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Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net.

Identifieur interne : 000B41 ( Main/Exploration ); précédent : 000B40; suivant : 000B42

Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net.

Auteurs : Gang Sa [République populaire de Chine] ; Jun Yao [République populaire de Chine] ; Chen Deng [République populaire de Chine] ; Jian Liu [République populaire de Chine] ; Yinan Zhang [République populaire de Chine] ; Zhimei Zhu [République populaire de Chine] ; Yuhong Zhang [République populaire de Chine] ; Xujun Ma [République populaire de Chine] ; Rui Zhao [République populaire de Chine] ; Shanzhi Lin [République populaire de Chine] ; Cunfu Lu [République populaire de Chine] ; Andrea Polle [République populaire de Chine, Allemagne] ; Shaoliang Chen [République populaire de Chine]

Source :

RBID : pubmed:30756398

Descripteurs français

English descriptors

Abstract

Salt stress is an important environmental cue impeding poplar nitrogen nutrition. Here, we characterized the impact of salinity on proton-driven nitrate fluxes in ectomycorrhizal roots and the importance of a Hartig net for nitrate uptake. We employed two Paxillus involutus strains for root colonization: MAJ, which forms typical ectomycorrhizal structures (mantle and Hartig net), and NAU, colonizing roots with a thin, loose hyphal sheath. Fungus-colonized and noncolonized Populus × canescens were exposed to sodium chloride and used to measure root surface pH, nitrate (NO3- ) flux and transcription of NO3- transporters (NRTs; PcNRT1.1, -1.2, -2.1), and plasmalemma proton ATPases (HAs; PcHA4, -8, -11). Paxillus colonization enhanced root NO3- uptake, decreased surface pH, and stimulated NRTs and HA4 of the host regardless the presence or absence of a Hartig net. Under salt stress, noncolonized roots exhibited strong net NO3- efflux, whereas beneficial effects of fungal colonization on surface pH and HAs prevented NO3- loss. Inhibition of HAs abolished NO3- influx under all conditions. We found that stimulation of HAs was crucial for the beneficial influence of ectomycorrhiza on NO3- uptake, whereas the presence of a Hartig net was not required for improved NO3- translocation. Mycorrhizas may contribute to host adaptation to salt-affected environments by keeping up NO3- nutrition.

DOI: 10.1111/nph.15740
PubMed: 30756398
PubMed Central: PMC6594093


Affiliations:


