An Arabidopsis Secondary Metabolite Directly Targets Expression of the Bacterial Type III Secretion System to Inhibit Bacterial Virulence

Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact mechanisms are often unknown. Here, we show that the Arabidopsis defense compound sulforaphane (SFN) functions primarily by inhibiting Pseudo...

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Published in:Cell host & microbe Vol. 27; no. 4; p. 601
Main Authors: Wang, Wei, Yang, Jing, Zhang, Jian, Liu, Yong-Xin, Tian, Caiping, Qu, Baoyuan, Gao, Chulei, Xin, Peiyong, Cheng, Shujing, Zhang, Wenjing, Miao, Pei, Li, Lei, Zhang, Xiaojuan, Chu, Jinfang, Zuo, Jianru, Li, Jiayang, Bai, Yang, Lei, Xiaoguang, Zhou, Jian-Min
Format: Journal Article
Language:English
Published: United States 08.04.2020
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ISSN:1934-6069, 1934-6069
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Abstract Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact mechanisms are often unknown. Here, we show that the Arabidopsis defense compound sulforaphane (SFN) functions primarily by inhibiting Pseudomonas syringae type III secretion system (TTSS) genes, which are essential for pathogenesis. Plants lacking the aliphatic glucosinolate pathway, which do not accumulate SFN, were unable to attenuate TTSS gene expression and exhibited increased susceptibility to P. syringae strains that cannot detoxify SFN. Chemoproteomics analyses showed that SFN covalently modified the cysteine at position 209 of HrpS, a key transcription factor controlling TTSS gene expression. Site-directed mutagenesis and functional analyses further confirmed that Cys209 was responsible for bacterial sensitivity to SFN in vitro and sensitivity to plant defenses conferred by the aliphatic glucosinolate pathway. Collectively, these results illustrate a previously unknown mechanism by which plants disarm a pathogenic bacterium.
AbstractList Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact mechanisms are often unknown. Here, we show that the Arabidopsis defense compound sulforaphane (SFN) functions primarily by inhibiting Pseudomonas syringae type III secretion system (TTSS) genes, which are essential for pathogenesis. Plants lacking the aliphatic glucosinolate pathway, which do not accumulate SFN, were unable to attenuate TTSS gene expression and exhibited increased susceptibility to P. syringae strains that cannot detoxify SFN. Chemoproteomics analyses showed that SFN covalently modified the cysteine at position 209 of HrpS, a key transcription factor controlling TTSS gene expression. Site-directed mutagenesis and functional analyses further confirmed that Cys209 was responsible for bacterial sensitivity to SFN in vitro and sensitivity to plant defenses conferred by the aliphatic glucosinolate pathway. Collectively, these results illustrate a previously unknown mechanism by which plants disarm a pathogenic bacterium.Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact mechanisms are often unknown. Here, we show that the Arabidopsis defense compound sulforaphane (SFN) functions primarily by inhibiting Pseudomonas syringae type III secretion system (TTSS) genes, which are essential for pathogenesis. Plants lacking the aliphatic glucosinolate pathway, which do not accumulate SFN, were unable to attenuate TTSS gene expression and exhibited increased susceptibility to P. syringae strains that cannot detoxify SFN. Chemoproteomics analyses showed that SFN covalently modified the cysteine at position 209 of HrpS, a key transcription factor controlling TTSS gene expression. Site-directed mutagenesis and functional analyses further confirmed that Cys209 was responsible for bacterial sensitivity to SFN in vitro and sensitivity to plant defenses conferred by the aliphatic glucosinolate pathway. Collectively, these results illustrate a previously unknown mechanism by which plants disarm a pathogenic bacterium.
Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact mechanisms are often unknown. Here, we show that the Arabidopsis defense compound sulforaphane (SFN) functions primarily by inhibiting Pseudomonas syringae type III secretion system (TTSS) genes, which are essential for pathogenesis. Plants lacking the aliphatic glucosinolate pathway, which do not accumulate SFN, were unable to attenuate TTSS gene expression and exhibited increased susceptibility to P. syringae strains that cannot detoxify SFN. Chemoproteomics analyses showed that SFN covalently modified the cysteine at position 209 of HrpS, a key transcription factor controlling TTSS gene expression. Site-directed mutagenesis and functional analyses further confirmed that Cys209 was responsible for bacterial sensitivity to SFN in vitro and sensitivity to plant defenses conferred by the aliphatic glucosinolate pathway. Collectively, these results illustrate a previously unknown mechanism by which plants disarm a pathogenic bacterium.
Author Liu, Yong-Xin
Wang, Wei
Gao, Chulei
Miao, Pei
Li, Jiayang
Lei, Xiaoguang
Zhang, Jian
Zhang, Xiaojuan
Zhou, Jian-Min
Chu, Jinfang
Zhang, Wenjing
Qu, Baoyuan
Zuo, Jianru
Xin, Peiyong
Bai, Yang
Yang, Jing
Tian, Caiping
Cheng, Shujing
Li, Lei
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  fullname: Wang, Wei
  organization: State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China
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  organization: State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Beijing Institute of Lifeomics, Beijing 102206, China
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  surname: Zhang
  fullname: Zhang, Jian
  organization: Department of Chemical Biology, College of Chemistry and Molecular Engineering, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, Synthetic and Functional Biomolecules Center and Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China
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  organization: Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany
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  organization: State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: jmzhou@genetics.ac.cn
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Keywords defense compound
glucosinolate
Arabidopsis
Pseudomonas syringae
Type III Secretion System
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Snippet Plants deploy a variety of secondary metabolites to fend off pathogen attack. Although defense compounds are generally considered toxic to microbes, the exact...
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SubjectTerms Arabidopsis - metabolism
Bacterial Proteins - drug effects
Cysteine - drug effects
Cysteine - metabolism
Disease Resistance
Gene Expression Regulation, Bacterial
Isothiocyanates - metabolism
Isothiocyanates - pharmacology
Plant Diseases - microbiology
Pseudomonas syringae - drug effects
Pseudomonas syringae - metabolism
Secondary Metabolism
Transcription Factors - drug effects
Type III Secretion Systems - drug effects
Type III Secretion Systems - genetics
Title An Arabidopsis Secondary Metabolite Directly Targets Expression of the Bacterial Type III Secretion System to Inhibit Bacterial Virulence
URI https://www.ncbi.nlm.nih.gov/pubmed/32272078
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