Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae
Graphical abstract
Introduction
The primary wall that surrounds cells in growing and succulent plant tissues plays a critical role in balancing the osmotic forces in living cells, preventing them from bursting but still allowing them to grow in a controlled, oriented manner.1, 2 Thus, by controlling the morphological development of individual plant cells, cell walls directly regulate plant growth and morphology. The primary cell wall consists of cellulose microfibrils embedded in a matrix composed primarily of polysaccharides.1 The major components of this matrix are pectins and hemicelluloses. The most abundant hemicellulosic polysaccharide in the primary cell wall of most vascular plants is xyloglucan (XyG), which is synthesized in the Golgi and exported to the apoplasm in soluble form.3 XyG spontaneously and avidly binds to the surface of cellulose microfibrils, and is thereby incorporated into the xyloglucan/cellulose network, which forms a major load bearing structure in the primary cell walls of most higher plants.2, 4
XyGs have a cellulosic backbone composed of (1→4)-linked β-d-Glcp residues to which α-d-Xylp residues are linked at O-6. XyGs are highly branched polysaccharides, that have been classified as ‘XXXG-type’ or ‘XXGG-type’,5 depending on the number and distribution of side chains that are attached to the backbone. XyGs containing XXXXG-type subunits, which have five β-d-Glcp residues in the backbone, have also been isolated from seeds.6 The majority of higher plants produce XXXG-type XyGs, in which three of every four β-d-Glcp residues in the backbone have an α-d-Xylp residue at O-6, and the remaining, unbranched β-d-Glcp residues are regularly spaced along the backbone. Typically, XXXG-type XyGs have three different side chain structures, α-d-Xylp- (represented by the letter X), β-d-Galp-(1→2)-α-d-Xylp- (represented by the letter L), and α-l-Fucp-(1→2)-β-d-Galp-(1→2)-α-d-Xylp- (represented by the letter F). Thus, a typical XXXG-type XyG is composed predominantly of the oligosaccharide subunits XXXG, XXFG, XXLG, and XLFG. (See Fry et al.7 and footnotes of Table 2 for further description of this nomenclature.) As shown in Table 1, Table 2, the fucosylated XXXG-type structure is conserved in taxonomically diverse plant species, including, for example, pines (gymnosperms), legumes (dicotyledonous angiosperms), and onions (monocotyledonous angiosperms). Conservation of the α-l-Fucp-(1→2)-β-d-Galp-(1→2)-α-d-Xylp- side chains in such a wide range of plant species suggests functional importance. However, genetically modified A. thaliana plants that lack the AtFut1 activity that is responsible for the transfer of α-l-Fucp residues to xyloglucans appear to grow normally under greenhouse conditions.8
Certain Solanaceous asterids such as tobacco and tomato (see Table 1 for taxonomic classification) produce atypical XyGs that contain α-l-Araf and/or β-d-Galp residues but lack α-l-Fucp residues (Table 2). Solanaceous XyGs also have an atypical XXGG-type branching pattern, in which two unbranched Glc residues follow two branched residues.9, 10 One of the two adjacent unbranched Glc residues often has an O-acetyl substituent at O-6. It is not known how the structural modifications affect the biophysical properties of the XyG, or how the plant compensates for the loss of a conserved structural feature such as fucosyl residue-containing side chains or an XXXG-type branching pattern. In order to shed light on the evolutionary processes that could have given rise to the observed structural diversity, xyloglucans from several plants in the subclass Asteridae were isolated and structurally characterized.
Section snippets
Results and discussion
Alcohol-insoluble residue (AIR), which consists primarily of cell-wall material, was prepared from the leaf tissues of several Asterid species, and two separate XyG oligosaccharide fractions were prepared from each of these AIR samples. One fraction was prepared by treating depectinated cell wall material (AIR) with a xyloglucan-specific endoglucanase (XEG), which releases XyG oligosaccharides (XyGOs) from the enzyme-accessible XyG domain in the cell wall.11 The other fraction was prepared by
Selection of plants
Plants were selected to represent a broad range of Lamiid and Campanulid orders within the subclass Asteridae. Lamiid species included plants from the order Solanales (tomato—Lycopersicon esculentum, tobacco—Nicotiana tabacum, giant sweet peppers—Capsicum annuum, morning glory—Ipomea purpurea), the order Lamiales (Plantain—Plantago major, Basil—Ocimum basilicum), and the order Gentianales (oleander—Nerium oleander). Campanulid species included plants from the order Asterales (dusty miller—
Acknowledgments
This research was funded by the U.S. Department of Energy (grant no. DE-FG05-93ER20220) and by the U.S. Department of Energy-funded Center for Plant and Complex Carbohydrates (grant no. DE-FG05-93ER20097). The authors would like to thank Novozymes A/S for the xyloglucan-specific endoglucanase (XEG) and Dr. Carl Bergmann of the CCRC for pectin-degrading enzymes used in this study.
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