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Paxillus involutus-Facilitated Cd2+ Influx through Plasma Membrane Ca2+-Permeable Channels Is Stimulated by H2O2 and H+-ATPase in Ectomycorrhizal Populus × canescens under Cadmium Stress.

Identifieur interne : 001A34 ( Main/Exploration ); précédent : 001A33; suivant : 001A35

Paxillus involutus-Facilitated Cd2+ Influx through Plasma Membrane Ca2+-Permeable Channels Is Stimulated by H2O2 and H+-ATPase in Ectomycorrhizal Populus × canescens under Cadmium Stress.

Auteurs : Yuhong Zhang [République populaire de Chine] ; Gang Sa [République populaire de Chine] ; Yinan Zhang [République populaire de Chine] ; Zhimei Zhu [République populaire de Chine] ; Shurong Deng [République populaire de Chine] ; Jian Sun [République populaire de Chine] ; Nianfei Li [République populaire de Chine] ; Jing Li [République populaire de Chine] ; Jun Yao [République populaire de Chine] ; Nan Zhao [République populaire de Chine] ; Rui Zhao [République populaire de Chine] ; Xujun Ma [République populaire de Chine] ; Andrea Polle [Allemagne] ; Shaoliang Chen [République populaire de Chine]

Source :

RBID : pubmed:28111579

Abstract

Using a Non-invasive Micro-test Technique, flux profiles of Cd2+, Ca2+, and H+ were investigated in axenically grown cultures of two strains of Paxillus involutus (MAJ and NAU), ectomycorrhizae formed by these fungi with the woody Cd2+-hyperaccumulator, Populus × canescens, and non-mycorrhizal (NM) roots. The influx of Cd2+ increased in fungal mycelia, NM and ectomycorrhizal (EM) roots upon a 40-min shock, after short-term (ST, 24 h), or long-term (LT, 7 days) exposure to a hydroponic environment of 50 μM CdCl2. Cd2+ treatments (shock, ST, and LT) decreased Ca2+ influx in NM and EM roots but led to an enhanced influx of Ca2+ in axenically grown EM cultures of the two P. involutus isolates. The susceptibility of Cd2+ flux to typical Ca2+ channel blockers (LaCl3, GdCl3, verapamil, and TEA) in fungal mycelia and poplar roots indicated that the Cd2+ entry occurred mainly through Ca2+-permeable channels in the plasma membrane (PM). Cd2+ treatment resulted in H2O2 production. H2O2 exposure accelerated the entry of Cd2+ and Ca2+ in NM and EM roots. Cd2+ further stimulated H+ pumping activity benefiting NM and EM roots to maintain an acidic environment, which favored the entry of Cd2+ across the PM. A scavenger of reactive oxygen species, DMTU, and an inhibitor of PM H+-ATPase, orthovanadate, decreased Ca2+ and Cd2+ influx in NM and EM roots, suggesting that the entry of Cd2+ through Ca2+-permeable channels is stimulated by H2O2 and H+ pumps. Compared to NM roots, EM roots exhibited higher Cd2+-fluxes under shock, ST, and LT Cd2+ treatments. We conclude that ectomycorrhizal P. × canescens roots retained a pronounced H2O2 production and a high H+-pumping activity, which activated PM Ca2+ channels and thus facilitated a high influx of Cd2+ under Cd2+ stress.

DOI: 10.3389/fpls.2016.01975
PubMed: 28111579
PubMed Central: PMC5216326


Affiliations:


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Le document en format XML

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<i>Paxillus involutus</i>
-Facilitated Cd
<sup>2+</sup>
Influx through Plasma Membrane Ca
<sup>2+</sup>
-Permeable Channels Is Stimulated by H
<sub>2</sub>
O
<sub>2</sub>
and H
<sup>+</sup>
-ATPase in Ectomycorrhizal
<i>Populus</i>
×
<i>canescens</i>
under Cadmium Stress.</title>
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<country xml:lang="fr">République populaire de Chine</country>
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<name sortKey="Yao, Jun" sort="Yao, Jun" uniqKey="Yao J" first="Jun" last="Yao">Jun Yao</name>
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<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
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<title xml:lang="en">
<i>Paxillus involutus</i>
-Facilitated Cd
<sup>2+</sup>
Influx through Plasma Membrane Ca
<sup>2+</sup>
-Permeable Channels Is Stimulated by H
<sub>2</sub>
O
<sub>2</sub>
and H
<sup>+</sup>
-ATPase in Ectomycorrhizal
<i>Populus</i>
×
<i>canescens</i>
under Cadmium Stress.</title>
<author>
<name sortKey="Zhang, Yuhong" sort="Zhang, Yuhong" uniqKey="Zhang Y" first="Yuhong" last="Zhang">Yuhong Zhang</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sa, Gang" sort="Sa, Gang" uniqKey="Sa G" first="Gang" last="Sa">Gang Sa</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Yinan" sort="Zhang, Yinan" uniqKey="Zhang Y" first="Yinan" last="Zhang">Yinan Zhang</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Zhu, Zhimei" sort="Zhu, Zhimei" uniqKey="Zhu Z" first="Zhimei" last="Zhu">Zhimei Zhu</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Deng, Shurong" sort="Deng, Shurong" uniqKey="Deng S" first="Shurong" last="Deng">Shurong Deng</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sun, Jian" sort="Sun, Jian" uniqKey="Sun J" first="Jian" last="Sun">Jian Sun</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Life Science, Jiangsu Normal University Xuzhou, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Life Science, Jiangsu Normal University Xuzhou</wicri:regionArea>
<wicri:noRegion>Jiangsu Normal University Xuzhou</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Li, Nianfei" sort="Li, Nianfei" uniqKey="Li N" first="Nianfei" last="Li">Nianfei Li</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Li, Jing" sort="Li, Jing" uniqKey="Li J" first="Jing" last="Li">Jing Li</name>
<affiliation wicri:level="1">
<nlm:affiliation>School of Computer Science and Technology, Henan Polytechnic University Jiaozuo, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>School of Computer Science and Technology, Henan Polytechnic University Jiaozuo</wicri:regionArea>
<wicri:noRegion>Henan Polytechnic University Jiaozuo</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Yao, Jun" sort="Yao, Jun" uniqKey="Yao J" first="Jun" last="Yao">Jun Yao</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Zhao, Nan" sort="Zhao, Nan" uniqKey="Zhao N" first="Nan" last="Zhao">Nan Zhao</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Zhao, Rui" sort="Zhao, Rui" uniqKey="Zhao R" first="Rui" last="Zhao">Rui Zhao</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Ma, Xujun" sort="Ma, Xujun" uniqKey="Ma X" first="Xujun" last="Ma">Xujun Ma</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Polle, Andrea" sort="Polle, Andrea" uniqKey="Polle A" first="Andrea" last="Polle">Andrea Polle</name>
<affiliation wicri:level="1">
<nlm:affiliation>Büsgen-Institut, Forstbotanik und Baumphysiologie, Georg-August-Universität Göttingen Göttingen, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Büsgen-Institut, Forstbotanik und Baumphysiologie, Georg-August-Universität Göttingen Göttingen</wicri:regionArea>
<wicri:noRegion>Georg-August-Universität Göttingen Göttingen</wicri:noRegion>
<wicri:noRegion>Georg-August-Universität Göttingen Göttingen</wicri:noRegion>
<wicri:noRegion>Georg-August-Universität Göttingen Göttingen</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Chen, Shaoliang" sort="Chen, Shaoliang" uniqKey="Chen S" first="Shaoliang" last="Chen">Shaoliang Chen</name>
<affiliation wicri:level="1">
<nlm:affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Biological Sciences and Technology, Beijing Forestry University Beijing</wicri:regionArea>
