Elsevier

Carbohydrate Research

Volume 340, Issue 11, 15 August 2005, Pages 1826-1840
Carbohydrate Research

Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae

https://doi.org/10.1016/j.carres.2005.04.016Get rights and content

Abstract

The structures of xyloglucans from several plants in the subclass Asteridae were examined to determine how their structures vary in different taxonomic orders. Xyloglucans, solubilized from plant cell walls by a sequential (enzymatic and chemical) extraction procedure, were isolated, and their structures were characterized by NMR spectroscopy and mass spectrometry. All campanulids examined, including Lactuca sativa (lettuce, order Asterales), Tenacetum ptarmiciflorum (dusty miller, order Asterales), and Daucus carota (carrot, order Apiales), produce typical xyloglucans that have an XXXG-type branching pattern and contain α-d-Xylp-, β-d-Galp-(1→2)-α-d-Xylp-, and α-l-Fucp-(1→2)-β-d-Galp-(1→2)-α-d-Xylp- side chains. However, the lamiids produce atypical xyloglucans. For example, previous analyses showed that Capsicum annum (pepper) and Lycopersicon esculentum (tomato), two species in the order Solanales, and Olea europaea (olive, order Lamiales) produce xyloglucans that contain arabinosyl and galactosyl residues, but lack fucosyl residues. The XXGG-type xyloglucans produced by Solanaceous species are less branched than the XXXG-type xyloglucan produced by Olea europaea. This study shows that Ipomoea pupurea (morning glory, order Solanales), Ocimum basilicum (basil, order Lamiales), and Plantago major (plantain, order Lamiales) all produce xyloglucans that lack fucosyl residues and have an unusual XXGGG-type branching pattern in which the basic repeating core contains five glucose subunits in the backbone. Furthermore, Neruim oleander (order Gentianales) produces an XXXG-type xyloglucan that contains arabinosyl, galactosyl, and fucosyl residues. The appearance of this intermediate xyloglucan structure in oleander has implications regarding the evolutionary development of xyloglucan structure and its role in primary plant cell walls.

Graphical abstract

XSG̲GGXSGXSGG̲GGXSGGXLGG̲GGXLGG

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.

References (43)

  • D.J. Cosgrove

    Plant Physiol. Biochem.

    (2000)
  • S. Levy et al.

    Curr. Opin. Cell Biol.

    (1992)
  • M.S. Buckeridge et al.

    Carbohydr. Res.

    (1997)
  • W.S. York et al.

    Carbohydr. Res.

    (1996)
  • W.S. York et al.

    Carbohydr. Res.

    (1990)
  • Z.H. Jia et al.

    Carbohydr. Res.

    (2003)
  • I.M. Sims et al.

    Carbohydr. Res.

    (1996)
  • E. Vierhuis et al.

    Carbohydr. Res.

    (2001)
  • A. Otter et al.

    J. Magn. Reson. Ser. B

    (1995)
  • K. Kakegawa et al.

    Phytochemistry

    (1998)
  • T. Watanabe et al.

    Carbohydr. Res.

    (1984)
  • I. Braccini et al.

    Carbohydr. Res.

    (1995)
  • T. Hayashi et al.

    Carbohydr. Res.

    (1988)
  • C.M.G.C. Renard et al.

    Carbohydr. Res.

    (1992)
  • D.K. Watt et al.

    Carbohydr. Polym.

    (1999)
  • S. Hantus et al.

    Carbohydr. Res.

    (1997)
  • M.M.H. Huisman et al.

    Carbohydr. Polym.

    (2000)
  • B. Ray et al.

    Carbohydr. Res.

    (2004)
  • S.G. Ring et al.

    Phytochemistry

    (1981)
  • L.L. Kiefer et al.

    Phytochemistry

    (1989)
  • M.A. O’Neill et al.

    The composition and structures of primary cell walls

  • Cited by (194)

    View all citing articles on Scopus
    View full text