The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots.
Identifieur interne : 000689 ( Main/Exploration ); précédent : 000688; suivant : 000690The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots.
Auteurs : Kevin R. Cope [États-Unis] ; Adeline Bascaules [France] ; Thomas B. Irving [États-Unis] ; Muthusubramanian Venkateshwaran [États-Unis] ; Junko Maeda [États-Unis] ; Kevin Garcia [États-Unis] ; Tomás A. Rush [États-Unis] ; Cathleen Ma [États-Unis] ; Jessy Labbé [États-Unis] ; Sara Jawdy [États-Unis] ; Edward Steigerwald [États-Unis] ; Jonathan Setzke [États-Unis] ; Emmeline Fung [États-Unis] ; Kimberly G. Schnell [États-Unis] ; Yunqian Wang [États-Unis] ; Nathaniel Schlief [États-Unis] ; Heike Bücking [États-Unis] ; Steven H. Strauss [États-Unis] ; Fabienne Maillet [France] ; Patricia Jargeat [États-Unis, France] ; Guillaume Bécard [France] ; Virginie Puech-Pagès [France] ; Jean-Michel Ané [États-Unis]Source :
- The Plant cell [ 1532-298X ] ; 2019.
Descripteurs français
- KwdFr :
- Calcium (métabolisme), Calcium-Calmodulin-Dependent Protein Kinases (génétique), Calcium-Calmodulin-Dependent Protein Kinases (métabolisme), Canaux calciques (métabolisme), Laccaria (métabolisme), Lipopolysaccharides (composition chimique), Lipopolysaccharides (métabolisme), Mycorhizes (croissance et développement), Mycorhizes (métabolisme), Mycorhizes (physiologie), Populus (génétique), Populus (métabolisme), Racines de plante (composition chimique), Racines de plante (croissance et développement), Racines de plante (microbiologie), Racines de plante (métabolisme), Régulation de l'expression des gènes végétaux (MeSH), Symbiose (physiologie), Transduction du signal (MeSH), Végétaux génétiquement modifiés (MeSH).
- MESH :
- composition chimique : Lipopolysaccharides, Racines de plante.
- croissance et développement : Mycorhizes, Racines de plante.
- génétique : Calcium-Calmodulin-Dependent Protein Kinases, Populus.
- microbiologie : Racines de plante.
- métabolisme : Calcium, Calcium-Calmodulin-Dependent Protein Kinases, Canaux calciques, Laccaria, Lipopolysaccharides, Mycorhizes, Populus, Racines de plante.
- physiologie : Mycorhizes, Symbiose.
- Régulation de l'expression des gènes végétaux, Transduction du signal, Végétaux génétiquement modifiés.
English descriptors
- KwdEn :
- Calcium (metabolism), Calcium Channels (metabolism), Calcium-Calmodulin-Dependent Protein Kinases (genetics), Calcium-Calmodulin-Dependent Protein Kinases (metabolism), Gene Expression Regulation, Plant (MeSH), Laccaria (metabolism), Lipopolysaccharides (chemistry), Lipopolysaccharides (metabolism), Mycorrhizae (growth & development), Mycorrhizae (metabolism), Mycorrhizae (physiology), Plant Roots (chemistry), Plant Roots (growth & development), Plant Roots (metabolism), Plant Roots (microbiology), Plants, Genetically Modified (MeSH), Populus (genetics), Populus (metabolism), Signal Transduction (MeSH), Symbiosis (physiology).
- MESH :
- chemical , chemistry : Lipopolysaccharides.
- chemical , genetics : Calcium-Calmodulin-Dependent Protein Kinases.
- chemical , metabolism : Calcium, Calcium Channels, Calcium-Calmodulin-Dependent Protein Kinases, Lipopolysaccharides.
- chemistry : Plant Roots.
- genetics : Populus.
- growth & development : Mycorrhizae, Plant Roots.
- metabolism : Laccaria, Mycorrhizae, Plant Roots, Populus.
- microbiology : Plant Roots.
- physiology : Mycorrhizae, Symbiosis.
- Gene Expression Regulation, Plant, Plants, Genetically Modified, Signal Transduction.
