Exogenous GABA promotes adaptation and growth by altering the carbon and nitrogen metabolic flux in poplar seedlings under low nitrogen conditions.
Identifieur interne : 000410 ( Main/Exploration ); précédent : 000409; suivant : 000411Exogenous GABA promotes adaptation and growth by altering the carbon and nitrogen metabolic flux in poplar seedlings under low nitrogen conditions.
Auteurs : Wei Chen [République populaire de Chine] ; Chen Meng [Allemagne] ; Jing Ji [République populaire de Chine] ; Mai-He Li [Suisse, République populaire de Chine] ; Xiaoman Zhang ; Yanyan Wu [République populaire de Chine] ; Tiantian Xie [République populaire de Chine] ; Changjian Du [République populaire de Chine] ; Jiacheng Sun [République populaire de Chine] ; Zeping Jiang [République populaire de Chine] ; Shengqing Shi [République populaire de Chine]Source :
- Tree physiology [ 1758-4469 ] ; 2020.
Abstract
Nitrogen (N) deficiency adversely affects tree growth. Additionally, γ-aminobutyric acid (GABA) is closely associated with growth and stress responses because of its effects on carbon (C) and N metabolism. However, little is known about its roles related to plant adaptations to N-deficient conditions. In this study, we analyzed the effects of GABA (0, 2, and 10 mM) applications on the growth traits and physiological responses of poplar (Populus alba × Populus glandulosa '84 K') seedlings under high N (HN) and low N (LN) conditions. We found that the added GABA interacted with N to affect more than half of the studied parameters, with greater effects in LN plants than in HN plants. Under LN conditions, the GABA application tended to increase poplar growth, accompanied by increased xylem fiber cell length and xylem width. In stems, exogenous GABA increased the abundance of non-structural carbohydrates (starch and sugars) and tricarboxylic acid cycle intermediates (succinate, malate, and citrate), but had the opposite effect on the structural C contents (hemicellulose and lignin). Meanwhile, exogenous GABA increased the total soluble protein contents in leaves and stems, accompanied by significant increases in nitrate reductase, nitrite reductase, and glutamine synthetase activities in leaves, but significant decreases in those (except for the increased glutamate synthetase activity) in stems. A multiple factorial analysis indicated that the nitrate assimilation pathway substantially influences poplar survival and growth in the presence of GABA under LN conditions. Interestingly, GABA applications also considerably attenuated the LN-induced increase in the activities of leaf antioxidant enzymes, including peroxidase and catalase, implying that GABA may regulate the relative allocation of C and N for growth activities by decreasing the energy cost associated with stress defense. Our results suggest that GABA enhances poplar growth and adaptation by regulating the C and N metabolic flux under N-deficient conditions.
DOI: 10.1093/treephys/tpaa101
PubMed: 32776117
Affiliations:
- Allemagne, République populaire de Chine, Suisse
- Bavière, District de Haute-Bavière, Dongbei, Jilin
- Changchun, Munich, Pékin
- Université technique de Munich
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first="Yanyan" last="Wu">Yanyan Wu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xie, Tiantian" sort="Xie, Tiantian" uniqKey="Xie T" first="Tiantian" last="Xie">Tiantian Xie</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Du, Changjian" sort="Du, Changjian" uniqKey="Du C" first="Changjian" last="Du">Changjian Du</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the 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Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Meng, Chen" sort="Meng, Chen" uniqKey="Meng C" first="Chen" last="Meng">Chen Meng</name><affiliation wicri:level="4"><nlm:affiliation>Bavarian Center for Biomolecular Mass Spectrometry, Technische Universität München, Freising 85354, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Bavarian Center for Biomolecular Mass Spectrometry, Technische Universität München, Freising 85354</wicri:regionArea><wicri:noRegion>85354</wicri:noRegion><orgName type="university">Université technique de Munich</orgName><placeName><settlement type="city">Munich</settlement><region type="land" nuts="1">Bavière</region><region type="district" nuts="2">District de Haute-Bavière</region></placeName></affiliation></author><author><name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Li, Mai He" sort="Li, Mai He" uniqKey="Li M" first="Mai-He" last="Li">Mai-He Li</name><affiliation wicri:level="1"><nlm:affiliation>Forest dynamics, Swiss Federal Research Institute WSL, Zuercherstrasse 111, CH-8903 Birmensdorf, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Forest dynamics, Swiss Federal Research Institute WSL, Zuercherstrasse 111, CH-8903 Birmensdorf</wicri:regionArea><wicri:noRegion>CH-8903 Birmensdorf</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Erguna Forest-Steppe Ecotone Research Station, CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Erguna Forest-Steppe Ecotone Research Station, CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016</wicri:regionArea><wicri:noRegion>Shenyang 110016</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Geographical Processes and Ecological Security in Changbai Mountains, Ministry of Education, School of Geographical Sciences, Northeast Normal University, Changchun 130024, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Geographical Processes and Ecological Security in Changbai Mountains, Ministry of Education, School of Geographical Sciences, Northeast Normal University, Changchun 130024</wicri:regionArea><placeName><settlement type="city">Changchun</settlement><region type="province">Jilin</region><region type="groupement">Dongbei</region></placeName></affiliation></author><author><name sortKey="Zhang, Xiaoman" sort="Zhang, Xiaoman" uniqKey="Zhang X" first="Xiaoman" last="Zhang">Xiaoman Zhang</name><affiliation><nlm:affiliation>College of Landscape Architecture, Hebei Agricultural University.