The poplar Phi class glutathione transferase: expression, activity and structure of GSTF1.
Identifieur interne : 002006 ( Main/Exploration ); précédent : 002005; suivant : 002007The poplar Phi class glutathione transferase: expression, activity and structure of GSTF1.
Auteurs : Henri Pégeot [France] ; Cha San Koh [France] ; Benjamin Petre [France] ; Sandrine Mathiot [France] ; Sébastien Duplessis [France] ; Arnaud Hecker [France] ; Claude Didierjean [France] ; Nicolas Rouhier [France]Source :
- Frontiers in plant science [ 1664-462X ] ; 2014.
Abstract
Glutathione transferases (GSTs) constitute a superfamily of enzymes with essential roles in cellular detoxification and secondary metabolism in plants as in other organisms. Several plant GSTs, including those of the Phi class (GSTFs), require a conserved catalytic serine residue to perform glutathione (GSH)-conjugation reactions. Genomic analyses revealed that terrestrial plants have around ten GSTFs, eight in the Populus trichocarpa genome, but their physiological functions and substrates are mostly unknown. Transcript expression analyses showed a predominant expression of all genes both in reproductive (female flowers, fruits, floral buds) and vegetative organs (leaves, petioles). Here, we show that the recombinant poplar GSTF1 (PttGSTF1) possesses peroxidase activity toward cumene hydroperoxide and GSH-conjugation activity toward model substrates such as 2,4-dinitrochlorobenzene, benzyl and phenetyl isothiocyanate, 4-nitrophenyl butyrate and 4-hydroxy-2-nonenal but interestingly not on previously identified GSTF-class substrates. In accordance with analytical gel filtration data, crystal structure of PttGSTF1 showed a canonical dimeric organization with bound GSH or 2-(N-morpholino)ethanesulfonic acid molecules. The structure of these protein-substrate complexes allowed delineating the residues contributing to both the G and H sites that form the active site cavity. In sum, the presence of GSTF1 transcripts and proteins in most poplar organs especially those rich in secondary metabolites such as flowers and fruits, together with its GSH-conjugation activity and its documented stress-responsive expression suggest that its function is associated with the catalytic transformation of metabolites and/or peroxide removal rather than with ligandin properties as previously reported for other GSTFs.
DOI: 10.3389/fpls.2014.00712
PubMed: 25566286
PubMed Central: PMC4274894
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INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux</wicri:regionArea><wicri:noRegion>UMR1136 Champenoux</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Koh, Cha San" sort="Koh, Cha San" uniqKey="Koh C" first="Cha San" last="Koh">Cha San Koh</name><affiliation wicri:level="4"><nlm:affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>UMR 7036 Vandoeuvre-lès-Nancy</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Petre, Benjamin" sort="Petre, Benjamin" uniqKey="Petre B" first="Benjamin" last="Petre">Benjamin Petre</name><affiliation wicri:level="4"><nlm:affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux</wicri:regionArea><wicri:noRegion>UMR1136 Champenoux</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Mathiot, Sandrine" sort="Mathiot, Sandrine" uniqKey="Mathiot S" first="Sandrine" last="Mathiot">Sandrine Mathiot</name><affiliation wicri:level="4"><nlm:affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>UMR 7036 Vandoeuvre-lès-Nancy</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sébastien" last="Duplessis">Sébastien Duplessis</name><affiliation wicri:level="4"><nlm:affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux</wicri:regionArea><wicri:noRegion>UMR1136 Champenoux</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Hecker, Arnaud" sort="Hecker, Arnaud" uniqKey="Hecker A" first="Arnaud" last="Hecker">Arnaud Hecker</name><affiliation wicri:level="4"><nlm:affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux</wicri:regionArea><wicri:noRegion>UMR1136 Champenoux</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Didierjean, Claude" sort="Didierjean, Claude" uniqKey="Didierjean C" first="Claude" last="Didierjean">Claude Didierjean</name><affiliation wicri:level="4"><nlm:affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>UMR 7036 Vandoeuvre-lès-Nancy</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author><author><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name><affiliation wicri:level="4"><nlm:affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux</wicri:regionArea><wicri:noRegion>UMR1136 Champenoux</wicri:noRegion><orgName type="university">Université de Lorraine</orgName><placeName><settlement type="city">Nancy</settlement><settlement type="city">Metz</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region></placeName></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Glutathione transferases (GSTs) constitute a superfamily of enzymes with essential roles in cellular detoxification and secondary metabolism in plants as in other organisms. Several plant GSTs, including those of the Phi class (GSTFs), require a conserved catalytic serine residue to perform glutathione (GSH)-conjugation reactions. Genomic analyses revealed that terrestrial plants have around ten GSTFs, eight in the Populus trichocarpa genome, but their physiological functions and substrates are mostly unknown. Transcript expression analyses showed a predominant expression of all genes both in reproductive (female flowers, fruits, floral buds) and vegetative organs (leaves, petioles). Here, we show that the recombinant poplar GSTF1 (PttGSTF1) possesses peroxidase activity toward cumene hydroperoxide and GSH-conjugation activity toward model substrates such as 2,4-dinitrochlorobenzene, benzyl and phenetyl isothiocyanate, 4-nitrophenyl butyrate and 4-hydroxy-2-nonenal but interestingly