Abstract
Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor Compared with the wild-type Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.
DOI: 10.1105/tpc.18.00676
PubMed: 31416823
PubMed Central: PMC6790088
Affiliations:
- France, États-Unis
- Dakota du Sud, Midi-Pyrénées, Occitanie (région administrative), Oregon, Tennessee, Wisconsin
- Castanet-Tolosan, Toulouse
Links toward previous steps (curation, corpus...)
Le document en format XML
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Strauss</name><affiliation wicri:level="2"><nlm:affiliation>Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Oregon</region></placeName><wicri:cityArea>Department of Forest Ecosystems and Society, Oregon State University, Corvallis</wicri:cityArea></affiliation></author><author><name sortKey="Maillet, Fabienne" sort="Maillet, Fabienne" uniqKey="Maillet F" first="Fabienne" last="Maillet">Fabienne Maillet</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Jargeat, Patricia" sort="Jargeat, Patricia" uniqKey="Jargeat P" first="Patricia" last="Jargeat">Patricia Jargeat</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge</wicri:cityArea></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Toulouse</settlement></placeName></affiliation></author><author><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Puech Pages, Virginie" sort="Puech Pages, Virginie" uniqKey="Puech Pages V" first="Virginie" last="Puech-Pagès">Virginie Puech-Pagès</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Ane, Jean Michel" sort="Ane, Jean Michel" uniqKey="Ane J" first="Jean-Michel" last="Ané">Jean-Michel Ané</name><affiliation wicri:level="1"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706 jeanmichel.ane@wisc.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:regionArea><wicri:noRegion>Madison</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31416823</idno><idno type="pmid">31416823</idno><idno type="doi">10.1105/tpc.18.00676</idno><idno type="pmc">PMC6790088</idno><idno type="wicri:Area/Main/Corpus">000753</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000753</idno><idno type="wicri:Area/Main/Curation">000753</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000753</idno><idno type="wicri:Area/Main/Exploration">000753</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The Ectomycorrhizal Fungus <i>Laccaria bicolor</i> Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize <i>Populus</i> Roots.</title><author><name sortKey="Cope, Kevin R" sort="Cope, Kevin R" uniqKey="Cope K" first="Kevin R" last="Cope">Kevin R. Cope</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Bascaules, Adeline" sort="Bascaules, Adeline" uniqKey="Bascaules A" first="Adeline" last="Bascaules">Adeline Bascaules</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Irving, Thomas B" sort="Irving, Thomas B" uniqKey="Irving T" first="Thomas B" last="Irving">Thomas B. Irving</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Venkateshwaran, Muthusubramanian" sort="Venkateshwaran, Muthusubramanian" uniqKey="Venkateshwaran M" first="Muthusubramanian" last="Venkateshwaran">Muthusubramanian Venkateshwaran</name><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Maeda, Junko" sort="Maeda, Junko" uniqKey="Maeda J" first="Junko" last="Maeda">Junko Maeda</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Garcia, Kevin" sort="Garcia, Kevin" uniqKey="Garcia K" first="Kevin" last="Garcia">Kevin Garcia</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Rush, Tomas A" sort="Rush, Tomas A" uniqKey="Rush T" first="Tomás A" last="Rush">Tomás A. Rush</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Ma, Cathleen" sort="Ma, Cathleen" uniqKey="Ma C" first="Cathleen" last="Ma">Cathleen Ma</name><affiliation wicri:level="2"><nlm:affiliation>Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Oregon</region></placeName><wicri:cityArea>Department of Forest Ecosystems and Society, Oregon State University, Corvallis</wicri:cityArea></affiliation></author><author><name sortKey="Labbe, Jessy" sort="Labbe, Jessy" uniqKey="Labbe J" first="Jessy" last="Labbé">Jessy Labbé</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge</wicri:cityArea></affiliation></author><author><name sortKey="Jawdy, Sara" sort="Jawdy, Sara" uniqKey="Jawdy S" first="Sara" last="Jawdy">Sara