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Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants.

Identifieur interne : 000066 ( Main/Corpus ); précédent : 000065; suivant : 000067

Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants.

Auteurs : Shuangshuang Wang ; Aiqun Chen ; Kun Xie ; Xiaofeng Yang ; Zhenzhen Luo ; Jiadong Chen ; Dechao Zeng ; Yuhan Ren ; Congfan Yang ; Lingxiao Wang ; Huimin Feng ; Damar Lizbeth L Pez-Arredondo ; Luis Rafael Herrera-Estrella ; Guohua Xu

Source :

RBID : pubmed:32586957

English descriptors

Abstract

Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungus Rhizophagus irregularis remarkably promoted rice (Oryza sativa) growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO3- supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter gene OsNPF4.5 in rice roots, and its orthologs ZmNPF4.5 in Zea mays and SbNPF4.5 in Sorghum bicolor OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO3- transport activity when expressed in Xenopus laevis oocytes. Moreover, knockout of OsNPF4.5 resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO3- was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO3- acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species.

DOI: 10.1073/pnas.2000926117
PubMed: 32586957
PubMed Central: PMC7368293

Links to Exploration step

pubmed:32586957

Le document en format XML

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<name sortKey="L Pez Arredondo, Damar Lizbeth" sort="L Pez Arredondo, Damar Lizbeth" uniqKey="L Pez Arredondo D" first="Damar Lizbeth" last="L Pez-Arredondo">Damar Lizbeth L Pez-Arredondo</name>
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<nlm:affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<name sortKey="Zeng, Dechao" sort="Zeng, Dechao" uniqKey="Zeng D" first="Dechao" last="Zeng">Dechao Zeng</name>
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<name sortKey="Ren, Yuhan" sort="Ren, Yuhan" uniqKey="Ren Y" first="Yuhan" last="Ren">Yuhan Ren</name>
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<name sortKey="Yang, Congfan" sort="Yang, Congfan" uniqKey="Yang C" first="Congfan" last="Yang">Congfan Yang</name>
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<nlm:affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
</affiliation>
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<name sortKey="Wang, Lingxiao" sort="Wang, Lingxiao" uniqKey="Wang L" first="Lingxiao" last="Wang">Lingxiao Wang</name>
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<nlm:affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<name sortKey="Feng, Huimin" sort="Feng, Huimin" uniqKey="Feng H" first="Huimin" last="Feng">Huimin Feng</name>
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<nlm:affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
</affiliation>
</author>
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<name sortKey="L Pez Arredondo, Damar Lizbeth" sort="L Pez Arredondo, Damar Lizbeth" uniqKey="L Pez Arredondo D" first="Damar Lizbeth" last="L Pez-Arredondo">Damar Lizbeth L Pez-Arredondo</name>
<affiliation>
<nlm:affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
</affiliation>
<affiliation>
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</affiliation>
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<name sortKey="Herrera Estrella, Luis Rafael" sort="Herrera Estrella, Luis Rafael" uniqKey="Herrera Estrella L" first="Luis Rafael" last="Herrera-Estrella">Luis Rafael Herrera-Estrella</name>
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<nlm:affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China; chenaq8@njau.edu.cn ghxu@njau.edu.cn luis.herrera-estrella@ttu.edu.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Sciences, Texas Tech University, Lubbock, TX 79409.</nlm:affiliation>
</affiliation>
<affiliation>
<nlm:affiliation>Laboratorio Nacional de Genómica para la Biodiversidad, Unidad de Genómica Avanzada del Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36500 Irapuato, Mexico.</nlm:affiliation>
</affiliation>
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<term>Anion Transport Proteins (genetics)</term>
<term>Anion Transport Proteins (metabolism)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Glomeromycota (physiology)</term>
<term>Mycorrhizae (physiology)</term>
<term>Nitrates (metabolism)</term>
<term>Nitrogen (metabolism)</term>
<term>Oryza (genetics)</term>
<term>Oryza (growth & development)</term>
<term>Oryza (metabolism)</term>
<term>Oryza (microbiology)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Roots (genetics)</term>
<term>Plant Roots (growth & development)</term>
<term>Plant Roots (metabolism)</term>
<term>Plant Roots (microbiology)</term>
<term>Sorghum (genetics)</term>
<term>Sorghum (metabolism)</term>
<term>Sorghum (microbiology)</term>
<term>Zea mays (genetics)</term>
<term>Zea mays (metabolism)</term>
<term>Zea mays (microbiology)</term>
</keywords>
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<term>Anion Transport Proteins</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Anion Transport Proteins</term>
<term>Nitrates</term>
<term>Nitrogen</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Oryza</term>
<term>Plant Roots</term>
<term>Sorghum</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Oryza</term>
<term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Oryza</term>
<term>Plant Roots</term>
<term>Sorghum</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Oryza</term>
<term>Plant Roots</term>
<term>Sorghum</term>
<term>Zea mays</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Glomeromycota</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
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<div type="abstract" xml:lang="en">Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungus
<i>Rhizophagus irregularis</i>
remarkably promoted rice (
<i>Oryza sativa</i>
) growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO
<sub>3</sub>
<sup>-</sup>
supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter gene
<i>OsNPF4.5</i>
in rice roots, and its orthologs
<i>ZmNPF4.5</i>
in
<i>Zea mays</i>
and
<i>SbNPF4.5</i>
in
<i>Sorghum bicolor</i>
OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO
<sub>3</sub>
<sup>-</sup>
transport activity when expressed in
<i>Xenopus laevis</i>
oocytes. Moreover, knockout of
<i>OsNPF4.5</i>
resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO
<sub>3</sub>
<sup>-</sup>
was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO
<sub>3</sub>
<sup>-</sup>
acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species.</div>
</front>
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<Day>21</Day>
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<DateRevised>
<Year>2020</Year>
<Month>09</Month>
<Day>21</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>117</Volume>
<Issue>28</Issue>
<PubDate>
<Year>2020</Year>
<Month>07</Month>
<Day>14</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants.</ArticleTitle>
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<Abstract>
<AbstractText>Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungus
<i>Rhizophagus irregularis</i>
remarkably promoted rice (
<i>Oryza sativa</i>
) growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO
<sub>3</sub>
<sup>-</sup>
supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter gene
<i>OsNPF4.5</i>
in rice roots, and its orthologs
<i>ZmNPF4.5</i>
in
<i>Zea mays</i>
and
<i>SbNPF4.5</i>
in
<i>Sorghum bicolor</i>
OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO
<sub>3</sub>
<sup>-</sup>
transport activity when expressed in
<i>Xenopus laevis</i>
oocytes. Moreover, knockout of
<i>OsNPF4.5</i>
resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO
<sub>3</sub>
<sup>-</sup>
was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO
<sub>3</sub>
<sup>-</sup>
acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species.</AbstractText>
<CopyrightInformation>Copyright © 2020 the Author(s). Published by PNAS.</CopyrightInformation>
</Abstract>
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<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Shuangshuang</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<LastName>Chen</LastName>
<ForeName>Aiqun</ForeName>
<Initials>A</Initials>
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<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China; chenaq8@njau.edu.cn ghxu@njau.edu.cn luis.herrera-estrella@ttu.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<LastName>Xie</LastName>
<ForeName>Kun</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<ForeName>Xiaofeng</ForeName>
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<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<ForeName>Zhenzhen</ForeName>
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<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Jiadong</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<ForeName>Dechao</ForeName>
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<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<LastName>Ren</LastName>
<ForeName>Yuhan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Yang</LastName>
<ForeName>Congfan</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
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<ForeName>Lingxiao</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Feng</LastName>
<ForeName>Huimin</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>López-Arredondo</LastName>
<ForeName>Damar Lizbeth</ForeName>
<Initials>DL</Initials>
<Identifier Source="ORCID">0000-0001-7389-3143</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Sciences, Texas Tech University, Lubbock, TX 79409.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Herrera-Estrella</LastName>
<ForeName>Luis Rafael</ForeName>
<Initials>LR</Initials>
<Identifier Source="ORCID">0000-0001-7936-3856</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China; chenaq8@njau.edu.cn ghxu@njau.edu.cn luis.herrera-estrella@ttu.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Sciences, Texas Tech University, Lubbock, TX 79409.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratorio Nacional de Genómica para la Biodiversidad, Unidad de Genómica Avanzada del Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36500 Irapuato, Mexico.</Affiliation>
</AffiliationInfo>
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<LastName>Xu</LastName>
<ForeName>Guohua</ForeName>
<Initials>G</Initials>
<Identifier Source="ORCID">0000-0002-3283-2392</Identifier>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, 210095 Nanjing, China; chenaq8@njau.edu.cn ghxu@njau.edu.cn luis.herrera-estrella@ttu.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Ministry of Agriculture, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>06</Month>
<Day>25</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
</MedlineJournalInfo>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D027321">Anion Transport Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009566">Nitrates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C078921">nitrate transporters</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>N762921K75</RegistryNumber>
<NameOfSubstance UI="D009584">Nitrogen</NameOfSubstance>
</Chemical>
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<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D027321" MajorTopicYN="N">Anion Transport Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009566" MajorTopicYN="N">Nitrates</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D009584" MajorTopicYN="N">Nitrogen</DescriptorName>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012275" MajorTopicYN="N">Oryza</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D045868" MajorTopicYN="N">Sorghum</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003313" MajorTopicYN="N">Zea mays</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<Keyword MajorTopicYN="Y">OsNPF4.5</Keyword>
<Keyword MajorTopicYN="Y">RNA sequencing</Keyword>
<Keyword MajorTopicYN="Y">arbuscular mycorrhiza</Keyword>
<Keyword MajorTopicYN="Y">nitrate transporter</Keyword>
<Keyword MajorTopicYN="Y">nitrogen uptake</Keyword>
</KeywordList>
<CoiStatement>The authors declare no competing interest.</CoiStatement>
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<Citation>Plant Cell Physiol. 2017 Jun 1;58(6):1003-1017</Citation>
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