Structural characterisation of the pectic polysaccharide rhamnogalacturonan II using an acidic fingerprinting methodology

Séveno, Martial; Voxeur, Aline; Rihouey, Christophe; Wu, Aimin; Ishii, Tadashi; Chevalier, Christian; Ralet, Marie-Christine; Driouich, Azeddine; Marchant, Alan; Lerouge, Patrice

doi:10.1007/s00425-009-0996-1

Cited by 28 publications

(41 citation statements)

References 35 publications

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“…4, a and b). The fragmentation patterns were in full agreement with MS/MS data previously reported for the side chain A of Arabidopsis RG-II (18). This is the first reported fine structure of tomato RG-II, and the similarity with the Arabidopsis data further underlines the high level of RG II structural conservation in plants.…”

Section: Gme Silencing In Tomato Results In a Severe Reduction Of L-gsupporting

confidence: 78%

“…Due to the presence of an acidic-labile apiose residue at their reducing ends (Fig. 1), the side chains A and B can be specifically released by hydrolysis with 0.1 M trifluoracetic acid at 40°C (18). As shown in Fig.…”

Section: Gme Silencing In Tomato Results In a Severe Reduction Of L-gmentioning

confidence: 98%

“…Mild Acid Hydrolysis of RG-II-Mild acid hydrolysis was carried out as reported previously (18). One mg of purified RG-II was hydrolyzed in 200 l of 0.1 M trifluoroacetic acid for 16 h at 40°C.…”

Section: Methodsmentioning

confidence: 99%

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Silencing of the GDP-d-mannose 3,5-Epimerase Affects the Structure and Cross-linking of the Pectic Polysaccharide Rhamnogalacturonan II and Plant Growth in Tomato

Voxeur

Gilbert

Rihouey

et al. 2011

Journal of Biological Chemistry

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L-Galactose (L-Gal), a monosaccharide involved in L-ascorbate and rhamnogalacturonan II (RG-II) biosynthesis in plants, is produced in the cytosol by a GDP-D-mannose 3,5-epimerase (GME). It has been recently reported that the partial inactivation of GME induced growth defects affecting both cell division and cell expansion (Gilbert, L., Alhagdow, M., Nunes-Nesi, A., Quemener, B., Guillon, F., Bouchet, B., Faurobert, M., Gouble, B., Page, D., Garcia, V., Petit, J., Stevens, R., Causse, M., Fernie, A. R., Lahaye, M., Rothan, C., and Baldet, P. (2009) Plant J. 60, 499 -508). In the present study, we show that the silencing of the two GME genes in tomato leaves resulted in approximately a 60% decrease in terminal L-Gal content in the side chain A of RG-II as well as in a lower capacity of RG-II to perform in muro cross-linking. In addition, we show that unlike supplementation with L-Gal or ascorbate, supplementation of GME-silenced lines with boric acid was able to restore both the wild-type growth phenotype of tomato seedlings and an efficient in muro boronmediated cross-linking of RG-II. Our findings suggest that developmental phenotypes in GME-deficient lines are due to the structural alteration of RG-II and further underline the crucial role of the cross-linking of RG-II in the formation of the pectic network required for normal plant growth and development.In plant cells, L-galactose (L-Gal) is a monosaccharide that is synthesized by epimerization of GDP-D-mannose into GDP-Lgalactose (GDP-L-Gal) via the action of a cytosolic GDP-Dmannose 3,5-epimerase (GME, 2 EC 5.1.3.18) (1). GDP-L-Gal is used for the biosynthesis of L-ascorbate and cell wall polysaccharides. It can be converted into free L-Gal in the cytosol by a specific phosphorylase and phosphatase, and then into L-ascorbate (2, 3). Alternatively, GDP-L-Gal can be transferred into the Golgi apparatus and incorporated into cell wall polymers by the action of L-galactosyltransferases. So far, L-Gal has mainly been identified in rhamnogalacturonan II (RG-II) (4).Much attention has been paid to the biosynthesis of L-ascorbate to investigate the function of this vitamin as an antioxidant and as a regulator of plant development. No viable ascorbateless plants have ever been reported, thereby suggesting that vitamin C may be important for plant growth. Recently, it has been demonstrated that the partial inactivation of the GME in RNAi-silenced tomato (Solanum lycopersicum) lines resulted in a 40 -60% decrease of L-ascorbate content as well as growth defects affecting both cell division and cell expansion (5). These transgenic tomato lines also exhibited increased fragility and loss of fruit firmness. Furthermore, supplementation of RNAisilenced lines with L-Gal was able to restore the wild-type levels of L-ascorbate but did not rescue the growth defects (5). Together, these data suggest that growth phenotypes in GMEdeficient lines are most likely related to the alteration of L-Galcontaining polysaccharides such as RG-II rather than to L-ascorbate deficiency.Pecti...

