The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity.
Identifieur interne : 000028 ( Main/Exploration ); précédent : 000027; suivant : 000029The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity.
Auteurs : Tuan Minh Tran [Singapour] ; Zhiming Ma [Singapour] ; Alexander Triebl [Singapour] ; Sangeeta Nath [Inde] ; Yingying Cheng [Singapour] ; Ben-Qiang Gong [République populaire de Chine] ; Xiao Han [Singapour] ; Junqi Wang [République populaire de Chine] ; Jian-Feng Li [République populaire de Chine] ; Markus R. Wenk [Singapour] ; Federico Torta [Singapour] ; Satyajit Mayor [Inde] ; Liang Yang [Singapour, République populaire de Chine] ; Yansong Miao [Singapour]Source :
- Life science alliance [ 2575-1077 ] ; 2020.
Abstract
Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern-triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern-triggered host immunity.
DOI: 10.26508/lsa.202000720
PubMed: 32788227
PubMed Central: PMC7425213
Affiliations:
- Inde, République populaire de Chine, Singapour
- Guangdong
- Jiangmen, Shenzhen
- Université nationale de Singapour
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last="Tran">Tuan Minh Tran</name><affiliation wicri:level="1"><nlm:affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>School of Biological Sciences, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Ma, Zhiming" sort="Ma, Zhiming" uniqKey="Ma Z" first="Zhiming" last="Ma">Zhiming Ma</name><affiliation wicri:level="1"><nlm:affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>School of Biological Sciences, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Triebl, Alexander" sort="Triebl, Alexander" uniqKey="Triebl A" first="Alexander" last="Triebl">Alexander Triebl</name><affiliation wicri:level="4"><nlm:affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore</wicri:regionArea><orgName type="university">Université nationale de Singapour</orgName></affiliation></author><author><name sortKey="Nath, Sangeeta" sort="Nath, Sangeeta" uniqKey="Nath S" first="Sangeeta" last="Nath">Sangeeta Nath</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Stem Cell Biology and Regenerative Medicine, Bangalore, India.</nlm:affiliation><country xml:lang="fr">Inde</country><wicri:regionArea>Institute for Stem Cell Biology and Regenerative Medicine, 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Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Gong, Ben Qiang" sort="Gong, Ben Qiang" uniqKey="Gong B" first="Ben-Qiang" last="Gong">Ben-Qiang Gong</name><affiliation wicri:level="3"><nlm:affiliation>School of Life Sciences, Sun Yat-sen University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Sun Yat-sen University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Han, Xiao" sort="Han, Xiao" uniqKey="Han X" first="Xiao" last="Han">Xiao Han</name><affiliation wicri:level="1"><nlm:affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>School of Biological Sciences, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Junqi" sort="Wang, Junqi" uniqKey="Wang J" first="Junqi" last="Wang">Junqi Wang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Biology, Southern University of Science and Technology, Shenzhen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Biology, Southern University of Science and Technology, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Li, Jian Feng" sort="Li, Jian Feng" uniqKey="Li J" first="Jian-Feng" last="Li">Jian-Feng Li</name><affiliation wicri:level="3"><nlm:affiliation>School of Life Sciences, Sun Yat-sen University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, Sun Yat-sen University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Wenk, Markus R" sort="Wenk, Markus R" uniqKey="Wenk M" first="Markus R" last="Wenk">Markus R. Wenk</name><affiliation wicri:level="4"><nlm:affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore</wicri:regionArea><orgName type="university">Université nationale de Singapour</orgName></affiliation></author><author><name sortKey="Torta, Federico" sort="Torta, Federico" uniqKey="Torta F" first="Federico" last="Torta">Federico Torta</name><affiliation wicri:level="4"><nlm:affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore</wicri:regionArea><orgName type="university">Université nationale de Singapour</orgName></affiliation></author><author><name sortKey="Mayor, Satyajit" sort="Mayor, Satyajit" uniqKey="Mayor S" first="Satyajit" last="Mayor">Satyajit Mayor</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Stem Cell Biology and Regenerative Medicine, Bangalore, India.</nlm:affiliation><country xml:lang="fr">Inde</country><wicri:regionArea>Institute for Stem Cell Biology and Regenerative Medicine, Bangalore</wicri:regionArea><wicri:noRegion>Bangalore</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>National Centre for Biological Sciences, Tata Institute for Fundamental Research, Bangalore, India.</nlm:affiliation><country xml:lang="fr">Inde</country><wicri:regionArea>National Centre for Biological Sciences, Tata Institute for Fundamental Research, Bangalore</wicri:regionArea><wicri:noRegion>Bangalore</wicri:noRegion></affiliation></author><author><name sortKey="Yang, Liang" sort="Yang, Liang" uniqKey="Yang L" first="Liang" last="Yang">Liang Yang</name><affiliation wicri:level="1"><nlm:affiliation>Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>School of Medicine, Southern University of Science and Technology, Shenzhen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Medicine, Southern University of Science and Technology, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Miao, Yansong" sort="Miao, Yansong" uniqKey="Miao Y" first="Yansong" last="Miao">Yansong Miao</name><affiliation wicri:level="1"><nlm:affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore yansongm@ntu.edu.sg.