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Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa.

Identifieur interne : 001218 ( Main/Exploration ); précédent : 001217; suivant : 001219

Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa.

Auteurs : Ying-Chung Jimmy Lin [République populaire de Chine, Taïwan, États-Unis] ; Hao Chen [États-Unis] ; Quanzi Li [République populaire de Chine] ; Wei Li [République populaire de Chine, États-Unis] ; Jack P. Wang [République populaire de Chine, États-Unis] ; Rui Shi [États-Unis] ; Sermsawat Tunlaya-Anukit [États-Unis] ; Peng Shuai [États-Unis, République populaire de Chine] ; Zhifeng Wang [République populaire de Chine] ; Hongyan Ma [République populaire de Chine] ; Huiyu Li [République populaire de Chine, États-Unis] ; Ying-Hsuan Sun [Taïwan] ; Ronald R. Sederoff [États-Unis] ; Vincent L. Chiang [États-Unis]

Source :

RBID : pubmed:29078399

Descripteurs français

English descriptors

Abstract

Secondary cell wall (SCW) biosynthesis is the biological process that generates wood, an important renewable feedstock for materials and energy. NAC domain transcription factors, particularly Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND) proteins, are known to regulate SCW differentiation. The regulation of VND and SND is important to maintain homeostasis for plants to avoid abnormal growth and development. We previously identified a splice variant, PtrSND1-A2IR , derived from PtrSND1-A2 as a dominant-negative regulator, which suppresses the transactivation of all PtrSND1 family members. PtrSND1-A2IR also suppresses the self-activation of the PtrSND1 family members except for its cognate transcription factor, PtrSND1-A2, suggesting the existence of an unknown factor needed to regulate PtrSND1-A2 Here, a splice variant, PtrVND6-C1IR , derived from PtrVND6-C1 was discovered that suppresses the protein functions of all PtrVND6 family members. PtrVND6-C1IR also suppresses the expression of all PtrSND1 members, including PtrSND1-A2, demonstrating that PtrVND6-C1IR is the previously unidentified regulator of PtrSND1-A2 We also found that PtrVND6-C1IR cannot suppress the expression of its cognate transcription factor, PtrVND6-C1PtrVND6-C1 is suppressed by PtrSND1-A2IR Both PtrVND6-C1IR and PtrSND1-A2IR cannot suppress their cognate transcription factors but can suppress all members of the other family. The results indicate that the splice variants from the PtrVND6 and PtrSND1 family may exert reciprocal cross-regulation for complete transcriptional regulation of these two families in wood formation. This reciprocal cross-regulation between families suggests a general mechanism among NAC domain proteins and likely other transcription factors, where intron-retained splice variants provide an additional level of regulation.

DOI: 10.1073/pnas.1714422114
PubMed: 29078399
PubMed Central: PMC5692596


Affiliations:


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Le document en format XML

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<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>
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<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>
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<wicri:regionArea>Department of Life Sciences, College of Life Science, National Taiwan University, Taipei 10617</wicri:regionArea>
<wicri:noRegion>Taipei 10617</wicri:noRegion>
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<affiliation wicri:level="1">
<nlm:affiliation>Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</nlm:affiliation>
<country xml:lang="fr">Taïwan</country>
<wicri:regionArea>Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617</wicri:regionArea>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002</wicri:regionArea>
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<name sortKey="Ma, Hongyan" sort="Ma, Hongyan" uniqKey="Ma H" first="Hongyan" last="Ma">Hongyan Ma</name>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin</wicri:regionArea>
<wicri:noRegion>Harbin</wicri:noRegion>
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<name sortKey="Li, Huiyu" sort="Li, Huiyu" uniqKey="Li H" first="Huiyu" last="Li">Huiyu Li</name>
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<affiliation wicri:level="2">
<nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 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="Sun, Ying Hsuan" sort="Sun, Ying Hsuan" uniqKey="Sun Y" first="Ying-Hsuan" last="Sun">Ying-Hsuan Sun</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Forestry, National Chung Hsing University, Taichung 40227, Taiwan.</nlm:affiliation>
<country xml:lang="fr">Taïwan</country>
<wicri:regionArea>Department of Forestry, National Chung Hsing University, Taichung 40227</wicri:regionArea>
<wicri:noRegion>Taichung 40227</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sederoff, Ronald R" sort="Sederoff, Ronald R" uniqKey="Sederoff R" first="Ronald R" last="Sederoff">Ronald R. Sederoff</name>
<affiliation wicri:level="1">
<nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695; ron_sederoff@ncsu.edu vchiang@ncsu.edu.</nlm:affiliation>
<country wicri:rule="url">États-Unis</country>
<wicri:regionArea>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh</wicri:regionArea>
<wicri:noRegion>Raleigh</wicri:noRegion>
</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; ron_sederoff@ncsu.edu vchiang@ncsu.edu.</nlm:affiliation>
<country wicri:rule="url">États-Unis</country>
<wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin</wicri:regionArea>
<wicri:noRegion>Harbin</wicri:noRegion>
</affiliation>
<affiliation wicri:level="2">
<nlm:affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 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>
</analytic>
<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2017" type="published">2017</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Alternative Splicing (MeSH)</term>
<term>Cell Wall (genetics)</term>
<term>Cell Wall (metabolism)</term>
<term>Cloning, Molecular (MeSH)</term>
<term>DNA, Plant (MeSH)</term>
<term>Gene Expression Regulation, Plant (genetics)</term>
<term>Gene Regulatory Networks (MeSH)</term>
<term>Genes, Plant (MeSH)</term>
<term>Homeostasis (MeSH)</term>
<term>Multigene Family (MeSH)</term>
<term>Nuclear Proteins (MeSH)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Leaves (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Shoots (genetics)</term>
<term>Plant Shoots (metabolism)</term>
<term>Populus (genetics)</term>
<term>Populus (metabolism)</term>
<term>Recombinant Proteins (genetics)</term>
<term>Transcription Factors (genetics)</term>
<term>Transcription Factors (metabolism)</term>
<term>Transcriptional Activation (genetics)</term>
<term>Transcriptome (MeSH)</term>
<term>Wood (genetics)</term>
<term>Wood (growth & development)</term>
<term>Xylem (genetics)</term>
<term>Xylem (growth & development)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>ADN des plantes (MeSH)</term>
<term>Activation de la transcription (génétique)</term>
<term>Bois (croissance et développement)</term>
<term>Bois (génétique)</term>
<term>Clonage moléculaire (MeSH)</term>
<term>Facteurs de transcription (génétique)</term>
<term>Facteurs de transcription (métabolisme)</term>
<term>Famille multigénique (MeSH)</term>
<term>Feuilles de plante (génétique)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Gènes de plante (MeSH)</term>
<term>Homéostasie (MeSH)</term>
<term>Paroi cellulaire (génétique)</term>
<term>Paroi cellulaire (métabolisme)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Pousses de plante (génétique)</term>
<term>Pousses de plante (métabolisme)</term>
<term>Protéines nucléaires (MeSH)</term>
<term>Protéines recombinantes (génétique)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (génétique)</term>
<term>Réseaux de régulation génique (MeSH)</term>
<term>Transcriptome (MeSH)</term>
