Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis.
Identifieur interne : 000169 ( Main/Exploration ); précédent : 000168; suivant : 000170Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis.
Auteurs : Luuk Rutten [Pays-Bas] ; Kana Miyata [Pays-Bas] ; Yuda Purwana Roswanjaya [Pays-Bas, Indonésie] ; Rik Huisman [Pays-Bas] ; Fengjiao Bu [Pays-Bas] ; Marijke Hartog [Pays-Bas] ; Sidney Linders [Pays-Bas] ; Robin Van Velzen [Pays-Bas] ; Arjan Van Zeijl [Pays-Bas] ; Ton Bisseling [Pays-Bas] ; Wouter Kohlen [Pays-Bas] ; Rene Geurts [Pays-Bas]Source :
- Plant physiology [ 1532-2548 ] ; 2020.
Abstract
Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus Parasponia (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes Lotus japonicus and Medicago truncatula showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 (L. japonicus) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; M. truncatula). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, Parasponia spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic Frankia spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in Parasponia andersonii, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysM-type receptors controlling nodulation in P. andersonii: PanLYK1, PanLYK3, PanNFP1, and PanNFP2 These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and Parasponia spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.
DOI: 10.1104/pp.19.01420
PubMed: 32669419
PubMed Central: PMC7536700
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wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000091</idno><idno type="wicri:Area/Main/Curation">000091</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000091</idno><idno type="wicri:Area/Main/Exploration">000091</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis.</title><author><name sortKey="Rutten, Luuk" sort="Rutten, Luuk" uniqKey="Rutten L" first="Luuk" last="Rutten">Luuk Rutten</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Miyata, Kana" sort="Miyata, Kana" uniqKey="Miyata K" first="Kana" last="Miyata">Kana Miyata</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Roswanjaya, Yuda Purwana" sort="Roswanjaya, Yuda Purwana" uniqKey="Roswanjaya Y" first="Yuda Purwana" last="Roswanjaya">Yuda Purwana Roswanjaya</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Centre of Technology for Agricultural Production, Agency for the Assessment and Application of Technology, 10340 Jakarta, Indonesia.</nlm:affiliation><country xml:lang="fr">Indonésie</country><wicri:regionArea>Centre of Technology for Agricultural Production, Agency for the Assessment and Application of Technology, 10340 Jakarta</wicri:regionArea><wicri:noRegion>10340 Jakarta</wicri:noRegion></affiliation></author><author><name sortKey="Huisman, Rik" sort="Huisman, Rik" uniqKey="Huisman R" first="Rik" last="Huisman">Rik Huisman</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Bu, Fengjiao" sort="Bu, Fengjiao" uniqKey="Bu F" first="Fengjiao" last="Bu">Fengjiao Bu</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Hartog, Marijke" sort="Hartog, Marijke" uniqKey="Hartog M" first="Marijke" last="Hartog">Marijke Hartog</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Linders, Sidney" sort="Linders, Sidney" uniqKey="Linders S" first="Sidney" last="Linders">Sidney Linders</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Van Velzen, Robin" sort="Van Velzen, Robin" uniqKey="Van Velzen R" first="Robin" last="Van Velzen">Robin Van Velzen</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Biosystematics Group, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Biosystematics Group, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Van Zeijl, Arjan" sort="Van Zeijl, Arjan" uniqKey="Van Zeijl A" first="Arjan" last="Van Zeijl">Arjan Van Zeijl</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Bisseling, Ton" sort="Bisseling, Ton" uniqKey="Bisseling T" first="Ton" last="Bisseling">Ton Bisseling</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Kohlen, Wouter" sort="Kohlen, Wouter" uniqKey="Kohlen W" first="Wouter" last="Kohlen">Wouter Kohlen</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author><author><name sortKey="Geurts, Rene" sort="Geurts, Rene" uniqKey="Geurts R" first="Rene" last="Geurts">Rene Geurts</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands rene.geurts@wur.nl.</nlm:affiliation><country wicri:rule="url">Pays-Bas</country><wicri:regionArea>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen</wicri:regionArea><orgName type="university">Université de Wageningue</orgName><placeName><settlement type="city">Wageningue</settlement><region nuts="2">Gueldre (province)</region></placeName></affiliation></author></analytic><series><title level="j">Plant physiology</title><idno type="eISSN">1532-2548</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus <i>Parasponia</i> (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes <i>Lotus japonicus</i> and <i>Medicago truncatula</i> showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 (<i>L. japonicus</i>) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; <i>M. truncatula</i>). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, <i>Parasponia</i> spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic <i>Frankia</i> spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in <i>Parasponia andersonii</i>, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysM-type receptors controlling nodulation in <i>P. andersonii</i>: <i>PanLYK1</i>, <i>PanLYK3</i>, <i>PanNFP1</i>, and <i>PanNFP2</i> These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and <i>Parasponia</i> spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32669419</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>16</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-2548</ISSN><JournalIssue CitedMedium="Internet"><Volume>184</Volume><Issue>2</Issue><PubDate><Year>2020</Year><Month>10</Month></PubDate></JournalIssue><Title>Plant physiology</Title><ISOAbbreviation>Plant Physiol</ISOAbbreviation></Journal><ArticleTitle>Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis.</ArticleTitle><Pagination><MedlinePgn>1004-1023</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.19.01420</ELocationID><Abstract><AbstractText>Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus <i>Parasponia</i> (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes <i>Lotus japonicus</i> and <i>Medicago truncatula</i> showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 (<i>L. japonicus</i>) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; <i>M. truncatula</i>). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, <i>Parasponia</i> spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic <i>Frankia</i> spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in <i>Parasponia andersonii</i>, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysM-type receptors controlling nodulation in <i>P. andersonii</i>: <i>PanLYK1</i>, <i>PanLYK3</i>, <i>PanNFP1</i>, and <i>PanNFP2</i> These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and <i>Parasponia</i> spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.</AbstractText><CopyrightInformation>© 2020 The Authors. All Rights Reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Rutten</LastName><ForeName>Luuk</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0002-6239-2404</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Miyata</LastName><ForeName>Kana</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Roswanjaya</LastName><ForeName>Yuda Purwana</ForeName><Initials>YP</Initials><Identifier Source="ORCID">0000-0002-8195-8100</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre of Technology for Agricultural Production, Agency for the Assessment and Application of Technology, 10340 Jakarta, Indonesia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huisman</LastName><ForeName>Rik</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0001-7494-7721</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bu</LastName><ForeName>Fengjiao</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0001-7467-994X</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hartog</LastName><ForeName>Marijke</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Linders</LastName><ForeName>Sidney</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Velzen</LastName><ForeName>Robin</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-6444-7608</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Biosystematics Group, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>van Zeijl</LastName><ForeName>Arjan</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0003-3067-9782</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bisseling</LastName><ForeName>Ton</ForeName><Initials>T</Initials><Identifier Source="ORCID">0000-0001-5494-8786</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kohlen</LastName><ForeName>Wouter</ForeName><Initials>W</Initials><Identifier Source="ORCID">0000-0001-9057-2392</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Geurts</LastName><ForeName>Rene</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-6443-2289</Identifier><AffiliationInfo><Affiliation>Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands rene.geurts@wur.nl.</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>2020</Year><Month>07</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant 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last="Geurts">Rene Geurts</name><name sortKey="Hartog, Marijke" sort="Hartog, Marijke" uniqKey="Hartog M" first="Marijke" last="Hartog">Marijke Hartog</name><name sortKey="Huisman, Rik" sort="Huisman, Rik" uniqKey="Huisman R" first="Rik" last="Huisman">Rik Huisman</name><name sortKey="Kohlen, Wouter" sort="Kohlen, Wouter" uniqKey="Kohlen W" first="Wouter" last="Kohlen">Wouter Kohlen</name><name sortKey="Linders, Sidney" sort="Linders, Sidney" uniqKey="Linders S" first="Sidney" last="Linders">Sidney Linders</name><name sortKey="Miyata, Kana" sort="Miyata, Kana" uniqKey="Miyata K" first="Kana" last="Miyata">Kana Miyata</name><name sortKey="Roswanjaya, Yuda Purwana" sort="Roswanjaya, Yuda Purwana" uniqKey="Roswanjaya Y" first="Yuda Purwana" last="Roswanjaya">Yuda Purwana Roswanjaya</name><name sortKey="Van Velzen, Robin" sort="Van Velzen, Robin" uniqKey="Van Velzen R" first="Robin" last="Van Velzen">Robin Van Velzen</name><name sortKey="Van Velzen, Robin" sort="Van Velzen, Robin" uniqKey="Van Velzen R" first="Robin" last="Van Velzen">Robin Van Velzen</name><name sortKey="Van Zeijl, Arjan" sort="Van Zeijl, Arjan" uniqKey="Van Zeijl A" first="Arjan" last="Van Zeijl">Arjan Van Zeijl</name></country><country name="Indonésie"><noRegion><name sortKey="Roswanjaya, Yuda Purwana" sort="Roswanjaya, Yuda Purwana" uniqKey="Roswanjaya Y" first="Yuda Purwana" last="Roswanjaya">Yuda Purwana Roswanjaya</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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