The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.
Identifieur interne : 000105 ( Main/Corpus ); précédent : 000104; suivant : 000106The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.
Auteurs : Rafał Zdrzałek ; Sophien Kamoun ; Ryohei Terauchi ; Hiromasa Saitoh ; Mark J. BanfieldSource :
- PloS one [ 1932-6203 ] ; 2020.
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : NLR Proteins, Plant Proteins.
- chemical , metabolism : NLR Proteins, Plant Proteins.
- cytology : Oryza.
- metabolism : Oryza.
- Amino Acid Motifs, Amino Acid Sequence, Cell Death, Protein Binding, Protein Domains.
Abstract
Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.
DOI: 10.1371/journal.pone.0238616
PubMed: 32931489
PubMed Central: PMC7491719
Links to Exploration step
pubmed:32931489Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.</title><author><name sortKey="Zdrzalek, Rafal" sort="Zdrzalek, Rafal" uniqKey="Zdrzalek R" first="Rafał" last="Zdrzałek">Rafał Zdrzałek</name><affiliation><nlm:affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Terauchi, Ryohei" sort="Terauchi, Ryohei" uniqKey="Terauchi R" first="Ryohei" last="Terauchi">Ryohei Terauchi</name><affiliation><nlm:affiliation>Division of Genomics and Breeding, Iwate Biotechnology Research Centre, Iwate, Japan.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.</nlm:affiliation></affiliation></author><author><name sortKey="Saitoh, Hiromasa" sort="Saitoh, Hiromasa" uniqKey="Saitoh H" first="Hiromasa" last="Saitoh">Hiromasa Saitoh</name><affiliation><nlm:affiliation>Laboratory of Plant Symbiotic and Parasitic Microbes, Department of Molecular Microbiology, Faculty of Life Sciences, Tokyo University of Agriculture, Tokyo, Japan.</nlm:affiliation></affiliation></author><author><name sortKey="Banfield, Mark J" sort="Banfield, Mark J" uniqKey="Banfield M" first="Mark J" last="Banfield">Mark J. Banfield</name><affiliation><nlm:affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32931489</idno><idno type="pmid">32931489</idno><idno type="doi">10.1371/journal.pone.0238616</idno><idno type="pmc">PMC7491719</idno><idno type="wicri:Area/Main/Corpus">000105</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000105</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.</title><author><name sortKey="Zdrzalek, Rafal" sort="Zdrzalek, Rafal" uniqKey="Zdrzalek R" first="Rafał" last="Zdrzałek">Rafał Zdrzałek</name><affiliation><nlm:affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name><affiliation><nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Terauchi, Ryohei" sort="Terauchi, Ryohei" uniqKey="Terauchi R" first="Ryohei" last="Terauchi">Ryohei Terauchi</name><affiliation><nlm:affiliation>Division of Genomics and Breeding, Iwate Biotechnology Research Centre, Iwate, Japan.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.</nlm:affiliation></affiliation></author><author><name sortKey="Saitoh, Hiromasa" sort="Saitoh, Hiromasa" uniqKey="Saitoh H" first="Hiromasa" last="Saitoh">Hiromasa Saitoh</name><affiliation><nlm:affiliation>Laboratory of Plant Symbiotic and Parasitic Microbes, Department of Molecular Microbiology, Faculty of Life Sciences, Tokyo University of Agriculture, Tokyo, Japan.</nlm:affiliation></affiliation></author><author><name sortKey="Banfield, Mark J" sort="Banfield, Mark J" uniqKey="Banfield M" first="Mark J" last="Banfield">Mark J. Banfield</name><affiliation><nlm:affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</nlm:affiliation></affiliation></author></analytic><series><title level="j">PloS one</title><idno type="eISSN">1932-6203</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Motifs (MeSH)</term><term>Amino Acid Sequence (MeSH)</term><term>Cell Death (MeSH)</term><term>NLR Proteins (chemistry)</term><term>NLR Proteins (metabolism)</term><term>Oryza (cytology)</term><term>Oryza (metabolism)</term><term>Plant Proteins (chemistry)</term><term>Plant Proteins (metabolism)</term><term>Protein Binding (MeSH)</term><term>Protein Domains (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>NLR Proteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>NLR Proteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Oryza</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Oryza</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Motifs</term><term>Amino Acid Sequence</term><term>Cell Death</term><term>Protein Binding</term><term>Protein Domains</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32931489</PMID><DateCompleted><Year>2020</Year><Month>10</Month><Day>28</Day></DateCompleted><DateRevised><Year>2020</Year><Month>10</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>15</Volume><Issue>9</Issue><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.