The AREB1 Transcription Factor Influences Histone Acetylation to Regulate Drought Responses and Tolerance in Populus trichocarpa.
Identifieur interne : 000691 ( Main/Exploration ); précédent : 000690; suivant : 000692The AREB1 Transcription Factor Influences Histone Acetylation to Regulate Drought Responses and Tolerance in Populus trichocarpa.
Auteurs : Shuang Li [République populaire de Chine] ; Ying-Chung Jimmy Lin [République populaire de Chine, États-Unis, Taïwan] ; Pengyu Wang [République populaire de Chine] ; Baofeng Zhang [République populaire de Chine] ; Meng Li [République populaire de Chine] ; Su Chen [République populaire de Chine] ; Rui Shi [États-Unis] ; Sermsawat Tunlaya-Anukit [États-Unis] ; Xinying Liu [République populaire de Chine] ; Zhifeng Wang [République populaire de Chine] ; Xiufang Dai [République populaire de Chine] ; Jing Yu [République populaire de Chine] ; Chenguang Zhou [République populaire de Chine] ; Baoguang Liu [République populaire de Chine] ; Jack P. Wang [République populaire de Chine, États-Unis] ; Vincent L. Chiang [États-Unis] ; Wei Li [États-Unis]Source :
- The Plant cell [ 1532-298X ] ; 2019.
Descripteurs français
- KwdFr :
- Acide abscissique (métabolisme), Activation de la transcription (MeSH), Acétylation (MeSH), Facteur de croissance végétal (métabolisme), Facteurs de transcription (génétique), Facteurs de transcription (métabolisme), Histone (métabolisme), Histone acetyltransferases (génétique), Histone acetyltransferases (métabolisme), Maturation post-traductionnelle des protéines (MeSH), Motifs nucléotidiques (MeSH), Phénotype (MeSH), Populus (génétique), Populus (physiologie), Protéines végétales (génétique), Protéines végétales (métabolisme), RNA polymerase II (génétique), RNA polymerase II (métabolisme), Régions promotrices (génétique) (génétique), Régulation de l'expression des gènes végétaux (MeSH), Sécheresses (MeSH).
- MESH :
- génétique : Facteurs de transcription, Histone acetyltransferases, Populus, Protéines végétales, RNA polymerase II, Régions promotrices (génétique).
- métabolisme : Acide abscissique, Facteur de croissance végétal, Facteurs de transcription, Histone, Histone acetyltransferases, Protéines végétales, RNA polymerase II.
- physiologie : Populus.
- Activation de la transcription, Acétylation, Maturation post-traductionnelle des protéines, Motifs nucléotidiques, Phénotype, Régulation de l'expression des gènes végétaux, Sécheresses.
English descriptors
- KwdEn :
- Abscisic Acid (metabolism), Acetylation (MeSH), Droughts (MeSH), Gene Expression Regulation, Plant (MeSH), Histone Acetyltransferases (genetics), Histone Acetyltransferases (metabolism), Histones (metabolism), Nucleotide Motifs (MeSH), Phenotype (MeSH), Plant Growth Regulators (metabolism), Plant Proteins (genetics), Plant Proteins (metabolism), Populus (genetics), Populus (physiology), Promoter Regions, Genetic (genetics), Protein Processing, Post-Translational (MeSH), RNA Polymerase II (genetics), RNA Polymerase II (metabolism), Transcription Factors (genetics), Transcription Factors (metabolism), Transcriptional Activation (MeSH).
- MESH :
- chemical , genetics : Histone Acetyltransferases, Plant Proteins, RNA Polymerase II, Transcription Factors.
- chemical , metabolism : Abscisic Acid, Histone Acetyltransferases, Histones, Plant Growth Regulators, Plant Proteins, RNA Polymerase II, Transcription Factors.
- genetics : Populus, Promoter Regions, Genetic.
- physiology : Populus.
