MYB Transcription Factor161 Mediates Feedback Regulation of Secondary wall-associated NAC-Domain1 Family Genes for Wood Formation.
Identifieur interne : 000284 ( Main/Exploration ); précédent : 000283; suivant : 000285MYB Transcription Factor161 Mediates Feedback Regulation of Secondary wall-associated NAC-Domain1 Family Genes for Wood Formation.
Auteurs : Zhifeng Wang [République populaire de Chine] ; Yuli Mao [République populaire de Chine] ; Yanjiao Guo [République populaire de Chine] ; Jinghui Gao [République populaire de Chine] ; Xinying Liu [République populaire de Chine] ; Shuang Li [République populaire de Chine] ; Ying-Chung Jimmy Lin [République populaire de Chine, Taïwan] ; Hao Chen [République populaire de Chine, États-Unis] ; Jack P. Wang [République populaire de Chine, États-Unis] ; Vincent L. Chiang [République populaire de Chine, États-Unis] ; Wei Li [République populaire de Chine]Source :
- Plant physiology [ 1532-2548 ] ; 2020.
Abstract
Wood formation is a complex process that involves cell differentiation, cell expansion, secondary wall deposition, and programmed cell death. We constructed a four-layer wood formation transcriptional regulatory network (TRN) in Populus trichocarpa (black cottonwood) that has four Secondary wall-associated NAC-Domain1 (PtrSND1) transcription factor (TF) family members as the top-layer regulators. We characterized the function of a MYB (PtrMYB161) TF in this PtrSND1-TRN, using transgenic Ptrichocarpa cells and whole plants. PtrMYB161 is a third-layer regulator that directly transactivates five wood formation genes. Overexpression of PtrMYB161 in P. trichocarpa (OE-PtrMYB161) led to reduced wood, altered cell type proportions, and inhibited growth. Integrative analysis of wood cell-based chromatin-binding assays with OE-PtrMYB161 transcriptomics revealed a feedback regulation system in the PtrSND1-TRN, where PtrMYB161 represses all four top-layer regulators and one second-layer regulator, PtrMYB021, possibly affecting many downstream TFs in, and likely beyond, the TRN, to generate the observed phenotypic changes. Our data also suggested that the PtrMYB161's repressor function operates through interaction of the base PtrMYB161 target-binding system with gene-silencing cofactors. PtrMYB161 protein does not contain any known negative regulatory domains. CRISPR-based mutants of PtrMYB161 in P. trichocarpa exhibited phenotypes similar to the wild type, suggesting that PtrMYB161's activator functions are redundant among many TFs. Our work demonstrated that PtrMYB161 binds to multiple sets of target genes, a feature that allows it to function as an activator as well as a repressor. The balance of the two functions may be important to the establishment of regulatory homeostasis for normal growth and development.
DOI: 10.1104/pp.20.01033
PubMed: 32943464
PubMed Central: PMC7608153
Affiliations:
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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.</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="2"><nlm:affiliation>Department of Forest Biomaterials, 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 Forest Biomaterials, 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 weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">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></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno 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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="Mao, Yuli" sort="Mao, Yuli" uniqKey="Mao Y" first="Yuli" last="Mao">Yuli Mao</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="Guo, Yanjiao" sort="Guo, Yanjiao" uniqKey="Guo Y" first="Yanjiao" last="Guo">Yanjiao Guo</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="Gao, Jinghui" sort="Gao, Jinghui" uniqKey="Gao J" first="Jinghui" last="Gao">Jinghui Gao</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, 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="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 weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">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="1"><nlm:affiliation>Department of Life Science 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 Science 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="Chen, Hao" sort="Chen, Hao" uniqKey="Chen H" first="Hao" last="Chen">Hao 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><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="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.</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="2"><nlm:affiliation>Department of Forest Biomaterials, 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 Forest Biomaterials, 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 weili2015@nefu.edu.cn.