A new bacteria-free strategy induced by MaGal2 facilitates pinewood nematode escape immune response from its vector beetle.
Identifieur interne : 000228 ( Main/Exploration ); précédent : 000227; suivant : 000229A new bacteria-free strategy induced by MaGal2 facilitates pinewood nematode escape immune response from its vector beetle.
Auteurs : Chi Zhang [République populaire de Chine] ; Jacob D. Wickham [République populaire de Chine] ; Lilin Zhao [République populaire de Chine] ; Jianghua Sun [République populaire de Chine]Source :
- Insect science [ 1744-7917 ] ; 2020.
Abstract
Symbiotic microbes play a crucial role in regulating parasite-host interactions; however, the role of bacterial associates in parasite-host interactions requires elucidation. In this study, we showed that, instead of introducing numerous symbiotic bacteria, dispersal of 4th-stage juvenile (JIV ) pinewood nematodes (PWNs), Bursaphelenchus xylophilus, only introduced few bacteria to its vector beetle, Monochamus alternatus (Ma). JIV showed weak binding ability to five dominant bacteria species isolated from the beetles' pupal chamber. This was especially the case for binding to the opportunistic pathogenic species Serratia marcescens; the nematodes' bacteria binding ability at this critical stage when it infiltrates Ma for dispersal was much weaker compared with Caenorhabditis elegans, Diplogasteroides asiaticus, and propagative-stage PWN. The associated bacterium S. marcescens, which was isolated from the beetles' pupal chambers, was unfavorable to Ma, because it caused a higher mortality rate upon injection into tracheae. In addition, S. marcescens in the tracheae caused more immune effector disorders compared with PWN alone. Ma_Galectin2 (MaGal2), a pattern-recognition receptor, was up-regulated following PWN loading. Recombinant MaGal2 protein formed aggregates with five dominant associated bacteria in vitro. Moreover, MaGal2 knockdown beetles had up-regulated prophenoloxidase gene expression, increased phenoloxidase activity, and decreased PWN loading. Our study revealed a previously unknown strategy for immune evasion of this plant pathogen inside its vector, and provides novel insights into the role of bacteria in parasite-host interactions.
DOI: 10.1111/1744-7917.12823
PubMed: 32443173
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Wickham</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhao, Lilin" sort="Zhao, Lilin" uniqKey="Zhao L" first="Lilin" last="Zhao">Lilin Zhao</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Sun, Jianghua" sort="Sun, Jianghua" uniqKey="Sun J" first="Jianghua" last="Sun">Jianghua Sun</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">Insect science</title><idno type="eISSN">1744-7917</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">Symbiotic microbes play a crucial role in regulating parasite-host interactions; however, the role of bacterial associates in parasite-host interactions requires elucidation. In this study, we showed that, instead of introducing numerous symbiotic bacteria, dispersal of 4th-stage juvenile (J<sub>IV</sub> ) pinewood nematodes (PWNs), Bursaphelenchus xylophilus, only introduced few bacteria to its vector beetle, Monochamus alternatus (Ma). J<sub>IV</sub> showed weak binding ability to five dominant bacteria species isolated from the beetles' pupal chamber. This was especially the case for binding to the opportunistic pathogenic species Serratia marcescens; the nematodes' bacteria binding ability at this critical stage when it infiltrates Ma for dispersal was much weaker compared with Caenorhabditis elegans, Diplogasteroides asiaticus, and propagative-stage PWN. The associated bacterium S. marcescens, which was isolated from the beetles' pupal chambers, was unfavorable to Ma, because it caused a higher mortality rate upon injection into tracheae. In addition, S. marcescens in the tracheae caused more immune effector disorders compared with PWN alone. Ma_Galectin2 (MaGal2), a pattern-recognition receptor, was up-regulated following PWN loading. Recombinant MaGal2 protein formed aggregates with five dominant associated bacteria in vitro. Moreover, MaGal2 knockdown beetles had up-regulated prophenoloxidase gene expression, increased phenoloxidase activity, and decreased PWN loading. Our study revealed a previously unknown strategy for immune evasion of this plant pathogen inside its vector, and provides novel insights into the role of bacteria in parasite-host interactions.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32443173</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>21</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1744-7917</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>May</Month><Day>22</Day></PubDate></JournalIssue><Title>Insect science</Title><ISOAbbreviation>Insect Sci</ISOAbbreviation></Journal><ArticleTitle>A new bacteria-free strategy induced by MaGal2 facilitates pinewood nematode escape immune response from its vector beetle.