A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis.
Identifieur interne : 000302 ( Main/Corpus ); précédent : 000301; suivant : 000303A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis.
Auteurs : Tian Zeng ; Luis Rodriguez-Moreno ; Artem Mansurkhodzaev ; Peng Wang ; Willy Van Den Berg ; Virginie Gasciolli ; Sylvain Cottaz ; Sébastien Fort ; Bart P H J. Thomma ; Jean-Jacques Bono ; Ton Bisseling ; Erik LimpensSource :
- The New phytologist [ 1469-8137 ] ; 2020.
English descriptors
- KwdEn :
- Amino Acid Motifs (MeSH), Amino Acid Sequence (MeSH), Chitin (analogs & derivatives), Chitin (metabolism), Chitinases (metabolism), Fungal Proteins (chemistry), Fungal Proteins (genetics), Fungal Proteins (metabolism), Gene Silencing (MeSH), Genes, Fungal (MeSH), Glomeromycota (genetics), Glomeromycota (physiology), Host-Pathogen Interactions (MeSH), Lysine (metabolism), Mycelium (metabolism), Mycorrhizae (genetics), Mycorrhizae (physiology), Plant Immunity (MeSH), Symbiosis (MeSH).
- MESH :
- chemical , analogs & derivatives : Chitin.
- chemical , chemistry : Fungal Proteins.
- chemical , genetics : Fungal Proteins.
- chemical , metabolism : Chitin, Chitinases, Fungal Proteins, Lysine.
- genetics : Glomeromycota, Mycorrhizae.
- metabolism : Mycelium.
- physiology : Glomeromycota, Mycorrhizae.
- Amino Acid Motifs, Amino Acid Sequence, Gene Silencing, Genes, Fungal, Host-Pathogen Interactions, Plant Immunity, Symbiosis.
Abstract
Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient-depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin-triggered immune responses during symbiosis. In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM. RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin-oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin-triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host-induced gene silencing of RiSLM greatly reduces fungal colonization levels. Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin-triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi.
DOI: 10.1111/nph.16245
PubMed: 31596956
PubMed Central: PMC6916333
Links to Exploration step
pubmed:31596956Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis.</title><author><name sortKey="Zeng, Tian" sort="Zeng, Tian" uniqKey="Zeng T" first="Tian" last="Zeng">Tian Zeng</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Rodriguez Moreno, Luis" sort="Rodriguez Moreno, Luis" uniqKey="Rodriguez Moreno L" first="Luis" last="Rodriguez-Moreno">Luis Rodriguez-Moreno</name><affiliation><nlm:affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Mansurkhodzaev, Artem" sort="Mansurkhodzaev, Artem" uniqKey="Mansurkhodzaev A" first="Artem" last="Mansurkhodzaev">Artem Mansurkhodzaev</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Peng" sort="Wang, Peng" uniqKey="Wang P" first="Peng" last="Wang">Peng Wang</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Van Den Berg, Willy" sort="Van Den Berg, Willy" uniqKey="Van Den Berg W" first="Willy" last="Van Den Berg">Willy Van Den Berg</name><affiliation><nlm:affiliation>Laboratory of Biochemistry, Wageningen University & Research, 6708 WE, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Gasciolli, Virginie" sort="Gasciolli, Virginie" uniqKey="Gasciolli V" first="Virginie" last="Gasciolli">Virginie Gasciolli</name><affiliation><nlm:affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Cottaz, Sylvain" sort="Cottaz, Sylvain" uniqKey="Cottaz S" first="Sylvain" last="Cottaz">Sylvain Cottaz</name><affiliation><nlm:affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</nlm:affiliation></affiliation></author><author><name sortKey="Fort, Sebastien" sort="Fort, Sebastien" uniqKey="Fort S" first="Sébastien" last="Fort">Sébastien Fort</name><affiliation><nlm:affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</nlm:affiliation></affiliation></author><author><name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name><affiliation><nlm:affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bono, Jean Jacques" sort="Bono, Jean Jacques" uniqKey="Bono J" first="Jean-Jacques" last="Bono">Jean-Jacques Bono</name><affiliation><nlm:affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Bisseling, Ton" sort="Bisseling, Ton" uniqKey="Bisseling T" first="Ton" last="Bisseling">Ton Bisseling</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Limpens, Erik" sort="Limpens, Erik" uniqKey="Limpens E" first="Erik" last="Limpens">Erik Limpens</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:31596956</idno><idno type="pmid">31596956</idno><idno type="doi">10.1111/nph.16245</idno><idno type="pmc">PMC6916333</idno><idno type="wicri:Area/Main/Corpus">000302</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000302</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis.</title><author><name sortKey="Zeng, Tian" sort="Zeng, Tian" uniqKey="Zeng T" first="Tian" last="Zeng">Tian Zeng</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Rodriguez Moreno, Luis" sort="Rodriguez Moreno, Luis" uniqKey="Rodriguez Moreno L" first="Luis" last="Rodriguez-Moreno">Luis Rodriguez-Moreno</name><affiliation><nlm:affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Mansurkhodzaev, Artem" sort="Mansurkhodzaev, Artem" uniqKey="Mansurkhodzaev A" first="Artem" last="Mansurkhodzaev">Artem Mansurkhodzaev</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Peng" sort="Wang, Peng" uniqKey="Wang P" first="Peng" last="Wang">Peng Wang</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Van Den Berg, Willy" sort="Van Den Berg, Willy" uniqKey="Van Den Berg W" first="Willy" last="Van Den Berg">Willy Van Den Berg</name><affiliation><nlm:affiliation>Laboratory of Biochemistry, Wageningen University & Research, 6708 WE, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Gasciolli, Virginie" sort="Gasciolli, Virginie" uniqKey="Gasciolli V" first="Virginie" last="Gasciolli">Virginie Gasciolli</name><affiliation><nlm:affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Cottaz, Sylvain" sort="Cottaz, Sylvain" uniqKey="Cottaz S" first="Sylvain" last="Cottaz">Sylvain Cottaz</name><affiliation><nlm:affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</nlm:affiliation></affiliation></author><author><name sortKey="Fort, Sebastien" sort="Fort, Sebastien" uniqKey="Fort S" first="Sébastien" last="Fort">Sébastien Fort</name><affiliation><nlm:affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</nlm:affiliation></affiliation></author><author><name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name><affiliation><nlm:affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Bono, Jean Jacques" sort="Bono, Jean Jacques" uniqKey="Bono J" first="Jean-Jacques" last="Bono">Jean-Jacques Bono</name><affiliation><nlm:affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</nlm:affiliation></affiliation></author><author><name sortKey="Bisseling, Ton" sort="Bisseling, Ton" uniqKey="Bisseling T" first="Ton" last="Bisseling">Ton Bisseling</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Limpens, Erik" sort="Limpens, Erik" uniqKey="Limpens E" first="Erik" last="Limpens">Erik Limpens</name><affiliation><nlm:affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</nlm:affiliation></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><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Motifs (MeSH)</term><term>Amino Acid Sequence (MeSH)</term><term>Chitin (analogs & derivatives)</term><term>Chitin (metabolism)</term><term>Chitinases (metabolism)</term><term>Fungal Proteins (chemistry)</term><term>Fungal Proteins (genetics)</term><term>Fungal Proteins (metabolism)</term><term>Gene Silencing (MeSH)</term><term>Genes, Fungal (MeSH)</term><term>Glomeromycota (genetics)</term><term>Glomeromycota (physiology)</term><term>Host-Pathogen Interactions (MeSH)</term><term>Lysine (metabolism)</term><term>Mycelium (metabolism)</term><term>Mycorrhizae (genetics)</term><term>Mycorrhizae (physiology)</term><term>Plant Immunity (MeSH)</term><term>Symbiosis (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en"><term>Chitin</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Fungal Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Fungal Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Chitin</term><term>Chitinases</term><term>Fungal Proteins</term><term>Lysine</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Glomeromycota</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Mycelium</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Glomeromycota</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Motifs</term><term>Amino Acid Sequence</term><term>Gene Silencing</term><term>Genes, Fungal</term><term>Host-Pathogen Interactions</term><term>Plant Immunity</term><term>Symbiosis</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient-depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin-triggered immune responses during symbiosis. In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM. RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin-oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin-triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host-induced gene silencing of RiSLM greatly reduces fungal colonization levels. Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin-triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31596956</PMID><DateCompleted><Year>2020</Year><Month>11</Month><Day>11</Day></DateCompleted><DateRevised><Year>2020</Year><Month>11</Month><Day>11</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>225</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>01</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis.</ArticleTitle><Pagination><MedlinePgn>448-460</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16245</ELocationID><Abstract><AbstractText>Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient-depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin-triggered immune responses during symbiosis. In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM. RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin-oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin-triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host-induced gene silencing of RiSLM greatly reduces fungal colonization levels. Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin-triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi.</AbstractText><CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zeng</LastName><ForeName>Tian</ForeName><Initials>T</Initials><Identifier Source="ORCID">0000-0002-0315-7658</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rodriguez-Moreno</LastName><ForeName>Luis</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0003-2385-8782</Identifier><AffiliationInfo><Affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mansurkhodzaev</LastName><ForeName>Artem</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Peng</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van den Berg</LastName><ForeName>Willy</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Laboratory of Biochemistry, Wageningen University & Research, 6708 WE, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gasciolli</LastName><ForeName>Virginie</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cottaz</LastName><ForeName>Sylvain</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fort</LastName><ForeName>Sébastien</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-6133-9900</Identifier><AffiliationInfo><Affiliation>CNRS, CERMAV, University Grenoble Alpes, UPR 5301, 38041, Grenoble, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thomma</LastName><ForeName>Bart P H J</ForeName><Initials>BPHJ</Initials><Identifier Source="ORCID">0000-0003-4125-4181</Identifier><AffiliationInfo><Affiliation>Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bono</LastName><ForeName>Jean-Jacques</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bisseling</LastName><ForeName>Ton</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Limpens</LastName><ForeName>Erik</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0002-9668-4085</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Wageningen University & Research, 6708 PB, Wageningen, the Netherlands.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>11</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C493484">oligochitosan</NameOfSubstance></Chemical><Chemical><RegistryNumber>1398-61-4</RegistryNumber><NameOfSubstance UI="D002686">Chitin</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.2.1.14</RegistryNumber><NameOfSubstance UI="D002688">Chitinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>K3Z4F929H6</RegistryNumber><NameOfSubstance UI="D008239">Lysine</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D020816" MajorTopicYN="N">Amino Acid Motifs</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002686" MajorTopicYN="N">Chitin</DescriptorName><QualifierName UI="Q000031" MajorTopicYN="N">analogs & derivatives</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002688" MajorTopicYN="N">Chitinases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020868" MajorTopicYN="N">Gene Silencing</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005800" MajorTopicYN="N">Genes, Fungal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D054884" MajorTopicYN="N">Host-Pathogen Interactions</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008239" MajorTopicYN="N">Lysine</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D025282" MajorTopicYN="N">Mycelium</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D057865" MajorTopicYN="Y">Plant Immunity</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">LysM</Keyword><Keyword MajorTopicYN="Y">arbuscular mycorrhiza</Keyword><Keyword MajorTopicYN="Y">chitin</Keyword><Keyword MajorTopicYN="Y">effector</Keyword><Keyword MajorTopicYN="Y">plant immunity</Keyword><Keyword MajorTopicYN="Y">symbiosis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>02</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>09</Month><Day>24</Day></PubMedPubDate><PubMedPubDate 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