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The Cotton Apoplastic Protein CRR1 Stabilizes Chitinase 28 to Facilitate Defense against the Fungal Pathogen Verticillium dahliae.

Identifieur interne : 000370 ( Main/Exploration ); précédent : 000369; suivant : 000371

The Cotton Apoplastic Protein CRR1 Stabilizes Chitinase 28 to Facilitate Defense against the Fungal Pathogen Verticillium dahliae.

Auteurs : Li-Bo Han [République populaire de Chine] ; Yuan-Bao Li [République populaire de Chine] ; Fu-Xin Wang [République populaire de Chine] ; Wen-Yan Wang [République populaire de Chine] ; Jun Liu [République populaire de Chine] ; Jia-He Wu [République populaire de Chine] ; Nai-Qin Zhong [République populaire de Chine] ; Shen-Jie Wu [République populaire de Chine] ; Gai-Li Jiao [République populaire de Chine] ; Hai-Yun Wang [République populaire de Chine] ; Gui-Xian Xia [République populaire de Chine]

Source :

RBID : pubmed:30651348

Descripteurs français

English descriptors

Abstract

The apoplast serves as the first battlefield between the plant hosts and invading microbes; therefore, work on plant-pathogen interactions has increasingly focused on apoplastic immunity. In this study, we identified three proteins in the apoplast of cotton (Gossypium sp) root cells during interaction of the plant with the fungal pathogen Verticillium dahliae Among these proteins, cotton host cells secrete chitinase 28 (Chi28) and the Cys-rich repeat protein 1 (CRR1), while the pathogen releases the protease VdSSEP1. Biochemical analysis demonstrated that VdSSEP1 hydrolyzed Chi28, but CRR1 protected Chi28 from cleavage by Verticillium dahliae secretory Ser protease 1 (VdSSEP1). In accordance with the in vitro results, CRR1 interacted with Chi28 in yeast and plant cells and attenuated the observed decrease in Chi28 level that occurred in the apoplast of plant cells upon pathogen attack. Knockdown of CRR1 or Chi28 in cotton plants resulted in higher susceptibility to V. dahliae infection, and overexpression of CRR1 increased plant resistance to Vdahliae, the fungus Botrytis cinerea, and the oomycete Phytophthora parasitica var nicotianae By contrast, knockout of VdSSEP1 in V. dahliae destroyed the pathogenicity of this fungus. Together, our results provide compelling evidence for a multilayered interplay of factors in cotton apoplastic immunity.

DOI: 10.1105/tpc.18.00390
PubMed: 30651348
PubMed Central: PMC6447012


Affiliations:


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<term>Chitinases (genetics)</term>
<term>Chitinases (metabolism)</term>
<term>Disease Resistance (genetics)</term>
<term>Gene Expression Regulation, Plant (genetics)</term>
<term>Gene Expression Regulation, Plant (physiology)</term>
<term>Gossypium (genetics)</term>
<term>Gossypium (metabolism)</term>
<term>Gossypium (microbiology)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Verticillium (pathogenicity)</term>
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<term>Chitinase (génétique)</term>
<term>Chitinase (métabolisme)</term>
<term>Gossypium (génétique)</term>
<term>Gossypium (microbiologie)</term>
<term>Gossypium (métabolisme)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (génétique)</term>
<term>Régulation de l'expression des gènes végétaux (physiologie)</term>
<term>Résistance à la maladie (génétique)</term>
<term>Verticillium (pathogénicité)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Chitinases</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Chitinases</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Disease Resistance</term>
<term>Gene Expression Regulation, Plant</term>
<term>Gossypium</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Chitinase</term>
<term>Gossypium</term>
<term>Maladies des plantes</term>
<term>Protéines végétales</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Résistance à la maladie</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Gossypium</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Gossypium</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Gossypium</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Chitinase</term>
<term>Gossypium</term>
<term>Protéines végétales</term>
</keywords>
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<term>Verticillium</term>
</keywords>
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<term>Verticillium</term>
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<term>Régulation de l'expression des gènes végétaux</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
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<front>
<div type="abstract" xml:lang="en">The apoplast serves as the first battlefield between the plant hosts and invading microbes; therefore, work on plant-pathogen interactions has increasingly focused on apoplastic immunity. In this study, we identified three proteins in the apoplast of cotton (
<i>Gossypium</i>
sp) root cells during interaction of the plant with the fungal pathogen
<i>Verticillium dahliae</i>
Among these proteins, cotton host cells secrete chitinase 28 (Chi28) and the Cys-rich repeat protein 1 (CRR1), while the pathogen releases the protease VdSSEP1. Biochemical analysis demonstrated that VdSSEP1 hydrolyzed Chi28, but CRR1 protected Chi28 from cleavage by
<i>Verticillium dahliae</i>
secretory Ser protease 1 (VdSSEP1). In accordance with the in vitro results, CRR1 interacted with Chi28 in yeast and plant cells and attenuated the observed decrease in Chi28 level that occurred in the apoplast of plant cells upon pathogen attack. Knockdown of
<i>CRR1</i>
or
<i>Chi28</i>
in cotton plants resulted in higher susceptibility to
<i>V. dahliae</i>
infection, and overexpression of
<i>CRR1</i>
increased plant resistance to
<i>V</i>
<i>dahliae</i>
, the fungus
<i>Botrytis cinerea</i>
, and the oomycete
<i>Phytophthora parasitica</i>
var
<i>nicotianae</i>
By contrast, knockout of
<i>VdSSEP1</i>
in
<i>V. dahliae</i>
destroyed the pathogenicity of this fungus. Together, our results provide compelling evidence for a multilayered interplay of factors in cotton apoplastic immunity.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">30651348</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>02</Month>
<Day>20</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>03</Month>
<Day>09</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-298X</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>31</Volume>
<Issue>2</Issue>
<PubDate>
<Year>2019</Year>
<Month>02</Month>
</PubDate>
</JournalIssue>
<Title>The Plant cell</Title>
<ISOAbbreviation>Plant Cell</ISOAbbreviation>
</Journal>
<ArticleTitle>The Cotton Apoplastic Protein CRR1 Stabilizes Chitinase 28 to Facilitate Defense against the Fungal Pathogen
<i>Verticillium dahliae</i>
.</ArticleTitle>
<Pagination>
<MedlinePgn>520-536</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1105/tpc.18.00390</ELocationID>
<Abstract>
<AbstractText>The apoplast serves as the first battlefield between the plant hosts and invading microbes; therefore, work on plant-pathogen interactions has increasingly focused on apoplastic immunity. In this study, we identified three proteins in the apoplast of cotton (
<i>Gossypium</i>
sp) root cells during interaction of the plant with the fungal pathogen
<i>Verticillium dahliae</i>
Among these proteins, cotton host cells secrete chitinase 28 (Chi28) and the Cys-rich repeat protein 1 (CRR1), while the pathogen releases the protease VdSSEP1. Biochemical analysis demonstrated that VdSSEP1 hydrolyzed Chi28, but CRR1 protected Chi28 from cleavage by
<i>Verticillium dahliae</i>
secretory Ser protease 1 (VdSSEP1). In accordance with the in vitro results, CRR1 interacted with Chi28 in yeast and plant cells and attenuated the observed decrease in Chi28 level that occurred in the apoplast of plant cells upon pathogen attack. Knockdown of
<i>CRR1</i>
or
<i>Chi28</i>
in cotton plants resulted in higher susceptibility to
<i>V. dahliae</i>
infection, and overexpression of
<i>CRR1</i>