</nlm:affiliation><country wicri:rule="url">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></analytic><series><title level="j">Plant physiology</title><idno type="eISSN">1532-2548</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Wood formation is a complex process that involves cell differentiation, cell expansion, secondary wall deposition, and programmed cell death. We constructed a four-layer wood formation transcriptional regulatory network (TRN) in <i>Populus trichocarpa</i> (black cottonwood) that has four Secondary wall-associated NAC-Domain1 (PtrSND1) transcription factor (TF) family members as the top-layer regulators. We characterized the function of a MYB (PtrMYB161) TF in this PtrSND1-TRN, using transgenic <i>P</i><i>trichocarpa</i> cells and whole plants. PtrMYB161 is a third-layer regulator that directly transactivates five wood formation genes. Overexpression of <i>PtrMYB161</i> in <i>P. trichocarpa</i> (<i>OE</i>-<i>PtrMYB161</i>) led to reduced wood, altered cell type proportions, and inhibited growth. Integrative analysis of wood cell-based chromatin-binding assays with <i>OE</i>-<i>PtrMYB161</i> transcriptomics revealed a feedback regulation system in the PtrSND1-TRN, where PtrMYB161 represses all four top-layer regulators and one second-layer regulator, PtrMYB021, possibly affecting many downstream TFs in, and likely beyond, the TRN, to generate the observed phenotypic changes. Our data also suggested that the PtrMYB161's repressor function operates through interaction of the base PtrMYB161 target-binding system with gene-silencing cofactors. PtrMYB161 protein does not contain any known negative regulatory domains. CRISPR-based mutants of <i>PtrMYB161</i> in <i>P. trichocarpa</i> exhibited phenotypes similar to the wild type, suggesting that PtrMYB161's activator functions are redundant among many TFs. Our work demonstrated that PtrMYB161 binds to multiple sets of target genes, a feature that allows it to function as an activator as well as a repressor. The balance of the two functions may be important to the establishment of regulatory homeostasis for normal growth and development.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32943464</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-2548</ISSN><JournalIssue CitedMedium="Internet"><Volume>184</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>11</Month></PubDate></JournalIssue><Title>Plant physiology</Title><ISOAbbreviation>Plant Physiol</ISOAbbreviation></Journal><ArticleTitle>MYB Transcription Factor161 Mediates Feedback Regulation of <i>Secondary wall-associated NAC-Domain1</i> Family Genes for Wood Formation.</ArticleTitle><Pagination><MedlinePgn>1389-1406</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.20.01033</ELocationID><Abstract><AbstractText>Wood formation is a complex process that involves cell differentiation, cell expansion, secondary wall deposition, and programmed cell death. We constructed a four-layer wood formation transcriptional regulatory network (TRN) in <i>Populus trichocarpa</i> (black cottonwood) that has four Secondary wall-associated NAC-Domain1 (PtrSND1) transcription factor (TF) family members as the top-layer regulators. We characterized the function of a MYB (PtrMYB161) TF in this PtrSND1-TRN, using transgenic <i>P</i><i>trichocarpa</i> cells and whole plants. PtrMYB161 is a third-layer regulator that directly transactivates five wood formation genes. Overexpression of <i>PtrMYB161</i> in <i>P. trichocarpa</i> (<i>OE</i>-<i>PtrMYB161</i>) led to reduced wood, altered cell type proportions, and inhibited growth. Integrative analysis of wood cell-based chromatin-binding assays with <i>OE</i>-<i>PtrMYB161</i> transcriptomics revealed a feedback regulation system in the PtrSND1-TRN, where PtrMYB161 represses all four top-layer regulators and one second-layer regulator, PtrMYB021, possibly affecting many downstream TFs in, and likely beyond, the TRN, to generate the observed phenotypic changes. Our data also suggested that the PtrMYB161's repressor function operates through interaction of the base PtrMYB161 target-binding system with gene-silencing cofactors. PtrMYB161 protein does not contain any known negative regulatory domains. CRISPR-based mutants of <i>PtrMYB161</i> in <i>P. trichocarpa</i> exhibited phenotypes similar to the wild type, suggesting that PtrMYB161's activator functions are redundant among many TFs. Our work demonstrated that PtrMYB161 binds to multiple sets of target genes, a feature that allows it to function as an activator as well as a repressor. The balance of the two functions may be important to the establishment of regulatory homeostasis for normal growth and development.</AbstractText><CopyrightInformation>© 2020 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Zhifeng</ForeName><Initials>Z</Initials><Identifier Source="ORCID">0000-0002-1153-4337</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mao</LastName><ForeName>Yuli</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guo</LastName><ForeName>Yanjiao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gao</LastName><ForeName>Jinghui</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0002-8190-855X</Identifier><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>Xinying</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0002-9737-0897</Identifier><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>Shuang</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China weili2015@nefu.edu.cn.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Ying-Chung Jimmy</ForeName><Initials>YJ</Initials><Identifier Source="ORCID">0000-0001-7120-4690</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Life Science and Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Hao</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0002-6415-993X</Identifier><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 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