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Le document en format XML

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<name sortKey="Zhu, Zhimei" sort="Zhu, Zhimei" uniqKey="Zhu Z" first="Zhimei" last="Zhu">Zhimei Zhu</name>
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<name sortKey="Chen, Shaoliang" sort="Chen, Shaoliang" uniqKey="Chen S" first="Shaoliang" last="Chen">Shaoliang Chen</name>
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<name sortKey="Deng, Chen" sort="Deng, Chen" uniqKey="Deng C" first="Chen" last="Deng">Chen Deng</name>
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<name sortKey="Liu, Jian" sort="Liu, Jian" uniqKey="Liu J" first="Jian" last="Liu">Jian Liu</name>
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<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083</wicri:regionArea>
<wicri:noRegion>100083</wicri:noRegion>
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<name sortKey="Zhang, Yinan" sort="Zhang, Yinan" uniqKey="Zhang Y" first="Yinan" last="Zhang">Yinan Zhang</name>
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<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083</wicri:regionArea>
<wicri:noRegion>100083</wicri:noRegion>
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<name sortKey="Zhu, Zhimei" sort="Zhu, Zhimei" uniqKey="Zhu Z" first="Zhimei" last="Zhu">Zhimei Zhu</name>
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<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>100083</wicri:noRegion>
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<name sortKey="Zhang, Yuhong" sort="Zhang, Yuhong" uniqKey="Zhang Y" first="Yuhong" last="Zhang">Yuhong Zhang</name>
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<name sortKey="Ma, Xujun" sort="Ma, Xujun" uniqKey="Ma X" first="Xujun" last="Ma">Xujun Ma</name>
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<name sortKey="Zhao, Rui" sort="Zhao, Rui" uniqKey="Zhao R" first="Rui" last="Zhao">Rui Zhao</name>
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<name sortKey="Lin, Shanzhi" sort="Lin, Shanzhi" uniqKey="Lin S" first="Shanzhi" last="Lin">Shanzhi Lin</name>
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<name sortKey="Lu, Cunfu" sort="Lu, Cunfu" uniqKey="Lu C" first="Cunfu" last="Lu">Cunfu Lu</name>
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<name sortKey="Polle, Andrea" sort="Polle, Andrea" uniqKey="Polle A" first="Andrea" last="Polle">Andrea Polle</name>
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<wicri:noRegion>100083</wicri:noRegion>
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<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Forest Botany and Tree Physiology, University of Goettingen, Göttingen, 37077</wicri:regionArea>
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<region type="land" nuts="2">Basse-Saxe</region>
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<name sortKey="Chen, Shaoliang" sort="Chen, Shaoliang" uniqKey="Chen S" first="Shaoliang" last="Chen">Shaoliang Chen</name>
<affiliation wicri:level="1">
<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083</wicri:regionArea>
<wicri:noRegion>100083</wicri:noRegion>
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<series>
<title level="j">The New phytologist</title>
<idno type="eISSN">1469-8137</idno>
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<date when="2019" type="published">2019</date>
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<term>Cell Membrane (drug effects)</term>
<term>Cell Membrane (metabolism)</term>
<term>Hydrogen-Ion Concentration (MeSH)</term>
<term>Membrane Transport Proteins (metabolism)</term>
<term>Mycorrhizae (metabolism)</term>
<term>Nitrate Reductase (metabolism)</term>
<term>Nitrates (metabolism)</term>
<term>Nitrite Reductases (metabolism)</term>
<term>Populus (microbiology)</term>
<term>Proton-Translocating ATPases (metabolism)</term>
<term>Salinity (MeSH)</term>
<term>Sodium Chloride (pharmacology)</term>
<term>Stress, Physiological (drug effects)</term>
<term>Vanadates (pharmacology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Chlorure de sodium (pharmacologie)</term>
<term>Concentration en ions d'hydrogène (MeSH)</term>
<term>Membrane cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Membrane cellulaire (métabolisme)</term>
<term>Mycorhizes (métabolisme)</term>
<term>Nitrate reductase (métabolisme)</term>
<term>Nitrates (métabolisme)</term>
<term>Nitrite reductases (métabolisme)</term>
<term>Populus (microbiologie)</term>
<term>Proton-Translocating ATPases (métabolisme)</term>
<term>Protéines de transport membranaire (métabolisme)</term>
<term>Salinité (MeSH)</term>
<term>Stress physiologique (effets des médicaments et des substances chimiques)</term>
<term>Vanadates (pharmacologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Membrane Transport Proteins</term>
<term>Nitrate Reductase</term>
<term>Nitrates</term>
<term>Nitrite Reductases</term>
<term>Proton-Translocating ATPases</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Cell Membrane</term>
<term>Stress, Physiological</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Membrane cellulaire</term>
<term>Stress physiologique</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Membrane</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Membrane cellulaire</term>
<term>Mycorhizes</term>
<term>Nitrate reductase</term>
<term>Nitrates</term>
<term>Nitrite reductases</term>
<term>Proton-Translocating ATPases</term>
<term>Protéines de transport membranaire</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Chlorure de sodium</term>
<term>Vanadates</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Sodium Chloride</term>
<term>Vanadates</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Hydrogen-Ion Concentration</term>
<term>Salinity</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Concentration en ions d'hydrogène</term>
<term>Salinité</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Salt stress is an important environmental cue impeding poplar nitrogen nutrition. Here, we characterized the impact of salinity on proton-driven nitrate fluxes in ectomycorrhizal roots and the importance of a Hartig net for nitrate uptake. We employed two Paxillus involutus strains for root colonization: MAJ, which forms typical ectomycorrhizal structures (mantle and Hartig net), and NAU, colonizing roots with a thin, loose hyphal sheath. Fungus-colonized and noncolonized Populus × canescens were exposed to sodium chloride and used to measure root surface pH, nitrate (NO
<sub>3</sub>
<sup>-</sup>
) flux and transcription of NO
<sub>3</sub>
<sup>-</sup>
transporters (NRTs; PcNRT1.1, -1.2, -2.1), and plasmalemma proton ATPases (HAs; PcHA4, -8, -11). Paxillus colonization enhanced root NO
<sub>3</sub>
<sup>-</sup>
uptake, decreased surface pH, and stimulated NRTs and HA4 of the host regardless the presence or absence of a Hartig net. Under salt stress, noncolonized roots exhibited strong net NO
<sub>3</sub>
<sup>-</sup>
efflux, whereas beneficial effects of fungal colonization on surface pH and HAs prevented NO
<sub>3</sub>
<sup>-</sup>
loss. Inhibition of HAs abolished NO
<sub>3</sub>
<sup>-</sup>
influx under all conditions. We found that stimulation of HAs was crucial for the beneficial influence of ectomycorrhiza on NO