<term>Xylème (croissance et développement)</term>
<term>Xylème (génétique)</term>
<term>Épissage alternatif (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Plant Proteins</term>
<term>Recombinant Proteins</term>
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Plant Proteins</term>
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" type="chemical" xml:lang="en">
<term>DNA, Plant</term>
<term>Nuclear Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Bois</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Cell Wall</term>
<term>Gene Expression Regulation, Plant</term>
<term>Plant Leaves</term>
<term>Plant Shoots</term>
<term>Populus</term>
<term>Transcriptional Activation</term>
<term>Wood</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Wood</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Activation de la transcription</term>
<term>Bois</term>
<term>Facteurs de transcription</term>
<term>Feuilles de plante</term>
<term>Paroi cellulaire</term>
<term>Populus</term>
<term>Pousses de plante</term>
<term>Protéines recombinantes</term>
<term>Protéines végétales</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Wall</term>
<term>Plant Leaves</term>
<term>Plant Shoots</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Facteurs de transcription</term>
<term>Feuilles de plante</term>
<term>Paroi cellulaire</term>
<term>Populus</term>
<term>Pousses de plante</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Alternative Splicing</term>
<term>Cloning, Molecular</term>
<term>Gene Regulatory Networks</term>
<term>Genes, Plant</term>
<term>Homeostasis</term>
<term>Multigene Family</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>ADN des plantes</term>
<term>Clonage moléculaire</term>
<term>Famille multigénique</term>
<term>Gènes de plante</term>
<term>Homéostasie</term>
<term>Protéines nucléaires</term>
<term>Réseaux de régulation génique</term>
<term>Transcriptome</term>
<term>Épissage alternatif</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Secondary cell wall (SCW) biosynthesis is the biological process that generates wood, an important renewable feedstock for materials and energy. NAC domain transcription factors, particularly Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND) proteins, are known to regulate SCW differentiation. The regulation of VND and SND is important to maintain homeostasis for plants to avoid abnormal growth and development. We previously identified a splice variant,
<i>PtrSND1-A2</i>
<sup>
<i>IR</i>
</sup>
, derived from
<i>PtrSND1-A2</i>
as a dominant-negative regulator, which suppresses the transactivation of all
<i>PtrSND1</i>
family members. PtrSND1-A2
<sup>IR</sup>
also suppresses the self-activation of the PtrSND1 family members except for its cognate transcription factor, PtrSND1-A2, suggesting the existence of an unknown factor needed to regulate
<i>PtrSND1-A2</i>
Here, a splice variant,
<i>PtrVND6-C1</i>
<sup>
<i>IR</i>
</sup>
, derived from
<i>PtrVND6-C1</i>
was discovered that suppresses the protein functions of all
<i>PtrVND6</i>
family members. PtrVND6-C1
<sup>IR</sup>
also suppresses the expression of all
<i>PtrSND1</i>
members, including
<i>PtrSND1-A2</i>
, demonstrating that PtrVND6-C1
<sup>IR</sup>
is the previously unidentified regulator of
<i>PtrSND1-A2</i>
We also found that PtrVND6-C1
<sup>IR</sup>
cannot suppress the expression of its cognate transcription factor,
<i>PtrVND6-C1</i>
<i>PtrVND6-C1</i>
is suppressed by PtrSND1-A2
<sup>IR</sup>
Both PtrVND6-C1
<sup>IR</sup>
and PtrSND1-A2
<sup>IR</sup>
cannot suppress their cognate transcription factors but can suppress all members of the other family. The results indicate that the splice variants from the
<i>PtrVND6</i>
and
<i>PtrSND1</i>
family may exert reciprocal cross-regulation for complete transcriptional regulation of these two families in wood formation. This reciprocal cross-regulation between families suggests a general mechanism among NAC domain proteins and likely other transcription factors, where intron-retained splice variants provide an additional level of regulation.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">29078399</PMID>
<DateCompleted>
<Year>2018</Year>
<Month>06</Month>
<Day>19</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>114</Volume>
<Issue>45</Issue>
<PubDate>
<Year>2017</Year>
<Month>11</Month>
<Day>07</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in
<i>Populus trichocarpa</i>
.</ArticleTitle>
<Pagination>
<MedlinePgn>E9722-E9729</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1714422114</ELocationID>
<Abstract>
<AbstractText>Secondary cell wall (SCW) biosynthesis is the biological process that generates wood, an important renewable feedstock for materials and energy. NAC domain transcription factors, particularly Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND) proteins, are known to regulate SCW differentiation. The regulation of VND and SND is important to maintain homeostasis for plants to avoid abnormal growth and development. We previously identified a splice variant,