<wicri:noRegion>Beijing Forestry University Beijing</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Frontiers in plant science</title>
<idno type="ISSN">1664-462X</idno>
<imprint>
<date when="2016" type="published">2016</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">Using a Non-invasive Micro-test Technique, flux profiles of Cd
<sup>2+</sup>
, Ca
<sup>2+</sup>
, and H
<sup>+</sup>
were investigated in axenically grown cultures of two strains of
<i>Paxillus involutus</i>
(MAJ and NAU), ectomycorrhizae formed by these fungi with the woody Cd
<sup>2+</sup>
-hyperaccumulator,
<i>Populus</i>
×
<i>canescens</i>
, and non-mycorrhizal (NM) roots. The influx of Cd
<sup>2+</sup>
increased in fungal mycelia, NM and ectomycorrhizal (EM) roots upon a 40-min shock, after short-term (ST, 24 h), or long-term (LT, 7 days) exposure to a hydroponic environment of 50 μM CdCl
<sub>2</sub>
. Cd
<sup>2+</sup>
treatments (shock, ST, and LT) decreased Ca
<sup>2+</sup>
influx in NM and EM roots but led to an enhanced influx of Ca
<sup>2+</sup>
in axenically grown EM cultures of the two
<i>P. involutus</i>
isolates. The susceptibility of Cd
<sup>2+</sup>
flux to typical Ca
<sup>2+</sup>
channel blockers (LaCl
<sub>3</sub>
, GdCl
<sub>3</sub>
, verapamil, and TEA) in fungal mycelia and poplar roots indicated that the Cd
<sup>2+</sup>
entry occurred mainly through Ca
<sup>2+</sup>
-permeable channels in the plasma membrane (PM). Cd
<sup>2+</sup>
treatment resulted in H
<sub>2</sub>
O
<sub>2</sub>
production. H
<sub>2</sub>
O
<sub>2</sub>
exposure accelerated the entry of Cd
<sup>2+</sup>
and Ca
<sup>2+</sup>
in NM and EM roots. Cd
<sup>2+</sup>
further stimulated H
<sup>+</sup>
pumping activity benefiting NM and EM roots to maintain an acidic environment, which favored the entry of Cd
<sup>2+</sup>
across the PM. A scavenger of reactive oxygen species, DMTU, and an inhibitor of PM H
<sup>+</sup>
-ATPase, orthovanadate, decreased Ca
<sup>2+</sup>
and Cd
<sup>2+</sup>
influx in NM and EM roots, suggesting that the entry of Cd
<sup>2+</sup>
through Ca
<sup>2+</sup>
-permeable channels is stimulated by H
<sub>2</sub>
O
<sub>2</sub>
and H
<sup>+</sup>
pumps. Compared to NM roots, EM roots exhibited higher Cd
<sup>2+</sup>
-fluxes under shock, ST, and LT Cd
<sup>2+</sup>
treatments. We conclude that ectomycorrhizal
<i>P.</i>
×
<i>canescens</i>
roots retained a pronounced H
<sub>2</sub>
O
<sub>2</sub>
production and a high H
<sup>+</sup>
-pumping activity, which activated PM Ca
<sup>2+</sup>
channels and thus facilitated a high influx of Cd
<sup>2+</sup>
under Cd
<sup>2+</sup>
stress.</div>
</front>
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<DateRevised>
<Year>2020</Year>
<Month>10</Month>
<Day>01</Day>
</DateRevised>
<Article PubModel="Electronic-eCollection">
<Journal>
<ISSN IssnType="Print">1664-462X</ISSN>
<JournalIssue CitedMedium="Print">
<Volume>7</Volume>
<PubDate>
<Year>2016</Year>
</PubDate>
</JournalIssue>
<Title>Frontiers in plant science</Title>
<ISOAbbreviation>Front Plant Sci</ISOAbbreviation>
</Journal>
<ArticleTitle>
<i>Paxillus involutus</i>
-Facilitated Cd
<sup>2+</sup>
Influx through Plasma Membrane Ca
<sup>2+</sup>
-Permeable Channels Is Stimulated by H
<sub>2</sub>
O
<sub>2</sub>
and H
<sup>+</sup>
-ATPase in Ectomycorrhizal
<i>Populus</i>
×
<i>canescens</i>
under Cadmium Stress.</ArticleTitle>
<Pagination>
<MedlinePgn>1975</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2016.01975</ELocationID>
<Abstract>
<AbstractText>Using a Non-invasive Micro-test Technique, flux profiles of Cd
<sup>2+</sup>
, Ca
<sup>2+</sup>
, and H
<sup>+</sup>
were investigated in axenically grown cultures of two strains of
<i>Paxillus involutus</i>
(MAJ and NAU), ectomycorrhizae formed by these fungi with the woody Cd
<sup>2+</sup>
-hyperaccumulator,
<i>Populus</i>
×
<i>canescens</i>
, and non-mycorrhizal (NM) roots. The influx of Cd
<sup>2+</sup>
increased in fungal mycelia, NM and ectomycorrhizal (EM) roots upon a 40-min shock, after short-term (ST, 24 h), or long-term (LT, 7 days) exposure to a hydroponic environment of 50 μM CdCl
<sub>2</sub>
. Cd
<sup>2+</sup>
treatments (shock, ST, and LT) decreased Ca
<sup>2+</sup>
influx in NM and EM roots but led to an enhanced influx of Ca