</nlm:affiliation><wicri:noCountry code="subField">Hebei Agricultural University</wicri:noCountry></affiliation></author><author><name sortKey="Wu, Yanyan" sort="Wu, Yanyan" uniqKey="Wu Y" first="Yanyan" last="Wu">Yanyan Wu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xie, Tiantian" sort="Xie, Tiantian" uniqKey="Xie T" first="Tiantian" last="Xie">Tiantian Xie</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Du, Changjian" sort="Du, Changjian" uniqKey="Du C" first="Changjian" last="Du">Changjian Du</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Sun, Jiacheng" sort="Sun, Jiacheng" uniqKey="Sun J" first="Jiacheng" last="Sun">Jiacheng Sun</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Jiang, Zeping" sort="Jiang, Zeping" uniqKey="Jiang Z" first="Zeping" last="Jiang">Zeping Jiang</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Ecology and Environment of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Ecology and Environment of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Shi, Shengqing" sort="Shi, Shengqing" uniqKey="Shi S" first="Shengqing" last="Shi">Shengqing Shi</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">Tree physiology</title><idno type="eISSN">1758-4469</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Nitrogen (N) deficiency adversely affects tree growth. Additionally, γ-aminobutyric acid (GABA) is closely associated with growth and stress responses because of its effects on carbon (C) and N metabolism. However, little is known about its roles related to plant adaptations to N-deficient conditions. In this study, we analyzed the effects of GABA (0, 2, and 10 mM) applications on the growth traits and physiological responses of poplar (Populus alba × Populus glandulosa '84 K') seedlings under high N (HN) and low N (LN) conditions. We found that the added GABA interacted with N to affect more than half of the studied parameters, with greater effects in LN plants than in HN plants. Under LN conditions, the GABA application tended to increase poplar growth, accompanied by increased xylem fiber cell length and xylem width. In stems, exogenous GABA increased the abundance of non-structural carbohydrates (starch and sugars) and tricarboxylic acid cycle intermediates (succinate, malate, and citrate), but had the opposite effect on the structural C contents (hemicellulose and lignin). Meanwhile, exogenous GABA increased the total soluble protein contents in leaves and stems, accompanied by significant increases in nitrate reductase, nitrite reductase, and glutamine synthetase activities in leaves, but significant decreases in those (except for the increased glutamate synthetase activity) in stems. A multiple factorial analysis indicated that the nitrate assimilation pathway substantially influences poplar survival and growth in the presence of GABA under LN conditions. Interestingly, GABA applications also considerably attenuated the LN-induced increase in the activities of leaf antioxidant enzymes, including peroxidase and catalase, implying that GABA may regulate the relative allocation of C and N for growth activities by decreasing the energy cost associated with stress defense. Our results suggest that GABA enhances poplar growth and adaptation by regulating the C and N metabolic flux under N-deficient conditions.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32776117</PMID><DateRevised><Year>2020</Year><Month>08</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1758-4469</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Aug</Month><Day>08</Day></PubDate></JournalIssue><Title>Tree physiology</Title><ISOAbbreviation>Tree Physiol</ISOAbbreviation></Journal><ArticleTitle>Exogenous GABA promotes adaptation and growth by altering the carbon and nitrogen metabolic flux in poplar seedlings under low nitrogen conditions.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">tpaa101</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1093/treephys/tpaa101</ELocationID><Abstract><AbstractText>Nitrogen (N) deficiency adversely affects tree growth. Additionally, γ-aminobutyric acid (GABA) is closely associated with growth and stress responses because of its effects on carbon (C) and N metabolism. However, little is known about its roles related to plant adaptations to N-deficient conditions. In this study, we analyzed the effects of GABA (0, 2, and 10 mM) applications on the growth traits and physiological responses of poplar (Populus alba × Populus glandulosa '84 K') seedlings under high N (HN) and low N (LN) conditions. We found that the added GABA interacted with N to affect more than half of the studied parameters, with greater effects in LN plants than in HN plants. Under LN conditions, the GABA application tended to increase poplar growth, accompanied by increased xylem fiber cell length and xylem width. In stems, exogenous GABA increased the abundance of non-structural carbohydrates (starch and sugars) and tricarboxylic acid cycle intermediates (succinate, malate, and citrate), but