The Regulation of Cellulose Biosynthesis in Plants

Abstract

Cell walls define the shape of plant cells, controlling the extent and orientation of cell elongation, and hence organ growth. The main load-bearing component of plant cell walls is cellulose, and how plants regulate its biosynthesis during development and in response to various environmental perturbations is a central question in plant biology. Cellulose is synthesized by cellulose synthase (CESA) complexes (CSCs) that are assembled in the Golgi apparatus and then delivered to the plasma membrane (PM), where they actively synthesize cellulose. CSCs travel along cortical microtubule paths that define the orientation of synthesis of the cellulose microfibrils. CSCs recycle between the PM and various intracellular compartments, and this trafficking plays an important role in determining the level of cellulose synthesized. In this review, we summarize recent findings in CESA complex organization, CESA posttranslational modifications and trafficking, and other components that interact with CESAs. We also discuss cell wall integrity maintenance, with a focus on how this impacts cellulose biosynthesis.

Figure 1.

Schematic Representations of the Structure of a CESA Protein and a CSC. (A) Domain structure of a CESA. The intracellular N-terminal domain contains a Zn binding domain and a variable region and is followed by two transmembrane domains. The large cytoplasmic central catalytic domain is divided into the conserved region, which flanks the plant-specific region on both sides, the variable region(s), which includes the class-specific region, and the conserved region(s). The six subsequent transmembrane domains are followed by the cytoplasmic C-terminal domain. CESA1 phosphorylations on various Ser and Thr residues are indicated (source: PhosPhAt 4.0, Zulawski et al., 2013; and references in the text). Several cysteines in the cytoplasmic loop and within the C-terminal domain that are s-acylated in CESA7 (Kumar 2016b) are depicted in pink. C, cellulose chain; CR1, conserved region 1; CR2, conserved region 2; P-CR, plant-specifc region; S, Ser; T, Thr. (B) A schematic representation of a CSC consisting of 18 individual CESA proteins. The model is consistent with the rules outlined by Hill et al. (2014) and assumes that: a CSC is composed of six lobes that contain three CESA isoforms; the contacts between different isoforms is conserved; and the number of CESAs in each lobe is divisible by three. (C) A model of a cellulose microfibril consisting of five layers of cellulose chains in a “34443” arrangement (C = cellulose chain).

Figure 2.

A Cartoon of CSC Trafficking and the Other Components of the CSC Machinery. CSCs are assembled in the Golgi apparatus where they physically interact with STL proteins that assist their assembly and distribution in the Golgi. CSCs move through the TGN and follow the exocytosis route to the PM, where their insertion sites coincide with the pausing of the Golgi along the CMTs. The insertion of CSCs in the PM is preceded by POM2/CSI1, the exocyst complex, and PTL, which are required for CSC delivery. The CESA-interacting proteins SHOU4/4L negatively affect CSC exocytosis. POM2/CSI1 proteins also act as linkers between CSCs and CMTs and are necessary for the formation of SmaCCs/MASCs. The CC1 and CC2 belong to the CSCs, associate with SmaCCs/MASCs under salt stress and mediate the CMT and CSC dynamics, allowing for their recovery. CMU proteins regulate proper CMT spacing during cellulose biosynthesis. KOR is a component of CSCs required for optimal cellulose biosynthesis and COB is necessary for proper microfibril orientation. The SOS5 and FEI1/2 leucine-rich repeat-RLKs mediate cellulose biosynthesis and CrRLK1L THE1 inhibits cell expansion upon perturbation of cellulose biosynthesis. CSCs undergo CME that requires the AP2 complex and TPLATE complex members such as TWD40-1, TPLATE, and TML. The endocytosed CSCs may undergo recycling back to the PM or might be targeted for degradation.