</ArticleTitle><Pagination><MedlinePgn>e0238616</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0238616</ELocationID><Abstract><AbstractText>Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zdrzałek</LastName><ForeName>Rafał</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0003-3669-924X</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kamoun</LastName><ForeName>Sophien</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-0290-0315</Identifier><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Terauchi</LastName><ForeName>Ryohei</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-0095-4651</Identifier><AffiliationInfo><Affiliation>Division of Genomics and Breeding, Iwate Biotechnology Research Centre, Iwate, Japan.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saitoh</LastName><ForeName>Hiromasa</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0002-0124-9276</Identifier><AffiliationInfo><Affiliation>Laboratory of Plant Symbiotic and Parasitic Microbes, Department of Molecular Microbiology, Faculty of Life Sciences, Tokyo University of Agriculture, Tokyo, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Banfield</LastName><ForeName>Mark J</ForeName><Initials>MJ</Initials><Identifier Source="ORCID">0000-0001-8921-3835</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/M011216/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/P012574</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/M02198X </GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United 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MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012275" MajorTopicYN="N">Oryza</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="Y">cytology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName></MeshHeading></MeshHeadingList><CoiStatement>The authors have declared that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate 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IdType="pubmed">28808003</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2014 Apr 18;344(6181):299-303</Citation><ArticleIdList><ArticleId IdType="pubmed">24744375</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2019 Apr;222(2):938-953</Citation><ArticleIdList><ArticleId IdType="pubmed">30585636</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Pathog. 2015 Feb 26;11(2):e1004674</Citation><ArticleIdList><ArticleId IdType="pubmed">25719542</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2017 Aug;38:59-67</Citation><ArticleIdList><ArticleId IdType="pubmed">28494248</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 1999 Nov;20(3):317-32</Citation><ArticleIdList><ArticleId IdType="pubmed">10571892</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2006 Aug;18(8):2082-93</Citation><ArticleIdList><ArticleId IdType="pubmed">16844906</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2017 Nov 17;358(6365):888-893</Citation><ArticleIdList><ArticleId IdType="pubmed">29146805</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2016 Nov 8;113(45):12856-12861</Citation><ArticleIdList><ArticleId IdType="pubmed">27791121</ArticleId></ArticleIdList></Reference><Reference><Citation>EMBO J. 2014 Sep 1;33(17):1941-59</Citation><ArticleIdList><ArticleId IdType="pubmed">25024433</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2006 Feb;18(2):491-501</Citation><ArticleIdList><ArticleId IdType="pubmed">16387833</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2018 Feb;30(2):285-299</Citation><ArticleIdList><ArticleId IdType="pubmed">29382771</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell Environ. 2018 Oct;41(10):2313-2327</Citation><ArticleIdList><ArticleId IdType="pubmed">29790585</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2017 Jul 25;114(30):8113-8118</Citation><ArticleIdList><ArticleId IdType="pubmed">28698366</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2019 Apr 5;364(6435):</Citation><ArticleIdList><ArticleId IdType="pubmed">30948527</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Biol. 2018 Dec 12;16(12):e2005821</Citation><ArticleIdList><ArticleId IdType="pubmed">30540748</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2019 Aug;50:82-94</Citation><ArticleIdList><ArticleId IdType="pubmed">31063902</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2019 Aug 23;365(6455):793-799</Citation><ArticleIdList><ArticleId IdType="pubmed">31439792</ArticleId></ArticleIdList></Reference><Reference><Citation>Elife. 2015 Aug 25;4:</Citation><ArticleIdList><ArticleId IdType="pubmed">26304198</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2015 Oct 23;350(6259):404-9</Citation><ArticleIdList><ArticleId IdType="pubmed">26449474</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Pathog. 