Chapter 1
The Biosynthesis and Function of Polysaccharide Components of the Plant Cell Wall

Ryusuke Yokoyama, Naoki Shinohara, Rin Asaoka, Hideki Narukawa and Kazuhiko Nishitani

Laboratory of Plant Cell Wall Biology, Graduate School of Life Sciences, Tohoku University, Sendai, Japan

Introduction

The cell wall of land plants consists of three layers, namely the middle lamella, the primary cell wall, and the secondary cell wall. The middle lamella is directly derived from the cell plate generated during cytokinesis and the primary cell wall is deposited onto the middle lamella during the cell expansion process. The two cell wall layers are generally found in all cell types, whereas the secondary wall is deposited onto the primary cell wall in certain specific cell types after cell expansion has ceased (Albersheim et al., 2011; Fig. 1.1).

Figure 1.1 Various types of plant cells defined by the cell wall: (a–c) immunofluorescence labeling with monoclonal antibodies against cell wall polysaccharide epitopes; (a) JIM5, specific to homogalacturonan with a low degree of methylesterification; (b, c) CCRC-M1, specific to fucosylated xyloglucan; (d, e) bright field images of unstained specimens; (f) histochemical staining of lignin with phloroglucinol-HCl. A, parenchyma of Oryza sativa; B, spongy mesophyll of Fagus crenata; C, vascular of O. sativa; D, E and F, epidermis, trichome and xylem of A. thaliana, respectively.

The three layers differ from each other in terms of their chemical nature and physical properties, and they serve different biological functions. Although both the primary and secondary cell walls directly function as a mechanical housing capable of resisting both turgor pressure from the inside out and compression force from the outside in, only the primary cell wall can extend or deform in response to the force applied and thereby determine the direction and rate of cell expansion (Burgert and Frantzl, 2007; Wasterneys and Collings, 2007; Fig. 1.1). In addition to these mechanical roles, the primary cell wall functions as an information processing system. Typical functions include non-cell-autonomous regulation of cell differentiation via apoplastic signaling (Irving and Gehring, 2012; Wolf et al., 2012a), particularly in meristems, defensive responses to pathogens and parasites (Bradley et al., 1992; Vorwerk et al., 2004), and interactions with symbionts. The dynamics of the primary cell wall therefore play a pivotal role in determining cell shape and function during development and in response to environmental stimuli. Accordingly, in this chapter we will focus on the primary cell wall and the dynamic aspects of its major components, namely cellulose and matrix polysaccharides, in relation to its function.

Overview of the Plant Cell Wall

Plants devote a considerable amount of energy to constructing and maintaining the architecture of the plant cell wall, which is a biphasic composite consisting of crystalline microfibrils and an amorphous gel-like matrix; the former is embedded in the latter, which is intelligent enough to be able to self-organize and regulate cell shape and function during growth and, hence, the morphology of land plants.

For its assembly, remodeling, and disassembly, various types of structural and functional components must be secreted into the cell wall space. These include polysaccharides, structural proteins, enzymes, and small signaling molecules. Examination of the increasing number of currently available genome sequences of land plants tells us that each plant genome contains several thousand cell-wall-related genes which are implicated in biosynthesis, modification, and disassembly of the cell wall, and their regulation with respect to transcription, membrane trafficking, and enzyme actions (Henrissat et al., 2001; Coutinho et al., 2003; Somerville et al., 2004; Yokoyama and Nishitani, 2004; Brown et al., 2005). The presence of such a large number of genes and proteins committed to cell wall dynamics apparently reflects the fact that cell wall type is dependent upon cell type, of which there are estimated to be more than 40 in a land plant. Transcriptomic analysis has demonstrated that different cell types have different expression patterns of cell-wall-related genes (Zhu and Wang, 2000; Demura et al., 2002; Birnbaum et al., 2003; Imoto et al., 2005; Demura and Fukuda, 2007).

