Negative regulators of plant immunity derived from cinnamyl alcohol dehydrogenases are targeted by multiple Phytophthora Avr3a-like effectors.
Identifieur interne : 000446 ( Main/Exploration ); précédent : 000445; suivant : 000447Negative regulators of plant immunity derived from cinnamyl alcohol dehydrogenases are targeted by multiple Phytophthora Avr3a-like effectors.
Auteurs : Tingting Li [République populaire de Chine] ; Qinhu Wang [République populaire de Chine] ; Ruirui Feng [République populaire de Chine] ; Licai Li [République populaire de Chine] ; Liwen Ding [République populaire de Chine] ; Guangjin Fan [République populaire de Chine] ; Weiwei Li [République populaire de Chine] ; Yu Du [République populaire de Chine] ; Meixiang Zhang [République populaire de Chine] ; Guiyan Huang [République populaire de Chine] ; Patrick Sch Fer [Royaume-Uni] ; Yuling Meng [République populaire de Chine] ; Brett M. Tyler [États-Unis] ; Weixing Shan [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2019.
Abstract
Oomycete pathogens secrete numerous effectors to manipulate host immunity. While some effectors share a conserved structural fold, it remains unclear if any have conserved host targets. Avr3a-like family effectors, which are related to Phytophthora infestans effector PiAvr3a and are widely distributed across diverse clades of Phytophthora species, were used to study this question. By using yeast-two-hybrid, bimolecular fluorescence complementation and co-immunoprecipitation assays, we identified members of the plant cinnamyl alcohol dehydrogenase 7 (CAD7) subfamily as targets of multiple Avr3a-like effectors from Phytophthora pathogens. The CAD7 subfamily has expanded in plant genomes but lost the lignin biosynthetic activity of canonical CAD subfamilies. In turn, we identified CAD7s as negative regulators of plant immunity that are induced by Phytophthora infection. Moreover, AtCAD7 was stabilized by Avr3a-like effectors and involved in suppression of pathogen-associated molecular pattern-triggered immunity, including callose deposition, reactive oxygen species burst and WRKY33 expression. Our results reveal CAD7 subfamily proteins as negative regulators of plant immunity that are exploited by multiple Avr3a-like effectors to promote infection in different host plants.
DOI: 10.1111/nph.16139
PubMed: 31436314
Affiliations:
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712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. 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last="Li">Tingting Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Qinhu" sort="Wang, Qinhu" uniqKey="Wang Q" first="Qinhu" last="Wang">Qinhu Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Feng, Ruirui" sort="Feng, Ruirui" uniqKey="Feng R" first="Ruirui" last="Feng">Ruirui Feng</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Li, Licai" sort="Li, Licai" uniqKey="Li L" first="Licai" last="Li">Licai Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Ding, Liwen" sort="Ding, Liwen" uniqKey="Ding L" first="Liwen" last="Ding">Liwen Ding</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Fan, Guangjin" sort="Fan, Guangjin" uniqKey="Fan G" first="Guangjin" last="Fan">Guangjin Fan</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Li, Weiwei" sort="Li, Weiwei" uniqKey="Li W" first="Weiwei" last="Li">Weiwei Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Du, Yu" sort="Du, Yu" uniqKey="Du Y" first="Yu" last="Du">Yu Du</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Meixiang" sort="Zhang, Meixiang" uniqKey="Zhang M" first="Meixiang" last="Zhang">Meixiang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Huang, Guiyan" sort="Huang, Guiyan" uniqKey="Huang G" first="Guiyan" last="Huang">Guiyan Huang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Sch Fer, Patrick" sort="Sch Fer, Patrick" uniqKey="Sch Fer P" first="Patrick" last="Sch Fer">Patrick Sch Fer</name><affiliation wicri:level="1"><nlm:affiliation>School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL</wicri:regionArea><wicri:noRegion>CV4 7AL</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry, CV4 7AL, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry, CV4 7AL</wicri:regionArea><wicri:noRegion>CV4 7AL</wicri:noRegion></affiliation></author><author><name sortKey="Meng, Yuling" sort="Meng, Yuling" uniqKey="Meng Y" first="Yuling" last="Meng">Yuling Meng</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author><author><name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name><affiliation wicri:level="1"><nlm:affiliation>Center for Genome Research and Biocomputing and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Genome Research and Biocomputing and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331</wicri:regionArea><wicri:noRegion>97331</wicri:noRegion></affiliation></author><author><name sortKey="Shan, Weixing" sort="Shan, Weixing" uniqKey="Shan W" first="Weixing" last="Shan">Weixing Shan</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100</wicri:regionArea><wicri:noRegion>712100</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Oomycete pathogens secrete numerous effectors to manipulate host immunity. While some effectors share a conserved structural fold, it remains unclear if any have conserved host targets. Avr3a-like family effectors, which are related to Phytophthora infestans effector PiAvr3a and are widely distributed across diverse clades of Phytophthora species, were used to study this question. By using yeast-two-hybrid, bimolecular fluorescence complementation and co-immunoprecipitation assays, we identified members of the plant cinnamyl alcohol dehydrogenase 7 (CAD7) subfamily as targets of multiple Avr3a-like effectors from Phytophthora pathogens. The CAD7 subfamily has expanded in plant genomes but lost the lignin biosynthetic activity of canonical CAD subfamilies. In turn, we identified CAD7s as negative regulators of plant immunity that are induced by Phytophthora infection. Moreover, AtCAD7 was stabilized by Avr3a-like effectors and involved in suppression of pathogen-associated molecular pattern-triggered immunity, including callose deposition, reactive oxygen species burst and WRKY33 expression. Our results reveal CAD7 subfamily proteins as negative regulators of plant immunity that are exploited by multiple Avr3a-like effectors to promote infection in different host plants.