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A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane.

Identifieur interne : 000B05 ( Main/Exploration ); précédent : 000B04; suivant : 000B06

A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane.

Auteurs : Ronelle Roth [Royaume-Uni] ; Marco Chiapello [Suisse, Royaume-Uni] ; Héctor Montero [Royaume-Uni] ; Peter Gehrig [Suisse] ; Jonas Grossmann [Suisse] ; Kevin O'Holleran [Royaume-Uni] ; Denise Hartken [Royaume-Uni] ; Fergus Walters [Royaume-Uni] ; Shu-Yi Yang [Royaume-Uni] ; Stefan Hillmer [Allemagne] ; Karin Schumacher [Allemagne] ; Sarah Bowden [Royaume-Uni] ; Melanie Craze [Royaume-Uni] ; Emma J. Wallington [Royaume-Uni] ; Akio Miyao [Japon] ; Ruairidh Sawers [Mexique] ; Enrico Martinoia [Suisse] ; Uta Paszkowski [Royaume-Uni, Suisse]

Source :

RBID : pubmed:30410018

Descripteurs français

English descriptors

Abstract

In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrient-delivering arbuscular mycorrhizal (AM) fungi. Establishment of AM symbioses includes transient, intracellular formation of fungal feeding structures, the arbuscules. A plant-derived peri-arbuscular membrane (PAM) surrounds the arbuscules, mediating reciprocal nutrient exchange. Signaling at the PAM must be well coordinated to achieve this dynamic cellular intimacy. Here, we identify the PAM-specific Arbuscular Receptor-like Kinase 1 (ARK1) from maize and rice to condition sustained AM symbiosis. Mutation of rice ARK1 causes a significant reduction in vesicles, the fungal storage structures, and a concomitant reduction in overall root colonization by the AM fungus Rhizophagus irregularis. Arbuscules, although less frequent in the ark1 mutant, are morphologically normal. Co-cultivation with wild-type plants restores vesicle and spore formation, suggesting ARK1 function is required for the completion of the fungal life-cycle, thereby defining a functional stage, post arbuscule development.

DOI: 10.1038/s41467-018-06865-z
PubMed: 30410018
PubMed Central: PMC6224560


Affiliations:


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Le document en format XML

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<name sortKey="Craze, Melanie" sort="Craze, Melanie" uniqKey="Craze M" first="Melanie" last="Craze">Melanie Craze</name>
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<name sortKey="Wallington, Emma J" sort="Wallington, Emma J" uniqKey="Wallington E" first="Emma J" last="Wallington">Emma J. Wallington</name>
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<name sortKey="Grossmann, Jonas" sort="Grossmann, Jonas" uniqKey="Grossmann J" first="Jonas" last="Grossmann">Jonas Grossmann</name>
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<name sortKey="Hartken, Denise" sort="Hartken, Denise" uniqKey="Hartken D" first="Denise" last="Hartken">Denise Hartken</name>
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<name sortKey="Walters, Fergus" sort="Walters, Fergus" uniqKey="Walters F" first="Fergus" last="Walters">Fergus Walters</name>
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<nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</nlm:affiliation>
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<name sortKey="Yang, Shu Yi" sort="Yang, Shu Yi" uniqKey="Yang S" first="Shu-Yi" last="Yang">Shu-Yi Yang</name>
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<nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</nlm:affiliation>
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<settlement type="city">Cambridge</settlement>
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<name sortKey="Hillmer, Stefan" sort="Hillmer, Stefan" uniqKey="Hillmer S" first="Stefan" last="Hillmer">Stefan Hillmer</name>
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<nlm:affiliation>Electron Microscopy Core Facility, University of Heidelberg, Im Neuenheimer Feld 345, 69120, Heidelberg, Germany.</nlm:affiliation>
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<region type="land" nuts="1">Bade-Wurtemberg</region>
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</author>
<author>
<name sortKey="Schumacher, Karin" sort="Schumacher, Karin" uniqKey="Schumacher K" first="Karin" last="Schumacher">Karin Schumacher</name>
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<nlm:affiliation>Centre for Organismal Studies, University of Heidelberg, Im Neuenheimer Feld 230, 69120, Heidelberg, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
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<placeName>
<region type="land" nuts="1">Bade-Wurtemberg</region>
<region type="district" nuts="2">District de Karlsruhe</region>
<settlement type="city">Heidelberg</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Bowden, Sarah" sort="Bowden, Sarah" uniqKey="Bowden S" first="Sarah" last="Bowden">Sarah Bowden</name>
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<nlm:affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
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</affiliation>
</author>
<author>
<name sortKey="Craze, Melanie" sort="Craze, Melanie" uniqKey="Craze M" first="Melanie" last="Craze">Melanie Craze</name>
<affiliation wicri:level="1">
<nlm:affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</nlm:affiliation>
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<author>
<name sortKey="Wallington, Emma J" sort="Wallington, Emma J" uniqKey="Wallington E" first="Emma J" last="Wallington">Emma J. Wallington</name>
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<nlm:affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</nlm:affiliation>
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<author>
<name sortKey="Miyao, Akio" sort="Miyao, Akio" uniqKey="Miyao A" first="Akio" last="Miyao">Akio Miyao</name>
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<nlm:affiliation>National Agriculture and Food Research Organization, Advanced Genomics Breeding Section, Institute of Crop Science, 2-1-2, Kannondai, Tsukuba, Ibaraki, 305-8518, Japan.</nlm:affiliation>
<country xml:lang="fr">Japon</country>
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<author>
<name sortKey="Sawers, Ruairidh" sort="Sawers, Ruairidh" uniqKey="Sawers R" first="Ruairidh" last="Sawers">Ruairidh Sawers</name>
<affiliation wicri:level="1">
<nlm:affiliation>Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados, 36821, Irapuato, GTO, Mexico.</nlm:affiliation>
<country xml:lang="fr">Mexique</country>
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<author>
<name sortKey="Martinoia, Enrico" sort="Martinoia, Enrico" uniqKey="Martinoia E" first="Enrico" last="Martinoia">Enrico Martinoia</name>
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<author>
<name sortKey="Paszkowski, Uta" sort="Paszkowski, Uta" uniqKey="Paszkowski U" first="Uta" last="Paszkowski">Uta Paszkowski</name>
<affiliation wicri:level="4">
<nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK. up220@cam.ac.uk.</nlm:affiliation>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
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<settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:affiliation>Department of Plant Molecular Biology, University of Lausanne, Biophore, 1015, Lausanne, Switzerland. up220@cam.ac.uk.</nlm:affiliation>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Plant Molecular Biology, University of Lausanne, Biophore, 1015, Lausanne</wicri:regionArea>
<placeName>
<settlement type="city">Lausanne</settlement>
<region nuts="3" type="region">Canton de Vaud</region>
</placeName>
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<series>
<title level="j">Nature communications</title>
<idno type="eISSN">2041-1723</idno>
<imprint>
