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Gain-of-function mutation of AtDICE1, encoding a putative endoplasmic reticulum-localized membrane protein, causes defects in anisotropic cell elongation by disturbing cell wall integrity in Arabidopsis.

Identifieur interne : 000E83 ( Main/Exploration ); précédent : 000E82; suivant : 000E84

Gain-of-function mutation of AtDICE1, encoding a putative endoplasmic reticulum-localized membrane protein, causes defects in anisotropic cell elongation by disturbing cell wall integrity in Arabidopsis.

Auteurs : Phi-Yen Le [Corée du Sud] ; Hyung-Woo Jeon [Corée du Sud] ; Min-Ha Kim [Corée du Sud] ; Eung-Jun Park [Corée du Sud] ; Hyoshin Lee [Corée du Sud] ; Indeok Hwang [États-Unis] ; Kyung-Hwan Han [États-Unis] ; Jae-Heung Ko [Corée du Sud]

Source :

RBID : pubmed:29659701

Descripteurs français

English descriptors

Abstract

Background and Aims

Anisotropic cell elongation depends on cell wall relaxation and cellulose microfibril arrangement. The aim of this study was to characterize the molecular function of AtDICE1 encoding a novel transmembrane protein involved in anisotropic cell elongation in Arabidopsis.

Methods

Phenotypic characterizations of transgenic Arabidopsis plants mis-regulating AtDICE1 expression with different pharmacological treatments were made, and biochemical, cell biological and transcriptome analyses were performed.

Key Results

Upregulation of AtDICE1 in Arabidopsis (35S::AtDICE1) resulted in severe dwarfism, probably caused by defects in anisotropic cell elongation. Epidermal cell swelling was evident in all tissues, and abnormal secondary wall thickenings were observed in pith cells of stems. These phenotypes were reproduced not only by inducible expression of AtDICE1 but also by overexpression of its poplar homologue in Arabidopsis. RNA interference suppression lines of AtDICE1 resulted in no observable phenotypic changes. Interestingly, wild-type plants treated with isoxaben, a cellulose biosynthesis inhibitor, phenocopied the 35S::AtDICE1 plants, suggesting that cellulose biosynthesis was compromised in the 35S::AtDICE1 plants. Indeed, disturbed cortical microtubule arrangements in 35S::AtDICE1/GFP-TuA6 plants were observed, and the cellulose content was significantly reduced in 35S::AtDICE1 plants. A promoter::GUS analysis showed that AtDICE1 is mainly expressed in vascular tissue, and transient expression of GFP:AtDICE1 in tobacco suggests that AtDICE1 is probably localized in the endoplasmic reticulum (ER). In addition, the external N-terminal conserved domain of AtDICE1 was found to be necessary for AtDICE1 function. Whole transcriptome analyses of 35S::AtDICE1 revealed that many genes involved in cell wall modification and stress/defence responses were mis-regulated.

Conclusions

AtDICE1, a novel ER-localized transmembrane protein, may contribute to anisotropic cell elongation in the formation of vascular tissue by affecting cellulose biosynthesis.


DOI: 10.1093/aob/mcy049
PubMed: 29659701
PubMed Central: PMC6025203


Affiliations:


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Le document en format XML

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<keywords scheme="KwdEn" xml:lang="en">
<term>Anisotropy (MeSH)</term>
<term>Arabidopsis (cytology)</term>
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (physiology)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Arabidopsis Proteins (metabolism)</term>
<term>Cell Enlargement (MeSH)</term>
<term>Cell Wall (metabolism)</term>
<term>Cellulose (metabolism)</term>
<term>Endoplasmic Reticulum (metabolism)</term>
<term>Endoplasmic Reticulum Stress (MeSH)</term>
<term>Gain of Function Mutation (MeSH)</term>
<term>Membrane Proteins (genetics)</term>
<term>Membrane Proteins (metabolism)</term>
<term>Microtubules (metabolism)</term>
<term>Phenotype (MeSH)</term>
<term>Plant Vascular Bundle (cytology)</term>
<term>Plant Vascular Bundle (genetics)</term>
<term>Plant Vascular Bundle (physiology)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Populus (genetics)</term>
<term>Promoter Regions, Genetic (genetics)</term>
<term>Tobacco (cytology)</term>
<term>Tobacco (genetics)</term>
<term>Tobacco (physiology)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Anisotropie (MeSH)</term>
<term>Arabidopsis (cytologie)</term>
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (physiologie)</term>
<term>Augmentation de la taille cellulaire (MeSH)</term>
<term>Cellulose (métabolisme)</term>
<term>Faisceau vasculaire des plantes (cytologie)</term>
<term>Faisceau vasculaire des plantes (génétique)</term>
<term>Faisceau vasculaire des plantes (physiologie)</term>
<term>Microtubules (métabolisme)</term>
<term>Mutation gain de fonction (MeSH)</term>
<term>Paroi cellulaire (métabolisme)</term>
<term>Phénotype (MeSH)</term>
<term>Populus (génétique)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines d'Arabidopsis (métabolisme)</term>
<term>Protéines membranaires (génétique)</term>
<term>Protéines membranaires (métabolisme)</term>
<term>Régions promotrices (génétique) (génétique)</term>
<term>Réticulum endoplasmique (métabolisme)</term>
<term>Stress du réticulum endoplasmique (MeSH)</term>
<term>Tabac (cytologie)</term>
<term>Tabac (génétique)</term>
<term>Tabac (physiologie)</term>
<term>Transcriptome (MeSH)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Arabidopsis Proteins</term>
<term>Membrane Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="cytologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Faisceau vasculaire des plantes</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en">
<term>Arabidopsis</term>
<term>Plant Vascular Bundle</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Arabidopsis</term>
<term>Plant Vascular Bundle</term>
<term>Populus</term>
<term>Promoter Regions, Genetic</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Arabidopsis</term>
<term>Faisceau vasculaire des plantes</term>
<term>Populus</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines membranaires</term>
<term>Régions promotrices (génétique)</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Arabidopsis Proteins</term>
<term>Cell Wall</term>
<term>Cellulose</term>
<term>Endoplasmic Reticulum</term>
<term>Membrane Proteins</term>
<term>Microtubules</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Cellulose</term>
<term>Microtubules</term>
<term>Paroi cellulaire</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines membranaires</term>
<term>Réticulum endoplasmique</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Faisceau vasculaire des plantes</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Arabidopsis</term>
<term>Plant Vascular Bundle</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Anisotropy</term>
<term>Cell Enlargement</term>
<term>Endoplasmic Reticulum Stress</term>
<term>Gain of Function Mutation</term>
<term>Phenotype</term>
<term>Plants, Genetically Modified</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Anisotropie</term>
<term>Augmentation de la taille cellulaire</term>
<term>Mutation gain de fonction</term>
<term>Phénotype</term>
<term>Stress du réticulum endoplasmique</term>
<term>Transcriptome</term>
<term>Végétaux génétiquement modifiés</term>
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<front>
<div type="abstract" xml:lang="en">
<p>
<b>Background and Aims</b>
</p>
<p>Anisotropic cell elongation depends on cell wall relaxation and cellulose microfibril arrangement. The aim of this study was to characterize the molecular function of AtDICE1 encoding a novel transmembrane protein involved in anisotropic cell elongation in Arabidopsis.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>Methods</b>
</p>
<p>Phenotypic characterizations of transgenic Arabidopsis plants mis-regulating AtDICE1 expression with different pharmacological treatments were made, and biochemical, cell biological and transcriptome analyses were performed.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>Key Results</b>
</p>
