Imbalanced Regulation of Fungal Nutrient Transports According to Phosphate Availability in a Symbiocosm Formed by Poplar, Sorghum, and Rhizophagus irregularis.
Identifieur interne : 000896 ( Main/Exploration ); précédent : 000895; suivant : 000897Imbalanced Regulation of Fungal Nutrient Transports According to Phosphate Availability in a Symbiocosm Formed by Poplar, Sorghum, and Rhizophagus irregularis.
Auteurs : Silvia Calabrese [Suisse] ; Loic Cusant [France] ; Alexis Sarazin [Suisse] ; Annette Niehl [Suisse] ; Alexander Erban [Allemagne] ; Daphnée Brulé [Suisse, France] ; Ghislaine Recorbet [France] ; Daniel Wipf [France] ; Christophe Roux [France] ; Joachim Kopka [Allemagne] ; Thomas Boller [Suisse] ; Pierre-Emmanuel Courty [Suisse, France]Source :
- Frontiers in plant science [ 1664-462X ] ; 2019.
Abstract
In arbuscular mycorrhizal (AM) symbiosis, key components of nutrient uptake and exchange are specialized transporters that facilitate nutrient transport across membranes. As phosphate is a nutrient and a regulator of nutrient exchanges, we investigated the effect of P availability to extraradical mycelium (ERM) on both plant and fungus transcriptomes and metabolomes in a symbiocosm system. By perturbing nutrient exchanges under the control of P, our objectives were to identify new fungal genes involved in nutrient transports, and to characterize in which extent the fungus differentially modulates its metabolism when interacting with two different plant species. We performed transportome analysis on the ERM and intraradical mycelium of the AM fungus Rhizophagus irregularis associated to Populus trichocarpa and Sorghum bicolor under high and low P availability in ERM, using quantitative RT-PCR and Illumina mRNA-sequencing. We observed that mycorrhizal symbiosis induces expression of specific phosphate and ammonium transporters in both plants. Furthermore, we identified new AM-inducible transporters and showed that a subset of phosphate transporters is regulated independently of symbiotic nutrient exchange. mRNA-Sequencing revealed that the fungal transportome was not similarly regulated in the two host plant species according to P availability. Mirroring this effect, many plant carbohydrate transporters were down-regulated in P. trichocarpa mycorrhizal root tissue. Metabolome analysis revealed further that AM root colonization led to a modification of root primary metabolism under low and high P availability and to a decrease of primary metabolite pools in general. Moreover, the down regulation of the sucrose transporters suggests that the plant limits carbohydrate long distance transport (i.e. from shoot to the mycorrhizal roots). By simultaneous uptake/reuptake of nutrients from the apoplast at the biotrophic interface, plant and fungus are both able to control reciprocal nutrient fluxes.
DOI: 10.3389/fpls.2019.01617
PubMed: 31921260
PubMed Central: PMC6920215
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Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon</wicri:regionArea><placeName><region type="region">Bourgogne-Franche-Comté</region><region type="old region">Bourgogne</region><settlement type="city">Dijon</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31921260</idno><idno type="pmid">31921260</idno><idno type="doi">10.3389/fpls.2019.01617</idno><idno type="pmc">PMC6920215</idno><idno type="wicri:Area/Main/Corpus">000518</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000518</idno><idno type="wicri:Area/Main/Curation">000518</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000518</idno><idno type="wicri:Area/Main/Exploration">000518</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Imbalanced Regulation of Fungal Nutrient Transports According to Phosphate Availability in a Symbiocosm Formed by Poplar, Sorghum, and <i>Rhizophagus irregularis</i>.</title><author><name sortKey="Calabrese, Silvia" sort="Calabrese, Silvia" uniqKey="Calabrese S" first="Silvia" last="Calabrese">Silvia Calabrese</name><affiliation wicri:level="1"><nlm:affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel</wicri:regionArea><wicri:noRegion>Basel</wicri:noRegion></affiliation></author><author><name sortKey="Cusant, Loic" sort="Cusant, Loic" uniqKey="Cusant L" first="Loic" last="Cusant">Loic Cusant</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan</wicri:regionArea><wicri:noRegion>Castanet-Tolosan</wicri:noRegion><wicri:noRegion>Castanet-Tolosan</wicri:noRegion></affiliation></author><author><name sortKey="Sarazin, Alexis" sort="Sarazin, Alexis" uniqKey="Sarazin A" first="Alexis" last="Sarazin">Alexis Sarazin</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology at the Swiss Federal Institute of Technology Zurich, Zurich, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Biology at the Swiss Federal Institute of Technology Zurich, Zurich</wicri:regionArea><wicri:noRegion>Zurich</wicri:noRegion></affiliation></author><author><name sortKey="Niehl, Annette" sort="Niehl, Annette" uniqKey="Niehl A" first="Annette" last="Niehl">Annette Niehl</name><affiliation wicri:level="1"><nlm:affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel</wicri:regionArea><wicri:noRegion>Basel</wicri:noRegion></affiliation></author><author><name sortKey="Erban, Alexander" sort="Erban, Alexander" uniqKey="Erban A" first="Alexander" last="Erban">Alexander Erban</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm</wicri:regionArea><wicri:noRegion>Potsdam-Golm</wicri:noRegion><wicri:noRegion>Potsdam-Golm</wicri:noRegion><wicri:noRegion>Potsdam-Golm</wicri:noRegion></affiliation></author><author><name sortKey="Brule, Daphnee" sort="Brule, Daphnee" uniqKey="Brule D" first="Daphnée" last="Brulé">Daphnée Brulé</name><affiliation wicri:level="1"><nlm:affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel</wicri:regionArea><wicri:noRegion>Basel</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon</wicri:regionArea><placeName><region type="region">Bourgogne-Franche-Comté</region><region type="old region">Bourgogne</region><settlement type="city">Dijon</settlement></placeName></affiliation></author><author><name sortKey="Recorbet, Ghislaine" sort="Recorbet, Ghislaine" uniqKey="Recorbet G" first="Ghislaine" last="Recorbet">Ghislaine Recorbet</name><affiliation wicri:level="3"><nlm:affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon</wicri:regionArea><placeName><region type="region">Bourgogne-Franche-Comté</region><region type="old region">Bourgogne</region><settlement type="city">Dijon</settlement></placeName></affiliation></author><author><name sortKey="Wipf, Daniel" sort="Wipf, Daniel" uniqKey="Wipf D" first="Daniel" last="Wipf">Daniel Wipf</name><affiliation wicri:level="3"><nlm:affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon</wicri:regionArea><placeName><region type="region">Bourgogne-Franche-Comté</region><region type="old region">Bourgogne</region><settlement type="city">Dijon</settlement></placeName></affiliation></author><author><name sortKey="Roux, Christophe" sort="Roux, Christophe" uniqKey="Roux C" first="Christophe" last="Roux">Christophe Roux</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan</wicri:regionArea><wicri:noRegion>Castanet-Tolosan</wicri:noRegion><wicri:noRegion>Castanet-Tolosan</wicri:noRegion></affiliation></author><author><name sortKey="Kopka, Joachim" sort="Kopka, Joachim" uniqKey="Kopka J" first="Joachim" last="Kopka">Joachim Kopka</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm</wicri:regionArea><wicri:noRegion>Potsdam-Golm</wicri:noRegion><wicri:noRegion>Potsdam-Golm</wicri:noRegion><wicri:noRegion>Potsdam-Golm</wicri:noRegion></affiliation></author><author><name sortKey="Boller, Thomas" sort="Boller, Thomas" uniqKey="Boller T" first="Thomas" last="Boller">Thomas Boller</name><affiliation wicri:level="1"><nlm:affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel</wicri:regionArea><wicri:noRegion>Basel</wicri:noRegion></affiliation></author><author><name sortKey="Courty, Pierre Emmanuel" sort="Courty, Pierre Emmanuel" uniqKey="Courty P" first="Pierre-Emmanuel" last="Courty">Pierre-Emmanuel Courty</name><affiliation wicri:level="1"><nlm:affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel</wicri:regionArea><wicri:noRegion>Basel</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon</wicri:regionArea><placeName><region type="region">Bourgogne-Franche-Comté</region><region type="old region">Bourgogne</region><settlement type="city">Dijon</settlement></placeName></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In arbuscular mycorrhizal (AM) symbiosis, key components of nutrient uptake and exchange are specialized transporters that facilitate nutrient transport across membranes. As phosphate is a nutrient and a regulator of nutrient exchanges, we investigated the effect of P availability to extraradical mycelium (ERM) on both plant and fungus transcriptomes and metabolomes in a symbiocosm system. By perturbing nutrient exchanges under the control of P, our objectives were to identify new fungal genes involved in nutrient transports, and to characterize in which extent the fungus differentially modulates its metabolism when interacting with two different plant species. We performed transportome analysis on the ERM and intraradical mycelium of the AM fungus <i>Rhizophagus irregularis</i> associated to <i>Populus