Structural Polysaccharides in Molecular Architecture of Plant Cell Walls- from Algae to Hardwoods

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Structural Polysaccharides in Molecular Architecture of Plant Cell Walls- from Algae to Hardwoods STRUCTURAL POLYSACCHARIDES IN MOLECULAR ARCHITECTURE OF PLANT CELL WALLS- FROM ALGAE TO HARDWOODS R.H. ATALLA AND J.M. HACKNEY USDA Forest Service, Forest Products Laboratory,1 One Gifford Pinchot Drive, Madison, WI 53705-2398 ABSTRACT The structural polysaccharides are a family of polymers of hexoses and pentoses that occur in all plant cell walls. The distinguishing characteristic of these polymers is a ß-1.4-linked backbone. The most common among these is cellulose. which is the lin­ ear homopolymer of anhydroglucose. These polysaccharides are capable of aggregating into highly ordered structures that are the primary determinants of the mechanical and physical properties of cell walls. An overview of the variations in patterns of structural-polysaccharide aggregation within cell walls is presented here. Among the majority of the algae cellulose is the domi­ nant structural polysaccharide: thus the habit of aggregation is dominated by the patterns of cellulose. Among primitive plants. other structural polysaccharides represent a larger fraction of cell-wall mass and cellulose is less dominant. In woody tissues of higher plants. structural polysaccharides are the major components of the cell wall, and the patterns of aggregation are again dominated by the characteristic habits of cellulose. Within the phylogenetic framework, higher levels of morphological development apparently involve greater complexity in the molecular architecture of the cell walls and a finer level of blending of the components of aggregates at the molecular level. INTRODUCTION The primary structural components of plant cell walls are a group of polymers with backbones made up of ß-1.4-linked monosaccharides. The dominant polymer is. in most instances, cellulose; it is the homopolymer of anhydroglucose shown here schematically. The manner of coaggregation of cellulose with other cell-wall constituents varies widely. In material terms, the different forms of coaggregation include composite structures in which the cellulosic component can be viewed as a separate phase embedded in a matrix of other constituents, genuine blends wherein the mixing of the constituents is at the molecular level. and more complex architectures that are intermediate between, or combinations of, these two forms of organization. We recently began a survey of this range of variation and its relationship to the phylogeny of source species from various divisions of photo­ synthetic organisms. We provide here an overview of these findings and discuss levels of 1 The Forest Products Laboratory is maintained in cooperation with the University of Wisconsin. This article was written anti prepared by U.S. Government employees on official time, and it is therefore in the public domain and not subject to copyright. 2 organizational complexity at the molecular level as they relate to the morphological com­ plexity of organisms within the evolutionary scheme of the plant kingdom. To establish an appropriate perspective, we begin by discussing variation in patterns of cellulose aggregation when it occurs either in pure form in the native state or in a form that allows easy isolation with mild procedures that do not perturb its native orga­ nization. In order to provide a framework for assessing the structures in which noncellu­ losic polysaccharides occur in significant quantities. we also consider extensions of the methodologies used to characterize the structures of cellulose. We conclude with an overview of a preliminary survey of cell-wall structural polysaccharides from a wide range of sources representing different levels of morphological development among photosyn­ thetic organisms. STRUCTURE AND STATES OF CELLULOSE AGGREGATION Cellulose generally is regarded as the component responsible for much of the me­ chanical strength of the cell wall. Its unique structural properties result from its ability to retain a semicrystalline state of aggregation even in an aqueous environment; this is unusual for a polysaccharide. Two conceptual frameworks are combined to describe states of cellulose aggregation. The first is one applied frequently to semicrystalline polymers: the other is employed for polymorphic crystalline solids. Within the first of these frameworks. cellulose is typical of the general class of linear homopolymers. usually described as semicrystalline. that can aggregate to form microcrystalline domains. On the other hand. the crystalline domains of cellulose can occur in more than one crystal lattice form: hence its classification as polymorphic. Characterizing the physical structure of cellulose requires identification of the allomorph of the crystalline domains as well as an assessment of the balance between crystalli ne and amorpholis microdomains. Three different levels of structure define a particular state of aggregation. The primary structure refers to the chemical structure that reflects the pattern of covalent bonding; for cellulose it is fairly well established and is usually not in question. The next level, the secondary structure, is that of the conformations of individual molecules. It defines the relative disposition in space of the repeat units of an individual molecule given the constraints imposed by conformational energy considerations and by the packing of the molecules in a particular state of aggregation. This level of structure is important in spectroscopic studies, where the energy levels at which transitions occur are determined by the values of the internal coordinates that define molecular conformations. The final level, that of tertiary structure, reflects the arrangement of the molecules relative to each other in a particular state of aggregation whether this state is amorphous or is associated with one or another of the allomorphs contributing to the polymorphic state of cellulose crystallinity. This is the level of structure probed by diffractometric measurements, which are inherently most sensitive to the three-dimensional organization represented by a particular state of aggregation. Keeping in mind that different levels of structure represent a hierarchy of structures nested within each other is important. The specification of a secondary structure has implicit within it a specification of the primary structure. A precise definition of the tertiary structure, in turn, has implicit within it an equally precise definition of both primary and secondary structures. I n fact, for low -molecular-weight compounds that can form single crystals, the determination of tertiary structure through diffractometric studies can be carried out with sufficient precision to characterize both primary and secondary structures as well. In contrast, the diffractometric, data for polymeric materials are much more lim­ ited in content, and it becomes necessary to complement them with structural infor­ mation derived from studies carried out on monomers or oligomers and information derived from investigative techniques that provide additional independent information about the structure. One consequence of the uncertainties is that different investigators, emphasizing different sources of structural information to complement the diffractometric data, arrive at different views concerning the distinguishing features of the structures of cellulose. The different approaches to structural analysis have been reviewed by Atalla [1,2]. In the following discussion the primary focus will be on the native forms of cellulose. Native Cellulose Early studies of cellulose structure relied primarily on x-ray diffractometry [3,4]. These necessarily addressed the issue of tertiary structure, and because of the infor­ mation content limitations of the diffractometric data, much uncertainty remained with respect to secondary structure. The difficulty of determining structure was compounded by the finding that different native celluloses possessed different unit cells. Thus, the al­ gal celluloses gave patterns that seemed to require 8-chain unit cells. while the somewhat less crystalline, higher-plant celluloses appeared to possess 2-chain unit cells. The two classes of celluloses also had very different infrared spectra in the O-H stretching region. suggesting different patterns of’ hydrogen bonding [5]. This uncertainty was compensated for in structural calculations by introducing seem­ ingly plausible assumptions that the lattice possessed the symmetry of space group P21 and that the twofold-helix axis was coincident with the chain axis. All disallowed reflec­ tions were assumed negligible in the structural calculations. The validity of these assump­ tions has been questioned by many investigators. More recent diffractometric studies also remain in conflict with respect to the details of the tertiary structure; French et al. have noted that the data do not allow discrimination between parallel up. parallel down. or anti parallel structures [6]. During the past two decades, a number of new structure-sensitive techniques have been developed, and they have been applied to studies of cellulose. These have been particularly valuable because they are capable of probing secondary structure directly. The techniques include Raman spectroscopy and solid-state 13C nuclear magnetic reso­ nance (NMR) in the experimental arena and conformational energy calculations in the theoretical domain. They have been used in more recent analyses of structure-related phenomena in cellulose to complement the information available from the diffractometric measurements. Raman Spectroscopy Raman spectroscopy is the
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