The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis.
Identifieur interne : 000020 ( Main/Exploration ); précédent : 000019; suivant : 000021The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis.
Auteurs : Jianlong Zhao [République populaire de Chine, France] ; Joffrey Mejias [France] ; Michaël Quentin [France] ; Yongpan Chen [République populaire de Chine, France] ; Janice De Almeida-Engler [France] ; Zhenchuan Mao [République populaire de Chine] ; Qinghua Sun [République populaire de Chine] ; Qian Liu [République populaire de Chine] ; Bingyan Xie [République populaire de Chine] ; Pierre Abad [France] ; Bruno Favery [France] ; Heng Jian [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Large amounts of effectors are secreted by the oesophageal glands of plant-parasitic nematodes, but their molecular mode of action remains largely unknown. We characterized a Meloidogyne incognita protein disulphide isomerase (PDI)-like effector protein (MiPDI1) that facilitates nematode parasitism. In situ hybridization showed that MiPDI1 was expressed specifically in the subventral glands of M. incognita. It was significantly upregulated during parasitic stages. Immunolocalization demonstrated MiPDI1 secretion in planta during nematode migration and within the feeding cells. Host-induced silencing of the MiPDI1 gene affected the ability of the nematode to infect the host, whereas MiPDI1 expression in Arabidopsis increased susceptibility to M. incognita, providing evidence for a key role of MiPDI1 in M. incognita parasitism. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays showed that MiPDI1 interacted with a tomato stress-associated protein (SlSAP12) orthologous to the redox-regulated AtSAP12, which plays an important role in plant responses to abiotic and biotic stresses. SAP12 silencing or knocking out in Nicotiana benthamiana and Arabidopsis increased susceptibility to M. incognita. Our results suggest that MiPDI1 acts as a pathogenicity factor promoting disease by fine-tuning SAP-mediated responses at the interface of redox signalling, defence and stress acclimation in Solanaceae and Arabidopsis.
DOI: 10.1111/nph.16745
PubMed: 32542658
Affiliations:
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wicri:level="1"><nlm:affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081</wicri:regionArea><wicri:noRegion>100081</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Mejias, Joffrey" sort="Mejias, Joffrey" uniqKey="Mejias J" first="Joffrey" last="Mejias">Joffrey Mejias</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Quentin, Michael" sort="Quentin, Michael" uniqKey="Quentin M" first="Michaël" last="Quentin">Michaël Quentin</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Chen, Yongpan" sort="Chen, Yongpan" uniqKey="Chen Y" first="Yongpan" last="Chen">Yongpan Chen</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193</wicri:regionArea><wicri:noRegion>100193</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="De Almeida Engler, Janice" sort="De Almeida Engler, Janice" uniqKey="De Almeida Engler J" first="Janice" last="De Almeida-Engler">Janice De Almeida-Engler</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Mao, Zhenchuan" sort="Mao, Zhenchuan" uniqKey="Mao Z" first="Zhenchuan" last="Mao">Zhenchuan Mao</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081</wicri:regionArea><wicri:noRegion>100081</wicri:noRegion></affiliation></author><author><name sortKey="Sun, Qinghua" sort="Sun, Qinghua" uniqKey="Sun Q" first="Qinghua" last="Sun">Qinghua Sun</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081</wicri:regionArea><wicri:noRegion>100081</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Qian" sort="Liu, Qian" uniqKey="Liu Q" first="Qian" last="Liu">Qian Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193</wicri:regionArea><wicri:noRegion>100193</wicri:noRegion></affiliation></author><author><name sortKey="Xie, Bingyan" sort="Xie, Bingyan" uniqKey="Xie B" first="Bingyan" last="Xie">Bingyan Xie</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081</wicri:regionArea><wicri:noRegion>100081</wicri:noRegion></affiliation></author><author><name sortKey="Abad, Pierre" sort="Abad, Pierre" uniqKey="Abad P" first="Pierre" last="Abad">Pierre Abad</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Favery, Bruno" sort="Favery, Bruno" uniqKey="Favery B" first="Bruno" last="Favery">Bruno Favery</name><affiliation wicri:level="3"><nlm:affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903</wicri:regionArea><placeName><region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region></placeName></affiliation></author><author><name sortKey="Jian, Heng" sort="Jian, Heng" uniqKey="Jian H" first="Heng" last="Jian">Heng Jian</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193</wicri:regionArea><wicri:noRegion>100193</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</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">Large amounts of effectors are secreted by the oesophageal glands of plant-parasitic nematodes, but their molecular mode of action remains largely unknown. We characterized a Meloidogyne incognita protein disulphide isomerase (PDI)-like effector protein (MiPDI1) that facilitates nematode parasitism. In situ hybridization showed that MiPDI1 was expressed specifically in the subventral glands of M. incognita. It was significantly upregulated during parasitic stages. Immunolocalization demonstrated MiPDI1 secretion in planta during nematode migration and within the feeding cells. Host-induced silencing of the MiPDI1 gene affected the ability of the nematode to infect the host, whereas MiPDI1 expression in Arabidopsis increased susceptibility to M. incognita, providing evidence for a key role of MiPDI1 in M. incognita parasitism. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays showed that MiPDI1 interacted with a tomato stress-associated protein (SlSAP12) orthologous to the redox-regulated AtSAP12, which plays an important role in plant responses to abiotic and biotic stresses. SAP12 silencing or knocking out in Nicotiana benthamiana and Arabidopsis increased susceptibility to M. incognita. Our results suggest that MiPDI1 acts as a pathogenicity factor promoting disease by fine-tuning SAP-mediated responses at the interface of redox signalling, defence and stress acclimation in Solanaceae and Arabidopsis.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32542658</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Jun</Month><Day>16</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16745</ELocationID><Abstract><AbstractText>Large amounts of effectors are secreted by the oesophageal glands of plant-parasitic nematodes, but their molecular mode of action remains largely unknown. We characterized a Meloidogyne incognita protein disulphide isomerase (PDI)-like effector protein (MiPDI1) that facilitates nematode parasitism. In situ hybridization showed that MiPDI1 was expressed specifically in the subventral glands of M. incognita. It was significantly upregulated during parasitic stages. Immunolocalization demonstrated MiPDI1 secretion in planta during nematode migration and within the feeding cells. Host-induced silencing of the MiPDI1 gene affected the ability of the nematode to infect the host, whereas MiPDI1 expression in Arabidopsis increased susceptibility to M. incognita, providing evidence for a key role of MiPDI1 in M. incognita parasitism. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays showed that MiPDI1 interacted with a tomato stress-associated protein (SlSAP12) orthologous to the redox-regulated AtSAP12, which plays an important role in plant responses to abiotic and biotic stresses. SAP12 silencing or knocking out in Nicotiana benthamiana and Arabidopsis increased susceptibility to M. incognita. Our results suggest that MiPDI1 acts as a pathogenicity factor promoting disease by fine-tuning SAP-mediated responses at the interface of redox signalling, defence and stress acclimation in Solanaceae and Arabidopsis.</AbstractText><CopyrightInformation>© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Jianlong</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-8179-6885</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mejias</LastName><ForeName>Joffrey</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-7663-0314</Identifier><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Quentin</LastName><ForeName>Michaël</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-8030-1203</Identifier><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Yongpan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Almeida-Engler</LastName><ForeName>Janice</ForeName><Initials>J</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-8312-672X</Identifier><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mao</LastName><ForeName>Zhenchuan</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Qinghua</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Qian</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xie</LastName><ForeName>Bingyan</ForeName><Initials>B</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-9640-8956</Identifier><AffiliationInfo><Affiliation>Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abad</LastName><ForeName>Pierre</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Favery</LastName><ForeName>Bruno</ForeName><Initials>B</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-3323-1852</Identifier><AffiliationInfo><Affiliation>INRAE, CNRS, ISA, Université Côte d'Azur, Sophia Antipolis, F-06903, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jian</LastName><ForeName>Heng</ForeName><Initials>H</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5908-3272</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, 100193, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>#ANR-11-LABX-0028-01</GrantID><Agency>ANR LabEx SIGNALIFE</Agency><Country></Country></Grant><Grant><GrantID>2017YFD0200601</GrantID><Agency>National Key Research and Development Program of China</Agency><Country></Country></Grant><Grant><GrantID>201606350083</GrantID><Agency>China Scholarship Council</Agency><Country></Country></Grant><Grant><GrantID>201806350108</GrantID><Agency>China Scholarship Council</Agency><Country></Country></Grant><Grant><GrantID>2013CB127501</GrantID><Agency>National Basic Research Program of China</Agency><Country></Country></Grant><Grant><GrantID>31571987</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>31772138</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><Agency>Ministère de l'Enseignement Supérieur, de la Recherche et de l'Innovation</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Arabidopsis thaliana
</Keyword><Keyword MajorTopicYN="N">Meloidogyne incognita
</Keyword><Keyword MajorTopicYN="N">Solanum lycopersicum
</Keyword><Keyword MajorTopicYN="N">effector</Keyword><Keyword MajorTopicYN="N">giant cells</Keyword><Keyword MajorTopicYN="N">plant-parasitic nematodes</Keyword><Keyword MajorTopicYN="N">redox</Keyword><Keyword MajorTopicYN="N">stress</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>6</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>6</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32542658</ArticleId><ArticleId IdType="doi">10.1111/nph.16745</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC et al. 2008. 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