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Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view.

Identifieur interne : 000628 ( Main/Corpus ); précédent : 000627; suivant : 000629

Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view.

Auteurs : Ingo Dreyer ; Olivia Spitz ; Kerstin Kanonenberg ; Karolin Montag ; Maria R. Handrich ; Sabahuddin Ahmad ; Stephan Schott-Verdugo ; Carlos Navarro-Retamal ; María E. Rubio-Meléndez ; Judith L. Gomez-Porras ; Janin Riedelsberger ; Marco A. Molina-Montenegro ; Antonella Succurro ; Alga Zuccaro ; Sven B. Gould ; Petra Bauer ; Lutz Schmitt ; Holger Gohlke

Source :

RBID : pubmed:30565261

English descriptors

Abstract

To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal (AM) symbiosis, we modelled mathematically the two-membrane system at the plant-fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant-fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet-laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton-coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton-coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet-laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena.

DOI: 10.1111/nph.15646
PubMed: 30565261
PubMed Central: PMC6667911

Links to Exploration step

pubmed:30565261

Le document en format XML

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<name sortKey="Kanonenberg, Kerstin" sort="Kanonenberg, Kerstin" uniqKey="Kanonenberg K" first="Kerstin" last="Kanonenberg">Kerstin Kanonenberg</name>
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<nlm:affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Handrich, Maria R" sort="Handrich, Maria R" uniqKey="Handrich M" first="Maria R" last="Handrich">Maria R. Handrich</name>
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<nlm:affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Ahmad, Sabahuddin" sort="Ahmad, Sabahuddin" uniqKey="Ahmad S" first="Sabahuddin" last="Ahmad">Sabahuddin Ahmad</name>
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<name sortKey="Schott Verdugo, Stephan" sort="Schott Verdugo, Stephan" uniqKey="Schott Verdugo S" first="Stephan" last="Schott-Verdugo">Stephan Schott-Verdugo</name>
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<name sortKey="Navarro Retamal, Carlos" sort="Navarro Retamal, Carlos" uniqKey="Navarro Retamal C" first="Carlos" last="Navarro-Retamal">Carlos Navarro-Retamal</name>
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<name sortKey="Rubio Melendez, Maria E" sort="Rubio Melendez, Maria E" uniqKey="Rubio Melendez M" first="María E" last="Rubio-Meléndez">María E. Rubio-Meléndez</name>
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<name sortKey="Gomez Porras, Judith L" sort="Gomez Porras, Judith L" uniqKey="Gomez Porras J" first="Judith L" last="Gomez-Porras">Judith L. Gomez-Porras</name>
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<name sortKey="Riedelsberger, Janin" sort="Riedelsberger, Janin" uniqKey="Riedelsberger J" first="Janin" last="Riedelsberger">Janin Riedelsberger</name>
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<nlm:affiliation>Instalación en la Academia, Núcleo Científico Multidisciplinario, Dirección de Investigación, Vicerrectoría Académica, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
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<name sortKey="Molina Montenegro, Marco A" sort="Molina Montenegro, Marco A" uniqKey="Molina Montenegro M" first="Marco A" last="Molina-Montenegro">Marco A. Molina-Montenegro</name>
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<nlm:affiliation>Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674, Koln, Germany.</nlm:affiliation>
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<name sortKey="Zuccaro, Alga" sort="Zuccaro, Alga" uniqKey="Zuccaro A" first="Alga" last="Zuccaro">Alga Zuccaro</name>
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<name sortKey="Gould, Sven B" sort="Gould, Sven B" uniqKey="Gould S" first="Sven B" last="Gould">Sven B. Gould</name>
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<nlm:affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Bauer, Petra" sort="Bauer, Petra" uniqKey="Bauer P" first="Petra" last="Bauer">Petra Bauer</name>
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<nlm:affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Schmitt, Lutz" sort="Schmitt, Lutz" uniqKey="Schmitt L" first="Lutz" last="Schmitt">Lutz Schmitt</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Gohlke, Holger" sort="Gohlke, Holger" uniqKey="Gohlke H" first="Holger" last="Gohlke">Holger Gohlke</name>
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<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>John von Neumann Institute for Computing (NIC), Jülich Supercomputing Centre (JSC) & Institute for Complex Systems - Structural Biochemistry (ICS-6), Forschungszentrum Jülich GmbH, 52425, Jülich, Germany.</nlm:affiliation>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