trichocarpa</i> and <i>Sorghum bicolor</i> under high and low P availability in ERM, using quantitative RT-PCR and Illumina mRNA-sequencing. We observed that mycorrhizal symbiosis induces expression of specific phosphate and ammonium transporters in both plants. Furthermore, we identified new AM-inducible transporters and showed that a subset of phosphate transporters is regulated independently of symbiotic nutrient exchange. mRNA-Sequencing revealed that the fungal transportome was not similarly regulated in the two host plant species according to P availability. Mirroring this effect, many plant carbohydrate transporters were down-regulated in <i>P. trichocarpa</i> mycorrhizal root tissue. Metabolome analysis revealed further that AM root colonization led to a modification of root primary metabolism under low and high P availability and to a decrease of primary metabolite pools in general. Moreover, the down regulation of the sucrose transporters suggests that the plant limits carbohydrate long distance transport (i.e. from shoot to the mycorrhizal roots). By simultaneous uptake/reuptake of nutrients from the apoplast at the biotrophic interface, plant and fungus are both able to control reciprocal nutrient fluxes.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">31921260</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>10</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Imbalanced Regulation of Fungal Nutrient Transports According to Phosphate Availability in a Symbiocosm Formed by Poplar, Sorghum, and <i>Rhizophagus irregularis</i>.</ArticleTitle><Pagination><MedlinePgn>1617</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2019.01617</ELocationID><Abstract><AbstractText>In arbuscular mycorrhizal (AM) symbiosis, key components of nutrient uptake and exchange are specialized transporters that facilitate nutrient transport across membranes. As phosphate is a nutrient and a regulator of nutrient exchanges, we investigated the effect of P availability to extraradical mycelium (ERM) on both plant and fungus transcriptomes and metabolomes in a symbiocosm system. By perturbing nutrient exchanges under the control of P, our objectives were to identify new fungal genes involved in nutrient transports, and to characterize in which extent the fungus differentially modulates its metabolism when interacting with two different plant species. We performed transportome analysis on the ERM and intraradical mycelium of the AM fungus <i>Rhizophagus irregularis</i> associated to <i>Populus trichocarpa</i> and <i>Sorghum bicolor</i> under high and low P availability in ERM, using quantitative RT-PCR and Illumina mRNA-sequencing. We observed that mycorrhizal symbiosis induces expression of specific phosphate and ammonium transporters in both plants. Furthermore, we identified new AM-inducible transporters and showed that a subset of phosphate transporters is regulated independently of symbiotic nutrient exchange. mRNA-Sequencing revealed that the fungal transportome was not similarly regulated in the two host plant species according to P availability. Mirroring this effect, many plant carbohydrate transporters were down-regulated in <i>P. trichocarpa</i> mycorrhizal root tissue. Metabolome analysis revealed further that AM root colonization led to a modification of root primary metabolism under low and high P availability and to a decrease of primary metabolite pools in general. Moreover, the down regulation of the sucrose transporters suggests that the plant limits carbohydrate long distance transport (i.e. from shoot to the mycorrhizal roots). By simultaneous uptake/reuptake of nutrients from the apoplast at the biotrophic interface, plant and fungus are both able to control reciprocal nutrient fluxes.</AbstractText><CopyrightInformation>Copyright © 2019 Calabrese, Cusant, Sarazin, Niehl, Erban, Brulé, Recorbet, Wipf, Roux, Kopka, Boller and Courty.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Calabrese</LastName><ForeName>Silvia</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cusant</LastName><ForeName>Loic</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sarazin</LastName><ForeName>Alexis</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Biology at the Swiss Federal Institute of Technology