Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice.
Identifieur interne : 000016 ( Main/Exploration ); précédent : 000015; suivant : 000017Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice.
Auteurs : Xuyan Mo [République populaire de Chine] ; Liyuan Zhang [République populaire de Chine] ; Yan Liu [République populaire de Chine] ; Xuan Wang [République populaire de Chine] ; Jiaqi Bai [République populaire de Chine] ; Kai Lu [République populaire de Chine] ; Shenshen Zou [République populaire de Chine] ; Hansong Dong [République populaire de Chine] ; Lei Chen [République populaire de Chine]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
Type III (T3) proteic effectors occupy most of the virulence determinants in eukaryote-pathogenic Gram-negative bacteria. During infection, bacteria may deploy a nanomachinery called translocon to deliver T3 effectors into host cells, wherein the effectors fulfill their pathological functions. T3 translocon is hypothetically assembled by bacterial translocators, which have been identified as one hydrophilic and two hydrophobic proteins in animal-pathogenic bacteria but remain unclear in plant pathogens. Now we characterize Hpa2, HrpF, and XopN proteins as concomitant T3 translocators in rice bacterial blight pathogen by analyzing pathological consequences of single, double, and triple gene knockout or genetic complementation. Based on these genetic analyses, Hpa2, HrpF, and XopN accordingly contribute to 46.9, 60.3, and 69.8% proportions of bacterial virulence on a susceptible rice variety. Virulence performances of Hpa2, HrpF, and XopN were attributed to their functions in essentially mediating from-bacteria-into-rice-cell translocation of PthXo1, the bacterial T3 effector characteristic of transcription factors targeting plant genes. On average, 61, 62, and 71% of PthXo1 translocation are provided correspondingly by Hpa2, HrpF, and XopN, while they cooperate to support PthXo1 translocation at a greater-than-95% extent. As a result, rice disease-susceptibility gene SWEET11, which is the regulatory target of PthXo1, is activated to confer bacterial virulence and induce the leaf blight disease in rice. Furthermore, the three translocators also undergo translocation, but only XopN is highly translocated to suppress rice defense responses, suggesting that different components of a T3 translocon deploy distinct virulence mechanisms in addition to the common function in mediating bacterial effector translocation.
DOI: 10.3389/fmicb.2020.01601
PubMed: 32793141
PubMed Central: PMC7390958
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first="Liyuan" last="Zhang">Liyuan Zhang</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Shandong Agricultural University, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Yan" sort="Liu, Yan" uniqKey="Liu Y" first="Yan" last="Liu">Yan Liu</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Xuan" sort="Wang, Xuan" uniqKey="Wang X" first="Xuan" last="Wang">Xuan Wang</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Bai, Jiaqi" sort="Bai, Jiaqi" uniqKey="Bai J" first="Jiaqi" last="Bai">Jiaqi Bai</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Lu, Kai" sort="Lu, Kai" uniqKey="Lu K" first="Kai" last="Lu">Kai Lu</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Shandong Agricultural University, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation></author><author><name sortKey="Zou, Shenshen" sort="Zou, Shenshen" uniqKey="Zou S" first="Shenshen" last="Zou">Shenshen Zou</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Shandong Agricultural University, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation></author><author><name sortKey="Dong, Hansong" sort="Dong, Hansong" uniqKey="Dong H" first="Hansong" last="Dong">Hansong Dong</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Shandong Agricultural University, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Lei" sort="Chen, Lei" uniqKey="Chen L" first="Lei" last="Chen">Lei Chen</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Shandong Agricultural University, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an</wicri:regionArea><wicri:noRegion>Tai'an</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</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">Type III (T3) proteic effectors occupy most of the virulence determinants in eukaryote-pathogenic Gram-negative bacteria. During infection, bacteria may deploy a nanomachinery called translocon to deliver T3 effectors into host cells, wherein the effectors fulfill their pathological functions. T3 translocon is hypothetically assembled by bacterial translocators, which have been identified as one hydrophilic and two hydrophobic proteins in animal-pathogenic bacteria but remain unclear in plant pathogens. Now we characterize Hpa2, HrpF, and XopN proteins as concomitant T3 translocators in rice bacterial blight pathogen by analyzing pathological