Revealing the structural and functional diversity of plant cell walls

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The extensive knowledge of the chemistry of isolated cell wall polymers, and that relating to the identification and partial annotation of gene families involved in their synthesis and modification, is not yet matched by a sophisticated understanding of the occurrence of the polymers within cell walls of the diverse cell types within a growing organ. Currently, the main sets of tools that are used to determine cell-type-specific configurations of cell wall polymers and aspects of cell wall microstructures are antibodies, carbohydrate-binding modules (CBMs) and microspectroscopies. As these tools are applied we see that cell wall polymers are extensively developmentally regulated and that there is a range of structurally distinct primary and secondary cell walls within organs and across species. The challenge now is to document cell wall structures in relation to diverse cell biological events and to integrate this knowledge with the emerging understanding of polymer functions.

Introduction

Plant cell walls are highly complex and dynamic cell compartments that underpin many aspects of cell development, organ growth and organ properties. In the study of cell walls in relation to growth mechanisms considerable knowledge of the component cell wall polysaccharides has been established and at the same time, schematic models of cell wall structure and of how the polysaccharide components of cell walls fit together to generate the appropriate properties have been proposed and refined [1]. However, such models are currently generic, aimed at understanding ‘the plant cell wall’ and generally propose a model that is applied to all primary or all secondary cell walls. Biochemical analyses and genome sequencing has led to a documentation of the, often large, gene families that are involved in the synthesis and modification of cell wall components, but the detailed understanding of how these sets of genes impact upon the construction and maintenance of cell walls during growth is limited. Central to all these studies are the actual cell walls that function in diverse cell types during growth. Cell walls generate the mechanical properties that deal with tensile and compressive forces and also regulate cell expansion and cell adhesion. We have only a limited knowledge of the diversity of the in situ cell wall macromolecular configurations that can occur in a developing organ [2]. In short, the known structural complexity of cell wall polysaccharide classes and the known extensive repertoires of carbohydrate active genes are not matched by a sophisticated view of polymer occurrences and functions within cell walls in the context of cells, tissues or organs.

Section snippets

Tools for the in situ analysis of cell wall polymers

In terms of cell wall biology and understanding the functional significance of development-specific or cell-type-specific wall configurations of polymers or the impact of physiological/environmental change we are still at the stage of tool development. Most knowledge of cell wall polymers is derived from the physicochemical analysis of fractionated walls and isolated polymers with the consequent loss of most spatial and developmental information. Tools are therefore needed to acquire this

Cell wall differentiation: building diverse primary and secondary cell walls

Meristems are constructed from cells with primary cell walls that generate and constrain turgor pressure. As an organ develops species-specific patterns of cell types differentiate—some of which develop secondary cell walls with properties to resist compressive stresses. Figure 1 shows sections of a stem of industrial hemp fluorescently tagged with probes for cellulose, xylan, pectic homogalacturonan (HG) and (1  4)-β-galactan. The hemp stem has a wide range of cell types and diverse primary and

Developmental dynamics of cell wall polymers

In addition to polymer configurations in mature cell types, cell walls are also altered during development and during cell expansion and cell separation processes. Two complementary studies on wheat and barley grain have spatially mapped the staged appearance of wall polymers in relation to endosperm development and show that (1  3)-β-glucan is deposited transiently and before (1  3)(1  4)-β-glucan and that arabinoxylan appears late in grain development [37, 38].

The pectic polymers, abundant in

Perspective

As imaging tools develop in scope, sensitivity and specificity the diversity of cell walls within and between species is beginning to be revealed with more sophistication. There are still several known structural features of cell walls that remain mysterious to us in terms of function as we do not have the capability to place them in the context of cell biological processes. Dedicated effort is now focusing on these neglected aspects of plant cell walls. The way ahead is clear in that we should

References and recommended reading

Papers of particular interest, published within the annual period of the review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The author acknowledges funding from the UK Biotechnology & Biological Sciences Research Council, the UK Department of Trade & Industry and EU research programmes.

References (50)

  • L. Filonova et al.

    Analysis of the surface of wood tissues and pulp fibers using carbohydrate-binding modules specific for crystalline cellulose and mannan

    Biomacromolecules

    (2007)
  • S.-Y. Ding et al.

    Versatile derivatives of carbohydrate-binding modules for imaging complex carbohydrates approaching the molecular level of resolution

    Biotechniques

    (2006)
  • L. McCartney et al.

    Differential recognition of plant cell walls by microbial xylan-specific carbohydrate-binding modules

    Proc Natl Acad Sci U S A

    (2006)
  • L.C. Gunnarsson et al.

    Engineered xyloglucan specificity in a carbohydrate-binding module

    Glycobiology

    (2006)
  • B.R. Urbanowicz et al.

    A tomato endo-β-1,4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules (CBM49)

    J Biol Chem

    (2007)
  • G. Mouille et al.

    Classification and identification of Arabidopsis cell wall mutants using Fourier-transform infrared (FT-IR) microspectroscopy

    Plant J

    (2003)
  • M.C. McCann et al.

    Neural network analyses of infrared spectra for classifying cell wall architectures

    Plant Physiol

    (2007)
  • N. Gierlinger et al.

    Chemical imaging of poplar wood cell walls by confocal Raman microscopy

    Plant Physiol

    (2006)
  • S. Phillippe et al.

    Characterization using Raman microspectroscopy of arabinoxylans in the walls of different cell types during development of wheat endosperm

    J Agric Food Chem

    (2006)
  • L. McCartney et al.

    Monoclonal antibodies to plant cell wall xylans and arabinoxylans

    J Histochem Cytochem

    (2005)
  • G.K. Zhou et al.

    The poplar glycosyltransferase GT47C is functionally conserved with Arabidopsis Fragile Fiber8

    Plant Cell Physiol

    (2006)
  • A.W. Blake et al.

    In situ analysis of cell wall polymers associated with phloem fibre cells in stems of hemp, Cannabis sativa L.

    Planta

    (2008)
  • C. Andème-Onzighi et al.

    Immunocytochemical characterization of early-developing flax fiber cell walls

    Protoplasma

    (2000)
  • J. Rösti et al.

    UDP-glucose 4-epimerase isoforms UGE2 and UGE4 cooperate in providing UDP-galactose for cell wall biosysnthesis and growth of Arabidopsis thaliana

    Plant Cell

    (2007)
  • C.G. Meloche et al.

    A cortical band of gelatinous fibers causes the coiling of redvine tendrils: a model based upon cytochemical and immunocytochemical studies

    Planta

    (2007)
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