Zurich, Zurich, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Niehl</LastName><ForeName>Annette</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Erban</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brulé</LastName><ForeName>Daphnée</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Recorbet</LastName><ForeName>Ghislaine</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wipf</LastName><ForeName>Daniel</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Roux</LastName><ForeName>Christophe</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, CNRS, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kopka</LastName><ForeName>Joachim</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Boller</LastName><ForeName>Thomas</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Courty</LastName><ForeName>Pierre-Emmanuel</ForeName><Initials>PE</Initials><AffiliationInfo><Affiliation>Department of Environmental Sciences, Botany, Zurich-Basel Plant Science Center, University of Basel, Basel, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Agroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Dijon, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>12</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">ammonium</Keyword><Keyword MajorTopicYN="N">arbuscular mycorrhizal fungi</Keyword><Keyword MajorTopicYN="N">carbohydrates transporters</Keyword><Keyword MajorTopicYN="N">extraradical mycelium</Keyword><Keyword MajorTopicYN="N">intraradical mycelium</Keyword><Keyword MajorTopicYN="N">lipid metabolism</Keyword><Keyword MajorTopicYN="N">phosphorus</Keyword><Keyword MajorTopicYN="N">symbiocosm</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>07</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>11</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31921260</ArticleId><ArticleId IdType="doi">10.3389/fpls.2019.01617</ArticleId><ArticleId IdType="pmc">PMC6920215</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Planta. 2005 Nov;222(4):688-98</Citation><ArticleIdList><ArticleId IdType="pubmed">16133217</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 2001 Oct;14(10):1140-8</Citation><ArticleIdList><ArticleId IdType="pubmed">11605953</ArticleId></ArticleIdList></Reference><Reference><Citation>Trends Plant Sci. 2016 Nov;21(11):937-950</Citation><ArticleIdList><ArticleId IdType="pubmed">27514454</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2005 Apr;42(2):236-50</Citation><ArticleIdList><ArticleId IdType="pubmed">15807785</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2013 May;198(3):853-65</Citation><ArticleIdList><ArticleId IdType="pubmed">23461653</ArticleId></ArticleIdList></Reference><Reference><Citation>PLoS One. 2012;7(10):e47643</Citation><ArticleIdList><ArticleId IdType="pubmed">23094070</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant. 2012 Nov;5(6):1346-58</Citation><ArticleIdList><ArticleId IdType="pubmed">22930732</ArticleId></ArticleIdList></Reference><Reference><Citation>Bioinformatics. 2003 Aug 12;19(12):1477-83</Citation><ArticleIdList><ArticleId IdType="pubmed">12912827</ArticleId></ArticleIdList></Reference><Reference><Citation>Front Microbiol. 2016 Mar 01;7:233</Citation><ArticleIdList><ArticleId IdType="pubmed">26973612</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2019 May;222(3):1584-1598</Citation><ArticleIdList><ArticleId IdType="pubmed">30636349</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2005 Dec;168(3):697-706</Citation><ArticleIdList><ArticleId IdType="pubmed">16313651</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Signal Behav. 2016;11(2):e1131372</Citation><ArticleIdList><ArticleId IdType="pubmed">26751110</ArticleId></ArticleIdList></Reference><Reference><Citation>J Biol Chem. 2002 Sep 6;277(36):32923-9</Citation><ArticleIdList><ArticleId IdType="pubmed">12042319</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2017 Jun 16;356(6343):1172-1175</Citation><ArticleIdList><ArticleId IdType="pubmed">28596307</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2010 Nov 25;468(7323):527-32</Citation><ArticleIdList><ArticleId IdType="pubmed">21107422</ArticleId></ArticleIdList></Reference><Reference><Citation>Planta. 2002 Nov;216(1):23-37</Citation><ArticleIdList><ArticleId IdType="pubmed">12430011</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2005 Jun 9;435(7043):819-23</Citation><ArticleIdList><ArticleId IdType="pubmed">15944705</ArticleId></ArticleIdList></Reference><Reference><Citation>Fungal Genet Biol. 2006 Feb;43(2):102-10</Citation><ArticleIdList><ArticleId IdType="pubmed">16386437</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2009;181(1):199-207</Citation><ArticleIdList><ArticleId IdType="pubmed">18811615</ArticleId></ArticleIdList></Reference><Reference><Citation>Appl Environ Microbiol. 2008 Sep;74(18):5792-801</Citation><ArticleIdList><ArticleId IdType="pubmed">18658284</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 1996 Jun;133(2):273-280</Citation><ArticleIdList><ArticleId IdType="pubmed">29681069</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2014 Aug;79(3):398-412</Citation><ArticleIdList><ArticleId IdType="pubmed">24888347</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell Environ. 