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

Marie Dumont, Arnaud Lehner, Muriel Bardor, Carole Burel, Boris Vauzeilles, Olivier Lerouxel, Charles T. Anderson, Jean Claude Mollet, Patrice Lerouge

Research output: Contribution to journalArticle

10 Citations (Scopus)

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 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. Significance Statement Genetic mutants are not always ideal for studying the roles of glycosyltransferases, due to redundancy and/or lethality. Here we demonstrate that fluoro-monosaccharide analogues, which inhibit sugar transferases, are useful tools for studying the functions of cell wall polysaccharides in plant development.

Original languageEnglish (US)
Pages (from-to)1137-1151
Number of pages15
JournalPlant Journal
Volume84
Issue number6
DOIs
StatePublished - Dec 1 2015

Fingerprint

Fucose
fucose
cell wall components
Cellular Structures
Cell Wall
cell growth
Polysaccharides
polysaccharides
cell walls
dimerization
root growth
Dimerization
glycosyltransferases
Growth
Glycosyltransferases
Plant Development
Monosaccharides
monosaccharides
Seedlings
Guanosine Diphosphate Sugars

All Science Journal Classification (ASJC) codes

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Dumont, M., Lehner, A., Bardor, M., Burel, C., Vauzeilles, B., Lerouxel, O., ... Lerouge, P. (2015). Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation. Plant Journal, 84(6), 1137-1151. 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 ; Lerouge, Patrice. / Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation. In: Plant Journal. 2015 ; Vol. 84, No. 6. pp. 1137-1151.
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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 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. Significance Statement Genetic mutants are not always ideal for studying the roles of glycosyltransferases, due to redundancy and/or lethality. Here we demonstrate that fluoro-monosaccharide analogues, which inhibit sugar transferases, are useful tools for studying the functions of cell wall polysaccharides in plant development.",
author = "Marie Dumont and Arnaud Lehner and Muriel Bardor and Carole Burel and Boris Vauzeilles and Olivier Lerouxel and Anderson, {Charles T.} and Mollet, {Jean Claude} and Patrice Lerouge",
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Dumont, M, Lehner, A, Bardor, M, Burel, C, Vauzeilles, B, Lerouxel, O, Anderson, CT, Mollet, JC & Lerouge, P 2015, 'Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation', Plant Journal, vol. 84, no. 6, pp. 1137-1151. https://doi.org/10.1111/tpj.13071

Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation. / Dumont, Marie; Lehner, Arnaud; Bardor, Muriel; Burel, Carole; Vauzeilles, Boris; Lerouxel, Olivier; Anderson, Charles T.; Mollet, Jean Claude; Lerouge, Patrice.

In: Plant Journal, Vol. 84, No. 6, 01.12.2015, p. 1137-1151.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Inhibition of fucosylation of cell wall components by 2-fluoro 2-deoxy- l -fucose induces defects in root cell elongation

AU - Dumont, Marie

AU - Lehner, Arnaud

AU - Bardor, Muriel

AU - Burel, Carole

AU - Vauzeilles, Boris

AU - Lerouxel, Olivier

AU - Anderson, Charles T.

AU - Mollet, Jean Claude

AU - Lerouge, Patrice

PY - 2015/12/1

Y1 - 2015/12/1

N2 - 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. Significance Statement Genetic mutants are not always ideal for studying the roles of glycosyltransferases, due to redundancy and/or lethality. Here we demonstrate that fluoro-monosaccharide analogues, which inhibit sugar transferases, are useful tools for studying the functions of cell wall polysaccharides in plant development.

AB - 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. Significance Statement Genetic mutants are not always ideal for studying the roles of glycosyltransferases, due to redundancy and/or lethality. Here we demonstrate that fluoro-monosaccharide analogues, which inhibit sugar transferases, are useful tools for studying the functions of cell wall polysaccharides in plant development.

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