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Title: Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation

Abstract

Screening of commercially available fluoro monosaccharides as putative growth inhibitors in Arabidopsis thaliana revealed that 2-fluoro 2-l-fucose (2F-Fuc) reduces root growth at micromolar concentrations. The inability of 2F-Fuc to affect an Atfkgp mutant that is defective in the fucose salvage pathway indicates that 2F-Fuc must be converted to its cognate GDP nucleotide sugar in order to inhibit root growth. Chemical analysis of cell wall polysaccharides and glycoproteins demonstrated that fucosylation of xyloglucans and of N-linked glycans is fully inhibited by 10 μm 2F-Fuc in Arabidopsis seedling roots, but genetic evidence indicates that these alterations are not responsible for the inhibition of root development by 2F-Fuc. Inhibition of fucosylation of cell wall polysaccharides also affected pectic rhamnogalacturonan-II (RG-II). At low concentrations, 2F-Fuc induced a decrease in RG-II dimerization. Both RG-II dimerization and root growth were partially restored in 2F-Fuc-treated seedlings by addition of boric acid, suggesting that the growth phenotype caused by 2F-Fuc was due to a deficiency of RG-II dimerization. Closer investigation of the 2F-Fuc-induced growth phenotype demonstrated that cell division is not affected by 2F-Fuc treatments. In contrast, the inhibitor suppressed elongation of root cells and promoted the emergence of adventitious roots. This study further emphasizes the importance ofmore » RG-II in cell elongation and the utility of glycosyltransferase inhibitors as new tools for studying the functions of cell wall polysaccharides in plant development. Moreover, supplementation experiments with borate suggest that the function of boron in plants might not be restricted to RG-II cross-linking, but that it might also be a signal molecule in the cell wall integrity-sensing mechanism.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1]
  1. Laboratoire Glycobiologie et Matrice Extracellulaire Végétale, EA 4358, IRIB, VASI, Normandie Université, 76821 Mont-Saint-Aignan France
  2. Institut de Chimie Moléculaire et des Matériaux d'Orsay (ICMMO) UMR CNRS 8182, Université de Paris Sud, 91405 Orsay France; Institut de Chimie des Substances Naturelles (ICSN) UPR CNRS 2301, 91198 Gif-sur-Yvette France; Click4Tag, Zone Luminy Biotech, Case 922, 163 Avenue de Luminy 13009 Marseille France
  3. Centre de Recherches sur les Macromolécules Végétales (CERMAV) - CNRS BP 53, 38041 Grenoble Cedex 9 France
  4. Department of Biology and Center for Lignocellulose Structure and Formation, Pennsylvania State University, University Park Pennsylvania USA
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1370829
DOE Contract Number:  
SC0001090
Resource Type:
Journal Article
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 84; Journal Issue: 6; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; biofuels (including algae and biomass), bio-inspired, membrane, carbon sequestration, materials and chemistry by design, synthesis (self-assembly)

Citation Formats

Dumont, Marie, Lehner, Arnaud, Bardor, Muriel, Burel, Carole, Vauzeilles, Boris, Lerouxel, Olivier, Anderson, Charles T., Mollet, Jean-Claude, and Lerouge, Patrice. Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation. United States: N. p., 2015. Web. doi:10.1111/tpj.13071.
Dumont, Marie, Lehner, Arnaud, Bardor, Muriel, Burel, Carole, Vauzeilles, Boris, Lerouxel, Olivier, Anderson, Charles T., Mollet, Jean-Claude, & Lerouge, Patrice. Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation. United States. https://doi.org/10.1111/tpj.13071
Dumont, Marie, Lehner, Arnaud, Bardor, Muriel, Burel, Carole, Vauzeilles, Boris, Lerouxel, Olivier, Anderson, Charles T., Mollet, Jean-Claude, and Lerouge, Patrice. 2015. "Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation". United States. https://doi.org/10.1111/tpj.13071.
@article{osti_1370829,
title = {Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation},
author = {Dumont, Marie and Lehner, Arnaud and Bardor, Muriel and Burel, Carole and Vauzeilles, Boris and Lerouxel, Olivier and Anderson, Charles T. and Mollet, Jean-Claude and Lerouge, Patrice},
abstractNote = {Screening of commercially available fluoro monosaccharides as putative growth inhibitors in Arabidopsis thaliana revealed that 2-fluoro 2-l-fucose (2F-Fuc) reduces root growth at micromolar concentrations. The inability of 2F-Fuc to affect an Atfkgp mutant that is defective in the fucose salvage pathway indicates that 2F-Fuc must be converted to its cognate GDP nucleotide sugar in order to inhibit root growth. Chemical analysis of cell wall polysaccharides and glycoproteins demonstrated that fucosylation of xyloglucans and of N-linked glycans is fully inhibited by 10 μm 2F-Fuc in Arabidopsis seedling roots, but genetic evidence indicates that these alterations are not responsible for the inhibition of root development by 2F-Fuc. Inhibition of fucosylation of cell wall polysaccharides also affected pectic rhamnogalacturonan-II (RG-II). At low concentrations, 2F-Fuc induced a decrease in RG-II dimerization. Both RG-II dimerization and root growth were partially restored in 2F-Fuc-treated seedlings by addition of boric acid, suggesting that the growth phenotype caused by 2F-Fuc was due to a deficiency of RG-II dimerization. Closer investigation of the 2F-Fuc-induced growth phenotype demonstrated that cell division is not affected by 2F-Fuc treatments. In contrast, the inhibitor suppressed elongation of root cells and promoted the emergence of adventitious roots. This study further emphasizes the importance of RG-II in cell elongation and the utility of glycosyltransferase inhibitors as new tools for studying the functions of cell wall polysaccharides in plant development. Moreover, supplementation experiments with borate suggest that the function of boron in plants might not be restricted to RG-II cross-linking, but that it might also be a signal molecule in the cell wall integrity-sensing mechanism.},
doi = {10.1111/tpj.13071},
url = {https://www.osti.gov/biblio/1370829}, journal = {The Plant Journal},
issn = {0960-7412},
number = 6,
volume = 84,
place = {United States},
year = {Tue Dec 01 00:00:00 EST 2015},
month = {Tue Dec 01 00:00:00 EST 2015}
}

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