2007 Mar;30(3):310-322</Citation><ArticleIdList><ArticleId IdType="pubmed">17263776</ArticleId></ArticleIdList></Reference><Reference><Citation>Annu Rev Plant Biol. 2011;62:227-50</Citation><ArticleIdList><ArticleId IdType="pubmed">21391813</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2017 Jun 16;356(6343):1175-1178</Citation><ArticleIdList><ArticleId IdType="pubmed">28596311</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 1998 Feb 1;116(2):447-53</Citation><ArticleIdList><ArticleId IdType="pubmed">9490752</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2006 Jul;141(3):1000-11</Citation><ArticleIdList><ArticleId IdType="pubmed">16679417</ArticleId></ArticleIdList></Reference><Reference><Citation>Planta. 2013 May;237(5):1267-77</Citation><ArticleIdList><ArticleId IdType="pubmed">23361889</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2009 May;150(1):73-83</Citation><ArticleIdList><ArticleId IdType="pubmed">19329566</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2016 Sep;211(4):1202-8</Citation><ArticleIdList><ArticleId IdType="pubmed">27136716</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2006 Feb;18(2):412-21</Citation><ArticleIdList><ArticleId IdType="pubmed">16387831</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 1998 Jan;10(1):105-17</Citation><ArticleIdList><ArticleId IdType="pubmed">9477574</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2009 Oct;151(2):809-19</Citation><ArticleIdList><ArticleId IdType="pubmed">19692536</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2014 Mar;164(3):1250-60</Citation><ArticleIdList><ArticleId IdType="pubmed">24468625</ArticleId></ArticleIdList></Reference><Reference><Citation>BMC Plant Biol. 2009 Jan 22;9:10</Citation><ArticleIdList><ArticleId IdType="pubmed">19161626</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 1995 Dec 7;378(6557):626-9</Citation><ArticleIdList><ArticleId IdType="pubmed">8524398</ArticleId></ArticleIdList></Reference><Reference><Citation>FEMS Microbiol Ecol. 2010 Apr;72(1):125-31</Citation><ArticleIdList><ArticleId IdType="pubmed">20459516</ArticleId></ArticleIdList></Reference><Reference><Citation>Trends Plant Sci. 2012 Jul;17(7):413-22</Citation><ArticleIdList><ArticleId IdType="pubmed">22513109</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2017 Jun;214(4):1631-1645</Citation><ArticleIdList><ArticleId IdType="pubmed">28380681</ArticleId></ArticleIdList></Reference><Reference><Citation>Fungal Genet Biol. 2011 Nov;48(11):1044-55</Citation><ArticleIdList><ArticleId IdType="pubmed">21907817</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2015 Apr;27(4):1352-66</Citation><ArticleIdList><ArticleId IdType="pubmed">25841038</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2017 Oct;29(10):2319-2335</Citation><ArticleIdList><ArticleId IdType="pubmed">28855333</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1720-5</Citation><ArticleIdList><ArticleId IdType="pubmed">17242358</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2009 Mar;57(5):798-809</Citation><ArticleIdList><ArticleId IdType="pubmed">18980647</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2018 Jan;93(2):338-354</Citation><ArticleIdList><ArticleId IdType="pubmed">29161754</ArticleId></ArticleIdList></Reference><Reference><Citation>J Chromatogr B Analyt Technol Biomed Life Sci. 2008 Aug 15;871(2):182-90</Citation><ArticleIdList><ArticleId IdType="pubmed">18501684</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 1996 May;9(4):233-42</Citation><ArticleIdList><ArticleId IdType="pubmed">8634476</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2019 Oct;224(1):396-408</Citation><ArticleIdList><ArticleId IdType="pubmed">31148173</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Mol Biol. 1999 Jun;40(3):479-86</Citation><ArticleIdList><ArticleId IdType="pubmed">10437831</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol Biochem. 2014 Feb;75:1-8</Citation><ArticleIdList><ArticleId IdType="pubmed">24361504</ArticleId></ArticleIdList></Reference><Reference><Citation>Curr Biol. 2019 Jun 17;29(12):2043-2050.e8</Citation><ArticleIdList><ArticleId IdType="pubmed">31178314</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2012 Jul;24(7):3074-86</Citation><ArticleIdList><ArticleId IdType="pubmed">22773752</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2009 Mar;57(6):1092-102</Citation><ArticleIdList><ArticleId IdType="pubmed">19054369</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol Plant Microbe Interact. 