Cellulose Biosynthesis in Higher Plants and the Role of the Cytoskeleton

Shundai Li, Center for Lignocellulose Structure and Formation/Pennsylvania State University, University Park, Pennsylvania, USA
Ying Gu, Center for Lignocellulose Structure and Formation/Pennsylvania State University, University Park, Pennsylvania, USA

Published online: October 2012

DOI: 10.1002/9780470015902.a0023745

Cellulose is a polysaccharide consisting of a linear chain of (14) 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 (14) 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 m. 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. (1999). 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 (1985). 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 (2000). Regions are coloured to follow those shown in Figure 2. (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 3a). Microtubules are labelled by red fluorescent protein (RFP) tagging of TUA5. Merge image shows CESA complexes co-align with underlying microtubules. Bar=5 m. Adapted from Gutierrez et al. (2009). 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 m. Reproduced from Baskin and Gu (2012). Copyright by Landes Bioscience.
close
 References
    Bashline L, DU J and Gu Y (2011) The trafficking and behavior of cellulose synthase and a glimpse of potential cellulose synthesis regulators. Frontiers of Biology 6: 377–383.
    Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215: 150–171.
    Baskin TI and Gu Y (2012) Making parallel lines meet: Transferring information from microtubules to extra-cellular matrix. Cell Adhesion & Migration 6: 1–5.
    Bessueille L, Sindt N, Guichardant M et al. (2009) Plasma membrane microdomains from hybrid aspen cells are involved in cell wall polysaccharide biosynthesis. Biochemical Journal 420: 93–103.
    Bringmann M, Li E, Sampathkumar A et al. (2012) POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24: 163–177.
    Cifuentes C, Bulone V and Emons AM (2010) Biosynthesis of callose and cellulose by detergent extracts of tobacco cell membranes and quantification of the polymers synthesized in vitro. Journal of Integrative Plant Biology 52: 221–233.
    book Collings DA (2008) "Crossed wires: Interactions and cross-talk between the microtubule and microfilament networks in plants" In: Peter N (ed.) Plant Cell Monographs: Plant Microtubules, Development, and Flexibilty, pp. 47–82. Berlin: Springer.
    Crowell EF, Bischoff V, Desprez T et al. (2009) Pausing of golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21: 1141–1154.
    Crowell EF, Gonneau M, Stierhof YD, Hofte H and Vernhettes S (2010) Regulated trafficking of cellulose synthases. Current Opinion in Plant Biology 13: 700–705.
    Doblin MS, Kurek I, Jacob-Wilk D and Delmer DP (2002) Cellulose biosynthesis in plants: From genes to rosettes. Plant and Cell Physiology 43: 1407–1420.
    Endler A and Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Molecular Plant 4: 199–211.
    Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138: 1404–1405.
    Gu Y and Somerville C (2010) Cellulose synthase interacting protein: A new factor in cellulose synthesis. Plant Signaling and Behavior 5: 1571–1574.
    Gu Y, Kaplinsky N, Bringmann M et al. (2010) Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proceedings of the National Academy of Sciences of the USA 107: 12866–12871.
    Gutierrez R, Grossmann G, Frommer WB and Ehrhardt DW (2010) Opportunities to explore plant membrane organization with super-resolution microscopy. Plant Physiology 154: 463–466.
    Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM and Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nature Cell Biology 11: 797–806.
    Haigler CH and Brown RM (1986) Transport of rosettes from the golgi-apparatus to the plasma-membrane in isolated mesophyll-cells of Zinnia-Elegans during differentiation to tracheary elements in suspension-culture. Protoplasma 134: 111–120.
    Harris D, Bulone V, Ding SY and DeBolt S (2010) Tools for cellulose analysis in plant cell walls. Plant Physiology 153: 420–426.
    Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. Journal of Theoretical Biology 48: 445–449.
    Hepler PK and Newcomb EH (1964) Microtubules and fibrils in the cytoplasm of coleus cells undergoing secondary wall deposition. Journal of Cell Biology 20: 529–532.
    Herth W (1980) Calcofluor white and Congo red inhibit chitin microfibril assembly of Poterioochromonas: Evidence for a gap between polymerization and microfibril formation. Journal of Cell Biology 87: 442–450.
    Herth W (1985) Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Planta 164: 12–21.
    Kimura S, Laosinchai W, Itoh T et al. (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11: 2075–2086.
    Kudlicka K and Brown RM Jr (1997) Cellulose and callose biosynthesis in higher plants (i. solubilization and separation of (1->3)- and (1->4)-[beta]-glucan synthase activities from mung Bean). Plant Physiology 115: 643–656.
    Lai-Kee-Him J, Chanzy H, Muller M et al. (2002) In vitro versus in vivo cellulose microfibrils from plant primary wall synthases: structural differences. Journal of Biological Chemistry 277: 36931–36939.
    Ledbetter MC and Porter KR (1964) Morphology of microtubules of plant cells. Science 144: 872–874.
    Lei L, Li S and Y G (2012) Cellulose synthase complexes: Composition and regulation. Frontiers in Plant Science 3: 1–6.
    Li S, Lei L, Somerville C and Gu Y (2012) Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proceedings of the National Academy of Sciences of the USA 109: 185–190.
    Lloyd C and Chan J (2008) The parallel lives of microtubules and cellulose microfibrils. Current Opinion in Plant Biology 11: 641–646.
    Mueller SC and Brown RM Jr (1980) Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. Journal of Cell Biology 84: 315–326.
    Nicol F, His I, Jauneau A et al. (1998) A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO Journal 17: 5563–5576.
    Pagant S, Bichet A, Sugimoto K et al. (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14: 2001–2013.
    Paredez AR, Somerville CR and Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491–1495.
    Richmond TA and Somerville CR (2000) The cellulose synthase superfamily. Plant Physiology 124: 495–498.
    Sampathkumar A, Lindeboom JJ, Debolt S et al. (2011) Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. Plant Cell 23: 2302–2313.
    Saxena IM, Lin FC and Brown RM Jr (1990) Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Molecular Biology 15: 673–683.
    Schindelman G, Morikami A, Jung J et al. (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes and Development 15: 1115–1127.
    Seagull RW (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibers. Protoplasma 159: 44–59.
    Somerville C (2006) Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology 22: 53–78.
    Wightman R and Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant Journal 54: 794–805.
    Wong HC, Fear AL, Calhoon RD et al. (1990) Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proceedings of the National Academy of Sciences of the USA 87: 8130–8134.
 Further Reading
    Bischoff V, Desprez T, Mouille G et al. (2011) Phytochrome regulation of cellulose synthesis in Arabidopsis. Current Biology 21: 1822–1827.
    Brown RM and Saxena IM (2005) Cellulose biosynthesis: Current views and evolving concepts. Annals of Botany 96: 9–21.
    Crowell EF, Gonneau M, Vernhettes S and Hofte H (2010) Regulation of anisotropic cell expansion in higher plants. Comptes Rendus Biologies 333: 320–324.
    Desprez T, Juraniec M, Crowell EF et al. (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 104: 15572–15577.
    Guerriero G, Fugelstad J and Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? Journal of Integrative Plant Biology 52: 161–175.
    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.

Related Sub-Topics:

Plant Cell Growth | Plant Genetics and Molecular Biology | Cell Cytoskeleton | Growth and Synthesis | Proteins: Structure, Function, Metabolism
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Cellulose Biosynthesis in Higher Plants and the Role of the Cytoskeleton
 
How to Cite close
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]