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Keywords:

  • cell wall;
  • cellulose;
  • cellulose synthesis;
  • nitric oxide;
  • plant development;
  • regulation

Cellulose is a central component in plant cell walls. In the primary cell wall (deposited in cells that are still expanding), it is a vital component of the load-bearing network and because of its physical properties is important in determining the orientation of cell expansion. After a period of cell expansion, some cells lay down a thick secondary cell wall inside the primary wall. The secondary cell wall provides plants with the mechanical properties that allow them to stand upright, and is a major component in properly functioning xylem vessels. Cellulose is one of the major components of secondary cell walls. The importance of cellulose in plant cell walls is reflected in it being the world's most abundant biopolymer, with an estimated 180 billion tonnes synthesized annually (Englehardt, 1995). Despite this importance, our understanding of how cellulose is synthesized, and how this synthesis is regulated, is still incomplete. In this issue of New Phytologist (pp. 386–396), Correa-Aragunde et al. describe how the signalling molecule nitric oxide (NO) modulates cellulose synthesis in tomato (Solanum lycopersicum) roots.

Pharmaceutical application of the NO donor sodium nitroprusside (SNP) was used to investigate incorporation of radiolabelled glucose into cellulose. Low (pmolar) concentrations of NO increased incorporation of radiolabelled glucose into the cellulose fraction in roots, whereas higher (nmolar) concentrations reduced incorporation into cellulose. These effects were transient and reversible, as determined by use of an NO scavenger. Microscopic analysis of root structure suggested that these differences were caused by effects on primary cell wall synthesis. Root length was reduced in plants treated with higher concentrations of NO and was accompanied by reduced cortical cell length and an apparent swelling of the root, phenotypes that are frequently observed in Arabidopsis mutants affected in primary cell wall cellulose synthesis. Three different cellulose synthase (CesA) catalytic subunits are generally considered to be required for cellulose synthesis, the three subunits being different in primary and secondary cell walls. Correa-Aragunde et al. identified three CesA transcripts from tomato cDNA libraries that are likely to be involved in primary cell wall cellulose synthesis, based on the similarity to three genes involved in this process in potato (Solanum tuberosum). The level of transcript of these three genes was slightly reduced by treatment with high concentrations of NO, suggesting that it may be at a transcriptional level that NO affects cellulose synthesis. Nitric oxide signalling in plants is an area in which there is still much to learn, and has been covered in a recent review (Wilson et al., 2008). It is clear, however, that NO is important as a signalling molecule in a number of processes in plants, and the description in this issue of its effect on modulating cellulose synthesis adds to a growing list of pathways that are affected by NO.

‘It is the organization of multiple glucan chains into microfibrils that is absolutely central to the physical properties that they confer once deposited in the cell wall.’

Cellulose synthesis is central to plant development, but the way in which it is regulated is still unclear and is currently an area of intense research. Cellulose is a simple polymer of unbranched β-1,4-linked glucan chains, with successive glucose residues inverted 180 degrees to form a flat ribbon in which the repeating unit is cellobiose. These parallel chains are then able to form extensive hydrogen bonds between individual glucan chains resulting in crystallization of multiple chains into cellulose microfibrils – insoluble, cable-like structures. It is the organization of multiple glucan chains into microfibrils that is absolutely central to the physical properties that they confer once deposited in the cell wall. This organized structure of the microfibril is a direct result of the organization of the protein complex that synthesizes cellulose. The plasma membrane-bound cellulose synthase complex (CSC) is a large (> 4 MDa) protein complex that includes multiple copies of three different CesA proteins. It is currently not known if there are any other protein components. The CSC can be visualized at the plasma membrane in freeze-fracture electron microscopy as hexameric structures, which gives rise to them being known as rosettes. It is the organization of multiple copies of the three CesA proteins into a defined arrangement that allows the simultaneous synthesis of multiple β-1,4-linked glucan chains in a conformation that allows them to hydrogen bond and crystallize into the functional unit of cellulose, the microfibril (Fig. 1). The three CesAs required are different in primary and secondary cell wall CSCs, and the presence and activity of all three proteins is required for correct cellulose synthesis (Gardiner et al., 2003; Taylor et al., 2003; Desprez et al., 2007; Persson et al., 2007).