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<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Spitz, Olivia" sort="Spitz, Olivia" uniqKey="Spitz O" first="Olivia" last="Spitz">Olivia Spitz</name>
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</affiliation>
<affiliation>
<nlm:affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<name sortKey="Kanonenberg, Kerstin" sort="Kanonenberg, Kerstin" uniqKey="Kanonenberg K" first="Kerstin" last="Kanonenberg">Kerstin Kanonenberg</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<nlm:affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
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<name sortKey="Montag, Karolin" sort="Montag, Karolin" uniqKey="Montag K" first="Karolin" last="Montag">Karolin Montag</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
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<name sortKey="Handrich, Maria R" sort="Handrich, Maria R" uniqKey="Handrich M" first="Maria R" last="Handrich">Maria R. Handrich</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Ahmad, Sabahuddin" sort="Ahmad, Sabahuddin" uniqKey="Ahmad S" first="Sabahuddin" last="Ahmad">Sabahuddin Ahmad</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Schott Verdugo, Stephan" sort="Schott Verdugo, Stephan" uniqKey="Schott Verdugo S" first="Stephan" last="Schott-Verdugo">Stephan Schott-Verdugo</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
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<author>
<name sortKey="Navarro Retamal, Carlos" sort="Navarro Retamal, Carlos" uniqKey="Navarro Retamal C" first="Carlos" last="Navarro-Retamal">Carlos Navarro-Retamal</name>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Rubio Melendez, Maria E" sort="Rubio Melendez, Maria E" uniqKey="Rubio Melendez M" first="María E" last="Rubio-Meléndez">María E. Rubio-Meléndez</name>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
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<name sortKey="Gomez Porras, Judith L" sort="Gomez Porras, Judith L" uniqKey="Gomez Porras J" first="Judith L" last="Gomez-Porras">Judith L. Gomez-Porras</name>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
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<name sortKey="Riedelsberger, Janin" sort="Riedelsberger, Janin" uniqKey="Riedelsberger J" first="Janin" last="Riedelsberger">Janin Riedelsberger</name>
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<nlm:affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Instalación en la Academia, Núcleo Científico Multidisciplinario, Dirección de Investigación, Vicerrectoría Académica, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
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<name sortKey="Molina Montenegro, Marco A" sort="Molina Montenegro, Marco A" uniqKey="Molina Montenegro M" first="Marco A" last="Molina-Montenegro">Marco A. Molina-Montenegro</name>
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<nlm:affiliation>Instituto de Ciencias Biológicas, Universidad de Talca, Avenida Lircay s/n, Talca, 3460000, Chile.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Universidad Católica del Norte, Avda. Larrondo 1281, Coquimbo, Chile.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Succurro, Antonella" sort="Succurro, Antonella" uniqKey="Succurro A" first="Antonella" last="Succurro">Antonella Succurro</name>
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<nlm:affiliation>Life and Medical Sciences (LIMES) Institute, University of Bonn, Carl-Troll-Str. 31, 53115 Bonn, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674, Koln, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Zuccaro, Alga" sort="Zuccaro, Alga" uniqKey="Zuccaro A" first="Alga" last="Zuccaro">Alga Zuccaro</name>
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<nlm:affiliation>Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674, Koln, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Gould, Sven B" sort="Gould, Sven B" uniqKey="Gould S" first="Sven B" last="Gould">Sven B. Gould</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Bauer, Petra" sort="Bauer, Petra" uniqKey="Bauer P" first="Petra" last="Bauer">Petra Bauer</name>
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<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Schmitt, Lutz" sort="Schmitt, Lutz" uniqKey="Schmitt L" first="Lutz" last="Schmitt">Lutz Schmitt</name>
<affiliation>
<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
</author>
<author>
<name sortKey="Gohlke, Holger" sort="Gohlke, Holger" uniqKey="Gohlke H" first="Holger" last="Gohlke">Holger Gohlke</name>
<affiliation>
<nlm:affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>John von Neumann Institute for Computing (NIC), Jülich Supercomputing Centre (JSC) & Institute for Complex Systems - Structural Biochemistry (ICS-6), Forschungszentrum Jülich GmbH, 52425, Jülich, Germany.</nlm:affiliation>