- Acetylation, Droughts, Gene Expression Regulation, Plant, Nucleotide Motifs, Phenotype, Protein Processing, Post-Translational, Transcriptional Activation.
Abstract
Plants develop tolerance to drought by activating genes with altered levels of epigenetic modifications. Specific transcription factors are involved in this activation, but the molecular connections within the regulatory system are unclear. Here, we analyzed genome-wide acetylated lysine residue 9 of histone H3 (H3K9ac) enrichment and examined its association with transcriptomes in Populus trichocarpa under drought stress. We revealed that abscisic acid-Responsive Element (ABRE) motifs in promoters of the drought-responsive genes PtrNAC006, PtrNAC007, and PtrNAC120 are involved in H3K9ac enhancement and activation of these genes. Overexpressing these PtrNAC genes in Ptrichocarpa resulted in strong drought-tolerance phenotypes. We showed that the ABRE binding protein PtrAREB1-2 binds to ABRE motifs associated with these PtrNAC genes and recruits the histone acetyltransferase unit ADA2b-GCN5, forming AREB1-ADA2b-GCN5 ternary protein complexes. Moreover, this recruitment enables GCN5-mediated histone acetylation to enhance H3K9ac and enrich RNA polymerase II specifically at these PtrNAC genes for the development of drought tolerance. CRISPR editing or RNA interference-mediated downregulation of any of the ternary members results in highly drought-sensitive Ptrichocarpa Thus, the combinatorial function of the ternary proteins establishes a coordinated histone acetylation and transcription factor-mediated gene activation for drought response and tolerance in Populus species.
DOI: 10.1105/tpc.18.00437
PubMed: 30538157
PubMed Central: PMC6482633
Affiliations:
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uniqKey="Chen S" first="Su" last="Chen">Su Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Rui" sort="Shi, Rui" uniqKey="Shi R" first="Rui" last="Shi">Rui Shi</name><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental 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Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Liu, Xinying" sort="Liu, Xinying" uniqKey="Liu X" first="Xinying" last="Liu">Xinying Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Zhifeng" sort="Wang, Zhifeng" uniqKey="Wang Z" first="Zhifeng" last="Wang">Zhifeng Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Dai, Xiufang" sort="Dai, Xiufang" uniqKey="Dai X" first="Xiufang" last="Dai">Xiufang Dai</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Yu, Jing" sort="Yu, Jing" uniqKey="Yu J" first="Jing" last="Yu">Jing Yu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Zhou, Chenguang" sort="Zhou, Chenguang" uniqKey="Zhou C" first="Chenguang" last="Zhou">Chenguang Zhou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Baoguang" sort="Liu, Baoguang" uniqKey="Liu B" first="Baoguang" last="Liu">Baoguang Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Jack P" sort="Wang, Jack P" uniqKey="Wang J" first="Jack P" last="Wang">Jack P. Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Chiang, Vincent L" sort="Chiang, Vincent L" uniqKey="Chiang V" first="Vincent L" last="Chiang">Vincent L. Chiang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Li, Wei" sort="Li, Wei" uniqKey="Li W" first="Wei" last="Li">Wei Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:30538157</idno><idno type="pmid">30538157</idno><idno type="doi">10.1105/tpc.18.00437</idno><idno type="pmc">PMC6482633</idno><idno type="wicri:Area/Main/Corpus">000B36</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000B36</idno><idno type="wicri:Area/Main/Curation">000B36</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000B36</idno><idno type="wicri:Area/Main/Exploration">000B36</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The AREB1 Transcription Factor Influences Histone Acetylation to Regulate Drought Responses and Tolerance in <i>Populus trichocarpa</i>.