</nlm:affiliation><country wicri:rule="url">Singapour</country><wicri:regionArea>School of Biological Sciences, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore, Singapore.</nlm:affiliation><country xml:lang="fr">Singapour</country><wicri:regionArea>School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author></analytic><series><title level="j">Life science alliance</title><idno type="eISSN">2575-1077</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">Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (<i>cis</i>-11-methyl-dodecenoic acid) produced by <i>Xanthomonas campestris</i> pv. <i>campestris</i> can suppress pathogen-associated molecular pattern-triggered immunity (PTI) in <i>Arabidopsis thaliana</i>, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of <i>Arabidopsis</i>, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern-triggered host immunity.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32788227</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">2575-1077</ISSN><JournalIssue CitedMedium="Internet"><Volume>3</Volume><Issue>10</Issue><PubDate><Year>2020</Year><Month>10</Month></PubDate></JournalIssue><Title>Life science alliance</Title><ISOAbbreviation>Life Sci Alliance</ISOAbbreviation></Journal><ArticleTitle>The bacterial quorum sensing signal DSF hijacks <i>Arabidopsis thaliana</i> sterol biosynthesis to suppress plant innate immunity.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e202000720</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.26508/lsa.202000720</ELocationID><Abstract><AbstractText>Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (<i>cis</i>-11-methyl-dodecenoic acid) produced by <i>Xanthomonas campestris</i> pv. <i>campestris</i> can suppress pathogen-associated molecular pattern-triggered immunity (PTI) in <i>Arabidopsis thaliana</i>, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of <i>Arabidopsis</i>, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern-triggered host immunity.</AbstractText><CopyrightInformation>© 2020 Tran et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Tran</LastName><ForeName>Tuan Minh</ForeName><Initials>TM</Initials><Identifier Source="ORCID">0000-0003-1533-6044</Identifier><AffiliationInfo><Affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Zhiming</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Triebl</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nath</LastName><ForeName>Sangeeta</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute for Stem Cell Biology and Regenerative Medicine, Bangalore, India.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Manipal Institute of Regenerative Medicine, Manipal Academy of Higher Education, Bangalore, India.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cheng</LastName><ForeName>Yingying</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gong</LastName><ForeName>Ben-Qiang</ForeName><Initials>BQ</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Sun Yat-sen University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Han</LastName><ForeName>Xiao</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, Nanyang Technological University, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Junqi</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biology, Southern University of Science and Technology, Shenzhen, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Jian-Feng</ForeName><Initials>JF</Initials><AffiliationInfo><Affiliation>School of Life Sciences, Sun Yat-sen University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wenk</LastName><ForeName>Markus R</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Torta</LastName><ForeName>Federico</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Singapore Lipidomics Incubator (SLING), Yoo Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mayor</LastName><ForeName>Satyajit</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute for Stem Cell Biology and Regenerative Medicine, Bangalore, India.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Centre for Biological Sciences, 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Wenk</name><name sortKey="Yang, Liang" sort="Yang, Liang" uniqKey="Yang L" first="Liang" last="Yang">Liang Yang</name></country><country name="Inde"><noRegion><name sortKey="Nath, Sangeeta" sort="Nath, Sangeeta" uniqKey="Nath S" first="Sangeeta" last="Nath">Sangeeta Nath</name></noRegion><name sortKey="Mayor, Satyajit" sort="Mayor, Satyajit" uniqKey="Mayor S" first="Satyajit" last="Mayor">Satyajit Mayor</name><name sortKey="Mayor, Satyajit" sort="Mayor, Satyajit" uniqKey="Mayor S" first="Satyajit" last="Mayor">Satyajit Mayor</name><name sortKey="Nath, Sangeeta" sort="Nath, Sangeeta" uniqKey="Nath S" first="Sangeeta" last="Nath">Sangeeta Nath</name></country><country name="République populaire de Chine"><region name="Guangdong"><name sortKey="Gong, Ben Qiang" sort="Gong, Ben Qiang" uniqKey="Gong B" first="Ben-Qiang" last="Gong">Ben-Qiang Gong</name></region><name sortKey="Li, Jian Feng" sort="Li, Jian Feng" uniqKey="Li J" first="Jian-Feng" last="Li">Jian-Feng Li</name><name sortKey="Wang, Junqi" sort="Wang, Junqi" uniqKey="Wang J" first="Junqi" last="Wang">Junqi Wang</name><name sortKey="Yang, Liang" sort="Yang, Liang" uniqKey="Yang L" first="Liang" last="Yang">Liang Yang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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