<i>PtrSND1-A2</i>
<sup>
<i>IR</i>
</sup>
, derived from
<i>PtrSND1-A2</i>
as a dominant-negative regulator, which suppresses the transactivation of all
<i>PtrSND1</i>
family members. PtrSND1-A2
<sup>IR</sup>
also suppresses the self-activation of the PtrSND1 family members except for its cognate transcription factor, PtrSND1-A2, suggesting the existence of an unknown factor needed to regulate
<i>PtrSND1-A2</i>
Here, a splice variant,
<i>PtrVND6-C1</i>
<sup>
<i>IR</i>
</sup>
, derived from
<i>PtrVND6-C1</i>
was discovered that suppresses the protein functions of all
<i>PtrVND6</i>
family members. PtrVND6-C1
<sup>IR</sup>
also suppresses the expression of all
<i>PtrSND1</i>
members, including
<i>PtrSND1-A2</i>
, demonstrating that PtrVND6-C1
<sup>IR</sup>
is the previously unidentified regulator of
<i>PtrSND1-A2</i>
We also found that PtrVND6-C1
<sup>IR</sup>
cannot suppress the expression of its cognate transcription factor,
<i>PtrVND6-C1</i>
<i>PtrVND6-C1</i>
is suppressed by PtrSND1-A2
<sup>IR</sup>
Both PtrVND6-C1
<sup>IR</sup>
and PtrSND1-A2
<sup>IR</sup>
cannot suppress their cognate transcription factors but can suppress all members of the other family. The results indicate that the splice variants from the
<i>PtrVND6</i>
and
<i>PtrSND1</i>
family may exert reciprocal cross-regulation for complete transcriptional regulation of these two families in wood formation. This reciprocal cross-regulation between families suggests a general mechanism among NAC domain proteins and likely other transcription factors, where intron-retained splice variants provide an additional level of regulation.</AbstractText>
<CopyrightInformation>Published under the PNAS license.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<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>Department of Life Sciences, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Hao</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Quanzi</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China.</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.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695.</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, NC 27695.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Shi</LastName>
<ForeName>Rui</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Crop and Soil Sciences Department, North Carolina State University, Raleigh, NC 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, NC 27695.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Shuai</LastName>
<ForeName>Peng</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, 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>Ma</LastName>
<ForeName>Hongyan</ForeName>
<Initials>H</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>Huiyu</ForeName>
<Initials>H</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, NC 27695.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sun</LastName>
<ForeName>Ying-Hsuan</ForeName>
<Initials>YH</Initials>
<AffiliationInfo>
<Affiliation>Department of Forestry, National Chung Hsing University, Taichung 40227, Taiwan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sederoff</LastName>
<ForeName>Ronald R</ForeName>
<Initials>RR</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695; ron_sederoff@ncsu.edu vchiang@ncsu.edu.</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; ron_sederoff@ncsu.edu vchiang@ncsu.edu.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695.</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>2017</Year>
<Month>10</Month>
<Day>23</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D018744">DNA, Plant</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009687">Nuclear Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011994">Recombinant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D017398" MajorTopicYN="N">Alternative Splicing</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002473" MajorTopicYN="N">Cell Wall</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003001" MajorTopicYN="N">Cloning, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018744" MajorTopicYN="N">DNA, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D053263" MajorTopicYN="N">Gene Regulatory Networks</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017343" MajorTopicYN="Y">Genes, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006706" MajorTopicYN="N">Homeostasis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005810" MajorTopicYN="Y">Multigene Family</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009687" MajorTopicYN="N">Nuclear Proteins</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018520" MajorTopicYN="N">Plant Shoots</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011994" MajorTopicYN="N">Recombinant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015533" MajorTopicYN="N">Transcriptional Activation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014934" MajorTopicYN="N">Wood</DescriptorName>
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