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<term>Biological Transport (MeSH)</term>
<term>Cell Membrane (metabolism)</term>
<term>Models, Biological (MeSH)</term>
<term>Mycorrhizae (metabolism)</term>
<term>Nitrogen (metabolism)</term>
<term>Phosphorus (metabolism)</term>
<term>Symbiosis (MeSH)</term>
<term>Thermodynamics (MeSH)</term>
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<term>Nitrogen</term>
<term>Phosphorus</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Membrane</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Biological Transport</term>
<term>Models, Biological</term>
<term>Symbiosis</term>
<term>Thermodynamics</term>
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<front>
<div type="abstract" xml:lang="en">To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal (AM) symbiosis, we modelled mathematically the two-membrane system at the plant-fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant-fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet-laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton-coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton-coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet-laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena.</div>
</front>
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<PMID Version="1">30565261</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>02</Month>
<Day>27</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>09</Month>
<Day>30</Day>
</DateRevised>
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<Journal>
<ISSN IssnType="Electronic">1469-8137</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>222</Volume>
<Issue>2</Issue>
<PubDate>
<Year>2019</Year>
<Month>04</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
<ISOAbbreviation>New Phytol</ISOAbbreviation>
</Journal>
<ArticleTitle>Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view.</ArticleTitle>
<Pagination>
<MedlinePgn>1043-1053</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15646</ELocationID>
<Abstract>
<AbstractText>To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal (AM) symbiosis, we modelled mathematically the two-membrane system at the plant-fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant-fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet-laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton-coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton-coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet-laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena.</AbstractText>
<CopyrightInformation>© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</CopyrightInformation>
</Abstract>
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<LastName>Dreyer</LastName>
<ForeName>Ingo</ForeName>
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<Identifier Source="ORCID">0000-0002-2781-0359</Identifier>
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<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
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<LastName>Spitz</LastName>
<ForeName>Olivia</ForeName>
<Initials>O</Initials>
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<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
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<LastName>Kanonenberg</LastName>
<ForeName>Kerstin</ForeName>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
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<LastName>Montag</LastName>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
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<LastName>Handrich</LastName>
<ForeName>Maria R</ForeName>
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<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
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<LastName>Ahmad</LastName>
<ForeName>Sabahuddin</ForeName>
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<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
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<ForeName>Stephan</ForeName>
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<Identifier Source="ORCID">0000-0003-0735-1404</Identifier>
<AffiliationInfo>
<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
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<LastName>Navarro-Retamal</LastName>
<ForeName>Carlos</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">0000-0001-9581-0206</Identifier>
<AffiliationInfo>
<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
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<LastName>Rubio-Meléndez</LastName>
<ForeName>María E</ForeName>
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<AffiliationInfo>
<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
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<LastName>Gomez-Porras</LastName>
<ForeName>Judith L</ForeName>
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<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