<date when="2018" type="published">2018</date>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Laser Capture Microdissection (MeSH)</term>
<term>Membrane Proteins (metabolism)</term>
<term>Membranes (MeSH)</term>
<term>Mutation (genetics)</term>
<term>Mycorrhizae (metabolism)</term>
<term>Mycorrhizae (ultrastructure)</term>
<term>Oryza (enzymology)</term>
<term>Oryza (microbiology)</term>
<term>Oryza (ultrastructure)</term>
<term>Plant Proteins (metabolism)</term>
<term>Promoter Regions, Genetic (genetics)</term>
<term>Protein-Serine-Threonine Kinases (metabolism)</term>
<term>Proteome (metabolism)</term>
<term>Receptors, Cell Surface (metabolism)</term>
<term>Symbiosis (MeSH)</term>
<term>Transcriptome (genetics)</term>
<term>Zea mays (metabolism)</term>
<term>Zea mays (microbiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Membranes (MeSH)</term>
<term>Microdissection au laser (MeSH)</term>
<term>Mutation (génétique)</term>
<term>Mycorhizes (métabolisme)</term>
<term>Mycorhizes (ultrastructure)</term>
<term>Oryza (enzymologie)</term>
<term>Oryza (microbiologie)</term>
<term>Oryza (ultrastructure)</term>
<term>Protein-Serine-Threonine Kinases (métabolisme)</term>
<term>Protéines membranaires (métabolisme)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Protéome (métabolisme)</term>
<term>Récepteurs de surface cellulaire (métabolisme)</term>
<term>Régions promotrices (génétique) (génétique)</term>
<term>Symbiose (MeSH)</term>
<term>Transcriptome (génétique)</term>
<term>Zea mays (microbiologie)</term>
<term>Zea mays (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Membrane Proteins</term>
<term>Plant Proteins</term>
<term>Protein-Serine-Threonine Kinases</term>
<term>Proteome</term>
<term>Receptors, Cell Surface</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Oryza</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Oryza</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Mutation</term>
<term>Promoter Regions, Genetic</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Mutation</term>
<term>Régions promotrices (génétique)</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Mycorrhizae</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Oryza</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Oryza</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Mycorhizes</term>
<term>Protein-Serine-Threonine Kinases</term>
<term>Protéines membranaires</term>
<term>Protéines végétales</term>
<term>Protéome</term>
<term>Récepteurs de surface cellulaire</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="ultrastructure" xml:lang="en">
<term>Mycorrhizae</term>
<term>Oryza</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Laser Capture Microdissection</term>
<term>Membranes</term>
<term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" qualifier="ultrastructure" xml:lang="fr">
<term>Membranes</term>
<term>Microdissection au laser</term>
<term>Mycorhizes</term>
<term>Oryza</term>
<term>Symbiose</term>
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<div type="abstract" xml:lang="en">In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrient-delivering arbuscular mycorrhizal (AM) fungi. Establishment of AM symbioses includes transient, intracellular formation of fungal feeding structures, the arbuscules. A plant-derived peri-arbuscular membrane (PAM) surrounds the arbuscules, mediating reciprocal nutrient exchange. Signaling at the PAM must be well coordinated to achieve this dynamic cellular intimacy. Here, we identify the PAM-specific Arbuscular Receptor-like Kinase 1 (ARK1) from maize and rice to condition sustained AM symbiosis. Mutation of rice ARK1 causes a significant reduction in vesicles, the fungal storage structures, and a concomitant reduction in overall root colonization by the AM fungus Rhizophagus irregularis. Arbuscules, although less frequent in the ark1 mutant, are morphologically normal. Co-cultivation with wild-type plants restores vesicle and spore formation, suggesting ARK1 function is required for the completion of the fungal life-cycle, thereby defining a functional stage, post arbuscule development.</div>
</front>
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<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">30410018</PMID>
<DateCompleted>
<Year>2019</Year>
<Month>05</Month>
<Day>03</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>03</Month>
<Day>09</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">2041-1723</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>9</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2018</Year>
<Month>11</Month>
<Day>08</Day>
</PubDate>
</JournalIssue>
<Title>Nature communications</Title>
<ISOAbbreviation>Nat Commun</ISOAbbreviation>
</Journal>
<ArticleTitle>A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane.</ArticleTitle>
<Pagination>
<MedlinePgn>4677</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1038/s41467-018-06865-z</ELocationID>
<Abstract>
<AbstractText>In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrient-delivering arbuscular mycorrhizal (AM) fungi. Establishment of AM symbioses includes transient, intracellular formation of fungal feeding structures, the arbuscules. A plant-derived peri-arbuscular membrane (PAM) surrounds the arbuscules, mediating reciprocal nutrient exchange. Signaling at the PAM must be well coordinated to achieve this dynamic cellular intimacy. Here, we identify the PAM-specific Arbuscular Receptor-like Kinase 1 (ARK1) from maize and rice to condition sustained AM symbiosis. Mutation of rice ARK1 causes a significant reduction in vesicles, the fungal storage structures, and a concomitant reduction in overall root colonization by the AM fungus Rhizophagus irregularis. Arbuscules, although less frequent in the ark1 mutant, are morphologically normal. Co-cultivation with wild-type plants restores vesicle and spore formation, suggesting ARK1 function is required for the completion of the fungal life-cycle, thereby defining a functional stage, post arbuscule development.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Roth</LastName>