Jawdy</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge</wicri:cityArea></affiliation></author><author><name sortKey="Steigerwald, Edward" sort="Steigerwald, Edward" uniqKey="Steigerwald E" first="Edward" last="Steigerwald">Edward Steigerwald</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Setzke, Jonathan" sort="Setzke, Jonathan" uniqKey="Setzke J" first="Jonathan" last="Setzke">Jonathan Setzke</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Fung, Emmeline" sort="Fung, Emmeline" uniqKey="Fung E" first="Emmeline" last="Fung">Emmeline Fung</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Schnell, Kimberly G" sort="Schnell, Kimberly G" uniqKey="Schnell K" first="Kimberly G" last="Schnell">Kimberly G. Schnell</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Wang, Yunqian" sort="Wang, Yunqian" uniqKey="Wang Y" first="Yunqian" last="Wang">Yunqian Wang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Schlief, Nathaniel" sort="Schlief, Nathaniel" uniqKey="Schlief N" first="Nathaniel" last="Schlief">Nathaniel Schlief</name><affiliation wicri:level="2"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author><author><name sortKey="Bucking, Heike" sort="Bucking, Heike" uniqKey="Bucking H" first="Heike" last="Bücking">Heike Bücking</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biology and Microbiology, South Dakota State University, Brookings, South Dakota 57007.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Dakota du Sud</region></placeName><wicri:cityArea>Department of Biology and Microbiology, South Dakota State University, Brookings</wicri:cityArea></affiliation></author><author><name sortKey="Strauss, Steven H" sort="Strauss, Steven H" uniqKey="Strauss S" first="Steven H" last="Strauss">Steven H. Strauss</name><affiliation wicri:level="2"><nlm:affiliation>Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Oregon</region></placeName><wicri:cityArea>Department of Forest Ecosystems and Society, Oregon State University, Corvallis</wicri:cityArea></affiliation></author><author><name sortKey="Maillet, Fabienne" sort="Maillet, Fabienne" uniqKey="Maillet F" first="Fabienne" last="Maillet">Fabienne Maillet</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Jargeat, Patricia" sort="Jargeat, Patricia" uniqKey="Jargeat P" first="Patricia" last="Jargeat">Patricia Jargeat</name><affiliation wicri:level="2"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Tennessee</region></placeName><wicri:cityArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge</wicri:cityArea></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Toulouse</settlement></placeName></affiliation></author><author><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Puech Pages, Virginie" sort="Puech Pages, Virginie" uniqKey="Puech Pages V" first="Virginie" last="Puech-Pagès">Virginie Puech-Pagès</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Midi-Pyrénées</region><settlement type="city">Castanet-Tolosan</settlement></placeName></affiliation></author><author><name sortKey="Ane, Jean Michel" sort="Ane, Jean Michel" uniqKey="Ane J" first="Jean-Michel" last="Ané">Jean-Michel Ané</name><affiliation wicri:level="1"><nlm:affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706 jeanmichel.ane@wisc.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Department of Bacteriology, University of Wisconsin, Madison</wicri:regionArea><wicri:noRegion>Madison</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Wisconsin</region></placeName><wicri:cityArea>Department of Agronomy, University of Wisconsin, Madison</wicri:cityArea></affiliation></author></analytic><series><title level="j">The Plant cell</title><idno type="eISSN">1532-298X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Calcium (metabolism)</term><term>Calcium Channels (metabolism)</term><term>Calcium-Calmodulin-Dependent Protein Kinases (genetics)</term><term>Calcium-Calmodulin-Dependent Protein Kinases (metabolism)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Laccaria (metabolism)</term><term>Lipopolysaccharides (chemistry)</term><term>Lipopolysaccharides (metabolism)</term><term>Mycorrhizae (growth & development)</term><term>Mycorrhizae (metabolism)</term><term>Mycorrhizae (physiology)</term><term>Plant Roots (chemistry)</term><term>Plant Roots (growth & development)</term><term>Plant Roots (metabolism)</term><term>Plant Roots (microbiology)</term><term>Plants, Genetically