consequences of single, double, and triple gene knockout or genetic complementation. Based on these genetic analyses, Hpa2, HrpF, and XopN accordingly contribute to 46.9, 60.3, and 69.8% proportions of bacterial virulence on a susceptible rice variety. Virulence performances of Hpa2, HrpF, and XopN were attributed to their functions in essentially mediating from-bacteria-into-rice-cell translocation of PthXo1, the bacterial T3 effector characteristic of transcription factors targeting plant genes. On average, 61, 62, and 71% of PthXo1 translocation are provided correspondingly by Hpa2, HrpF, and XopN, while they cooperate to support PthXo1 translocation at a greater-than-95% extent. As a result, rice disease-susceptibility gene <i>SWEET11</i>, which is the regulatory target of PthXo1, is activated to confer bacterial virulence and induce the leaf blight disease in rice. Furthermore, the three translocators also undergo translocation, but only XopN is highly translocated to suppress rice defense responses, suggesting that different components of a T3 translocon deploy distinct virulence mechanisms in addition to the common function in mediating bacterial effector translocation.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32793141</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>Three Proteins (Hpa2, HrpF and XopN) Are Concomitant Type III Translocators in Bacterial Blight Pathogen of Rice.</ArticleTitle><Pagination><MedlinePgn>1601</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.01601</ELocationID><Abstract><AbstractText>Type III (T3) proteic effectors occupy most of the virulence determinants in eukaryote-pathogenic Gram-negative bacteria. During infection, bacteria may deploy a nanomachinery called translocon to deliver T3 effectors into host cells, wherein the effectors fulfill their pathological functions. T3 translocon is hypothetically assembled by bacterial translocators, which have been identified as one hydrophilic and two hydrophobic proteins in animal-pathogenic bacteria but remain unclear in plant pathogens. Now we characterize Hpa2, HrpF, and XopN proteins as concomitant T3 translocators in rice bacterial blight pathogen by analyzing pathological consequences of single, double, and triple gene knockout or genetic complementation. Based on these genetic analyses, Hpa2, HrpF, and XopN accordingly contribute to 46.9, 60.3, and 69.8% proportions of bacterial virulence on a susceptible rice variety. Virulence performances of Hpa2, HrpF, and XopN were attributed to their functions in essentially mediating from-bacteria-into-rice-cell translocation of PthXo1, the bacterial T3 effector characteristic of transcription factors targeting plant genes. On average, 61, 62, and 71% of PthXo1 translocation are provided correspondingly by Hpa2, HrpF, and XopN, while they cooperate to support PthXo1 translocation at a greater-than-95% extent. As a result, rice disease-susceptibility gene <i>SWEET11</i>, which is the regulatory target of PthXo1, is activated to confer bacterial virulence and induce the leaf blight disease in rice. Furthermore, the three translocators also undergo translocation, but only XopN is highly translocated to suppress rice defense responses, suggesting that different components of a T3 translocon deploy distinct virulence mechanisms in addition to the common function in mediating bacterial effector translocation.</AbstractText><CopyrightInformation>Copyright © 2020 Mo, Zhang, Liu, Wang, Bai, Lu, Zou, Dong and Chen.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Mo</LastName><ForeName>Xuyan</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Liyuan</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Xuan</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bai</LastName><ForeName>Jiaqi</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Kai</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zou</LastName><ForeName>Shenshen</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dong</LastName><ForeName>Hansong</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Lei</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>College of Plant Protection, Shandong Agricultural University, Tai'an, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Molecular Biology Research Group, State Key Laboratory of Crop Biology, Tai'an, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Hpa2</Keyword><Keyword MajorTopicYN="N">HrpF</Keyword><Keyword MajorTopicYN="N">PthXo1</Keyword><Keyword MajorTopicYN="N">Xanthomonas oryzae pv. oryzae</Keyword><Keyword MajorTopicYN="N">XopN</Keyword><Keyword MajorTopicYN="N">type III translocator</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>27</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>8</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>15</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32793141</ArticleId><ArticleId 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