</title><author><name sortKey="Li, Shuang" sort="Li, Shuang" uniqKey="Li S" first="Shuang" last="Li">Shuang Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Lin, Ying Chung Jimmy" sort="Lin, Ying Chung Jimmy" uniqKey="Lin Y" first="Ying-Chung Jimmy" last="Lin">Ying-Chung Jimmy Lin</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Life Sciences and Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</nlm:affiliation><country xml:lang="fr">Taïwan</country><wicri:regionArea>Department of Life Sciences and Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617</wicri:regionArea><wicri:noRegion>Taipei 10617</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Pengyu" sort="Wang, Pengyu" uniqKey="Wang P" first="Pengyu" last="Wang">Pengyu Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Baofeng" sort="Zhang, Baofeng" uniqKey="Zhang B" first="Baofeng" last="Zhang">Baofeng Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Li, Meng" sort="Li, Meng" uniqKey="Li M" first="Meng" last="Li">Meng Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Su" sort="Chen, Su" uniqKey="Chen S" first="Su" last="Chen">Su Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Rui" sort="Shi, Rui" uniqKey="Shi R" first="Rui" last="Shi">Rui Shi</name><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Crop and Soil Science, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Department of Crop and Soil Science, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Tunlaya Anukit, Sermsawat" sort="Tunlaya Anukit, Sermsawat" uniqKey="Tunlaya Anukit S" first="Sermsawat" last="Tunlaya-Anukit">Sermsawat Tunlaya-Anukit</name><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Liu, Xinying" sort="Liu, Xinying" uniqKey="Liu X" first="Xinying" last="Liu">Xinying Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Zhifeng" sort="Wang, Zhifeng" uniqKey="Wang Z" first="Zhifeng" last="Wang">Zhifeng Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Dai, Xiufang" sort="Dai, Xiufang" uniqKey="Dai X" first="Xiufang" last="Dai">Xiufang Dai</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Yu, Jing" sort="Yu, Jing" uniqKey="Yu J" first="Jing" last="Yu">Jing Yu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Zhou, Chenguang" sort="Zhou, Chenguang" uniqKey="Zhou C" first="Chenguang" last="Zhou">Chenguang Zhou</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Baoguang" sort="Liu, Baoguang" uniqKey="Liu B" first="Baoguang" last="Liu">Baoguang Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Jack P" sort="Wang, Jack P" uniqKey="Wang J" first="Jack P" last="Wang">Jack P. Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Chiang, Vincent L" sort="Chiang, Vincent L" uniqKey="Chiang V" first="Vincent L" last="Chiang">Vincent L. Chiang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Caroline du Nord</region></placeName><wicri:cityArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:cityArea></affiliation></author><author><name sortKey="Li, Wei" sort="Li, Wei" uniqKey="Li W" first="Wei" last="Li">Wei Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040</wicri:regionArea><wicri:noRegion>Harbin 150040</wicri:noRegion></affiliation></author></analytic><series><title level="j">The Plant cell</title><idno type="eISSN">1532-298X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Abscisic Acid (metabolism)</term><term>Acetylation (MeSH)</term><term>Droughts (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Histone Acetyltransferases (genetics)</term><term>Histone Acetyltransferases (metabolism)</term><term>Histones (metabolism)</term><term>Nucleotide Motifs (MeSH)</term><term>Phenotype (MeSH)</term><term>Plant Growth Regulators (metabolism)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Populus (genetics)</term><term>Populus (physiology)</term><term>Promoter Regions, Genetic (genetics)</term><term>Protein Processing, Post-Translational (MeSH)</term><term>RNA Polymerase II (genetics)</term><term>RNA Polymerase II (metabolism)</term><term>Transcription Factors (genetics)</term><term>Transcription Factors (metabolism)</term><term>Transcriptional Activation (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Acide abscissique (métabolisme)</term><term>Activation de la transcription (MeSH)</term><term>Acétylation (MeSH)</term><term>Facteur de croissance végétal (métabolisme)</term><term>Facteurs de transcription (génétique)</term><term>Facteurs de transcription (métabolisme)</term><term>Histone (métabolisme)</term><term>Histone acetyltransferases (génétique)</term><term>Histone acetyltransferases (métabolisme)</term><term>Maturation post-traductionnelle des protéines (MeSH)</term><term>Motifs nucléotidiques (MeSH)</term><term>Phénotype (MeSH)</term><term>Populus (génétique)</term><term>Populus (physiologie)</term><term>Protéines végétales (génétique)</term><term>Protéines végétales (métabolisme)</term><term>RNA polymerase II (génétique)</term><term>RNA polymerase II (métabolisme)</term><term>Régions promotrices (génétique) (génétique)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Sécheresses (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Histone Acetyltransferases</term><term>Plant Proteins</term><term>RNA Polymerase II</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Abscisic Acid</term><term>Histone Acetyltransferases</term><term>Histones</term><term>Plant Growth Regulators</term><term>Plant Proteins</term><term>RNA Polymerase II</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term><term>Promoter Regions, Genetic</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Facteurs de transcription</term><term>Histone acetyltransferases</term><term>Populus</term><term>Protéines végétales</term><term>RNA polymerase II</term><term>Régions promotrices (génétique)</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Acide abscissique</term><term>Facteur de croissance végétal</term><term>Facteurs de transcription</term><term>Histone</term><term>Histone acetyltransferases</term><term>Protéines végétales</term><term>RNA polymerase II</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Acetylation</term><term>Droughts</term><term>Gene Expression Regulation, Plant</term><term>Nucleotide Motifs</term><term>Phenotype</term><term>Protein Processing, Post-Translational</term><term>Transcriptional Activation</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Activation de la transcription</term><term>Acétylation</term><term>Maturation post-traductionnelle des protéines</term><term>Motifs nucléotidiques</term><term>Phénotype</term><term>Régulation de l'expression des gènes végétaux</term><term>Sécheresses</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plants develop tolerance to drought by activating genes with altered levels of epigenetic modifications. Specific transcription factors are involved in this activation, but the molecular connections within the regulatory system are unclear. Here, we analyzed genome-wide acetylated lysine residue 9 of histone H3 (H3K9ac) enrichment and examined its association with transcriptomes in <i>Populus trichocarpa</i> under drought stress. We revealed that abscisic acid-Responsive Element (ABRE) motifs in promoters of the drought-responsive genes <i>PtrNAC006</i>, <i>PtrNAC007</i>, and <i>PtrNAC120</i> are involved in H3K9ac enhancement and activation of these genes. Overexpressing these <i>PtrNAC</i> genes in <i>P</i><i>trichocarpa</i> resulted in strong drought-tolerance phenotypes. We showed that the ABRE binding protein PtrAREB1-2 binds to ABRE motifs associated with these <i>PtrNAC</i> genes and recruits the histone acetyltransferase unit ADA2b-GCN5, forming AREB1-ADA2b-GCN5 ternary protein complexes. Moreover, this recruitment enables GCN5-mediated histone acetylation to enhance H3K9ac and enrich RNA polymerase II specifically at these <i>PtrNAC</i> genes for the development of drought tolerance. CRISPR editing or RNA interference-mediated downregulation of any of the ternary members results in highly drought-sensitive <i>P</i><i>trichocarpa</i> Thus, the combinatorial function of the ternary proteins establishes a coordinated histone acetylation and transcription factor-mediated gene activation for drought response and tolerance in <i>Populus</i> species.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30538157</PMID><DateCompleted><Year>2020</Year><Month>02</Month><Day>18</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>09</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-298X</ISSN><JournalIssue CitedMedium="Internet"><Volume>31</Volume><Issue>3</Issue><PubDate><Year>2019</Year><Month>03</Month></PubDate></JournalIssue><Title>The Plant cell</Title><ISOAbbreviation>Plant Cell</ISOAbbreviation></Journal><ArticleTitle>The AREB1 Transcription Factor Influences Histone Acetylation to Regulate Drought Responses and Tolerance in <i>Populus trichocarpa</i>.