Modified (MeSH)</term><term>Populus (genetics)</term><term>Populus (metabolism)</term><term>Signal Transduction (MeSH)</term><term>Symbiosis (physiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Calcium (métabolisme)</term><term>Calcium-Calmodulin-Dependent Protein Kinases (génétique)</term><term>Calcium-Calmodulin-Dependent Protein Kinases (métabolisme)</term><term>Canaux calciques (métabolisme)</term><term>Laccaria (métabolisme)</term><term>Lipopolysaccharides (composition chimique)</term><term>Lipopolysaccharides (métabolisme)</term><term>Mycorhizes (croissance et développement)</term><term>Mycorhizes (métabolisme)</term><term>Mycorhizes (physiologie)</term><term>Populus (génétique)</term><term>Populus (métabolisme)</term><term>Racines de plante (composition chimique)</term><term>Racines de plante (croissance et développement)</term><term>Racines de plante (microbiologie)</term><term>Racines de plante (métabolisme)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Symbiose (physiologie)</term><term>Transduction du signal (MeSH)</term><term>Végétaux génétiquement modifiés (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Lipopolysaccharides</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Calcium-Calmodulin-Dependent Protein Kinases</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Calcium</term><term>Calcium Channels</term><term>Calcium-Calmodulin-Dependent Protein Kinases</term><term>Lipopolysaccharides</term></keywords><keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Plant Roots</term></keywords><keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr"><term>Lipopolysaccharides</term><term>Racines de plante</term></keywords><keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Mycorhizes</term><term>Racines de plante</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Mycorrhizae</term><term>Plant Roots</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Calcium-Calmodulin-Dependent Protein Kinases</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Laccaria</term><term>Mycorrhizae</term><term>Plant Roots</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Racines de plante</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Roots</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Calcium</term><term>Calcium-Calmodulin-Dependent Protein Kinases</term><term>Canaux calciques</term><term>Laccaria</term><term>Lipopolysaccharides</term><term>Mycorhizes</term><term>Populus</term><term>Racines de plante</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Mycorhizes</term><term>Symbiose</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Mycorrhizae</term><term>Symbiosis</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation, Plant</term><term>Plants, Genetically Modified</term><term>Signal Transduction</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Régulation de l'expression des gènes végétaux</term><term>Transduction du signal</term><term>Végétaux génétiquement modifiés</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus <i>Laccaria bicolor</i> produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant <i>Populus</i> in a <i>CASTOR/POLLUX</i>-dependent manner. Nonsulfated LCOs enhanced lateral root development in <i>Populus</i> in a calcium/calmodulin-dependent protein kinase (<i>CCaMK</i>)-dependent manner, and sulfated LCOs enhanced the colonization of <i>Populus</i> by <i>L. bicolor</i> Compared with the wild-type <i>Populus</i>, the colonization of <i>CASTOR</i>/<i>POLLUX</i> and <i>CCaMK</i> RNA interference lines by <i>L. bicolor</i> was reduced. Our work demonstrates that similar to other root symbioses, <i>L. bicolor</i> uses the CSP for the full establishment of its mutualistic association with <i>Populus</i>.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31416823</PMID><DateCompleted><Year>2020</Year><Month>06</Month><Day>29</Day></DateCompleted><DateRevised><Year>2020</Year><Month>06</Month><Day>29</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-298X</ISSN><JournalIssue CitedMedium="Internet"><Volume>31</Volume><Issue>10</Issue><PubDate><Year>2019</Year><Month>10</Month></PubDate></JournalIssue><Title>The Plant cell</Title><ISOAbbreviation>Plant Cell</ISOAbbreviation></Journal><ArticleTitle>The Ectomycorrhizal Fungus <i>Laccaria bicolor</i> Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize <i>Populus</i> Roots.