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Figure 1. Model of the cellulose synthase rosette. (a) A ‘cross-section’ through a rosette is shown, each ‘lobe’ containing a number of catalytic subunits. The active sites of these subunits are cytosolic, and the extending cellulose microfibril crystallizes as it enters the cell wall. (b) Plan view. Each of the six ‘lobes’ is predicted to contain multiple copies of three different ‘types’ of cellulose synthase (CesA) proteins. The exact number of CesA proteins contained within a lobe, their stoichiometry and their specific interactions are currently unknown.

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Despite the importance of cellulose synthesis to plants, how it is regulated is not well understood. There are a number of different levels at which regulation of cellulose synthesis may occur, and much of our understanding has come from the use of the model plant Arabidopsis. Our current understanding of secondary cell wall cellulose synthesis is more advanced than that of primary cell wall synthesis, mainly because of the fact that plants lacking secondary cell wall cellulose are viable whereas plants lacking primary cell wall cellulose die at a very early stage of development. One consequence of a lack of secondary cell wall cellulose is a collapse of xylem vessels, a result of them being unable to withstand the negative pressure generated by the transpiration stream (Fig. 2) (Turner & Somerville, 1997). In Arabidopsis, a network of transcription factors have been identified that regulate secondary cell wall synthesis in different tissues (for a recent review of genes involved in regulating cellulose synthesis see Taylor, 2008 and references therein). These transcription factors appear to co-ordinately regulate synthesis of all the components of the secondary cell wall (cellulose, lignin and xylan). It is likely, however, that there is a cascade of transcription factors regulating secondary cell wall synthesis, and that further dissection of these networks may identify transcription factors involved in the activation of the individual pathways for the three major secondary cell wall polymers, including cellulose. A second level of regulation is likely to exist in the assembly of the CSC. The CSC is assembled in the endoplasmic reticulum and then transported intact to the plasma membrane. The way in which the three catalytic subunits are assembled into the rosette is currently unknown, but there is clearly a requirement for defined and specific interactions between the subunits, and the organization of such a large protein complex is likely to require the assistance provided by as yet unidentified molecular chaperones.

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Figure 2. Arabidopsis stem cross-sections of (a) wild-type and (b) a secondary cell wall cellulose-deficient mutant stained with toluidine blue. xe, xylem elements. Note the collapsed xylem elements in (b). Bars represent 0.05 mm.

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There is also a requirement for feedback regulation of cellulose synthesis from the cell wall, where the cellulose microfibrils are deposited, and the cytosol, where the catalytic domains of the proteins reside (Fig. 1a). One way in which this signalling across the plasma membrane could occur is by receptor kinases. These proteins, of which there is a diverse family of over 600 in plants, contain an extracellular ‘sensing’ domain and a linked intracellular kinase domain that can trigger a kinase cascade resulting in phosphorylation of target proteins (for a recent review of cell wall signalling see Humphrey et al., 2007). Phosphorylation sites on the cellulose synthase catalytic subunits have been identified (Nuhse et al., 2004; Taylor, 2007) but the precise role of phosphorylation at these sites has yet to be elucidated.

It is clear that there are multiple levels at which regulation of cellulose synthesis occurs. Despite its central role in plants, our knowledge of how cellulose synthesis is regulated is still very rudimentary and has to date mainly concentrated on developmental regulation. The study by Correa-Aragunde et al. in this issue demonstrating that NO affects cellulose synthesis in tomato roots contributes important knowledge on environmental regulation. Resolving some of the unanswered questions about cellulose synthesis is essential if we are to understand fundamental processes in plant development as well as better utilize the vast quantities of sugars contained in plant cell walls as a source of bio-energy to combat global climate change. Recent developments have given us hope that one day we may better understand the synthesis of cellulose, and how it is regulated both developmentally and environmentally.

Acknowledgements

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  2. Acknowledgements
  3. References

NGT is supported by a Royal Society University Research Fellowship.

References

  1. Top of page
  2. Acknowledgements
  3. References