2017 May 5;13(5):e1006376</Citation><ArticleIdList><ArticleId IdType="pubmed">28475615</ArticleId></ArticleIdList></Reference><Reference><Citation>Cell Host Microbe. 2019 Aug 14;26(2):193-201</Citation><ArticleIdList><ArticleId IdType="pubmed">31415752</ArticleId></ArticleIdList></Reference><Reference><Citation>EMBO J. 2000 Aug 1;19(15):4004-14</Citation><ArticleIdList><ArticleId IdType="pubmed">10921881</ArticleId></ArticleIdList></Reference><Reference><Citation>Arch Biochem Biophys. 2019 Jul 30;670:58-68</Citation><ArticleIdList><ArticleId IdType="pubmed">31071301</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2018 Aug;44:98-107</Citation><ArticleIdList><ArticleId IdType="pubmed">29597139</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2018 Jul;219(1):17-24</Citation><ArticleIdList><ArticleId IdType="pubmed">29131341</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2016 Apr;210(2):618-26</Citation><ArticleIdList><ArticleId IdType="pubmed">26848538</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant. 2019 Feb 4;12(2):248-262</Citation><ArticleIdList><ArticleId IdType="pubmed">30639751</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Genet. 2013;9(4):e1003465</Citation><ArticleIdList><ArticleId IdType="pubmed">23633962</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2016 Jan;28(1):146-59</Citation><ArticleIdList><ArticleId IdType="pubmed">26744216</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2019 Aug 23;365(6455):799-803</Citation><ArticleIdList><ArticleId IdType="pubmed">31439793</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2019 Apr 5;364(6435):</Citation><ArticleIdList><ArticleId IdType="pubmed">30948526</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Biol. 2016 Feb 19;14:8</Citation><ArticleIdList><ArticleId IdType="pubmed">26891798</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 2011 Aug;24(8):897-906</Citation><ArticleIdList><ArticleId IdType="pubmed">21539434</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Pathog. 2012;8(6):e1002752</Citation><ArticleIdList><ArticleId IdType="pubmed">22685408</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2019 Aug;50:121-131</Citation><ArticleIdList><ArticleId IdType="pubmed">31154077</ArticleId></ArticleIdList></Reference><Reference><Citation>Elife. 2019 Nov 27;8:</Citation><ArticleIdList><ArticleId IdType="pubmed">31774397</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2008 Mar;20(3):739-51</Citation><ArticleIdList><ArticleId IdType="pubmed">18344282</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2002 Nov;14(11):2929-39</Citation><ArticleIdList><ArticleId IdType="pubmed">12417711</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2016 May;171(1):658-74</Citation><ArticleIdList><ArticleId IdType="pubmed">26951433</ArticleId></ArticleIdList></Reference><Reference><Citation>Annu Rev Phytopathol. 2017 Aug 4;55:205-229</Citation><ArticleIdList><ArticleId IdType="pubmed">28637398</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2006 Apr;140(4):1233-45</Citation><ArticleIdList><ArticleId IdType="pubmed">16489136</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2017 Jan;29(1):156-168</Citation><ArticleIdList><ArticleId IdType="pubmed">28087830</ArticleId></ArticleIdList></Reference><Reference><Citation>J Biol Chem. 2018 Mar 2;293(9):3218-3233</Citation><ArticleIdList><ArticleId IdType="pubmed">29217772</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2012 Apr;158(4):1819-32</Citation><ArticleIdList><ArticleId IdType="pubmed">22331412</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2013 Jul;162(3):1510-28</Citation><ArticleIdList><ArticleId IdType="pubmed">23660837</ArticleId></ArticleIdList></Reference><Reference><Citation>Ann Bot. 2017 Mar 1;119(5):827-702</Citation><ArticleIdList><ArticleId IdType="pubmed">27562749</ArticleId></ArticleIdList></Reference><Reference><Citation>Front Plant Sci. 2014 Nov 25;5:606</Citation><ArticleIdList><ArticleId IdType="pubmed">25506347</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2018 Jun 22;360(6395):1300-1301</Citation><ArticleIdList><ArticleId IdType="pubmed">29930125</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2018 Oct 9;115(41):10218-10227</Citation><ArticleIdList><ArticleId IdType="pubmed">30254172</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):E2046-E2052</Citation><ArticleIdList><ArticleId IdType="pubmed">28159890</ArticleId></ArticleIdList></Reference><Reference><Citation>Elife. 