</ArticleTitle><Pagination><MedlinePgn>2386-2410</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1105/tpc.18.00676</ELocationID><Abstract><AbstractText>Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus <i>Laccaria bicolor</i> produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant <i>Populus</i> in a <i>CASTOR/POLLUX</i>-dependent manner. Nonsulfated LCOs enhanced lateral root development in <i>Populus</i> in a calcium/calmodulin-dependent protein kinase (<i>CCaMK</i>)-dependent manner, and sulfated LCOs enhanced the colonization of <i>Populus</i> by <i>L. bicolor</i> Compared with the wild-type <i>Populus</i>, the colonization of <i>CASTOR</i>/<i>POLLUX</i> and <i>CCaMK</i> RNA interference lines by <i>L. bicolor</i> was reduced. Our work demonstrates that similar to other root symbioses, <i>L. bicolor</i> uses the CSP for the full establishment of its mutualistic association with <i>Populus</i>.</AbstractText><CopyrightInformation>© 2019 American Society of Plant Biologists. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Cope</LastName><ForeName>Kevin R</ForeName><Initials>KR</Initials><Identifier Source="ORCID">0000-0003-0173-2871</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bascaules</LastName><ForeName>Adeline</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0002-6062-0119</Identifier><AffiliationInfo><Affiliation>Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Irving</LastName><ForeName>Thomas B</ForeName><Initials>TB</Initials><Identifier Source="ORCID">0000-0003-3040-4543</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Venkateshwaran</LastName><ForeName>Muthusubramanian</ForeName><Initials>M</Initials><Identifier Source="ORCID">0000-0001-7023-1988</Identifier><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maeda</LastName><ForeName>Junko</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0001-5792-9636</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Garcia</LastName><ForeName>Kevin</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0003-0821-1024</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rush</LastName><ForeName>Tomás A</ForeName><Initials>TA</Initials><Identifier Source="ORCID">0000-0002-3207-1466</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author 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53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schnell</LastName><ForeName>Kimberly G</ForeName><Initials>KG</Initials><Identifier Source="ORCID">0000-0002-9261-3028</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yunqian</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0002-6252-7233</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schlief</LastName><ForeName>Nathaniel</ForeName><Initials>N</Initials><Identifier Source="ORCID">0000-0003-4313-3260</Identifier><AffiliationInfo><Affiliation>Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bücking</LastName><ForeName>Heike</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0002-4040-0944</Identifier><AffiliationInfo><Affiliation>Department of Biology and Microbiology, South Dakota State University, Brookings, South Dakota 57007.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Strauss</LastName><ForeName>Steven H</ForeName><Initials>SH</Initials><Identifier Source="ORCID">0000-0001-9670-3082</Identifier><AffiliationInfo><Affiliation>Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maillet</LastName><ForeName>Fabienne</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0001-6285-4704</Identifier><AffiliationInfo><Affiliation>Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jargeat</LastName><ForeName>Patricia</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0002-6417-7425</Identifier><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bécard</LastName><ForeName>Guillaume</ForeName><Initials>G</Initials><Identifier 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53706.