Cellulose Biosynthesis in Higher Plants and the Role of the Cytoskeleton

Abstract

Cellulose is a polysaccharide consisting of a linear chain of β (1→4) linked D‐glucose and it is the most abundant polymer on earth. As a major structural component of the cell wall, cellulose accounts for about one‐third of plant mass. The regulation of cellulose biosynthesis is essential to plant development. Cellulose is synthesised by the cellulose synthase (CESA) complex in the plasma membrane. This article reviews the composition and regulation of the cellulose synthase complex with a focus on the role of cytoskeleton in higher plants. In this article, the evolving views in the field of cellulose biosynthesis are discussed and the unresolved questions, such as in vitro cellulose synthesis, structure of CESA and mechanism underlying microtubule–microfibril alignment hypothesis, are highlighted.

Key Concepts:

  • Cellulose is a polysaccharide consisting of a linear chain of β (1→4) linked D‐glucose.

  • Cellulose is synthesised by large membrane‐bound protein complexes known as cellulose synthase complexes (CSCs).

  • Microtubule–microfibril alignment hypothesis states that there is a causal link between the orientation of cortical microtubules and nascent microfibrils.

  • Primary cell wall surrounds all plant cells and is formed during cell division and expansion.

  • Secondary cell wall is formed between the primary cell wall and the plasma membrane in cells that are subject to mechanical stress.

Keywords: cellulose; cellulose synthase complex; rosette; microtubule; cytoskeleton

Figure 1.

Immunolabelling of membrane rosettes with CESA antibodies. (a) Freeze‐fractured replicas from vascular plant Vigna angularis were labelled with CESA antibodies. Many rosettes are labelled with antibodies. The inset shows an enlarged image of two rosettes with antibody labels. Bar=0.1 μm. Bar in inset=30 nm. (b) Scale model of primary and secondary antibody dimensions relative the 10 nm gold particle and 25 nm rosette dimensions. Adapted from Kimura et al.. Copyright by American Society of Plant Biologists.

Figure 2.

Comparison of predicted CESA protein structure from plants and bacteria. CESA protein from plants A. thaliana (O48946.1) and Gluconoacetobacter xylinus (CAA38487.1). The diagrams are aligned at the U4 region. Domains shown by colour blocks are: zinc‐finger domain (Zn, green); transmembrane domains (TMD, black); conserved regions (U1‐U4, blue); conserved region only present in plants (CR‐P, red) and class‐specific region (CSR, red). Phosphorylation sites (lightning mark, green).

Figure 3.

Visualisation of CESA complexes. (a) A heteromeric model for the CESA complexes. The rosettes (encircled for better visualisation) image is adapted from Herth . In a widely cited heteromeric model, a single rosette is composed of 36 CESA subunits of three isoforms that are illustrated by three different colours (Purple, red and brown). The topology of a single CESA subunit is shown on the left, adapted from Richmond and Somerville . Regions are coloured to follow those shown in Figure . (b) Co‐localisation of cellulose synthase complexes and microtubules. Cellulose synthase complexes are labelled by yellow fluorescent protein (YFP) tagging of CESA6 (shown as green circles in Figure a). Microtubules are labelled by red fluorescent protein (RFP) tagging of TUA5. Merge image shows CESA complexes co‐align with underlying microtubules. Bar=5 μm. Adapted from Gutierrez et al. . Copyright by Nature Publishing Group.

Figure 4.

Co‐localisation of CSI1, CESA complexes and microtubules. (a) Wild type seedlings coexpressing GFP‐CESA6 and RFP‐CSI1: the co‐alignment of CSI1 and CESA complexes is evident in the merged time‐averaged image. (b) Wild‐type seedlings co‐expressing YFP‐TUA5 and RFP‐CSI1: the co‐alignment of CSI1 and microtubules is evident in the merged time‐averaged image. (c) Wild type seedlings co‐expressing RFP‐TUA5 and YFP‐CESA6: the co‐alignment of CESA complexes and microtubules is evident in the merged time‐averaged image. (d) In csi1 seedlings co‐expressing YFP‐CESA6 and RFP‐TUA5, CESA particles are randomly distributed, their time‐averaged trajectories are apparently shorter and rarely co‐localised with microtubules. Note that the large, roughly circular structures in the GFP‐CESA6 (a) and YFP‐CESA6 (c, d) images are Golgi bodies. The time‐averaged images are projections of 60 frames (∼5 min) acquired at 5 s intervals. Bars=10 μm. Reproduced from Baskin and Gu . Copyright by Landes Bioscience.

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Mei Y, Gao HB, Yuan M and Xue HW (2012) The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development. Plant Cell 24: 1066–1080.

Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Current Opinion in Plant Biology 7: 651–660.

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Li, Shundai, and Gu, Ying(Oct 2012) Cellulose Biosynthesis in Higher Plants and the Role of the Cytoskeleton. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023745]