not on previously identified GSTF-class substrates. In accordance with analytical gel filtration data, crystal structure of PttGSTF1 showed a canonical dimeric organization with bound GSH or 2-(N-morpholino)ethanesulfonic acid molecules. The structure of these protein-substrate complexes allowed delineating the residues contributing to both the G and H sites that form the active site cavity. In sum, the presence of GSTF1 transcripts and proteins in most poplar organs especially those rich in secondary metabolites such as flowers and fruits, together with its GSH-conjugation activity and its documented stress-responsive expression suggest that its function is associated with the catalytic transformation of metabolites and/or peroxide removal rather than with ligandin properties as previously reported for other GSTFs. </div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">25566286</PMID><DateCompleted><Year>2015</Year><Month>01</Month><Day>08</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>29</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>5</Volume><PubDate><Year>2014</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>The poplar Phi class glutathione transferase: expression, activity and structure of GSTF1.</ArticleTitle><Pagination><MedlinePgn>712</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2014.00712</ELocationID><Abstract><AbstractText>Glutathione transferases (GSTs) constitute a superfamily of enzymes with essential roles in cellular detoxification and secondary metabolism in plants as in other organisms. Several plant GSTs, including those of the Phi class (GSTFs), require a conserved catalytic serine residue to perform glutathione (GSH)-conjugation reactions. Genomic analyses revealed that terrestrial plants have around ten GSTFs, eight in the Populus trichocarpa genome, but their physiological functions and substrates are mostly unknown. Transcript expression analyses showed a predominant expression of all genes both in reproductive (female flowers, fruits, floral buds) and vegetative organs (leaves, petioles). Here, we show that the recombinant poplar GSTF1 (PttGSTF1) possesses peroxidase activity toward cumene hydroperoxide and GSH-conjugation activity toward model substrates such as 2,4-dinitrochlorobenzene, benzyl and phenetyl isothiocyanate, 4-nitrophenyl butyrate and 4-hydroxy-2-nonenal but interestingly not on previously identified GSTF-class substrates. In accordance with analytical gel filtration data, crystal structure of PttGSTF1 showed a canonical dimeric organization with bound GSH or 2-(N-morpholino)ethanesulfonic acid molecules. The structure of these protein-substrate complexes allowed delineating the residues contributing to both the G and H sites that form the active site cavity. In sum, the presence of GSTF1 transcripts and proteins in most poplar organs especially those rich in secondary metabolites such as flowers and fruits, together with its GSH-conjugation activity and its documented stress-responsive expression suggest that its function is associated with the catalytic transformation of metabolites and/or peroxide removal rather than with ligandin properties as previously reported for other GSTFs. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Pégeot</LastName><ForeName>Henri</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Koh</LastName><ForeName>Cha San</ForeName><Initials>CS</Initials><AffiliationInfo><Affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Petre</LastName><ForeName>Benjamin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mathiot</LastName><ForeName>Sandrine</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duplessis</LastName><ForeName>Sébastien</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hecker</LastName><ForeName>Arnaud</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Didierjean</LastName><ForeName>Claude</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Faculté des Sciences et Technologies, Université de Lorraine, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France ; Faculté des Sciences et Technologies, CNRS, CRM2, Equipe BioMod, UMR 7036 Vandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rouhier</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Interactions Arbres - Microorganismes, Université de Lorraine, UMR1136 Vandoeuvre-lès-Nancy, France ; INRA, Interactions Arbres - Microorganismes, UMR1136 Champenoux, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>12</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus</Keyword><Keyword MajorTopicYN="N">crystallography</Keyword><Keyword MajorTopicYN="N">enzyme characterization</Keyword><Keyword MajorTopicYN="N">glutathione transferase</Keyword><Keyword MajorTopicYN="N">protein structure</Keyword><Keyword MajorTopicYN="N">transcript profiling</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2014</Year><Month>10</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2014</Year><Month>11</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2015</Year><Month>1</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2015</Year><Month>1</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2015</Year><Month>1</Month><Day>8</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">25566286</ArticleId><ArticleId 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Arnaud" uniqKey="Hecker A" first="Arnaud" last="Hecker">Arnaud Hecker</name><name sortKey="Koh, Cha San" sort="Koh, Cha San" uniqKey="Koh C" first="Cha San" last="Koh">Cha San Koh</name><name sortKey="Mathiot, Sandrine" sort="Mathiot, Sandrine" uniqKey="Mathiot S" first="Sandrine" last="Mathiot">Sandrine Mathiot</name><name sortKey="Petre, Benjamin" sort="Petre, Benjamin" uniqKey="Petre B" first="Benjamin" last="Petre">Benjamin Petre</name><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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