had the opposite effect on the structural C contents (hemicellulose and lignin). Meanwhile, exogenous GABA increased the total soluble protein contents in leaves and stems, accompanied by significant increases in nitrate reductase, nitrite reductase, and glutamine synthetase activities in leaves, but significant decreases in those (except for the increased glutamate synthetase activity) in stems. A multiple factorial analysis indicated that the nitrate assimilation pathway substantially influences poplar survival and growth in the presence of GABA under LN conditions. Interestingly, GABA applications also considerably attenuated the LN-induced increase in the activities of leaf antioxidant enzymes, including peroxidase and catalase, implying that GABA may regulate the relative allocation of C and N for growth activities by decreasing the energy cost associated with stress defense. Our results suggest that GABA enhances poplar growth and adaptation by regulating the C and N metabolic flux under N-deficient conditions.</AbstractText><CopyrightInformation>© The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Wei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meng</LastName><ForeName>Chen</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Bavarian Center for Biomolecular Mass Spectrometry, Technische Universität München, Freising 85354, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ji</LastName><ForeName>Jing</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Mai-He</ForeName><Initials>MH</Initials><AffiliationInfo><Affiliation>Forest dynamics, Swiss Federal Research Institute WSL, Zuercherstrasse 111, CH-8903 Birmensdorf, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Erguna Forest-Steppe Ecotone Research Station, CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Geographical Processes and Ecological Security in Changbai Mountains, Ministry of Education, School of Geographical Sciences, Northeast Normal University, Changchun 130024, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiaoman</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Landscape Architecture, Hebei Agricultural University.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Yanyan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xie</LastName><ForeName>Tiantian</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Changjian</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Jiacheng</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Zeping</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Ecology and Environment of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Shengqing</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, the Chinese Academy of Forestry, 1958 Box, Beijing 100091, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>08</Day></ArticleDate></Article><MedlineJournalInfo><Country>Canada</Country><MedlineTA>Tree Physiol</MedlineTA><NlmUniqueID>100955338</NlmUniqueID><ISSNLinking>0829-318X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus
</Keyword><Keyword MajorTopicYN="N">carbon metabolism</Keyword><Keyword MajorTopicYN="N">nitrogen deficiency</Keyword><Keyword MajorTopicYN="N">nitrogen metabolism</Keyword><Keyword MajorTopicYN="N">γ-aminobutyric acid</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>01</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>06</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32776117</ArticleId><ArticleId IdType="pii">5889937</ArticleId><ArticleId IdType="doi">10.1093/treephys/tpaa101</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Allemagne</li><li>République populaire de Chine</li><li>Suisse</li></country><region><li>Bavière</li><li>District de Haute-Bavière</li><li>Dongbei</li><li>Jilin</li></region><settlement><li>Changchun</li><li>Munich</li><li>Pékin</li></settlement><orgName><li>Université technique de Munich</li></orgName></list><tree><noCountry><name sortKey="Zhang, Xiaoman" sort="Zhang, Xiaoman" uniqKey="Zhang X" first="Xiaoman" last="Zhang">Xiaoman Zhang</name></noCountry><country name="République populaire de Chine"><noRegion><name sortKey="Chen, Wei" sort="Chen, Wei" uniqKey="Chen W" first="Wei" last="Chen">Wei Chen</name></noRegion><name sortKey="Du, Changjian" sort="Du, Changjian" uniqKey="Du C" first="Changjian" last="Du">Changjian Du</name><name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name><name sortKey="Jiang, Zeping" sort="Jiang, Zeping" uniqKey="Jiang Z" first="Zeping" last="Jiang">Zeping Jiang</name><name sortKey="Li, Mai He" sort="Li, Mai He" uniqKey="Li M" first="Mai-He" last="Li">Mai-He Li</name><name sortKey="Li, Mai He" sort="Li, Mai He" uniqKey="Li M" first="Mai-He" last="Li">Mai-He Li</name><name sortKey="Shi, Shengqing" sort="Shi, Shengqing" uniqKey="Shi S" first="Shengqing" last="Shi">Shengqing Shi</name><name sortKey="Sun, Jiacheng" sort="Sun, Jiacheng" uniqKey="Sun J" first="Jiacheng" last="Sun">Jiacheng Sun</name><name sortKey="Wu, Yanyan" sort="Wu, Yanyan" uniqKey="Wu Y" first="Yanyan" last="Wu">Yanyan Wu</name><name sortKey="Xie, Tiantian" sort="Xie, Tiantian" uniqKey="Xie T" first="Tiantian" last="Xie">Tiantian Xie</name></country><country name="Allemagne"><region name="Bavière"><name sortKey="Meng, Chen" sort="Meng, Chen" uniqKey="Meng C" first="Chen" last="Meng">Chen Meng</name></region></country><country name="Suisse"><noRegion><name sortKey="Li, Mai He" sort="Li, Mai He" uniqKey="Li M" first="Mai-He" last="Li">Mai-He Li</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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