Opinion
Cellulose Synthesis – Central Components and Their Evolutionary Relationships

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Highlights

The cellulose-synthesizing machinery is underpinned by several coexpressed gene products.

The core cellulose machinery is already present in Zygnmatophycae, coinciding with the emergence of preprophase band formation during cell division.

The emergence of CESAs, COBRAs, and THE-related components in the class of Klebsormidiophyceae is coincident with changes in the arrangement of the cellulose terminal complex.

Several cellulose synthesis-related components predate the typical CESA proteins.

The genes encoding the cellulose synthesis machinery are also coexpressed in the moss Physcomitrella.

Cellulose is an essential morphogenic polysaccharide that is central to the stability of plant cell walls and provides an important raw material for a range of plant-based fiber and fuel industries. The past decade has seen a substantial rise in the identification of cellulose synthesis-related components and in our understanding of how these components function. Much of this research has been conducted in Arabidopsis thaliana (arabidopsis); however, it has become increasingly evident that many of the components and their functions are conserved. We provide here an overview of cellulose synthesis ‘core’ components. The evolution and coexpression patterns of these components provide important insight into how cellulose synthesis evolved and the potential for the components to work as functional units during cellulose production.

Section snippets

Plant Cell Walls and Cellulose

Plant cells are surrounded by a relatively small number of distinct chemical polymers woven into precise 3D matrices – walls that shape the growth of cells and thus also plant tissues 1, 2. The make-up of cell walls varies between different cell types. and can change during development or as a consequence of environmental conditions [3]. For example, a dividing cell produces a callose-rich cell plate that matures into a cross-wall that separates the resulting daughter cells [4]. During

Central Components of Cellulose Synthesis

In vascular plants, the CSC typically consists of different heterotrimeric CESA configurations. For example, during primary wall synthesis the CSC contains CESA1, 3, and one CESA6-like subunit in arabidopsis (CESA2, 5, 6 or 9) 18, 19. By contrast, the secondary wall-synthesizing CSCs contain CESA4, 7, and 8 [20]. Although CESAs constitute the core catalytic components of CSCs, many proteins contribute to either the activity of the CESAs or to the trafficking and assembly of CSCs [21]. The CSCs

An Evolutionary Inventory of Cellulose-Related Components

To better understand how the cellulose synthesis-related machinery evolved, it is essential to first understand when the different components emerged during evolution. The Orthofinder platform [64] defines orthogroups as groups of genes that have descended from an ancestral gene. Including species from the Joint Genome Institute (JGI) Phytozome v12.1 database and the Green Algal Tree of Life project [65] for orthogroups that are closely related to cellulose synthesis, namely orthogroups

Transcriptional Coordination of Cellulose-Related Genes

Although the evolutionary inventory provides an overview of the presence and absence of different cellulose-related components in diverse species, it is unclear whether these components are dedicated to cellulose synthesis or perhaps also have other functions. The CESAs were originally identified via weak sequence similarity to bacterial cellulose synthase (CelA) proteins [68]. However, the majority of the associated components were identified via forward-genetic screens or coexpression

Concluding Remarks

Most of our understanding of how cellulose is produced in land plants stems from research undertaken in the model angiosperm arabidopsis [10]. However, many of the cellulose-related components identified in arabidopsis have closely related orthologs in other plant species [74]. The corresponding genes are typically similarly expressed, indicating that cellulose synthesis is driven largely through the control of gene expression 61, 75. Whereas much of these data were derived from seed plants, it

Acknowledgments

We would like to thank Drs Maria Flores, Stefanie Sprunck, and Thomas Dresselhaus for their gracious contribution of the gene expression profiles from Amborella. The Amborella data were generated as part of the European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) EVOREPRO consortium. We thank Dr Uli Felzmann from Science IT, University of Melbourne, for assistance with high-performance computing infrastructure. S.P. was supported by the Australian Research Council

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