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Section: Gme Silencing In Tomato Results In a Severe Reduction Of L-gsupporting

confidence: 78%

Section: Gme Silencing In Tomato Results In a Severe Reduction Of L-gmentioning

confidence: 98%

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Silencing of the GDP-d-mannose 3,5-Epimerase Affects the Structure and Cross-linking of the Pectic Polysaccharide Rhamnogalacturonan II and Plant Growth in Tomato

Voxeur

Gilbert

Rihouey

et al. 2011

Journal of Biological Chemistry

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“…Mild acid hydrolysis releases the side chains A–D of the complex pectin rhamnogalacturonan II (RG-II) from citrus pectin at their acid-labile branching points (Séveno et al, 2009). Y-type fragmentation patterns in positive ESI-MS/MS provide sequence information and enabled the structural identification while diagnostic ions derived by a loss of 296 and 340 Da resulting from cleavage of the AceA-rhamnose bond and ring-cleavage of AceA were found upon B-chain fragmentation.…”

Section: Selected Examplesmentioning

confidence: 99%

Mass Spectrometry for Characterizing Plant Cell Wall Polysaccharides

Bauer¹

2012

Front. Plant Sci.

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Mass spectrometry is a selective and powerful technique to obtain identification and structural information on compounds present in complex mixtures. Since it requires only small sample amount it is an excellent tool for researchers interested in detecting changes in composition of complex carbohydrates of plants. This mini-review gives an overview of common mass spectrometry techniques applied to the analysis of plant cell wall carbohydrates. It presents examples in which mass spectrometry has been used to elucidate the structure of oligosaccharides derived from hemicelluloses and pectins and illustrates how information on sequence, linkages, branching, and modifications are obtained from characteristic fragmentation patterns.

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“…Such natural differences typically involve variations in the external monosaccharides of a side chain (see Figure 1A) and have no discernible effect on borate cross-linking or plant growth. For example, side chain B exists predominantly as a heptasaccharide in Arabidopsis (Glushka et al, 2003) and rice (Thomas et al, 1989) RG-II and predominantly as a nonasaccharide in sycamore (Whitcombe et al, 1995), wine (Glushka et al, 2003), and citrus (Séveno et al, 2009). The B side chain of the RG-II isolated from the walls of several non-flowering plants contains terminal non-reducing 3- O -methyl rhamnose rather than terminal non-reducing rhamnose (Matsunaga et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

The Synthesis and Origin of the Pectic Polysaccharide Rhamnogalacturonan II – Insights from Nucleotide Sugar Formation and Diversity

Bar‐Peled¹,

Urbanowicz²,

O’Neill³

2012

Front. Plant Sci.

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There is compelling evidence showing that the structurally complex pectic polysaccharide rhamnogalacturonan II (RG-II) exists in the primary cell wall as a borate cross-linked dimer and that this dimer is required for the assembly of a functional wall and for normal plant growth and development. The results of several studies have also established that RG-II structure and cross-linking is conserved in vascular plants and that RG-II likely appeared early in the evolution of land plants. Two features that distinguish RG-II from other plant polysaccharides are that RG-II is composed of 13 different glycoses linked to each other by up to 22 different glycosidic linkages and that RG-II is the only polysaccharide known to contain both apiose and aceric acid. Thus, one key event in land plant evolution was the emergence of genes encoding nucleotide sugar biosynthetic enzymes that generate the activated forms of apiose and aceric acid required for RG-II synthesis. Many of the genes involved in the generation of the nucleotide sugars used for RG-II synthesis have been functionally characterized. By contrast, only one glycosyltransferase involved in the assembly of RG-II has been identified. Here we provide an overview of the formation of the activated sugars required for RG-II synthesis and point to the possible cellular and metabolic processes that could be involved in assembling and controlling the formation of a borate cross-linked RG-II molecule. We discuss how nucleotide sugar synthesis is compartmentalized and how this may control the flux of precursors to facilitate and regulate the formation of RG-II.

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Structural characterisation of the pectic polysaccharide rhamnogalacturonan II using an acidic fingerprinting methodology

Cited by 28 publications

References 35 publications

Silencing of the GDP-d-mannose 3,5-Epimerase Affects the Structure and Cross-linking of the Pectic Polysaccharide Rhamnogalacturonan II and Plant Growth in Tomato

Silencing of the GDP-d-mannose 3,5-Epimerase Affects the Structure and Cross-linking of the Pectic Polysaccharide Rhamnogalacturonan II and Plant Growth in Tomato

Mass Spectrometry for Characterizing Plant Cell Wall Polysaccharides

The Synthesis and Origin of the Pectic Polysaccharide Rhamnogalacturonan II – Insights from Nucleotide Sugar Formation and Diversity

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