increased plant resistance to
<i>V</i>
<i>dahliae</i>
, the fungus
<i>Botrytis cinerea</i>
, and the oomycete
<i>Phytophthora parasitica</i>
var
<i>nicotianae</i>
By contrast, knockout of
<i>VdSSEP1</i>
in
<i>V. dahliae</i>
destroyed the pathogenicity of this fungus. Together, our results provide compelling evidence for a multilayered interplay of factors in cotton apoplastic immunity.</AbstractText>
<CopyrightInformation>© 2019 American Society of Plant Biologists. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Han</LastName>
<ForeName>Li-Bo</ForeName>
<Initials>LB</Initials>
<Identifier Source="ORCID">0000-0001-7068-8160</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Crop Science, Plant Immunity Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Yuan-Bao</ForeName>
<Initials>YB</Initials>
<Identifier Source="ORCID">0000-0001-7238-2261</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Crop Science, Plant Immunity Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Fu-Xin</ForeName>
<Initials>FX</Initials>
<Identifier Source="ORCID">0000-0001-5851-8767</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Wen-Yan</ForeName>
<Initials>WY</Initials>
<Identifier Source="ORCID">0000-0001-7431-1862</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Jun</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0002-3255-269X</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wu</LastName>
<ForeName>Jia-He</ForeName>
<Initials>JH</Initials>
<Identifier Source="ORCID">0000-0003-0012-2174</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhong</LastName>
<ForeName>Nai-Qin</ForeName>
<Initials>NQ</Initials>
<Identifier Source="ORCID">0000-0002-1059-3140</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wu</LastName>
<ForeName>Shen-Jie</ForeName>
<Initials>SJ</Initials>
<Identifier Source="ORCID">0000-0003-4157-3852</Identifier>
<AffiliationInfo>
<Affiliation>Institute of Cotton Research, Shanxi Academy of Agricultural Sciences, Yuncheng, Shanxi 044000, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jiao</LastName>
<ForeName>Gai-Li</ForeName>
<Initials>GL</Initials>
<Identifier Source="ORCID">0000-0001-6967-2655</Identifier>
<AffiliationInfo>
<Affiliation>Institute of Cotton Research, Shanxi Academy of Agricultural Sciences, Yuncheng, Shanxi 044000, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Hai-Yun</ForeName>
<Initials>HY</Initials>
<Identifier Source="ORCID">0000-0001-9071-4346</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China wanghy@im.ac.cn xiagx@im.ac.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xia</LastName>
<ForeName>Gui-Xian</ForeName>
<Initials>GX</Initials>
<Identifier Source="ORCID">0000-0003-4426-9784</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China wanghy@im.ac.cn xiagx@im.ac.cn.</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>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>01</Month>
<Day>16</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Plant Cell</MedlineTA>
<NlmUniqueID>9208688</NlmUniqueID>
<ISSNLinking>1040-4651</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.2.1.14</RegistryNumber>
<NameOfSubstance UI="D002688">Chitinases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002688" MajorTopicYN="N">Chitinases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003368" MajorTopicYN="N">Gossypium</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020172" MajorTopicYN="N">Verticillium</DescriptorName>
<QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
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<Month>05</Month>
<Day>21</Day>
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<PubMedPubDate PubStatus="revised">
<Year>2018</Year>
<Month>12</Month>
<Day>12</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>01</Month>
<Day>09</Day>
</PubMedPubDate>
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<country>
<li>République populaire de Chine</li>
</country>
<settlement>
<li>Pékin</li>
</settlement>
</list>
<tree>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Han, Li Bo" sort="Han, Li Bo" uniqKey="Han L" first="Li-Bo" last="Han">Li-Bo Han</name>
</noRegion>
<name sortKey="Han, Li Bo" sort="Han, Li Bo" uniqKey="Han L" first="Li-Bo" last="Han">Li-Bo Han</name>
<name sortKey="Jiao, Gai Li" sort="Jiao, Gai Li" uniqKey="Jiao G" first="Gai-Li" last="Jiao">Gai-Li Jiao</name>
<name sortKey="Li, Yuan Bao" sort="Li, Yuan Bao" uniqKey="Li Y" first="Yuan-Bao" last="Li">Yuan-Bao Li</name>
<name sortKey="Li, Yuan Bao" sort="Li, Yuan Bao" uniqKey="Li Y" first="Yuan-Bao" last="Li">Yuan-Bao Li</name>
<name sortKey="Liu, Jun" sort="Liu, Jun" uniqKey="Liu J" first="Jun" last="Liu">Jun Liu</name>
<name sortKey="Wang, Fu Xin" sort="Wang, Fu Xin" uniqKey="Wang F" first="Fu-Xin" last="Wang">Fu-Xin Wang</name>
<name sortKey="Wang, Hai Yun" sort="Wang, Hai Yun" uniqKey="Wang H" first="Hai-Yun" last="Wang">Hai-Yun Wang</name>
<name sortKey="Wang, Wen Yan" sort="Wang, Wen Yan" uniqKey="Wang W" first="Wen-Yan" last="Wang">Wen-Yan Wang</name>
<name sortKey="Wu, Jia He" sort="Wu, Jia He" uniqKey="Wu J" first="Jia-He" last="Wu">Jia-He Wu</name>
<name sortKey="Wu, Shen Jie" sort="Wu, Shen Jie" uniqKey="Wu S" first="Shen-Jie" last="Wu">Shen-Jie Wu</name>
<name sortKey="Xia, Gui Xian" sort="Xia, Gui Xian" uniqKey="Xia G" first="Gui-Xian" last="Xia">Gui-Xian Xia</name>
<name sortKey="Zhong, Nai Qin" sort="Zhong, Nai Qin" uniqKey="Zhong N" first="Nai-Qin" last="Zhong">Nai-Qin Zhong</name>
</country>
</tree>
</affiliations>
</record>

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