</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><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant Cell</MedlineTA><NlmUniqueID>9208688</NlmUniqueID><ISSNLinking>1040-4651</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D015220">Calcium Channels</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D008070">Lipopolysaccharides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C023023">lipid-linked 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K" first="Kevin R" last="Cope">Kevin R. Cope</name></region><name sortKey="Ane, Jean Michel" sort="Ane, Jean Michel" uniqKey="Ane J" first="Jean-Michel" last="Ané">Jean-Michel Ané</name><name sortKey="Ane, Jean Michel" sort="Ane, Jean Michel" uniqKey="Ane J" first="Jean-Michel" last="Ané">Jean-Michel Ané</name><name sortKey="Bucking, Heike" sort="Bucking, Heike" uniqKey="Bucking H" first="Heike" last="Bücking">Heike Bücking</name><name sortKey="Cope, Kevin R" sort="Cope, Kevin R" uniqKey="Cope K" first="Kevin R" last="Cope">Kevin R. Cope</name><name sortKey="Fung, Emmeline" sort="Fung, Emmeline" uniqKey="Fung E" first="Emmeline" last="Fung">Emmeline Fung</name><name sortKey="Fung, Emmeline" sort="Fung, Emmeline" uniqKey="Fung E" first="Emmeline" last="Fung">Emmeline Fung</name><name sortKey="Garcia, Kevin" sort="Garcia, Kevin" uniqKey="Garcia K" first="Kevin" last="Garcia">Kevin Garcia</name><name sortKey="Garcia, Kevin" sort="Garcia, Kevin" uniqKey="Garcia K" first="Kevin" last="Garcia">Kevin Garcia</name><name sortKey="Irving, Thomas B" sort="Irving, Thomas B" uniqKey="Irving T" first="Thomas B" last="Irving">Thomas B. Irving</name><name sortKey="Irving, Thomas B" sort="Irving, Thomas B" uniqKey="Irving T" first="Thomas B" last="Irving">Thomas B. Irving</name><name sortKey="Jargeat, Patricia" sort="Jargeat, Patricia" uniqKey="Jargeat P" first="Patricia" last="Jargeat">Patricia Jargeat</name><name sortKey="Jawdy, Sara" sort="Jawdy, Sara" uniqKey="Jawdy S" first="Sara" last="Jawdy">Sara Jawdy</name><name sortKey="Labbe, Jessy" sort="Labbe, Jessy" uniqKey="Labbe J" first="Jessy" last="Labbé">Jessy Labbé</name><name sortKey="Ma, Cathleen" sort="Ma, Cathleen" uniqKey="Ma C" first="Cathleen" last="Ma">Cathleen Ma</name><name sortKey="Maeda, Junko" sort="Maeda, Junko" uniqKey="Maeda J" first="Junko" last="Maeda">Junko Maeda</name><name sortKey="Maeda, Junko" sort="Maeda, Junko" uniqKey="Maeda J" first="Junko" last="Maeda">Junko Maeda</name><name sortKey="Rush, Tomas A" sort="Rush, Tomas A" uniqKey="Rush T" first="Tomás A" last="Rush">Tomás A. Rush</name><name sortKey="Rush, Tomas A" sort="Rush, Tomas A" uniqKey="Rush T" first="Tomás A" last="Rush">Tomás A. Rush</name><name sortKey="Schlief, Nathaniel" sort="Schlief, Nathaniel" uniqKey="Schlief N" first="Nathaniel" last="Schlief">Nathaniel Schlief</name><name sortKey="Schlief, Nathaniel" sort="Schlief, Nathaniel" uniqKey="Schlief N" first="Nathaniel" last="Schlief">Nathaniel Schlief</name><name sortKey="Schnell, Kimberly G" sort="Schnell, Kimberly G" uniqKey="Schnell K" first="Kimberly G" last="Schnell">Kimberly G. Schnell</name><name sortKey="Schnell, Kimberly G" sort="Schnell, Kimberly G" uniqKey="Schnell K" first="Kimberly G" last="Schnell">Kimberly G. Schnell</name><name sortKey="Setzke, Jonathan" sort="Setzke, Jonathan" uniqKey="Setzke J" first="Jonathan" last="Setzke">Jonathan Setzke</name><name sortKey="Steigerwald, Edward" sort="Steigerwald, Edward" uniqKey="Steigerwald E" first="Edward" last="Steigerwald">Edward Steigerwald</name><name sortKey="Strauss, Steven H" sort="Strauss, Steven H" uniqKey="Strauss S" first="Steven H" last="Strauss">Steven H. Strauss</name><name sortKey="Venkateshwaran, Muthusubramanian" sort="Venkateshwaran, Muthusubramanian" uniqKey="Venkateshwaran M" first="Muthusubramanian" last="Venkateshwaran">Muthusubramanian Venkateshwaran</name><name sortKey="Wang, Yunqian" sort="Wang, Yunqian" uniqKey="Wang Y" first="Yunqian" last="Wang">Yunqian Wang</name></country><country name="France"><region name="Occitanie (région administrative)"><name sortKey="Bascaules, Adeline" sort="Bascaules, Adeline" uniqKey="Bascaules A" first="Adeline" last="Bascaules">Adeline Bascaules</name></region><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><name sortKey="Jargeat, Patricia" sort="Jargeat, Patricia" uniqKey="Jargeat P" first="Patricia" last="Jargeat">Patricia Jargeat</name><name sortKey="Maillet, Fabienne" sort="Maillet, Fabienne" uniqKey="Maillet F" first="Fabienne" last="Maillet">Fabienne Maillet</name><name sortKey="Puech Pages, Virginie" sort="Puech Pages, Virginie" uniqKey="Puech Pages V" first="Virginie" last="Puech-Pagès">Virginie Puech-Pagès</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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