Chemical Genetics Approach Identifies Abnormal Inflorescence Meristem 1 as a Putative Target of a Novel Sulfonamide That Protects Catalase2-Deficient Arabidopsis against Photorespiratory Stress.
Identifieur interne : 000274 ( Main/Exploration ); précédent : 000273; suivant : 000275Chemical Genetics Approach Identifies Abnormal Inflorescence Meristem 1 as a Putative Target of a Novel Sulfonamide That Protects Catalase2-Deficient Arabidopsis against Photorespiratory Stress.
Auteurs : Tom Van Der Meer [Belgique] ; Arno Verlee [Belgique] ; Patrick Willems [Belgique] ; Francis Impens [Belgique] ; Kris Gevaert [Belgique] ; Christa Testerink [Pays-Bas] ; Christian V. Stevens [Belgique] ; Frank Van Breusegem [Belgique] ; Pavel Kerchev [Belgique, République tchèque]Source :
- Cells [ 2073-4409 ] ; 2020.
Abstract
Alterations of hydrogen peroxide (H2O2) levels have a profound impact on numerous signaling cascades orchestrating plant growth, development, and stress signaling, including programmed cell death. To expand the repertoire of known molecular mechanisms implicated in H2O2 signaling, we performed a forward chemical screen to identify small molecules that could alleviate the photorespiratory-induced cell death phenotype of Arabidopsisthaliana mutants lacking H2O2-scavenging capacity by peroxisomal catalase2. Here, we report the characterization of pakerine, an m-sulfamoyl benzamide from the sulfonamide family. Pakerine alleviates the cell death phenotype of cat2 mutants exposed to photorespiration-promoting conditions and delays dark-induced senescence in wild-type Arabidopsis leaves. By using a combination of transcriptomics, metabolomics, and affinity purification, we identified abnormal inflorescence meristem 1 (AIM1) as a putative protein target of pakerine. AIM1 is a 3-hydroxyacyl-CoA dehydrogenase involved in fatty acid β-oxidation that contributes to jasmonic acid (JA) and salicylic acid (SA) biosynthesis. Whereas intact JA biosynthesis was not required for pakerine bioactivity, our results point toward a role for β-oxidation-dependent SA production in the execution of H2O2-mediated cell death.
DOI: 10.3390/cells9092026
PubMed: 32887516
PubMed Central: PMC7563276
Affiliations:
- Belgique, Pays-Bas, République tchèque
- Moravie, Province de Flandre-Orientale, Région flamande
- Brno, Gand
- Université de Gand
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Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation></author><author><name sortKey="Verlee, Arno" sort="Verlee, Arno" uniqKey="Verlee A" first="Arno" last="Verlee">Arno Verlee</name><affiliation wicri:level="4"><nlm:affiliation>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 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University, B-9052 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation></author><author><name sortKey="Impens, Francis" sort="Impens, Francis" uniqKey="Impens F" first="Francis" last="Impens">Francis Impens</name><affiliation wicri:level="1"><nlm:affiliation>VIB Proteomics Core, B-9000 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Proteomics Core, B-9000 Ghent</wicri:regionArea><wicri:noRegion>B-9000 Ghent</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>VIB Center for Medical Biotechnology, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Center for Medical Biotechnology, B-9052 Ghent</wicri:regionArea><wicri:noRegion>B-9052 Ghent</wicri:noRegion></affiliation></author><author><name sortKey="Gevaert, Kris" sort="Gevaert, Kris" uniqKey="Gevaert K" first="Kris" last="Gevaert">Kris Gevaert</name><affiliation wicri:level="4"><nlm:affiliation>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>VIB Center for Medical Biotechnology, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Center for Medical Biotechnology, B-9052 Ghent</wicri:regionArea><wicri:noRegion>B-9052 Ghent</wicri:noRegion></affiliation></author><author><name sortKey="Testerink, Christa" sort="Testerink, Christa" uniqKey="Testerink C" first="Christa" last="Testerink">Christa Testerink</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Plant Physiology, Plant Sciences Group, Wageningen University and Research, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Plant Physiology, Plant Sciences Group, Wageningen University and Research, 6708 PB Wageningen</wicri:regionArea><wicri:noRegion>6708 PB Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Stevens, Christian V" sort="Stevens, Christian V" uniqKey="Stevens C" first="Christian V" last="Stevens">Christian V. Stevens</name><affiliation wicri:level="4"><nlm:affiliation>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation></author><author><name sortKey="Van Breusegem, Frank" sort="Van Breusegem, Frank" uniqKey="Van Breusegem F" first="Frank" last="Van Breusegem">Frank Van Breusegem</name><affiliation wicri:level="1"><nlm:affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Center for Plant Systems Biology, B-9052 Ghent</wicri:regionArea><wicri:noRegion>B-9052 Ghent</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation></author><author><name sortKey="Kerchev, Pavel" sort="Kerchev, Pavel" uniqKey="Kerchev P" first="Pavel" last="Kerchev">Pavel Kerchev</name><affiliation wicri:level="1"><nlm:affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>VIB Center for Plant Systems Biology, B-9052 Ghent</wicri:regionArea><wicri:noRegion>B-9052 Ghent</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Department of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno</wicri:regionArea><placeName><settlement type="city">Brno</settlement><region>Moravie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Phytophthora Research Centre, Mendel University in Brno, 61300 Brno, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Phytophthora Research Centre, Mendel University in Brno, 61300 Brno</wicri:regionArea><placeName><settlement type="city">Brno</settlement><region>Moravie</region></placeName></affiliation></author></analytic><series><title level="j">Cells</title><idno type="eISSN">2073-4409</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">Alterations of hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) levels have a profound impact on numerous signaling cascades orchestrating plant growth, development, and