemical , metabolism : Adenosine Triphosphatases, Arabidopsis Proteins, Cysteine, Zinc.
- genetics : Arabidopsis.
- metabolism : Arabidopsis.
- Amino Acid Motifs, Species Specificity.
Abstract
The PIB ATPase heavy metal ATPase 4 (HMA4) has a central role in the zinc homeostasis network of Arabidopsis thaliana. This membrane protein loads metal from the pericycle cells into the xylem in roots, thereby allowing root to shoot metal translocation. Moreover, HMA4 is key for zinc hyperaccumulation as well as zinc and cadmium hypertolerance in the pseudometallophyte Arabidopsis halleri. The plant-specific cytosolic C-terminal extension of HMA4 is rich in putative metal-binding residues and has substantially diverged between A. thaliana and A. halleri. To clarify the function of the domain in both species, protein variants with truncated C-terminal extension, as well as with mutated di-Cys motifs and/or a His-stretch, were functionally characterized. We show that di-Cys motifs, but not the His-stretch, contribute to high affinity zinc binding and function in planta. We suggest that the HMA4 C-terminal extension is at least partly responsible for protein targeting to the plasma membrane. Finally, we reveal that the C-terminal extensions of both A. thaliana and A. halleri HMA4 proteins share similar function, despite marginally different zinc-binding capacity.
DOI: 10.1093/jxb/ery311
PubMed: 30137564
PubMed Central: PMC6255694
Links to Exploration step
pubmed:30137564Le document en format XML
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Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Laurent, Clementine" sort="Laurent, Clementine" uniqKey="Laurent C" first="Clémentine" last="Laurent">Clémentine Laurent</name><affiliation><nlm:affiliation>InBioS - Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Joris, Marine" sort="Joris, Marine" uniqKey="Joris M" first="Marine" last="Joris">Marine Joris</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Jadoul, Alice" sort="Jadoul, Alice" uniqKey="Jadoul A" first="Alice" last="Jadoul">Alice Jadoul</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Jiang, Dan" sort="Jiang, Dan" uniqKey="Jiang D" first="Dan" last="Jiang">Dan Jiang</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Bosman, Bernard" sort="Bosman, Bernard" uniqKey="Bosman B" first="Bernard" last="Bosman">Bernard Bosman</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Laboratory of Plant and Microbial Ecology, Department of Biology, Ecology, Evolution, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Carnol, Monique" sort="Carnol, Monique" uniqKey="Carnol M" first="Monique" last="Carnol">Monique Carnol</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Laboratory of Plant and Microbial Ecology, Department of Biology, Ecology, Evolution, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Motte, Patrick" sort="Motte, Patrick" uniqKey="Motte P" first="Patrick" last="Motte">Patrick Motte</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Xiao, Zhiguang" sort="Xiao, Zhiguang" uniqKey="Xiao Z" first="Zhiguang" last="Xiao">Zhiguang Xiao</name><affiliation><nlm:affiliation>School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Parkville, Victoria, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Galleni, Moreno" sort="Galleni, Moreno" uniqKey="Galleni M" first="Moreno" last="Galleni">Moreno Galleni</name><affiliation><nlm:affiliation>InBioS - Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Hanikenne, Marc" sort="Hanikenne, Marc" uniqKey="Hanikenne M" first="Marc" last="Hanikenne">Marc Hanikenne</name><affiliation><nlm:affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of experimental botany</title><idno type="eISSN">1460-2431</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adenosine Triphosphatases (genetics)</term><term>Adenosine Triphosphatases (metabolism)</term><term>Amino Acid Motifs (MeSH)</term><term>Arabidopsis (genetics)</term><term>Arabidopsis (metabolism)</term><term>Arabidopsis Proteins (genetics)</term><term>Arabidopsis Proteins (metabolism)</term><term>Cysteine (metabolism)</term><term>Species Specificity (MeSH)</term><term>Zinc (metabolism)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Adenosine Triphosphatases</term><term>Arabidopsis Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Adenosine Triphosphatases</term><term>Arabidopsis Proteins</term><term>Cysteine</term><term>Zinc</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Arabidopsis</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Arabidopsis</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Motifs</term><term>Species Specificity</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The PIB ATPase heavy metal ATPase 4 (HMA4) has a central role in the zinc homeostasis network of Arabidopsis thaliana. This membrane protein loads metal from the pericycle cells into the xylem in roots, thereby allowing root to shoot metal translocation. Moreover, HMA4 is key for zinc hyperaccumulation as well as zinc and cadmium hypertolerance in the pseudometallophyte Arabidopsis halleri. The plant-specific cytosolic C-terminal extension of HMA4 is rich in putative metal-binding residues and has substantially diverged between A. thaliana and A. halleri. To clarify the function of the domain in both species, protein variants with truncated C-terminal extension, as well as with mutated di-Cys motifs and/or a His-stretch, were functionally characterized. We show that di-Cys motifs, but not the His-stretch, contribute to high affinity zinc binding and function in planta. We suggest that the HMA4 C-terminal extension is at least partly responsible for protein targeting to the plasma membrane. Finally, we reveal that the C-terminal extensions of both A. thaliana and A. halleri HMA4 proteins share similar function, despite marginally different zinc-binding capacity.