<p>Upregulation of AtDICE1 in Arabidopsis (35S::AtDICE1) resulted in severe dwarfism, probably caused by defects in anisotropic cell elongation. Epidermal cell swelling was evident in all tissues, and abnormal secondary wall thickenings were observed in pith cells of stems. These phenotypes were reproduced not only by inducible expression of AtDICE1 but also by overexpression of its poplar homologue in Arabidopsis. RNA interference suppression lines of AtDICE1 resulted in no observable phenotypic changes. Interestingly, wild-type plants treated with isoxaben, a cellulose biosynthesis inhibitor, phenocopied the 35S::AtDICE1 plants, suggesting that cellulose biosynthesis was compromised in the 35S::AtDICE1 plants. Indeed, disturbed cortical microtubule arrangements in 35S::AtDICE1/GFP-TuA6 plants were observed, and the cellulose content was significantly reduced in 35S::AtDICE1 plants. A promoter::GUS analysis showed that AtDICE1 is mainly expressed in vascular tissue, and transient expression of GFP:AtDICE1 in tobacco suggests that AtDICE1 is probably localized in the endoplasmic reticulum (ER). In addition, the external N-terminal conserved domain of AtDICE1 was found to be necessary for AtDICE1 function. Whole transcriptome analyses of 35S::AtDICE1 revealed that many genes involved in cell wall modification and stress/defence responses were mis-regulated.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>Conclusions</b>
</p>
<p>AtDICE1, a novel ER-localized transmembrane protein, may contribute to anisotropic cell elongation in the formation of vascular tissue by affecting cellulose biosynthesis.</p>
</div>
</front>
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<Year>2019</Year>
<Month>08</Month>
<Day>27</Day>
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<Year>2019</Year>
<Month>10</Month>
<Day>29</Day>
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<Volume>122</Volume>
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<Month>06</Month>
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<Title>Annals of botany</Title>
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<AbstractText Label="Background and Aims">Anisotropic cell elongation depends on cell wall relaxation and cellulose microfibril arrangement. The aim of this study was to characterize the molecular function of AtDICE1 encoding a novel transmembrane protein involved in anisotropic cell elongation in Arabidopsis.</AbstractText>
<AbstractText Label="Methods">Phenotypic characterizations of transgenic Arabidopsis plants mis-regulating AtDICE1 expression with different pharmacological treatments were made, and biochemical, cell biological and transcriptome analyses were performed.</AbstractText>
<AbstractText Label="Key Results">Upregulation of AtDICE1 in Arabidopsis (35S::AtDICE1) resulted in severe dwarfism, probably caused by defects in anisotropic cell elongation. Epidermal cell swelling was evident in all tissues, and abnormal secondary wall thickenings were observed in pith cells of stems. These phenotypes were reproduced not only by inducible expression of AtDICE1 but also by overexpression of its poplar homologue in Arabidopsis. RNA interference suppression lines of AtDICE1 resulted in no observable phenotypic changes. Interestingly, wild-type plants treated with isoxaben, a cellulose biosynthesis inhibitor, phenocopied the 35S::AtDICE1 plants, suggesting that cellulose biosynthesis was compromised in the 35S::AtDICE1 plants. Indeed, disturbed cortical microtubule arrangements in 35S::AtDICE1/GFP-TuA6 plants were observed, and the cellulose content was significantly reduced in 35S::AtDICE1 plants. A promoter::GUS analysis showed that AtDICE1 is mainly expressed in vascular tissue, and transient expression of GFP:AtDICE1 in tobacco suggests that AtDICE1 is probably localized in the endoplasmic reticulum (ER). In addition, the external N-terminal conserved domain of AtDICE1 was found to be necessary for AtDICE1 function. Whole transcriptome analyses of 35S::AtDICE1 revealed that many genes involved in cell wall modification and stress/defence responses were mis-regulated.</AbstractText>
<AbstractText Label="Conclusions">AtDICE1, a novel ER-localized transmembrane protein, may contribute to anisotropic cell elongation in the formation of vascular tissue by affecting cellulose biosynthesis.</AbstractText>
</Abstract>
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<LastName>Le</LastName>
<ForeName>Phi-Yen</ForeName>
<Initials>PY</Initials>
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<Affiliation>Department of Plant & Environmental New Resources, Kyung Hee University, Yongin, Republic of Korea.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jeon</LastName>
<ForeName>Hyung-Woo</ForeName>
<Initials>HW</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant & Environmental New Resources, Kyung Hee University, Yongin, Republic of Korea.</Affiliation>
</AffiliationInfo>
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<ForeName>Min-Ha</ForeName>
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<Affiliation>Department of Plant & Environmental New Resources, Kyung Hee University, Yongin, Republic of Korea.</Affiliation>
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<ForeName>Eung-Jun</ForeName>
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<Affiliation>Division of Forest Biotechnology, Korea Forest Research Institute, Suwon, Republic of Korea.</Affiliation>
</AffiliationInfo>
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<LastName>Lee</LastName>
<ForeName>Hyoshin</ForeName>
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