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">31436314</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>2019</Year><Month>Aug</Month><Day>22</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Negative regulators of plant immunity derived from cinnamyl alcohol dehydrogenases are targeted by multiple Phytophthora Avr3a-like effectors.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16139</ELocationID><Abstract><AbstractText>Oomycete pathogens secrete numerous effectors to manipulate host immunity. While some effectors share a conserved structural fold, it remains unclear if any have conserved host targets. Avr3a-like family effectors, which are related to Phytophthora infestans effector PiAvr3a and are widely distributed across diverse clades of Phytophthora species, were used to study this question. By using yeast-two-hybrid, bimolecular fluorescence complementation and co-immunoprecipitation assays, we identified members of the plant cinnamyl alcohol dehydrogenase 7 (CAD7) subfamily as targets of multiple Avr3a-like effectors from Phytophthora pathogens. The CAD7 subfamily has expanded in plant genomes but lost the lignin biosynthetic activity of canonical CAD subfamilies. In turn, we identified CAD7s as negative regulators of plant immunity that are induced by Phytophthora infection. Moreover, AtCAD7 was stabilized by Avr3a-like effectors and involved in suppression of pathogen-associated molecular pattern-triggered immunity, including callose deposition, reactive oxygen species burst and WRKY33 expression. Our results reveal CAD7 subfamily proteins as negative regulators of plant immunity that are exploited by multiple Avr3a-like effectors to promote infection in different host plants.</AbstractText><CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Tingting</ForeName><Initials>T</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5011-0174</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Qinhu</ForeName><Initials>Q</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1251-073X</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feng</LastName><ForeName>Ruirui</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Licai</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ding</LastName><ForeName>Liwen</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Guangjin</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Weiwei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Yu</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Meixiang</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huang</LastName><ForeName>Guiyan</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schäfer</LastName><ForeName>Patrick</ForeName><Initials>P</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-0366-6858</Identifier><AffiliationInfo><Affiliation>School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry, CV4 7AL, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meng</LastName><ForeName>Yuling</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tyler</LastName><ForeName>Brett M</ForeName><Initials>BM</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1549-2987</Identifier><AffiliationInfo><Affiliation>Center for Genome Research and Biocomputing and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shan</LastName><ForeName>Weixing</ForeName><Initials>W</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-7286-4041</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, 712100, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>31125022</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>31561143007</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>CARS-09</GrantID><Agency>China Agriculture Research System</Agency><Country></Country></Grant><Grant><GrantID>B18042</GrantID><Agency>State Administration of Foreign Experts Affairs</Agency><Country></Country></Grant><Grant><GrantID>BB/M017982/1</GrantID><Agency>BBSRC/EPSRC</Agency><Country></Country></Grant><Grant><GrantID>2017M623262</GrantID><Agency>China Postdoctoral Science Foundation</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>22</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">Phytophthora
</Keyword><Keyword MajorTopicYN="N">Avr3a</Keyword><Keyword MajorTopicYN="N">CAD7</Keyword><Keyword MajorTopicYN="N">RXLR effector</Keyword><Keyword MajorTopicYN="N">host target</Keyword><Keyword MajorTopicYN="N">plant immunity</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>06</Month><Day>05</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>08</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>8</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>8</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>8</Month><Day>23</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31436314</ArticleId><ArticleId IdType="doi">10.1111/nph.16139</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Anderson RG, Casady MS, Fee RA, Vaughan MM, Deb D, Fedkenheuer K, Huffaker A, Schmelz EA, Tyler BM, McDowell JM. 2012. 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