Structure of the xyloglucan produced by suspension-cultured tomato cells. Carbohydr Res

Department of Biochemistry and Molecular Biology, University of Georgia, Атина, Georgia, United States
Carbohydrate Research (Impact Factor: 1.92). 06/2003; 338(11):1197-208. DOI: 10.1016/S0008-6215(03)00079-X
Source: PubMed

ABSTRACT The xyloglucan secreted by suspension-cultured tomato (Lycopersicon esculentum) cells was structurally characterized by analysis of the oligosaccharides generated by treating the polysaccharide with a xyloglucan-specific endoglucanase (XEG). These oligosaccharide subunits were chemically reduced to form the corresponding oligoglycosyl alditols, which were isolated by high-performance liquid chromatography (HPLC). Thirteen of the oligoglycosyl alditols were structurally characterized by a combination of matrix-assisted laser-desorption ionization mass spectrometry and two-dimensional nuclear magnetic resonance (NMR) spectroscopy. Nine of the oligoglycosyl alditols (GXGGol, XXGGol, GSGGol, XSGGol, LXGGol, XTGGol, LSGGol, LLGGol, and LTGGol, [see, Fry, S.C.; York, W.S., et al., Physiologia Plantarum 1993, 89, 1-3, for this nomenclature]) are derived from oligosaccharide subunits that have a cellotetraose backbone. Very small amounts of oligoglycosyl alditols (XGGol, XGGXXGGol, XXGGXGGol, and XGGXSGGol) derived from oligosaccharide subunits that have a cellotriose or celloheptaose backbone were also purified and characterized. The results demonstrate that the xyloglucan secreted by suspension-cultured tomato cells is very complex and is composed predominantly of 'XXGG-type' subunits with a cellotetraose backbone. The rigorous characterization of the oligoglycosyl alditols and assignment of their 1H and 13C NMR spectra constitute a robust data set that can be used as the basis for rapid and accurate structural profiling of xyloglucans produced by Solanaceous plant species and the characterization of enzymes involved in the synthesis, modification, and breakdown of these polysaccharides.

