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Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus.

Identifieur interne : 001A78 ( Main/Exploration ); précédent : 001A77; suivant : 001A79

Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus.

Auteurs : Prashant S. Swamy [États-Unis] ; Hao Hu [États-Unis] ; Sivakumar Pattathil [États-Unis] ; Victoria J. Maloney [Canada] ; Hui Xiao [États-Unis] ; Liang-Jiao Xue [États-Unis] ; Jeng-Der Chung [Taïwan] ; Virgil E. Johnson [États-Unis] ; Yingying Zhu [États-Unis] ; Gary F. Peter [États-Unis] ; Michael G. Hahn [États-Unis] ; Shawn D. Mansfield [Canada] ; Scott A. Harding [États-Unis] ; Chung-Jui Tsai [États-Unis]

Source :

RBID : pubmed:26246616

Descripteurs français

English descriptors

Abstract

Cortical microtubules are integral to plant morphogenesis, cell wall synthesis, and stomatal behaviour, presumably by governing cellulose microfibril orientation. Genetic manipulation of tubulins often leads to abnormal plant development, making it difficult to probe additional roles of cortical microtubules in cell wall biogenesis. Here, it is shown that expressing post-translational C-terminal modification mimics of α-tubulin altered cell wall characteristics and guard cell dynamics in transgenic Populus tremula x alba that otherwise appear normal. 35S promoter-driven transgene expression was high in leaves but unusually low in xylem, suggesting high levels of tubulin transgene expression were not tolerated in wood-forming tissues during regeneration of transformants. Cellulose, hemicellulose, and lignin contents were unaffected in transgenic wood, but expression of cell wall-modifying enzymes, and extractability of lignin-bound pectin and xylan polysaccharides were increased in developing xylem. The results suggest that pectin and xylan polysaccharides deposited early during cell wall biogenesis are more sensitive to subtle tubulin perturbation than cellulose and matrix polysaccharides deposited later. Tubulin perturbation also affected guard cell behaviour, delaying drought-induced stomatal closure as well as light-induced stomatal opening in leaves. Pectins have been shown to confer cell wall flexibility critical for reversible stomatal movement, and results presented here are consistent with microtubule involvement in this process. Taken together, the data show the value of growth-compatible tubulin perturbations for discerning microtubule functions, and add to the growing body of evidence for microtubule involvement in non-cellulosic polysaccharide assembly during cell wall biogenesis.

DOI: 10.1093/jxb/erv383
PubMed: 26246616
PubMed Central: PMC4588895


Affiliations:


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<name sortKey="Xiao, Hui" sort="Xiao, Hui" uniqKey="Xiao H" first="Hui" last="Xiao">Hui Xiao</name>
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<name sortKey="Xue, Liang Jiao" sort="Xue, Liang Jiao" uniqKey="Xue L" first="Liang-Jiao" last="Xue">Liang-Jiao Xue</name>
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<name sortKey="Johnson, Virgil E" sort="Johnson, Virgil E" uniqKey="Johnson V" first="Virgil E" last="Johnson">Virgil E. Johnson</name>
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<name sortKey="Zhu, Yingying" sort="Zhu, Yingying" uniqKey="Zhu Y" first="Yingying" last="Zhu">Yingying Zhu</name>
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<name sortKey="Hahn, Michael G" sort="Hahn, Michael G" uniqKey="Hahn M" first="Michael G" last="Hahn">Michael G. Hahn</name>
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<name sortKey="Tsai, Chung Jui" sort="Tsai, Chung Jui" uniqKey="Tsai C" first="Chung-Jui" last="Tsai">Chung-Jui Tsai</name>
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<title level="j">Journal of experimental botany</title>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Cell Wall (physiology)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Stomata (physiology)</term>
<term>Populus (genetics)</term>
<term>Populus (physiology)</term>
<term>Protein Processing, Post-Translational (MeSH)</term>
<term>Tubulin (genetics)</term>
<term>Tubulin (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Maturation post-traductionnelle des protéines (MeSH)</term>
<term>Paroi cellulaire (physiologie)</term>
<term>Populus (génétique)</term>
<term>Populus (physiologie)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Stomates de plante (physiologie)</term>
<term>Tubuline (génétique)</term>
<term>Tubuline (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Plant Proteins</term>
<term>Tubulin</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Plant Proteins</term>
<term>Tubulin</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>
<term>Protéines végétales</term>
<term>Tubuline</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Protéines végétales</term>
<term>Tubuline</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Paroi cellulaire</term>
<term>Populus</term>
<term>Stomates de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Cell Wall</term>
<term>Plant Stomata</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
<term>Protein Processing, Post-Translational</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Maturation post-traductionnelle des protéines</term>
<term>Régulation de l'expression des gènes végétaux</term>
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<div type="abstract" xml:lang="en">Cortical microtubules are integral to plant morphogenesis, cell wall synthesis, and stomatal behaviour, presumably by governing cellulose microfibril orientation. Genetic manipulation of tubulins often leads to abnormal plant development, making it difficult to probe additional roles of cortical microtubules in cell wall biogenesis. Here, it is shown that expressing post-translational C-terminal modification mimics of α-tubulin altered cell wall characteristics and guard cell dynamics in transgenic Populus tremula x alba that otherwise appear normal. 35S promoter-driven transgene expression was high in leaves but unusually low in xylem, suggesting high levels of tubulin transgene expression were not tolerated in wood-forming tissues during regeneration of transformants. Cellulose, hemicellulose, and lignin contents were unaffected in transgenic wood, but expression of cell wall-modifying enzymes, and extractability of lignin-bound pectin and xylan polysaccharides were increased in developing xylem. The results suggest that pectin and xylan polysaccharides deposited early during cell wall biogenesis are more sensitive to subtle tubulin perturbation than cellulose and matrix polysaccharides deposited later. Tubulin perturbation also affected guard cell behaviour, delaying drought-induced stomatal closure as well as light-induced stomatal opening in leaves. Pectins have been shown to confer cell wall flexibility critical for reversible stomatal movement, and results presented here are consistent with microtubule involvement in this process. Taken together, the data show the value of growth-compatible tubulin perturbations for discerning microtubule functions, and add to the growing body of evidence for microtubule involvement in non-cellulosic polysaccharide assembly during cell wall biogenesis. </div>
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<Year>2016</Year>
<Month>07</Month>
<Day>19</Day>
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<Year>2018</Year>
<Month>11</Month>
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<Title>Journal of experimental botany</Title>
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<ArticleTitle>Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus.</ArticleTitle>
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<AbstractText>Cortical microtubules are integral to plant morphogenesis, cell wall synthesis, and stomatal behaviour, presumably by governing cellulose microfibril orientation. Genetic manipulation of tubulins often leads to abnormal plant development, making it difficult to probe additional roles of cortical microtubules in cell wall biogenesis. Here, it is shown that expressing post-translational C-terminal modification mimics of α-tubulin altered cell wall characteristics and guard cell dynamics in transgenic Populus tremula x alba that otherwise appear normal. 35S promoter-driven transgene expression was high in leaves but unusually low in xylem, suggesting high levels of tubulin transgene expression were not tolerated in wood-forming tissues during regeneration of transformants. Cellulose, hemicellulose, and lignin contents were unaffected in transgenic wood, but expression of cell wall-modifying enzymes, and extractability of lignin-bound pectin and xylan polysaccharides were increased in developing xylem. The results suggest that pectin and xylan polysaccharides deposited early during cell wall biogenesis are more sensitive to subtle tubulin perturbation than cellulose and matrix polysaccharides deposited later. Tubulin perturbation also affected guard cell behaviour, delaying drought-induced stomatal closure as well as light-induced stomatal opening in leaves. Pectins have been shown to confer cell wall flexibility critical for reversible stomatal movement, and results presented here are consistent with microtubule involvement in this process. Taken together, the data show the value of growth-compatible tubulin perturbations for discerning microtubule functions, and add to the growing body of evidence for microtubule involvement in non-cellulosic polysaccharide assembly during cell wall biogenesis. </AbstractText>
<CopyrightInformation>© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.</CopyrightInformation>
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<ForeName>Prashant S</ForeName>
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<LastName>Hu</LastName>
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<LastName>Tsai</LastName>
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