<sub>3</sub>
<sup>-</sup>
uptake, whereas the presence of a Hartig net was not required for improved NO
<sub>3</sub>
<sup>-</sup>
translocation. Mycorrhizas may contribute to host adaptation to salt-affected environments by keeping up NO
<sub>3</sub>
<sup>-</sup>
nutrition.</div>
</front>
</TEI>
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<DateCompleted>
<Year>2020</Year>
<Month>02</Month>
<Day>27</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>09</Month>
<Day>30</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1469-8137</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>222</Volume>
<Issue>4</Issue>
<PubDate>
<Year>2019</Year>
<Month>06</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
<ISOAbbreviation>New Phytol</ISOAbbreviation>
</Journal>
<ArticleTitle>Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net.</ArticleTitle>
<Pagination>
<MedlinePgn>1951-1964</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15740</ELocationID>
<Abstract>
<AbstractText>Salt stress is an important environmental cue impeding poplar nitrogen nutrition. Here, we characterized the impact of salinity on proton-driven nitrate fluxes in ectomycorrhizal roots and the importance of a Hartig net for nitrate uptake. We employed two Paxillus involutus strains for root colonization: MAJ, which forms typical ectomycorrhizal structures (mantle and Hartig net), and NAU, colonizing roots with a thin, loose hyphal sheath. Fungus-colonized and noncolonized Populus × canescens were exposed to sodium chloride and used to measure root surface pH, nitrate (NO
<sub>3</sub>
<sup>-</sup>
) flux and transcription of NO
<sub>3</sub>
<sup>-</sup>
transporters (NRTs; PcNRT1.1, -1.2, -2.1), and plasmalemma proton ATPases (HAs; PcHA4, -8, -11). Paxillus colonization enhanced root NO
<sub>3</sub>
<sup>-</sup>
uptake, decreased surface pH, and stimulated NRTs and HA4 of the host regardless the presence or absence of a Hartig net. Under salt stress, noncolonized roots exhibited strong net NO
<sub>3</sub>
<sup>-</sup>
efflux, whereas beneficial effects of fungal colonization on surface pH and HAs prevented NO
<sub>3</sub>
<sup>-</sup>
loss. Inhibition of HAs abolished NO
<sub>3</sub>
<sup>-</sup>
influx under all conditions. We found that stimulation of HAs was crucial for the beneficial influence of ectomycorrhiza on NO
<sub>3</sub>
<sup>-</sup>
uptake, whereas the presence of a Hartig net was not required for improved NO
<sub>3</sub>
<sup>-</sup>
translocation. Mycorrhizas may contribute to host adaptation to salt-affected environments by keeping up NO
<sub>3</sub>
<sup>-</sup>
nutrition.</AbstractText>
<CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation>
</Abstract>
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<Author ValidYN="Y">
<LastName>Sa</LastName>
<ForeName>Gang</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Gansu Provincial Key Laboratory of Aridland Crop Sciences, Gansu Agricultural University, Lanzhou, 730070, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yao</LastName>
<ForeName>Jun</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Deng</LastName>
<ForeName>Chen</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Liu</LastName>
<ForeName>Jian</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Zhang</LastName>
<ForeName>Yinan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhu</LastName>
<ForeName>Zhimei</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Yuhong</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ma</LastName>
<ForeName>Xujun</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Urat Desert-Grassland Research Station, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Science, Lanzhou, 730000, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhao</LastName>
<ForeName>Rui</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lin</LastName>
<ForeName>Shanzhi</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lu</LastName>
<ForeName>Cunfu</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Polle</LastName>
<ForeName>Andrea</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Forest Botany and Tree Physiology, University of Goettingen, Göttingen, 37077, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Shaoliang</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">0000-0001-7511-3067</Identifier>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Box 162, Beijing, 100083, China.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>03</Month>
<Day>14</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>New Phytol</MedlineTA>
<NlmUniqueID>9882884</NlmUniqueID>
<ISSNLinking>0028-646X</ISSNLinking>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
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</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009566">Nitrates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>3WHH0066W5</RegistryNumber>
<NameOfSubstance UI="D014638">Vanadates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>451W47IQ8X</RegistryNumber>
<NameOfSubstance UI="D012965">Sodium Chloride</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.7.-</RegistryNumber>
<NameOfSubstance UI="D009572">Nitrite Reductases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.7.99.4</RegistryNumber>
<NameOfSubstance UI="D050901">Nitrate Reductase</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 3.6.3.14</RegistryNumber>
<NameOfSubstance UI="D006180">Proton-Translocating ATPases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006863" MajorTopicYN="N">Hydrogen-Ion Concentration</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D026901" MajorTopicYN="N">Membrane Transport Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D050901" MajorTopicYN="N">Nitrate Reductase</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009566" MajorTopicYN="N">Nitrates</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009572" MajorTopicYN="N">Nitrite Reductases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006180" MajorTopicYN="N">Proton-Translocating ATPases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054712" MajorTopicYN="Y">Salinity</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012965" MajorTopicYN="N">Sodium Chloride</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013312" MajorTopicYN="Y">Stress, Physiological</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014638" MajorTopicYN="N">Vanadates</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Paxillus involutus </Keyword>
<Keyword MajorTopicYN="Y">MAJ</Keyword>
<Keyword MajorTopicYN="Y">NAU</Keyword>
<Keyword MajorTopicYN="Y">NO3− flux</Keyword>
<Keyword MajorTopicYN="Y">NRTs</Keyword>
<Keyword MajorTopicYN="Y">NaCl</Keyword>
<Keyword MajorTopicYN="Y">Poplar</Keyword>
<Keyword MajorTopicYN="Y">pH</Keyword>
</KeywordList>
</MedlineCitation>
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<Month>09</Month>
<Day>04</Day>
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<Month>02</Month>
<Day>01</Day>
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<name sortKey="Zhang, Yinan" sort="Zhang, Yinan" uniqKey="Zhang Y" first="Yinan" last="Zhang">Yinan Zhang</name>
<name sortKey="Zhang, Yuhong" sort="Zhang, Yuhong" uniqKey="Zhang Y" first="Yuhong" last="Zhang">Yuhong Zhang</name>
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