'Candidatus Liberibacter Asiaticus' SDE1 Effector Induces Huanglongbing Chlorosis by Downregulating Host DDX3 Gene.
Identifieur interne : 000248 ( Main/Exploration ); précédent : 000247; suivant : 000249'Candidatus Liberibacter Asiaticus' SDE1 Effector Induces Huanglongbing Chlorosis by Downregulating Host DDX3 Gene.
Auteurs : Yinghui Zhou [République populaire de Chine] ; Xiangying Wei [République populaire de Chine, États-Unis] ; Yanjiao Li [République populaire de Chine] ; Zhiqin Liu [République populaire de Chine] ; Yongping Duan [États-Unis] ; Huasong Zou [République populaire de Chine]Source :
- International journal of molecular sciences [ 1422-0067 ] ; 2020.
Abstract
'Candidatus Liberibacter asiaticus' (CLas) is the pathogenic bacterium that causes the disease Huanglongbing (HLB) in citrus and some model plants, such as Nicotiana benthamiana. After infection, CLas releases a set of effectors to modulate host responses. One of these critical effectors is Sec-delivered effector 1 (SDE1), which induces chlorosis and cell death in N. benthamiana. In this study, we revealed the DEAD-box RNA helicase (DDX3) interacts with SDE1. Gene silencing study revealed that knockdown of the NbDDX3 gene triggers leaf chlorosis, mimicking the primary symptom of CLas infection in N. benthamiana. The interactions between SDE1 and NbDDX3 were localized in the cell membrane. Overexpression of SDE1 resulted in suppression of NbDDX3 gene expression in N. benthamiana, which suggests a critical role of SDE1 in modulating NbDDX3 expression. Furthermore, we verified the interaction of SDE1 with citrus DDX3 (CsDDX3), and demonstrated that the expression of the CsDDX3 gene was significantly reduced in HLB-affected yellowing and mottled leaves of citrus. Thus, we provide molecular evidence that the downregulation of the host DDX3 gene is a crucial mechanism of leaf chlorosis in HLB-affected plants. The identification of CsDDX3 as a critical target of SDE1 and its association with HLB symptom development indicates that the DDX3 gene is an important target for gene editing, to interrupt the interaction between DDX3 and SDE1, and therefore interfere host susceptibility.
DOI: 10.3390/ijms21217996
PubMed: 33121168
PubMed Central: PMC7662370
Affiliations:
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type="pmid">33121168</idno><idno type="doi">10.3390/ijms21217996</idno><idno type="pmc">PMC7662370</idno><idno type="wicri:Area/Main/Corpus">000028</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000028</idno><idno type="wicri:Area/Main/Curation">000028</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000028</idno><idno type="wicri:Area/Main/Exploration">000028</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">'<i>Candidatus</i> Liberibacter Asiaticus' SDE1 Effector Induces Huanglongbing Chlorosis by Downregulating Host <i>DDX3</i> Gene.</title><author><name sortKey="Zhou, Yinghui" sort="Zhou, Yinghui" uniqKey="Zhou Y" first="Yinghui" last="Zhou">Yinghui Zhou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author><author><name sortKey="Wei, Xiangying" sort="Wei, Xiangying" uniqKey="Wei X" first="Xiangying" last="Wei">Xiangying Wei</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Oceanography, Minjiang University, Fuzhou 350108, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Oceanography, Minjiang University, Fuzhou 350108</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Li, Yanjiao" sort="Li, Yanjiao" uniqKey="Li Y" first="Yanjiao" last="Li">Yanjiao Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author><author><name sortKey="Liu, Zhiqin" sort="Liu, Zhiqin" uniqKey="Liu Z" first="Zhiqin" last="Liu">Zhiqin Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author><author><name sortKey="Duan, Yongping" sort="Duan, Yongping" uniqKey="Duan Y" first="Yongping" last="Duan">Yongping Duan</name><affiliation wicri:level="2"><nlm:affiliation>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Zou, Huasong" sort="Zou, Huasong" uniqKey="Zou H" first="Huasong" last="Zou">Huasong Zou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002</wicri:regionArea><placeName><settlement type="city">Fuzhou</settlement><region type="province">Fujian</region></placeName></affiliation></author></analytic><series><title level="j">International journal of molecular sciences</title><idno type="eISSN">1422-0067</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">'<i>Candidatus</i> Liberibacter asiaticus' (CLas) is the pathogenic bacterium that causes the disease Huanglongbing (HLB) in citrus and some model plants, such as <i>Nicotiana benthamiana</i>. After infection, CLas releases a set of effectors to modulate host responses. One of these critical effectors is Sec-delivered effector 1 (SDE1), which induces chlorosis and cell death in <i>N. benthamiana</i>. In this study, we revealed the DEAD-box RNA helicase (DDX3) interacts with SDE1. Gene silencing study revealed that knockdown of the <i>NbDDX3</i> gene triggers leaf chlorosis, mimicking the primary symptom of CLas infection in <i>N. benthamiana</i>. The interactions between SDE1 and NbDDX3 were localized in the cell membrane. Overexpression of <i>SDE1</i> resulted in suppression of <i>NbDDX3</i> gene expression in <i>N. benthamiana</i>, which suggests a critical role of <i>SDE1</i> in modulating <i>NbDDX3</i> expression. Furthermore, we verified the interaction of SDE1 with citrus DDX3 (CsDDX3), and demonstrated that the expression of the <i>CsDDX3</i> gene was significantly reduced in HLB-affected yellowing and mottled leaves of citrus. Thus, we provide molecular evidence that the downregulation of the host <i>DDX3</i> gene is a crucial mechanism of leaf chlorosis in HLB-affected plants. The identification of CsDDX3 as a critical target of SDE1 and its association with HLB symptom development indicates that the <i>DDX3</i> gene is an important target for gene editing, to interrupt the interaction between DDX3 and SDE1, and therefore interfere host susceptibility.