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    • "linked to the glucan backbone and was named arabinoXyG (Fig. 1B) (York et al., 1996; Jia et al., 2003, 2005; Hoffman et al., 2005). In tomato and tobacco, the most abundant fragments were XXGG and XSGG (Fig. 1B) (York et al., 1996; Sims et al., 1996; Vincken et al., 1997; Jia et al., 2003, 2005; Hsieh and Harris, 2009). Recently, Lampugnani et al. (2013) showed clear structural differences in the composition of XyG in Nicotiana alata pollen tubes. "
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    ABSTRACT: Background and Aims In flowering plants, fertilization relies on the delivery of the sperm cells carried by the pollen tube to the ovule. During the tip growth of the pollen tube, proper assembly of the cell wall polymers is required to maintain the mechanical properties of the cell wall. Xyloglucan (XyG) is a cell wall polymer known for maintaining the wall integrity and thus allowing cell expansion. In most angiosperms, the XyG of somatic cells is fucosylated, except in the Asterid clade (including the Solanaceae), where the fucosyl residues are replaced by arabinose, presumably due to an adaptive and/or selective diversification. However, it has been shown recently that XyG of Nicotiana alata pollen tubes is mostly fucosylated. The objective of the present work was to determine whether such structural differences between somatic and gametophytic cells are a common feature of Nicotiana and Solanum (more precisely tomato) genera. Methods XyGs of pollen tubes of domesticated (Solanum lycopersicum var. cerasiforme and var. Saint-Pierre) and wild (S. pimpinellifolium and S. peruvianum) tomatoes and tobacco (Nicotiana tabacum) were analysed by immunolabelling, oligosaccharide mass profiling and GC-MS analyses. Key Results Pollen tubes from all the species were labelled with the mAb CCRC-M1, a monoclonal antibody that recognizes epitopes associated with fucosylated XyG motifs. Analyses of the cell wall did not highlight major structural differences between previously studied N. alata and N. tabacum XyG. In contrast, XyG of tomato pollen tubes contained fucosylated and arabinosylated motifs. The highest levels of fucosylated XyG were found in pollen tubes from the wild species. Conclusions The results clearly indicate that the male gametophyte (pollen tube) and the sporophyte have structurally different XyG. This suggests that fucosylated XyG may have an important role in the tip growth of pollen tubes, and that they must have a specific set of functional XyG fucosyltransferases, which are yet to be characterized.
    Annals of Botany 11/2014; DOI:10.1093/aob/mcu218 · 3.30 Impact Factor
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    • "In addition to the more common substituents found in XyG side chains, such as galactosyl and fucosyl residues, other identified sugar moieties include arabinopyranose (Selaginella kraussiana and Equisetum hyemale), galacturonic acid (Arabidopsis root hair and Physcomitrella patens; Peña et al., 2008, 2012), xylopyranose (Argania spinosa; Ray et al., 2004), and arabinofuranose (Ceratopteris richardii, tomato, and Olea europaea; Vierhuis et al., 2001; Jia et al., 2003; Peña et al., 2008). The differences in XyG structure among these plants are presumably caused by sequence differences in the GTs. "
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    ABSTRACT: Xyloglucan is the dominant hemicellulose present in the primary cell walls of dicotyledonous plants. Unlike Arabidopsis xyloglucan, which contains galactosyl and fucosyl-substituents, tomato (Solanum lycopersicum) xyloglucan contains arabinofuranosyl-residues. To investigate the biological function of these differing substituents we used a functional complementation approach. Candidate glycosyltransferases were identified from tomato by using comparative genomics with known xyloglucan galactosyltransferase genes from Arabidopsis. These candidate genes were expressed in an Arabidopsis mutant lacking xyloglucan galactosylation and two of them resulted in the production of arabinosylated xyloglucan, a structure not previously found in this plant species. These genes may therefore encode xyloglucan arabinofuranosyltransferases. Moreover, the addition of arabinofuranosyl-residues to the xyloglucan of this Arabidopsis mutant rescued a growth and cell wall biomechanics phenotype, demonstrating that the function of xyloglucan in plant growth, development and mechanics has considerable flexibility in terms of the specific residues in the side chains. These experiments also highlight the potential of re-engineering the sugar substituents on plant wall polysaccharides without compromising growth or viability.
    Plant physiology 07/2013; 163(1). DOI:10.1104/pp.113.221788 · 7.39 Impact Factor
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    • "Since this study used higher concentrations of XEG and longer incubation times than the previous experiment by Jia et al. (2003), it is possible that the linkage between xyloglucan and glucan could be hydrolyzed, or that the contaminating glucan could be hydrolyzed with XEG. The occurrence of the glucan is in agreement with the finding that some soluble glucan forms when cellulose biosynthesis is inhibited by DCB (Encina et al., 2002). "
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    ABSTRACT: Bean cells that have been habituated to grow in a lethal concentration (12 μM) of 2,6-dichlorobenzonitrile (dichlobenil or DCB, a cellulose biosynthesis inhibitor) are known to have decreased cellulose content in their cell walls. Xyloglucan, which is bound to cellulose and together with it forms the main loading network of plant cell walls, has also been described to decrease in habituated cells, but whether the change on cellulose affects the xyloglucan structure besides its abundance has not been analyzed. Fragmentation analysis with xyloglucan-specific endoglucanase (XEG) and endocellulase revealed that habituation to DCB caused a change in the fine structure of xyloglucan, namely a decrease in fucosyl residues attached to the galactosyl-xylosyl residues along the glucan backbone. After the removal of herbicide from the medium (dehabituated cells), xyloglucan recovered its fucosyl residues. In addition, some cello-oligosaccharides could be detected only in habituated cells' xyloglucan digested by XEG and endocellulase, corresponding to a glucan covalently bound or co-precipitated with the hemicelluloses. These results show that structural flexibility of cell walls relies in part on the plasticity of xyloglucan composition and opens up new perspectives to further research in this field.
    Molecular Plant 05/2010; 3(3):603-9. DOI:10.1093/mp/ssq011 · 6.61 Impact Factor
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