PeSTZ1, a C2H2-type zinc finger transcription factor from Populus euphratica, enhances freezing tolerance through modulation of ROS scavenging by directly regulating PeAPX2.
Identifieur interne : 000796 ( Main/Exploration ); précédent : 000795; suivant : 000797PeSTZ1, a C2H2-type zinc finger transcription factor from Populus euphratica, enhances freezing tolerance through modulation of ROS scavenging by directly regulating PeAPX2.
Auteurs : Fang He [République populaire de Chine] ; Hui-Guang Li [République populaire de Chine] ; Jing-Jing Wang [République populaire de Chine] ; Yanyan Su [République populaire de Chine] ; Hou-Ling Wang [République populaire de Chine] ; Cong-Hua Feng [République populaire de Chine] ; Yanli Yang [République populaire de Chine] ; Meng-Xue Niu [République populaire de Chine] ; Chao Liu [République populaire de Chine] ; Weilun Yin [République populaire de Chine] ; Xinli Xia [République populaire de Chine]Source :
- Plant biotechnology journal [ 1467-7652 ] ; 2019.
Descripteurs français
- KwdFr :
- Ascorbate peroxidases (physiologie), Congélation (MeSH), Doigts de zinc (MeSH), Espèces réactives de l'oxygène (métabolisme), Facteurs de transcription (physiologie), Populus (génétique), Populus (physiologie), Protéines végétales (physiologie), Régulation de l'expression des gènes végétaux (MeSH), Végétaux génétiquement modifiés (physiologie).
- MESH :
- génétique : Populus.
- métabolisme : Espèces réactives de l'oxygène.
- physiologie : Ascorbate peroxidases, Facteurs de transcription, Populus, Protéines végétales, Végétaux génétiquement modifiés.
- Congélation, Doigts de zinc, Régulation de l'expression des gènes végétaux.
English descriptors
- KwdEn :
- Ascorbate Peroxidases (physiology), Freezing (MeSH), Gene Expression Regulation, Plant (MeSH), Plant Proteins (physiology), Plants, Genetically Modified (physiology), Populus (genetics), Populus (physiology), Reactive Oxygen Species (metabolism), Transcription Factors (physiology), Zinc Fingers (MeSH).
- MESH :
- chemical , metabolism : Reactive Oxygen Species.
- chemical , physiology : Ascorbate Peroxidases, Plant Proteins, Transcription Factors.
- genetics : Populus.
- physiology : Plants, Genetically Modified, Populus.
- Freezing, Gene Expression Regulation, Plant, Zinc Fingers.
Abstract
In the present study, PeSTZ1, a cysteine-2/histidine-2-type zinc finger transcription factor, was isolated from the desert poplar, Populus euphratica, which serves as a model stress adaptation system for trees. PeSTZ1 was preferentially expressed in the young stems and was significantly up-regulated during chilling and freezing treatments. PeSTZ1 was localized to the nucleus and bound specifically to the PeAPX2 promoter. To examine the potential functions of PeSTZ1, we overexpressed it in poplar 84K hybrids (Populus alba × Populus glandulosa), which are known to be stress-sensitive. Upon exposure to freezing stress, transgenic poplars maintained higher photosynthetic activity and dissipated more excess light energy (in the form of heat) than wild-type poplars. Thus, PeSTZ1 functions as a transcription activator to enhance freezing tolerance without sacrificing growth. Under freezing stress, PeSTZ1 acts upstream of ASCORBATE PEROXIDASE2 (PeAPX2) and directly regulates its expression by binding to its promoter. Activated PeAPX2 promotes cytosolic APX that scavenges reactive oxygen species (ROS) under cold stress. PeSTZ1 may operate in parallel with C-REPEAT-BINDING FACTORS to regulate COLD-REGULATED gene expression. Moreover, PeSTZ1 up-regulation reduces malondialdehyde and ROS accumulation by activating the antioxidant system. Taken together, these results suggested that overexpressing PeSTZ1 in 84K poplar enhances freezing tolerance through the modulation of ROS scavenging via the direct regulation of PeAPX2 expression.