</ArticleTitle><Pagination><MedlinePgn>663-686</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1105/tpc.18.00437</ELocationID><Abstract><AbstractText>Plants develop tolerance to drought by activating genes with altered levels of epigenetic modifications. Specific transcription factors are involved in this activation, but the molecular connections within the regulatory system are unclear. Here, we analyzed genome-wide acetylated lysine residue 9 of histone H3 (H3K9ac) enrichment and examined its association with transcriptomes in <i>Populus trichocarpa</i> under drought stress. We revealed that abscisic acid-Responsive Element (ABRE) motifs in promoters of the drought-responsive genes <i>PtrNAC006</i>, <i>PtrNAC007</i>, and <i>PtrNAC120</i> are involved in H3K9ac enhancement and activation of these genes. Overexpressing these <i>PtrNAC</i> genes in <i>P</i><i>trichocarpa</i> resulted in strong drought-tolerance phenotypes. We showed that the ABRE binding protein PtrAREB1-2 binds to ABRE motifs associated with these <i>PtrNAC</i> genes and recruits the histone acetyltransferase unit ADA2b-GCN5, forming AREB1-ADA2b-GCN5 ternary protein complexes. Moreover, this recruitment enables GCN5-mediated histone acetylation to enhance H3K9ac and enrich RNA polymerase II specifically at these <i>PtrNAC</i> genes for the development of drought tolerance. CRISPR editing or RNA interference-mediated downregulation of any of the ternary members results in highly drought-sensitive <i>P</i><i>trichocarpa</i> Thus, the combinatorial function of the ternary proteins establishes a coordinated histone acetylation and transcription factor-mediated gene activation for drought response and tolerance in <i>Populus</i> species.</AbstractText><CopyrightInformation>© 2019 American Society of Plant Biologists. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Shuang</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Ying-Chung Jimmy</ForeName><Initials>YJ</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Life Sciences and Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Pengyu</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Baofeng</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Meng</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Su</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Rui</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Crop and Soil Science, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tunlaya-Anukit</LastName><ForeName>Sermsawat</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Xinying</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Zhifeng</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dai</LastName><ForeName>Xiufang</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Jing</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Chenguang</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Baoguang</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jack P</ForeName><Initials>JP</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chiang</LastName><ForeName>Vincent L</ForeName><Initials>VL</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, North Carolina 27695.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Wei</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China vchiang@ncsu.edu weili2015@nefu.edu.cn.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>12</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant Cell</MedlineTA><NlmUniqueID>9208688</NlmUniqueID><ISSNLinking>1040-4651</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D006657">Histones</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010937">Plant Growth Regulators</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>72S9A8J5GW</RegistryNumber><NameOfSubstance UI="D000040">Abscisic Acid</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.3.1.48</RegistryNumber><NameOfSubstance UI="D051548">Histone Acetyltransferases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.7.