In addition to cell-type-specific variations, the chemical and physical nature of the cell wall is also hugely dependent upon the stages of growth and differentiation of the cell. This is rather self-evident as we have seen that the rate and direction of cell growth, and thus the final shape of the cell, is ultimately determined by the nature of the cell wall. Continued reduction in the tensile strength of the cell wall, which is termed ‘cell wall loosening’, is the direct cause of cell wall expansion followed by cell expansion, the ubiquitous process by which cell expansion is regulated. Accordingly, an anisotropic or localized modification of the primary cell wall within a cell will cause anisotropic cell growth, such as cell elongation in stem cortical cells and polarized cell expansion in leaf trichomes and pavement cells. The chemical and physical nature of the primary cell wall can therefore precisely determine the size and shape of individual cells and play a vital role in determining the morphology of the plant as a whole (Fig. 1.1; Somerville et al., 2004; Cosgrove, 2005).

By contrast, the secondary cell wall has a static structure consisting mainly of crystalline cellulose microfibrils impregnated with lignin and suberin, and is responsible for providing mechanical resistance as well as forming a diffusion barrier. In xylem and fiber cells, the secondary cell wall functions to resist compression force as well as tensile force, and it provides the cell with enough strength to support aerial parts of the plant body, or serves as a non-growing cellular pathway for the translocation of water and nutrients (Fig. 1.2; Demura and Fukuda, 2007). On the other hand, the diffusion resistance function of the secondary cell wall is most prominently found in the Casparian strip in the endodermis, in which lignin confers the hydrophobicity necessary for forming a diffusion barrier to the cell wall (Naseer et al., 2012). These functions of the secondary wall are not directly related to the determination of cell shape and are therefore not discussed in this chapter.

Figure 1.2 Cellulose/hemicellulose and pectin networks in the primary cell wall at successive stages of plant cell growth. (a) Processes of cell elongation and differentiation. (b) Major polymers and their likely arrangement in the cell wall. Newly secreted hemicelluloses (shown in black) and the other polymers (gray) are integrated into the cellulose/hemicellulose network.

Components of the Primary Cell Wall

The primary cell wall is composed of cellulose microfibrils, matrix polysaccharides, and structural proteins and can serve as an aqueous microenvironment harboring non-structural soluble components such as enzymes, signaling molecules, and ions (Carpita and Gibeaut, 1993; Cosgrove, 1997). In this section, we first describe the structural features of the cellulose microfibrils and two major matrix polysaccharides – pectin and hemicellulose – before describing how they are organized to form the dynamic architecture of the primary cell wall.

Basic Structure and Cellulose Microfibrils

A single microfibril in land plants is circular or square when observed in cross-section. The dimension of the cellulose microfibril in land plants has been estimated by transmission electron microscopy, X-ray scattering (Jakob et al., 1995), and solid-state 13C nuclear magnetic resonance (NMR) (Newman, 1999; Kennedy et al., 2007). The diameters suggested by these analyses range from 2.5 nm to 3.6 nm, which corresponds to 15–32 chains of β-1,4-glucan molecules (Somerville, 2006; Fernandes et al., 2011) if it is assumed that each chain occupies 0.317 nm2 (Nishiyama et al., 2002).

In cellulose microfibrils, there are two types of domains conforming to a triclinic (termed cellulose I-α) form and a monoclinic (termed cellulose I-β) form. In land plants, the I-β form predominates. In the crystalline domain, β-1,4-glucan chains are arranged in parallel and undergo self-association via several interactions, which include the formation of intramolecular hydrogen bonds at O3…O5 and O2…O5, an intermolecular hydrogen bond at O3…O3, and hydrophobic intermolecular interactions. This structure renders the cellulose microfibrils insoluble in water, immune to enzymatic attack, and resistant to chemical agents.

Another important characteristic of cellulose is its high tensile strength and elastic modulus. The latter is estimated to be between 124 and 155 GPa for the cellulose I-β form, values that are comparable to that of gray cast iron (Nishino et al., 1995). The crystallinity is frequently disrupted by dislocations, resulting in amorphous or para-crystalline regions in the microfibril. The cellulose microfibril therefore has a substructure consisting of highly organized crystalline domains linked together by less organized amorphous or para-crystalline regions (O'Sullivan, 1997; Nishiyama et al., 2002).

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