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<LastName>Riedelsberger</LastName>
<ForeName>Janin</ForeName>
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<Identifier Source="ORCID">0000-0002-4687-7495</Identifier>
<AffiliationInfo>
<Affiliation>Centro de Bioinformática y Simulación Molecular (CBSM), Facultad de Ingeniería, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Instalación en la Academia, Núcleo Científico Multidisciplinario, Dirección de Investigación, Vicerrectoría Académica, Universidad de Talca, 2 Norte 685, Talca, 3460000, Chile.</Affiliation>
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<LastName>Molina-Montenegro</LastName>
<ForeName>Marco A</ForeName>
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<Identifier Source="ORCID">0000-0001-6801-8942</Identifier>
<AffiliationInfo>
<Affiliation>Instituto de Ciencias Biológicas, Universidad de Talca, Avenida Lircay s/n, Talca, 3460000, Chile.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Universidad Católica del Norte, Avda. Larrondo 1281, Coquimbo, Chile.</Affiliation>
</AffiliationInfo>
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<LastName>Succurro</LastName>
<ForeName>Antonella</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">0000-0003-0227-2803</Identifier>
<AffiliationInfo>
<Affiliation>Life and Medical Sciences (LIMES) Institute, University of Bonn, Carl-Troll-Str. 31, 53115 Bonn, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674, Koln, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zuccaro</LastName>
<ForeName>Alga</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">0000-0002-8026-0114</Identifier>
<AffiliationInfo>
<Affiliation>Botanical Institute, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674, Koln, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gould</LastName>
<ForeName>Sven B</ForeName>
<Initials>SB</Initials>
<Identifier Source="ORCID">0000-0002-2038-8474</Identifier>
<AffiliationInfo>
<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Molecular Evolution, Heinrich Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Bauer</LastName>
<ForeName>Petra</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Botany, Heinrich-Heine University, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmitt</LastName>
<ForeName>Lutz</ForeName>
<Initials>L</Initials>
<Identifier Source="ORCID">0000-0002-1167-9819</Identifier>
<AffiliationInfo>
<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Biochemistry, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gohlke</LastName>
<ForeName>Holger</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">0000-0001-8613-1447</Identifier>
<AffiliationInfo>
<Affiliation>SFB 1208 - Identity and Dynamics of Membrane Systems - from Molecules to Cellular Functions, Heinrich Heine Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Pharmaceutical and Medicinal Chemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>John von Neumann Institute for Computing (NIC), Jülich Supercomputing Centre (JSC) & Institute for Complex Systems - Structural Biochemistry (ICS-6), Forschungszentrum Jülich GmbH, 52425, Jülich, Germany.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>SFB 1208</GrantID>
<Agency>Deutsche Forschungsgemeinschaft</Agency>
<Country>International</Country>
</Grant>
<Grant>
<GrantID>1150054</GrantID>
<Agency>Fondecyt</Agency>
<Country>International</Country>
</Grant>
<Grant>
<GrantID>3170434</GrantID>
<Agency>Fondecyt</Agency>
<Country>International</Country>
</Grant>
<Grant>
<GrantID>PAI77170035</GrantID>
<Agency>Convocatoria nacional subvención a la instalación en la academia</Agency>
<Country>International</Country>
</Grant>
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<Month>01</Month>
<Day>21</Day>
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<Country>England</Country>
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<NameOfSubstance UI="D010758">Phosphorus</NameOfSubstance>
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<Chemical>
<RegistryNumber>N762921K75</RegistryNumber>
<NameOfSubstance UI="D009584">Nitrogen</NameOfSubstance>
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<MeshHeading>
<DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008954" MajorTopicYN="N">Models, Biological</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009584" MajorTopicYN="N">Nitrogen</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010758" MajorTopicYN="N">Phosphorus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName>
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<Keyword MajorTopicYN="Y">modelling</Keyword>
<Keyword MajorTopicYN="Y">nutrient transport</Keyword>
<Keyword MajorTopicYN="Y">plant biophysics</Keyword>
<Keyword MajorTopicYN="Y">plant-fungus interaction</Keyword>
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<Month>12</Month>
<Day>07</Day>
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