2019 Sep 19;8:</Citation><ArticleIdList><ArticleId IdType="pubmed">31535976</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16463-8</Citation><ArticleIdList><ArticleId IdType="pubmed">21911370</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS One. 2008;3(11):e3647</Citation><ArticleIdList><ArticleId IdType="pubmed">18985154</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2005 Jul;43(2):284-98</Citation><ArticleIdList><ArticleId IdType="pubmed">15998314</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Plants. 2017 Jul 24;3:17115</Citation><ArticleIdList><ArticleId IdType="pubmed">28737762</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS One. 2019 Aug 28;14(8):e0221226</Citation><ArticleIdList><ArticleId IdType="pubmed">31461469</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2017 Aug;174(4):2038-2053</Citation><ArticleIdList><ArticleId IdType="pubmed">28652264</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2019 Apr;222(2):966-980</Citation><ArticleIdList><ArticleId IdType="pubmed">30582759</ArticleId></ArticleIdList></Reference><Reference><Citation>Cell Host Microbe. 2011 Mar 17;9(3):200-211</Citation><ArticleIdList><ArticleId IdType="pubmed">21402359</ArticleId></ArticleIdList></Reference><Reference><Citation>Cell Host Microbe. 2010 May 20;7(5):362-75</Citation><ArticleIdList><ArticleId IdType="pubmed">20478538</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2012 Aug;15(4):375-84</Citation><ArticleIdList><ArticleId IdType="pubmed">22658703</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Rev Genet. 2010 Aug;11(8):539-48</Citation><ArticleIdList><ArticleId IdType="pubmed">20585331</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):11637-11642</Citation><ArticleIdList><ArticleId IdType="pubmed">30355769</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Rev Immunol. 2016 Sep;16(9):537-52</Citation><ArticleIdList><ArticleId IdType="pubmed">27477127</ArticleId></ArticleIdList></Reference><Reference><Citation>Semin Cell Dev Biol. 2016 Aug;56:134-149</Citation><ArticleIdList><ArticleId IdType="pubmed">27208725</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2002 Oct;32(2):195-204</Citation><ArticleIdList><ArticleId IdType="pubmed">12383085</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS Pathog. 2016 Jul 18;12(7):e1005769</Citation><ArticleIdList><ArticleId IdType="pubmed">27427964</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Opin Plant Biol. 2014 Aug;20:69-74</Citation><ArticleIdList><ArticleId IdType="pubmed">24845576</ArticleId></ArticleIdList></Reference><Reference><Citation>J Biol Chem. 2015 May 1;290(18):11258-67</Citation><ArticleIdList><ArticleId IdType="pubmed">25792750</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Plants. 2018 Aug;4(8):576-585</Citation><ArticleIdList><ArticleId IdType="pubmed">29988155</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2010 Jul;22(7):2444-58</Citation><ArticleIdList><ArticleId IdType="pubmed">20601497</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14789-94</Citation><ArticleIdList><ArticleId IdType="pubmed">11121079</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2015 Oct 23;350(6259):399-404</Citation><ArticleIdList><ArticleId IdType="pubmed">26449475</ArticleId></ArticleIdList></Reference><Reference><Citation>Methods Mol Biol. 2011;712:181-94</Citation><ArticleIdList><ArticleId IdType="pubmed">21359809</ArticleId></ArticleIdList></Reference><Reference><Citation>Biochem Biophys Res Commun. 2006 Jan 13;339(2):459-62</Citation><ArticleIdList><ArticleId IdType="pubmed">16271351</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2020 Aug 18;:</Citation><ArticleIdList><ArticleId IdType="pubmed">32810286</ArticleId></ArticleIdList></Reference><Reference><Citation>Cell Host Microbe. 2011 Mar 17;9(3):187-199</Citation><ArticleIdList><ArticleId IdType="pubmed">21402358</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2016 Sep 6;113(36):10204-9</Citation><ArticleIdList><ArticleId IdType="pubmed">27555587</ArticleId></ArticleIdList></Reference><Reference><Citation>J Exp Bot. 2008;59(6):1383-97</Citation><ArticleIdList><ArticleId IdType="pubmed">18390848</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 2005 Jun;18(6):570-82</Citation><ArticleIdList><ArticleId IdType="pubmed">15986927</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2011 May 3;108(18):7619-24</Citation><ArticleIdList><ArticleId IdType="pubmed">21490299</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2531-6</Citation><ArticleIdList><ArticleId IdType="pubmed">17277084</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Biol. 2018 Feb 5;28(3):421-430.e4</Citation><ArticleIdList><ArticleId IdType="pubmed">29395922</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2010 Feb 1;61(3):507-18</Citation><ArticleIdList><ArticleId 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