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">33121168</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>14</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1422-0067</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>21</Issue><PubDate><Year>2020</Year><Month>Oct</Month><Day>27</Day></PubDate></JournalIssue><Title>International journal of molecular sciences</Title><ISOAbbreviation>Int J Mol Sci</ISOAbbreviation></Journal><ArticleTitle>'<i>Candidatus</i> Liberibacter Asiaticus' SDE1 Effector Induces Huanglongbing Chlorosis by Downregulating Host <i>DDX3</i> Gene.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E7996</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/ijms21217996</ELocationID><Abstract><AbstractText>'<i>Candidatus</i> Liberibacter asiaticus' (CLas) is the pathogenic bacterium that causes the disease Huanglongbing (HLB) in citrus and some model plants, such as <i>Nicotiana benthamiana</i>. After infection, CLas releases a set of effectors to modulate host responses. One of these critical effectors is Sec-delivered effector 1 (SDE1), which induces chlorosis and cell death in <i>N. benthamiana</i>. In this study, we revealed the DEAD-box RNA helicase (DDX3) interacts with SDE1. Gene silencing study revealed that knockdown of the <i>NbDDX3</i> gene triggers leaf chlorosis, mimicking the primary symptom of CLas infection in <i>N. benthamiana</i>. The interactions between SDE1 and NbDDX3 were localized in the cell membrane. Overexpression of <i>SDE1</i> resulted in suppression of <i>NbDDX3</i> gene expression in <i>N. benthamiana</i>, which suggests a critical role of <i>SDE1</i> in modulating <i>NbDDX3</i> expression. Furthermore, we verified the interaction of SDE1 with citrus DDX3 (CsDDX3), and demonstrated that the expression of the <i>CsDDX3</i> gene was significantly reduced in HLB-affected yellowing and mottled leaves of citrus. Thus, we provide molecular evidence that the downregulation of the host <i>DDX3</i> gene is a crucial mechanism of leaf chlorosis in HLB-affected plants. The identification of CsDDX3 as a critical target of SDE1 and its association with HLB symptom development indicates that the <i>DDX3</i> gene is an important target for gene editing, to interrupt the interaction between DDX3 and SDE1, and therefore interfere host susceptibility.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Yinghui</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0003-2596-9961</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Xiangying</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Institute of Oceanography, Minjiang University, Fuzhou 350108, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Yanjiao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Zhiqin</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duan</LastName><ForeName>Yongping</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>U.S. Horticultural Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Fort Pierce, FL 34945, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zou</LastName><ForeName>Huasong</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0001-5758-1975</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>31671988, 31872919</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Int J Mol Sci</MedlineTA><NlmUniqueID>101092791</NlmUniqueID><ISSNLinking>1422-0067</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Candidatus Liberibacter asiaticus</Keyword><Keyword MajorTopicYN="N">CsDDX3</Keyword><Keyword MajorTopicYN="N">NbDDX3</Keyword><Keyword MajorTopicYN="N">SDE1</Keyword><Keyword MajorTopicYN="N">chlorosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>10</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>10</Month><Day>25</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>30</Day><Hour>1</Hour><Minute>2</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33121168</ArticleId><ArticleId IdType="pii">ijms21217996</ArticleId><ArticleId IdType="doi">10.3390/ijms21217996</ArticleId><ArticleId IdType="pmc">PMC7662370</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Plant J. 2014 Jul;79(1):28-43</Citation><ArticleIdList><ArticleId IdType="pubmed">24724701</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2005 Jan;17(1):256-67</Citation><ArticleIdList><ArticleId IdType="pubmed">15598798</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS One. 2015 May 06;10(5):e0123939</Citation><ArticleIdList><ArticleId 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