DOI: 10.1111/pbi.13130
PubMed: 30977939
PubMed Central: PMC6790368
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Li, Hui Guang" sort="Li, Hui Guang" uniqKey="Li H" first="Hui-Guang" last="Li">Hui-Guang Li</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Jing Jing" sort="Wang, Jing Jing" uniqKey="Wang J" first="Jing-Jing" last="Wang">Jing-Jing 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Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yin, Weilun" sort="Yin, Weilun" uniqKey="Yin W" first="Weilun" last="Yin">Weilun Yin</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation 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Fang" uniqKey="He F" first="Fang" last="He">Fang He</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Li, Hui Guang" sort="Li, Hui Guang" uniqKey="Li H" first="Hui-Guang" last="Li">Hui-Guang Li</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Jing Jing" sort="Wang, Jing Jing" uniqKey="Wang J" first="Jing-Jing" last="Wang">Jing-Jing Wang</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Su, Yanyan" sort="Su, Yanyan" uniqKey="Su Y" first="Yanyan" last="Su">Yanyan Su</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Hou Ling" sort="Wang, Hou Ling" uniqKey="Wang H" first="Hou-Ling" last="Wang">Hou-Ling Wang</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Feng, Cong Hua" sort="Feng, Cong Hua" uniqKey="Feng C" first="Cong-Hua" last="Feng">Cong-Hua Feng</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yang, Yanli" sort="Yang, Yanli" uniqKey="Yang Y" first="Yanli" last="Yang">Yanli Yang</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Niu, Meng Xue" sort="Niu, Meng Xue" uniqKey="Niu M" first="Meng-Xue" last="Niu">Meng-Xue Niu</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Liu, Chao" sort="Liu, Chao" uniqKey="Liu C" first="Chao" last="Liu">Chao Liu</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yin, Weilun" sort="Yin, Weilun" uniqKey="Yin W" first="Weilun" last="Yin">Weilun Yin</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xia, Xinli" sort="Xia, Xinli" uniqKey="Xia X" first="Xinli" last="Xia">Xinli Xia</name><affiliation wicri:level="3"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">Plant biotechnology journal</title><idno type="eISSN">1467-7652</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Ascorbate Peroxidases (physiology)</term><term>Freezing (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Plant Proteins (physiology)</term><term>Plants, Genetically Modified (physiology)</term><term>Populus (genetics)</term><term>Populus (physiology)</term><term>Reactive Oxygen Species (metabolism)</term><term>Transcription Factors (physiology)</term><term>Zinc Fingers (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Ascorbate peroxidases (physiologie)</term><term>Congélation (MeSH)</term><term>Doigts de zinc (MeSH)</term><term>Espèces réactives de l'oxygène (métabolisme)</term><term>Facteurs de transcription (physiologie)</term><term>Populus (génétique)</term><term>Populus (physiologie)</term><term>Protéines végétales (physiologie)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Végétaux génétiquement modifiés (physiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Reactive Oxygen Species</term></keywords><keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en"><term>Ascorbate Peroxidases</term><term>Plant Proteins</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Espèces réactives de l'oxygène</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Ascorbate peroxidases</term><term>Facteurs de transcription</term><term>Populus</term><term>Protéines végétales</term><term>Végétaux génétiquement modifiés</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Plants, Genetically Modified</term><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Freezing</term><term>Gene Expression Regulation, Plant</term><term>Zinc Fingers</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Congélation</term><term>Doigts de zinc</term><term>Régulation de l'expression des gènes végétaux</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In the present study, PeSTZ1, a cysteine-2/histidine-2-type zinc finger transcription factor, was isolated from the desert poplar, Populus euphratica, which serves as a model stress adaptation system for trees. PeSTZ1 was preferentially expressed in the young stems and was significantly up-regulated during chilling and freezing treatments. PeSTZ1 was localized to the nucleus and bound specifically to the PeAPX2 promoter. To examine the potential functions of PeSTZ1, we overexpressed it in poplar 84K hybrids (Populus alba × Populus glandulosa), which are known to be stress-sensitive. Upon exposure to freezing stress, transgenic poplars maintained higher photosynthetic activity and dissipated more excess light energy (in the form of heat) than wild-type poplars. Thus, PeSTZ1 functions as a transcription activator to enhance freezing tolerance without sacrificing growth. Under freezing stress, PeSTZ1 acts upstream of ASCORBATE PEROXIDASE2 (PeAPX2) and directly regulates its expression by binding to its promoter. Activated PeAPX2 promotes cytosolic APX that scavenges reactive oxygen species (ROS) under cold stress. PeSTZ1 may operate in parallel with C-REPEAT-BINDING FACTORS to regulate COLD-REGULATED gene expression. Moreover, PeSTZ1 up-regulation reduces malondialdehyde and ROS accumulation by activating the antioxidant system. Taken together, these results suggested that overexpressing PeSTZ1 in 84K poplar enhances freezing tolerance through the modulation of ROS scavenging via the direct regulation of PeAPX2 expression.