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/1744-7917.12823</ELocationID><Abstract><AbstractText>Symbiotic microbes play a crucial role in regulating parasite-host interactions; however, the role of bacterial associates in parasite-host interactions requires elucidation. In this study, we showed that, instead of introducing numerous symbiotic bacteria, dispersal of 4th-stage juvenile (J<sub>IV</sub> ) pinewood nematodes (PWNs), Bursaphelenchus xylophilus, only introduced few bacteria to its vector beetle, Monochamus alternatus (Ma). J<sub>IV</sub> showed weak binding ability to five dominant bacteria species isolated from the beetles' pupal chamber. This was especially the case for binding to the opportunistic pathogenic species Serratia marcescens; the nematodes' bacteria binding ability at this critical stage when it infiltrates Ma for dispersal was much weaker compared with Caenorhabditis elegans, Diplogasteroides asiaticus, and propagative-stage PWN. The associated bacterium S. marcescens, which was isolated from the beetles' pupal chambers, was unfavorable to Ma, because it caused a higher mortality rate upon injection into tracheae. In addition, S. marcescens in the tracheae caused more immune effector disorders compared with PWN alone. Ma_Galectin2 (MaGal2), a pattern-recognition receptor, was up-regulated following PWN loading. Recombinant MaGal2 protein formed aggregates with five dominant associated bacteria in vitro. Moreover, MaGal2 knockdown beetles had up-regulated prophenoloxidase gene expression, increased phenoloxidase activity, and decreased PWN loading. Our study revealed a previously unknown strategy for immune evasion of this plant pathogen inside its vector, and provides novel insights into the role of bacteria in parasite-host interactions.</AbstractText><CopyrightInformation>© 2020 Institute of Zoology, Chinese Academy of Sciences.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Chi</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wickham</LastName><ForeName>Jacob D</ForeName><Initials>JD</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Lilin</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Jianghua</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-9465-3672</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>31630013</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><Agency>Frontier Science Key Project of the Chinese Academy of Sciences</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>05</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>Australia</Country><MedlineTA>Insect Sci</MedlineTA><NlmUniqueID>101266965</NlmUniqueID><ISSNLinking>1672-9609</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">galectin</Keyword><Keyword MajorTopicYN="N">immune evasion</Keyword><Keyword MajorTopicYN="N">pinewood nematode</Keyword><Keyword MajorTopicYN="N">symbiotic bacteria</Keyword><Keyword MajorTopicYN="N">vector beetle</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>04</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>05</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>5</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>5</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32443173</ArticleId><ArticleId IdType="doi">10.1111/1744-7917.12823</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Adams, A.S., Aylward, F.O., Adams, S.M., Erbilgin, N., Aukema, B.H., Currie, C.R., et al. 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FASEB Journal, 32, 4862-4877.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li></country><settlement><li>Pékin</li></settlement></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Zhang, Chi" sort="Zhang, Chi" uniqKey="Zhang C" first="Chi" last="Zhang">Chi Zhang</name></noRegion><name sortKey="Sun, Jianghua" sort="Sun, Jianghua" uniqKey="Sun J" first="Jianghua" last="Sun">Jianghua Sun</name><name sortKey="Sun, Jianghua" sort="Sun, Jianghua" uniqKey="Sun J" first="Jianghua" last="Sun">Jianghua Sun</name><name sortKey="Wickham, Jacob D" sort="Wickham, Jacob D" uniqKey="Wickham J" first="Jacob D" last="Wickham">Jacob D. Wickham</name><name sortKey="Zhang, Chi" sort="Zhang, Chi" uniqKey="Zhang C" first="Chi" last="Zhang">Chi Zhang</name><name sortKey="Zhao, Lilin" sort="Zhao, Lilin" uniqKey="Zhao L" first="Lilin" last="Zhao">Lilin Zhao</name><name sortKey="Zhao, Lilin" sort="Zhao, Lilin" uniqKey="Zhao L" first="Lilin" last="Zhao">Lilin Zhao</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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