<ForeName>Ronelle</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5566-8954</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK. rr472@cam.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chiapello</LastName>
<ForeName>Marco</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-7768-3047</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Molecular Biology, University of Lausanne, Biophore, 1015, Lausanne, Switzerland.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biochemistry, University of Cambridge, Cambridge, CB2 1QW, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Montero</LastName>
<ForeName>Héctor</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-8590-6394</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Gehrig</LastName>
<ForeName>Peter</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Functional Genomics Center, University and ETH Zürich, Winterthurerstr. 190, 8057, Zürich, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Grossmann</LastName>
<ForeName>Jonas</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Functional Genomics Center, University and ETH Zürich, Winterthurerstr. 190, 8057, Zürich, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>O'Holleran</LastName>
<ForeName>Kevin</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Cambridge Advanced Imaging Centre, University of Cambridge, Cambridge, CB2 3DY, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hartken</LastName>
<ForeName>Denise</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Walters</LastName>
<ForeName>Fergus</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yang</LastName>
<ForeName>Shu-Yi</ForeName>
<Initials>SY</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hillmer</LastName>
<ForeName>Stefan</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Electron Microscopy Core Facility, University of Heidelberg, Im Neuenheimer Feld 345, 69120, Heidelberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schumacher</LastName>
<ForeName>Karin</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Centre for Organismal Studies, University of Heidelberg, Im Neuenheimer Feld 230, 69120, Heidelberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bowden</LastName>
<ForeName>Sarah</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5105-076X</Identifier>
<AffiliationInfo>
<Affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Craze</LastName>
<ForeName>Melanie</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wallington</LastName>
<ForeName>Emma J</ForeName>
<Initials>EJ</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-3715-7901</Identifier>
<AffiliationInfo>
<Affiliation>The John Bingham Laboratory, National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0LE, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Miyao</LastName>
<ForeName>Akio</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2822-2866</Identifier>
<AffiliationInfo>
<Affiliation>National Agriculture and Food Research Organization, Advanced Genomics Breeding Section, Institute of Crop Science, 2-1-2, Kannondai, Tsukuba, Ibaraki, 305-8518, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sawers</LastName>
<ForeName>Ruairidh</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados, 36821, Irapuato, GTO, Mexico.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Martinoia</LastName>
<ForeName>Enrico</ForeName>
<Initials>E</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, 8008, Zürich, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Paszkowski</LastName>
<ForeName>Uta</ForeName>
<Initials>U</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-7279-7632</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK. up220@cam.ac.uk.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Plant Molecular Biology, University of Lausanne, Biophore, 1015, Lausanne, Switzerland. up220@cam.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BB/N008723/1</GrantID>
<Acronym>BB_</Acronym>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
</GrantList>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<Month>11</Month>
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</ArticleDate>
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<Country>England</Country>
<MedlineTA>Nat Commun</MedlineTA>
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<MeshHeading>
<DescriptorName UI="D061346" MajorTopicYN="N">Laser Capture Microdissection</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008565" MajorTopicYN="N">Membrane Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008566" MajorTopicYN="N">Membranes</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012275" MajorTopicYN="N">Oryza</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011401" MajorTopicYN="N">Promoter Regions, Genetic</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017346" MajorTopicYN="N">Protein-Serine-Threonine Kinases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020543" MajorTopicYN="N">Proteome</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011956" MajorTopicYN="N">Receptors, Cell Surface</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003313" MajorTopicYN="N">Zea mays</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
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