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Endoplasmic reticulum-localized UBC34 interaction with lignin repressors MYB221 and MYB156 regulates the transactivity of the transcription factors in Populus tomentosa.

Identifieur interne : 000988 ( Main/Exploration ); précédent : 000987; suivant : 000989

Endoplasmic reticulum-localized UBC34 interaction with lignin repressors MYB221 and MYB156 regulates the transactivity of the transcription factors in Populus tomentosa.

Auteurs : Lin Zheng [République populaire de Chine] ; Yajuan Chen [République populaire de Chine] ; Dong Ding [République populaire de Chine] ; Ying Zhou [République populaire de Chine] ; Liping Ding [République populaire de Chine] ; Jianhua Wei [République populaire de Chine] ; Hongzhi Wang [République populaire de Chine]

Source :

RBID : pubmed:30866808

Descripteurs français

English descriptors

Abstract

BACKGROUND

Regulation of lignin biosynthesis is known to occur at the level of transcription factors (TFs), of which R2R3-MYB family members have been proposed to play a central role via the AC cis-elements. Despite the important roles of TFs in lignin biosynthesis, the post-translational regulation of these TFs, particularly their ubiquitination regulation, has not been thoroughly explored.

RESULTS

We describe the discovery of a Populus tomentosa E2 ubiquitin-conjugating enzyme 34 (PtoUBC34), which is involved in the post-translational regulation of transactivation activity of lignin-associated transcriptional repressors PtoMYB221 and PtoMYB156. PtoUBC34 is localized at the endoplasmic reticulum (ER) membrane where it interacts with transcriptional repressors PtoMYB221 and PtoMYB156. This specific interaction allows for the translocation of TFs PtoMYB221 and PtoMYB156 to the ER and reduces their repression activity in a PtoUBC34 abundance-dependent manner. By taking a molecular biology approach with quantitative real-time polymerase chain reaction (qRT-PCR) analysis, we found that PtoUBC34 is expressed in all aboveground tissues of trees in P. tomentosa, and in particular, it is ubiquitous in all distinct differentiation stages across wood formation, including phloem differentiation, cambium maintaining, early and developing xylem differentiation, secondary cell wall thickening, and programmed cell death. Additionally, we discovered that PtoUBC34 is induced by treatment with sodium chloride and heat shock.

CONCLUSIONS

Our data suggest a possible mechanism by which lignin biosynthesis is regulated by ER-localized PtoUBC34 in poplar, probably through the ER-associated degradation (ERAD) of lignin-associated repressors PtoMYB221 and PtoMYB156.


DOI: 10.1186/s12870-019-1697-y
PubMed: 30866808
PubMed Central: PMC6416899


Affiliations:


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<name sortKey="Wei, Jianhua" sort="Wei, Jianhua" uniqKey="Wei J" first="Jianhua" last="Wei">Jianhua Wei</name>
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<name sortKey="Wang, Hongzhi" sort="Wang, Hongzhi" uniqKey="Wang H" first="Hongzhi" last="Wang">Hongzhi Wang</name>
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<term>Cell Wall (metabolism)</term>
<term>Endoplasmic Reticulum (metabolism)</term>
<term>Endoplasmic Reticulum-Associated Degradation (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Lignin (biosynthesis)</term>
<term>Phloem (genetics)</term>
<term>Phloem (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (genetics)</term>
<term>Populus (metabolism)</term>
<term>Transcription Factors (genetics)</term>
<term>Transcription Factors (metabolism)</term>
<term>Ubiquitin-Conjugating Enzymes (genetics)</term>
<term>Ubiquitin-Conjugating Enzymes (metabolism)</term>
<term>Wood (genetics)</term>
<term>Wood (metabolism)</term>
<term>Xylem (genetics)</term>
<term>Xylem (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Bois (génétique)</term>
<term>Bois (métabolisme)</term>
<term>Dégradation associée au réticulum endoplasmique (MeSH)</term>
<term>Facteurs de transcription (génétique)</term>
<term>Facteurs de transcription (métabolisme)</term>
<term>Lignine (biosynthèse)</term>
<term>Paroi cellulaire (métabolisme)</term>
<term>Phloème (génétique)</term>
<term>Phloème (métabolisme)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Réticulum endoplasmique (métabolisme)</term>
<term>Ubiquitin-conjugating enzymes (génétique)</term>
<term>Ubiquitin-conjugating enzymes (métabolisme)</term>
<term>Xylème (génétique)</term>
<term>Xylème (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en">
<term>Lignin</term>
</keywords>
<keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr">
<term>Lignine</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Phloem</term>
<term>Plant Proteins</term>
<term>Populus</term>
<term>Transcription Factors</term>
<term>Ubiquitin-Conjugating Enzymes</term>
<term>Wood</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Bois</term>
<term>Facteurs de transcription</term>
<term>Phloème</term>
<term>Populus</term>
<term>Protéines végétales</term>
<term>Ubiquitin-conjugating enzymes</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Wall</term>
<term>Endoplasmic Reticulum</term>
<term>Phloem</term>
<term>Plant Proteins</term>
<term>Populus</term>
<term>Transcription Factors</term>
<term>Ubiquitin-Conjugating Enzymes</term>
<term>Wood</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Bois</term>
<term>Facteurs de transcription</term>
<term>Paroi cellulaire</term>
<term>Phloème</term>
<term>Populus</term>
<term>Protéines végétales</term>
<term>Réticulum endoplasmique</term>
<term>Ubiquitin-conjugating enzymes</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Endoplasmic Reticulum-Associated Degradation</term>
<term>Gene Expression Regulation, Plant</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Dégradation associée au réticulum endoplasmique</term>
<term>Régulation de l'expression des gènes végétaux</term>
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<div type="abstract" xml:lang="en">
<p>
<b>BACKGROUND</b>
</p>
<p>Regulation of lignin biosynthesis is known to occur at the level of transcription factors (TFs), of which R2R3-MYB family members have been proposed to play a central role via the AC cis-elements. Despite the important roles of TFs in lignin biosynthesis, the post-translational regulation of these TFs, particularly their ubiquitination regulation, has not been thoroughly explored.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>RESULTS</b>
</p>
<p>We describe the discovery of a Populus tomentosa E2 ubiquitin-conjugating enzyme 34 (PtoUBC34), which is involved in the post-translational regulation of transactivation activity of lignin-associated transcriptional repressors PtoMYB221 and PtoMYB156. PtoUBC34 is localized at the endoplasmic reticulum (ER) membrane where it interacts with transcriptional repressors PtoMYB221 and PtoMYB156. This specific interaction allows for the translocation of TFs PtoMYB221 and PtoMYB156 to the ER and reduces their repression activity in a PtoUBC34 abundance-dependent manner. By taking a molecular biology approach with quantitative real-time polymerase chain reaction (qRT-PCR) analysis, we found that PtoUBC34 is expressed in all aboveground tissues of trees in P. tomentosa, and in particular, it is ubiquitous in all distinct differentiation stages across wood formation, including phloem differentiation, cambium maintaining, early and developing xylem differentiation, secondary cell wall thickening, and programmed cell death. Additionally, we discovered that PtoUBC34 is induced by treatment with sodium chloride and heat shock.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>CONCLUSIONS</b>
</p>
<p>Our data suggest a possible mechanism by which lignin biosynthesis is regulated by ER-localized PtoUBC34 in poplar, probably through the ER-associated degradation (ERAD) of lignin-associated repressors PtoMYB221 and PtoMYB156.</p>
</div>
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<Month>03</Month>
<Day>19</Day>
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<DateRevised>
<Year>2020</Year>
<Month>02</Month>
<Day>25</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">1471-2229</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>19</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2019</Year>
<Month>Mar</Month>
<Day>12</Day>
</PubDate>
</JournalIssue>
<Title>BMC plant biology</Title>
<ISOAbbreviation>BMC Plant Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Endoplasmic reticulum-localized UBC34 interaction with lignin repressors MYB221 and MYB156 regulates the transactivity of the transcription factors in Populus tomentosa.</ArticleTitle>
<Pagination>
<MedlinePgn>97</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1186/s12870-019-1697-y</ELocationID>
<Abstract>
<AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Regulation of lignin biosynthesis is known to occur at the level of transcription factors (TFs), of which R2R3-MYB family members have been proposed to play a central role via the AC cis-elements. Despite the important roles of TFs in lignin biosynthesis, the post-translational regulation of these TFs, particularly their ubiquitination regulation, has not been thoroughly explored.</AbstractText>
<AbstractText Label="RESULTS" NlmCategory="RESULTS">We describe the discovery of a Populus tomentosa E2 ubiquitin-conjugating enzyme 34 (PtoUBC34), which is involved in the post-translational regulation of transactivation activity of lignin-associated transcriptional repressors PtoMYB221 and PtoMYB156. PtoUBC34 is localized at the endoplasmic reticulum (ER) membrane where it interacts with transcriptional repressors PtoMYB221 and PtoMYB156. This specific interaction allows for the translocation of TFs PtoMYB221 and PtoMYB156 to the ER and reduces their repression activity in a PtoUBC34 abundance-dependent manner. By taking a molecular biology approach with quantitative real-time polymerase chain reaction (qRT-PCR) analysis, we found that PtoUBC34 is expressed in all aboveground tissues of trees in P. tomentosa, and in particular, it is ubiquitous in all distinct differentiation stages across wood formation, including phloem differentiation, cambium maintaining, early and developing xylem differentiation, secondary cell wall thickening, and programmed cell death. Additionally, we discovered that PtoUBC34 is induced by treatment with sodium chloride and heat shock.</AbstractText>
<AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Our data suggest a possible mechanism by which lignin biosynthesis is regulated by ER-localized PtoUBC34 in poplar, probably through the ER-associated degradation (ERAD) of lignin-associated repressors PtoMYB221 and PtoMYB156.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zheng</LastName>
<ForeName>Lin</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Yajuan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ding</LastName>
<ForeName>Dong</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhou</LastName>
<ForeName>Ying</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ding</LastName>
<ForeName>Liping</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wei</LastName>
<ForeName>Jianhua</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China. weijianhua@baafs.net.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China. weijianhua@baafs.net.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Hongzhi</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-9052-9319</Identifier>
<AffiliationInfo>
<Affiliation>Beijing Agro-Biotechnology Research Center, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China. wanghongzhi@baafs.net.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Beijing Academy of Agricultural and Forestry Sciences, No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097, People's Republic of China. wanghongzhi@baafs.net.cn.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>31770708</GrantID>
<Agency>National Natural Science Foundation of China</Agency>
<Country></Country>
</Grant>
<Grant>
<GrantID>31270593</GrantID>
<Agency>National Natural Science Foundation of China</Agency>
<Country></Country>
</Grant>
<Grant>
<GrantID>2016YFD0600104</GrantID>
<Agency>National Key R&D Program of China</Agency>
<Country></Country>
</Grant>
<Grant>
<GrantID>KJCX20170203</GrantID>
<Agency>Science Foundation of the Beijing Academy of Agriculture and Forestry Sciences</Agency>
<Country></Country>
</Grant>
<Grant>
<GrantID>2018ZX0802002</GrantID>
<Agency>National Key Program on Transgenic Research of China</Agency>
<Country></Country>
</Grant>
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<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>03</Month>
<Day>12</Day>
</ArticleDate>
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<Country>England</Country>
<MedlineTA>BMC Plant Biol</MedlineTA>
<NlmUniqueID>100967807</NlmUniqueID>
<ISSNLinking>1471-2229</ISSNLinking>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>9005-53-2</RegistryNumber>
<NameOfSubstance UI="D008031">Lignin</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 2.3.2.23</RegistryNumber>
<NameOfSubstance UI="D044763">Ubiquitin-Conjugating Enzymes</NameOfSubstance>
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<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002473" MajorTopicYN="N">Cell Wall</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004721" MajorTopicYN="N">Endoplasmic Reticulum</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060746" MajorTopicYN="Y">Endoplasmic Reticulum-Associated Degradation</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D008031" MajorTopicYN="N">Lignin</DescriptorName>
<QualifierName UI="Q000096" MajorTopicYN="Y">biosynthesis</QualifierName>
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<MeshHeading>
<DescriptorName UI="D052585" MajorTopicYN="N">Phloem</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
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<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="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">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="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D044763" MajorTopicYN="N">Ubiquitin-Conjugating Enzymes</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014934" MajorTopicYN="N">Wood</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D052584" MajorTopicYN="N">Xylem</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
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<Keyword MajorTopicYN="N">ER-associated degradation</Keyword>
<Keyword MajorTopicYN="N">Lignin biosynthesis</Keyword>
<Keyword MajorTopicYN="N">PtoMYB156</Keyword>
<Keyword MajorTopicYN="N">PtoMYB221</Keyword>
<Keyword MajorTopicYN="N">PtoUBC34</Keyword>
<Keyword MajorTopicYN="N">Transcriptional repressor</Keyword>
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<Year>2019</Year>
<Month>02</Month>
<Day>27</Day>
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