-</RegistryNumber><NameOfSubstance UI="D012319">RNA Polymerase II</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Plant Cell. 2019 Mar;31(3):559-560</RefSource><PMID Version="1">30573471</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D000040" MajorTopicYN="N">Abscisic Acid</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000107" MajorTopicYN="N">Acetylation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D055864" MajorTopicYN="N">Droughts</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051548" MajorTopicYN="N">Histone Acetyltransferases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006657" MajorTopicYN="N">Histones</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059372" MajorTopicYN="N">Nucleotide Motifs</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010641" MajorTopicYN="N">Phenotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010937" MajorTopicYN="N">Plant Growth Regulators</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</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="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011401" MajorTopicYN="N">Promoter Regions, Genetic</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011499" MajorTopicYN="Y">Protein Processing, Post-Translational</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012319" MajorTopicYN="N">RNA Polymerase II</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015533" MajorTopicYN="N">Transcriptional Activation</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>06</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>10</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>11</Month><Day>24</Day></PubMedPubDate><PubMedPubDate 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IdType="pubmed">25144270</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>Taïwan</li><li>États-Unis</li></country><region><li>Caroline du Nord</li></region></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Li, Shuang" sort="Li, Shuang" uniqKey="Li S" first="Shuang" last="Li">Shuang Li</name></noRegion><name sortKey="Chen, Su" sort="Chen, Su" uniqKey="Chen S" first="Su" last="Chen">Su Chen</name><name sortKey="Dai, Xiufang" sort="Dai, Xiufang" uniqKey="Dai X" first="Xiufang" last="Dai">Xiufang Dai</name><name sortKey="Li, Meng" sort="Li, Meng" uniqKey="Li M" first="Meng" last="Li">Meng Li</name><name sortKey="Lin, Ying Chung Jimmy" sort="Lin, Ying Chung Jimmy" uniqKey="Lin Y" first="Ying-Chung Jimmy" last="Lin">Ying-Chung Jimmy Lin</name><name sortKey="Liu, Baoguang" sort="Liu, Baoguang" uniqKey="Liu B" first="Baoguang" last="Liu">Baoguang Liu</name><name sortKey="Liu, Xinying" sort="Liu, Xinying" uniqKey="Liu X" first="Xinying" last="Liu">Xinying Liu</name><name sortKey="Wang, Jack P" sort="Wang, Jack P" uniqKey="Wang J" first="Jack P" last="Wang">Jack P. Wang</name><name sortKey="Wang, Pengyu" sort="Wang, Pengyu" uniqKey="Wang P" first="Pengyu" last="Wang">Pengyu Wang</name><name sortKey="Wang, Zhifeng" sort="Wang, Zhifeng" uniqKey="Wang Z" first="Zhifeng" last="Wang">Zhifeng Wang</name><name sortKey="Yu, Jing" sort="Yu, Jing" uniqKey="Yu J" first="Jing" last="Yu">Jing Yu</name><name sortKey="Zhang, Baofeng" sort="Zhang, Baofeng" uniqKey="Zhang B" first="Baofeng" last="Zhang">Baofeng Zhang</name><name sortKey="Zhou, Chenguang" sort="Zhou, Chenguang" uniqKey="Zhou C" first="Chenguang" last="Zhou">Chenguang Zhou</name></country><country name="États-Unis"><region name="Caroline du Nord"><name sortKey="Lin, Ying Chung Jimmy" sort="Lin, Ying Chung Jimmy" uniqKey="Lin Y" first="Ying-Chung Jimmy" last="Lin">Ying-Chung Jimmy Lin</name></region><name sortKey="Chiang, Vincent L" sort="Chiang, Vincent L" uniqKey="Chiang V" first="Vincent L" last="Chiang">Vincent L. Chiang</name><name sortKey="Chiang, Vincent L" sort="Chiang, Vincent L" uniqKey="Chiang V" first="Vincent L" last="Chiang">Vincent L. Chiang</name><name sortKey="Li, Wei" sort="Li, Wei" uniqKey="Li W" first="Wei" last="Li">Wei Li</name><name sortKey="Shi, Rui" sort="Shi, Rui" uniqKey="Shi R" first="Rui" last="Shi">Rui Shi</name><name sortKey="Shi, Rui" sort="Shi, Rui" uniqKey="Shi R" first="Rui" last="Shi">Rui Shi</name><name sortKey="Tunlaya Anukit, Sermsawat" sort="Tunlaya Anukit, Sermsawat" uniqKey="Tunlaya Anukit S" first="Sermsawat" last="Tunlaya-Anukit">Sermsawat Tunlaya-Anukit</name><name sortKey="Wang, Jack P" sort="Wang, Jack P" uniqKey="Wang J" first="Jack P" last="Wang">Jack P. Wang</name></country><country name="Taïwan"><noRegion><name sortKey="Lin, Ying Chung Jimmy" sort="Lin, Ying Chung Jimmy" uniqKey="Lin Y" first="Ying-Chung Jimmy" last="Lin">Ying-Chung Jimmy Lin</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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