stress signaling, including programmed cell death. To expand the repertoire of known molecular mechanisms implicated in H<sub>2</sub>O<sub>2</sub> signaling, we performed a forward chemical screen to identify small molecules that could alleviate the photorespiratory-induced cell death phenotype of <i>Arabidopsis</i><i>thaliana</i> mutants lacking H<sub>2</sub>O<sub>2</sub>-scavenging capacity by peroxisomal catalase2. Here, we report the characterization of pakerine, an <i>m</i>-sulfamoyl benzamide from the sulfonamide family. Pakerine alleviates the cell death phenotype of <i>cat2</i> mutants exposed to photorespiration-promoting conditions and delays dark-induced senescence in wild-type <i>Arabidopsis</i> leaves. By using a combination of transcriptomics, metabolomics, and affinity purification, we identified abnormal inflorescence meristem 1 (AIM1) as a putative protein target of pakerine. AIM1 is a 3-hydroxyacyl-CoA dehydrogenase involved in fatty acid β-oxidation that contributes to jasmonic acid (JA) and salicylic acid (SA) biosynthesis. Whereas intact JA biosynthesis was not required for pakerine bioactivity, our results point toward a role for β-oxidation-dependent SA production in the execution of H<sub>2</sub>O<sub>2</sub>-mediated cell death.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32887516</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>28</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2073-4409</ISSN><JournalIssue CitedMedium="Internet"><Volume>9</Volume><Issue>9</Issue><PubDate><Year>2020</Year><Month>Sep</Month><Day>02</Day></PubDate></JournalIssue><Title>Cells</Title><ISOAbbreviation>Cells</ISOAbbreviation></Journal><ArticleTitle>Chemical Genetics Approach Identifies Abnormal Inflorescence Meristem 1 as a Putative Target of a Novel Sulfonamide That Protects Catalase2-Deficient <i>Arabidopsis</i> against Photorespiratory Stress.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E2026</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/cells9092026</ELocationID><Abstract><AbstractText>Alterations of hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) levels have a profound impact on numerous signaling cascades orchestrating plant growth, development, and stress signaling, including programmed cell death. To expand the repertoire of known molecular mechanisms implicated in H<sub>2</sub>O<sub>2</sub> signaling, we performed a forward chemical screen to identify small molecules that could alleviate the photorespiratory-induced cell death phenotype of <i>Arabidopsis</i><i>thaliana</i> mutants lacking H<sub>2</sub>O<sub>2</sub>-scavenging capacity by peroxisomal catalase2. Here, we report the characterization of pakerine, an <i>m</i>-sulfamoyl benzamide from the sulfonamide family. Pakerine alleviates the cell death phenotype of <i>cat2</i> mutants exposed to photorespiration-promoting conditions and delays dark-induced senescence in wild-type <i>Arabidopsis</i> leaves. By using a combination of transcriptomics, metabolomics, and affinity purification, we identified abnormal inflorescence meristem 1 (AIM1) as a putative protein target of pakerine. AIM1 is a 3-hydroxyacyl-CoA dehydrogenase involved in fatty acid β-oxidation that contributes to jasmonic acid (JA) and salicylic acid (SA) biosynthesis. Whereas intact JA biosynthesis was not required for pakerine bioactivity, our results point toward a role for β-oxidation-dependent SA production in the execution of H<sub>2</sub>O<sub>2</sub>-mediated cell death.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>van der Meer</LastName><ForeName>Tom</ForeName><Initials>T</Initials><Identifier Source="ORCID">0000-0002-7535-0190</Identifier><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Verlee</LastName><ForeName>Arno</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Willems</LastName><ForeName>Patrick</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0003-4667-2294</Identifier><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Impens</LastName><ForeName>Francis</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0003-2886-9616</Identifier><AffiliationInfo><Affiliation>VIB Proteomics Core, B-9000 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>VIB Center for Medical Biotechnology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gevaert</LastName><ForeName>Kris</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, B-9000 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>VIB Center for Medical Biotechnology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Testerink</LastName><ForeName>Christa</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0001-6738-115X</Identifier><AffiliationInfo><Affiliation>Laboratory of Plant Physiology, Plant Sciences Group, Wageningen University and Research, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Stevens</LastName><ForeName>Christian V</ForeName><Initials>CV</Initials><Identifier Source="ORCID">0000-0003-4393-5327</Identifier><AffiliationInfo><Affiliation>Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Breusegem</LastName><ForeName>Frank</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kerchev</LastName><ForeName>Pavel</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech Republic.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Phytophthora Research Centre, Mendel University in Brno, 61300 Brno, Czech Republic.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Cells</MedlineTA><NlmUniqueID>101600052</NlmUniqueID><ISSNLinking>2073-4409</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">H2O2 signaling</Keyword><Keyword MajorTopicYN="N">abnormal inflorescence meristem 1</Keyword><Keyword MajorTopicYN="N">catalase2-deficient Arabidopsis</Keyword><Keyword MajorTopicYN="N">chemical genetics</Keyword><Keyword MajorTopicYN="N">photorespiration</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>07</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>08</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>9</Month><Day>5</Day><Hour>1</Hour><Minute>4</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>9</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>9</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId 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