Cellulose synthase complex organization and cellulose microfibril structure

Abstract

Cellulose consists of linear chains of β-1,4-linked glucose units, which are synthesized by the cellulose synthase complex (CSC). In plants, these chains associate in an ordered manner to form the cellulose microfibrils. Both the CSC and the local environment in which the individual chains coalesce to form the cellulose microfibril determine the structure and the unique physical properties of the microfibril. There are several recent reviews that cover many aspects of cellulose biosynthesis, which include trafficking of the complex to the plasma membrane and the relationship between the movement of the CSC and the underlying cortical microtubules (Bringmann et al. 2012 Trends Plant Sci.17, 666-674 (doi:10.1016/j.tplants.2012.06.003); Kumar & Turner 2015 Phytochemistry112, 91-99 (doi:10.1016/j.phytochem.2014.07.009); Schneider et al. 2016 Curr. Opin. Plant Biol.34, 9-16 (doi:10.1016/j.pbi.2016.07.007)). In this review, we will focus on recent advances in cellulose biosynthesis in plants, with an emphasis on our current understanding of the structure of individual catalytic subunits together with the local membrane environment where cellulose synthesis occurs. We will attempt to relate this information to our current knowledge of the structure of the cellulose microfibril and propose a model in which variations in the structure of the CSC have important implications for the structure of the cellulose microfibril produced.This article is part of a discussion meeting issue 'New horizons for cellulose nanotechnology'.

Keywords: cellulose; electron microscopy; microfibril; protein complex; synthesis.

Figure 1.

A summary of recent literature on the structure of cellulose microfibril. SANS, small-angle neutron scattering; WAXS, wide-angle X-ray scattering, ssNMR, solid-state nuclear magnetic resonance; FTIR, Fourier-transform infrared; WANS, wide-angle neutron scattering. (Online version in colour.)

Figure 2.

Domain structures of the plant and bacterial processive glucosyltransferases. CESA7 and CSLC4 from Arabidopsis and BCSA from Rhodobacter sphaeroides are shown as representative examples of proteins that all synthesize linear chains of β-1,4-linked glucans. Each grey bar is proportional to the protein size. The transmembrane (TM) helices are shown as black rectangles. The two clusters of TM helices indicated with black dashed lines border the central portion of all proteins that form the catalytic domain. The position of four conserved motifs (DDX, DXD, XED and QXXRW) found in the catalytic site are indicated. Higher plant CESA proteins contain two regions not present in BCSA and CSLC4, which are known as the plant-conserved region (P-CR) and the class-specific region (CSR). A small stretch of 31 amino acids from BCSA does, however, align in the middle of P-CR. A similar stretch is also present in CSLC4 in the corresponding position. The CSR is completely absent from CSLC4 and BCSA. The N terminal region of CESA also contains a RING type zinc finger and the variable region 1 (VR1). Both these motifs are largely absent from CSLC4 and BCSA. (Online version in colour.)

Figure 3.

Organization of CESA proteins within the CSC. (a) Models of CSC indicating that the CSC might be composed of either hetero (left-hand side) or homo (right-hand side) trimers of CESA proteins. (b) Freeze fracture TEM of the plasma membrane showing the CSC as six-lobed rosette. A large number of images taken suggest that the lobe might represent a unit of the CSC and, at various stages, the lobes may be displaced from the hexameric rosette to varying extent. The image is reproduced from Nixon et al. [34] under Creative Commons license. (c) A cartoon representation of distorted rosettes in which lobe interaction and/or structure is altered. (Online version in colour.)