2010 Jul;23(7):915-26</Citation><ArticleIdList><ArticleId IdType="pubmed">20521954</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2002 Oct;14(10):2413-29</Citation><ArticleIdList><ArticleId IdType="pubmed">12368495</ArticleId></ArticleIdList></Reference><Reference><Citation>Can J Microbiol. 2004 Apr;50(4):251-60</Citation><ArticleIdList><ArticleId IdType="pubmed">15213749</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Methods. 2008 Jul;5(7):621-8</Citation><ArticleIdList><ArticleId IdType="pubmed">18516045</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell. 2011 Oct;23(10):3812-23</Citation><ArticleIdList><ArticleId IdType="pubmed">21972259</ArticleId></ArticleIdList></Reference><Reference><Citation>Methods Enzymol. 2006;411:134-93</Citation><ArticleIdList><ArticleId IdType="pubmed">16939790</ArticleId></ArticleIdList></Reference><Reference><Citation>Microbiol Mol Biol Rev. 1998 Mar;62(1):1-34</Citation><ArticleIdList><ArticleId IdType="pubmed">9529885</ArticleId></ArticleIdList></Reference><Reference><Citation>Mycorrhiza. 2005 Nov;15(8):620-627</Citation><ArticleIdList><ArticleId IdType="pubmed">16133249</ArticleId></ArticleIdList></Reference><Reference><Citation>Science. 2006 Sep 15;313(5793):1596-604</Citation><ArticleIdList><ArticleId IdType="pubmed">16973872</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2011 May;190(3):794-804</Citation><ArticleIdList><ArticleId IdType="pubmed">21294738</ArticleId></ArticleIdList></Reference><Reference><Citation>Front Plant Sci. 2016 May 25;7:679</Citation><ArticleIdList><ArticleId IdType="pubmed">27252708</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2011 Aug;156(4):2141-54</Citation><ArticleIdList><ArticleId IdType="pubmed">21705655</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2006;172(1):35-46</Citation><ArticleIdList><ArticleId IdType="pubmed">16945087</ArticleId></ArticleIdList></Reference><Reference><Citation>J Mol Model. 2005 Jun;11(3):226-36</Citation><ArticleIdList><ArticleId IdType="pubmed">15889294</ArticleId></ArticleIdList></Reference><Reference><Citation>Planta. 2007 May;225(6):1431-45</Citation><ArticleIdList><ArticleId IdType="pubmed">17143616</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2019 Aug;223(3):1127-1142</Citation><ArticleIdList><ArticleId IdType="pubmed">30843207</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant J. 2004 Nov;40(4):488-99</Citation><ArticleIdList><ArticleId IdType="pubmed">15500465</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2001 Nov 22;414(6862):462-70</Citation><ArticleIdList><ArticleId IdType="pubmed">11719809</ArticleId></ArticleIdList></Reference><Reference><Citation>Methods Mol Biol. 2014;1166:171-97</Citation><ArticleIdList><ArticleId IdType="pubmed">24852636</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2014 Aug 5;111(31):11563-8</Citation><ArticleIdList><ArticleId IdType="pubmed">25053812</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Physiol. 2012 Jun;159(2):789-97</Citation><ArticleIdList><ArticleId IdType="pubmed">22517410</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell Physiol. 2010 Sep;51(9):1411-5</Citation><ArticleIdList><ArticleId IdType="pubmed">20627949</ArticleId></ArticleIdList></Reference><Reference><Citation>Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):E665-72</Citation><ArticleIdList><ArticleId IdType="pubmed">22355114</ArticleId></ArticleIdList></Reference><Reference><Citation>J Plant Physiol. 2011 Jul 15;168(11):1256-63</Citation><ArticleIdList><ArticleId IdType="pubmed">21489650</ArticleId></ArticleIdList></Reference><Reference><Citation>Nat Rev Mol Cell Biol. 2013 Jun;14(6):382-92</Citation><ArticleIdList><ArticleId IdType="pubmed">23698585</ArticleId></ArticleIdList></Reference><Reference><Citation>Eukaryot Cell. 2013 Nov;12(11):1554-62</Citation><ArticleIdList><ArticleId IdType="pubmed">24058172</ArticleId></ArticleIdList></Reference><Reference><Citation>Nature. 2006 Dec 14;444(7121):933-6</Citation><ArticleIdList><ArticleId IdType="pubmed">17167486</ArticleId></ArticleIdList></Reference><Reference><Citation>Plant Cell Physiol. 2017 Jun 1;58(6):1003-1017</Citation><ArticleIdList><ArticleId IdType="pubmed">28387868</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2005 Dec;168(3):687-96</Citation><ArticleIdList><ArticleId IdType="pubmed">16313650</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2014 Jul;203(2):646-56</Citation><ArticleIdList><ArticleId IdType="pubmed">24787049</ArticleId></ArticleIdList></Reference><Reference><Citation>New Phytol. 2007;174(1):137-50</Citation><ArticleIdList><ArticleId 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