<sup>2+</sup>
in axenically grown EM cultures of the two
<i>P. involutus</i>
isolates. The susceptibility of Cd
<sup>2+</sup>
flux to typical Ca
<sup>2+</sup>
channel blockers (LaCl
<sub>3</sub>
, GdCl
<sub>3</sub>
, verapamil, and TEA) in fungal mycelia and poplar roots indicated that the Cd
<sup>2+</sup>
entry occurred mainly through Ca
<sup>2+</sup>
-permeable channels in the plasma membrane (PM). Cd
<sup>2+</sup>
treatment resulted in H
<sub>2</sub>
O
<sub>2</sub>
production. H
<sub>2</sub>
O
<sub>2</sub>
exposure accelerated the entry of Cd
<sup>2+</sup>
and Ca
<sup>2+</sup>
in NM and EM roots. Cd
<sup>2+</sup>
further stimulated H
<sup>+</sup>
pumping activity benefiting NM and EM roots to maintain an acidic environment, which favored the entry of Cd
<sup>2+</sup>
across the PM. A scavenger of reactive oxygen species, DMTU, and an inhibitor of PM H
<sup>+</sup>
-ATPase, orthovanadate, decreased Ca
<sup>2+</sup>
and Cd
<sup>2+</sup>
influx in NM and EM roots, suggesting that the entry of Cd
<sup>2+</sup>
through Ca
<sup>2+</sup>
-permeable channels is stimulated by H
<sub>2</sub>
O
<sub>2</sub>
and H
<sup>+</sup>
pumps. Compared to NM roots, EM roots exhibited higher Cd
<sup>2+</sup>
-fluxes under shock, ST, and LT Cd
<sup>2+</sup>
treatments. We conclude that ectomycorrhizal
<i>P.</i>
×
<i>canescens</i>
roots retained a pronounced H
<sub>2</sub>
O
<sub>2</sub>
production and a high H
<sup>+</sup>
-pumping activity, which activated PM Ca
<sup>2+</sup>
channels and thus facilitated a high influx of Cd
<sup>2+</sup>
under Cd
<sup>2+</sup>
stress.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Yuhong</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sa</LastName>
<ForeName>Gang</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Yinan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhu</LastName>
<ForeName>Zhimei</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Deng</LastName>
<ForeName>Shurong</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sun</LastName>
<ForeName>Jian</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>College of Life Science, Jiangsu Normal University Xuzhou, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Nianfei</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Jing</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>School of Computer Science and Technology, Henan Polytechnic University Jiaozuo, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yao</LastName>
<ForeName>Jun</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhao</LastName>
<ForeName>Nan</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhao</LastName>
<ForeName>Rui</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ma</LastName>
<ForeName>Xujun</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Polle</LastName>
<ForeName>Andrea</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Büsgen-Institut, Forstbotanik und Baumphysiologie, Georg-August-Universität Göttingen Göttingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Shaoliang</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>College of Biological Sciences and Technology, Beijing Forestry University Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>01</Month>
<Day>06</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Switzerland</Country>
<MedlineTA>Front Plant Sci</MedlineTA>
<NlmUniqueID>101568200</NlmUniqueID>
<ISSNLinking>1664-462X</ISSNLinking>
</MedlineJournalInfo>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Cd2+-hyperaccumulator</Keyword>
<Keyword MajorTopicYN="N">MAJ</Keyword>
<Keyword MajorTopicYN="N">NAU</Keyword>
<Keyword MajorTopicYN="N">NMT</Keyword>
<Keyword MajorTopicYN="N">Paxillus involutus</Keyword>
<Keyword MajorTopicYN="N">ectomycorrhizal fungi</Keyword>
<Keyword MajorTopicYN="N">poplar</Keyword>
</KeywordList>
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<Year>2016</Year>
<Month>10</Month>
<Day>14</Day>
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<Year>2016</Year>
<Month>12</Month>
<Day>13</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2017</Year>
<Month>1</Month>
<Day>24</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<Year>2017</Year>
<Month>1</Month>
<Day>24</Day>
<Hour>6</Hour>
<Minute>1</Minute>
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