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">30977939</PMID><DateCompleted><Year>2020</Year><Month>03</Month><Day>05</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>05</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1467-7652</ISSN><JournalIssue CitedMedium="Internet"><Volume>17</Volume><Issue>11</Issue><PubDate><Year>2019</Year><Month>11</Month></PubDate></JournalIssue><Title>Plant biotechnology journal</Title><ISOAbbreviation>Plant Biotechnol J</ISOAbbreviation></Journal><ArticleTitle>PeSTZ1, a C2H2-type zinc finger transcription factor from Populus euphratica, enhances freezing tolerance through modulation of ROS scavenging by directly regulating PeAPX2.</ArticleTitle><Pagination><MedlinePgn>2169-2183</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/pbi.13130</ELocationID><Abstract><AbstractText>In the present study, PeSTZ1, a cysteine-2/histidine-2-type zinc finger transcription factor, was isolated from the desert poplar, Populus euphratica, which serves as a model stress adaptation system for trees. PeSTZ1 was preferentially expressed in the young stems and was significantly up-regulated during chilling and freezing treatments. PeSTZ1 was localized to the nucleus and bound specifically to the PeAPX2 promoter. To examine the potential functions of PeSTZ1, we overexpressed it in poplar 84K hybrids (Populus alba × Populus glandulosa), which are known to be stress-sensitive. Upon exposure to freezing stress, transgenic poplars maintained higher photosynthetic activity and dissipated more excess light energy (in the form of heat) than wild-type poplars. Thus, PeSTZ1 functions as a transcription activator to enhance freezing tolerance without sacrificing growth. Under freezing stress, PeSTZ1 acts upstream of ASCORBATE PEROXIDASE2 (PeAPX2) and directly regulates its expression by binding to its promoter. Activated PeAPX2 promotes cytosolic APX that scavenges reactive oxygen species (ROS) under cold stress. PeSTZ1 may operate in parallel with C-REPEAT-BINDING FACTORS to regulate COLD-REGULATED gene expression. Moreover, PeSTZ1 up-regulation reduces malondialdehyde and ROS accumulation by activating the antioxidant system. Taken together, these results suggested that overexpressing PeSTZ1 in 84K poplar enhances freezing tolerance through the modulation of ROS scavenging via the direct regulation of PeAPX2 expression.</AbstractText><CopyrightInformation>© 2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>He</LastName><ForeName>Fang</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Hui-Guang</ForeName><Initials>HG</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jing-Jing</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Su</LastName><ForeName>Yanyan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Hou-Ling</ForeName><Initials>HL</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feng</LastName><ForeName>Cong-Hua</ForeName><Initials>CH</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Yanli</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Niu</LastName><ForeName>Meng-Xue</ForeName><Initials>MX</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Chao</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Weilun</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xia</LastName><ForeName>Xinli</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0003-3731-4970</Identifier><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>04</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Plant Biotechnol J</MedlineTA><NlmUniqueID>101201889</NlmUniqueID><ISSNLinking>1467-7644</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D017382">Reactive Oxygen Species</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 1.11.1.11</RegistryNumber><NameOfSubstance UI="D060387">Ascorbate Peroxidases</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D060387" MajorTopicYN="N">Ascorbate Peroxidases</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005615" MajorTopicYN="Y">Freezing</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017382" MajorTopicYN="N">Reactive Oxygen Species</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016335" MajorTopicYN="N">Zinc Fingers</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">PeAPX2
</Keyword><Keyword MajorTopicYN="Y">PeSTZ1
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