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30137564</PMID><DateCompleted><Year>2019</Year><Month>10</Month><Day>15</Day></DateCompleted><DateRevised><Year>2019</Year><Month>10</Month><Day>15</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1460-2431</ISSN><JournalIssue CitedMedium="Internet"><Volume>69</Volume><Issue>22</Issue><PubDate><Year>2018</Year><Month>11</Month><Day>26</Day></PubDate></JournalIssue><Title>Journal of experimental botany</Title><ISOAbbreviation>J Exp Bot</ISOAbbreviation></Journal><ArticleTitle>di-Cysteine motifs in the C-terminus of plant HMA4 proteins confer nanomolar affinity for zinc and are essential for HMA4 function in vivo.</ArticleTitle><Pagination><MedlinePgn>5547-5560</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/jxb/ery311</ELocationID><Abstract><AbstractText>The PIB ATPase heavy metal ATPase 4 (HMA4) has a central role in the zinc homeostasis network of Arabidopsis thaliana. This membrane protein loads metal from the pericycle cells into the xylem in roots, thereby allowing root to shoot metal translocation. Moreover, HMA4 is key for zinc hyperaccumulation as well as zinc and cadmium hypertolerance in the pseudometallophyte Arabidopsis halleri. The plant-specific cytosolic C-terminal extension of HMA4 is rich in putative metal-binding residues and has substantially diverged between A. thaliana and A. halleri. To clarify the function of the domain in both species, protein variants with truncated C-terminal extension, as well as with mutated di-Cys motifs and/or a His-stretch, were functionally characterized. We show that di-Cys motifs, but not the His-stretch, contribute to high affinity zinc binding and function in planta. We suggest that the HMA4 C-terminal extension is at least partly responsible for protein targeting to the plasma membrane. Finally, we reveal that the C-terminal extensions of both A. thaliana and A. halleri HMA4 proteins share similar function, despite marginally different zinc-binding capacity.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lekeux</LastName><ForeName>Gilles</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>InBioS - Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Laurent</LastName><ForeName>Clémentine</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>InBioS - Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Joris</LastName><ForeName>Marine</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jadoul</LastName><ForeName>Alice</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Dan</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bosman</LastName><ForeName>Bernard</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Laboratory of Plant and Microbial Ecology, Department of Biology, Ecology, Evolution, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carnol</LastName><ForeName>Monique</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Laboratory of Plant and Microbial Ecology, Department of Biology, Ecology, Evolution, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Motte</LastName><ForeName>Patrick</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiao</LastName><ForeName>Zhiguang</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Parkville, Victoria, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Galleni</LastName><ForeName>Moreno</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>InBioS - Center for Protein Engineering (CIP), Biological Macromolecules, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hanikenne</LastName><ForeName>Marc</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>InBioS - PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>J Exp Bot</MedlineTA><NlmUniqueID>9882906</NlmUniqueID><ISSNLinking>0022-0957</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D029681">Arabidopsis Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.6.1.-</RegistryNumber><NameOfSubstance UI="D000251">Adenosine Triphosphatases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.6.1.3</RegistryNumber><NameOfSubstance UI="C477864">HMA4 protein, Arabidopsis</NameOfSubstance></Chemical><Chemical><RegistryNumber>J41CSQ7QDS</RegistryNumber><NameOfSubstance UI="D015032">Zinc</NameOfSubstance></Chemical><Chemical><RegistryNumber>K848JZ4886</RegistryNumber><NameOfSubstance UI="D003545">Cysteine</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000251" MajorTopicYN="N">Adenosine Triphosphatases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020816" MajorTopicYN="N">Amino Acid Motifs</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D029681" MajorTopicYN="N">Arabidopsis Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName 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