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Plant Physiol, January 2001, Vol. 125, pp. 127-130
How the Cell Wall Acquired a Cellular Context
Keith
Roberts*
John Innes Centre, Norwich N4 7UH, United Kingdom
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INTRODUCTION |
It seems that 25 years ago plant
cell walls were different than they are now. I don't mean physically
different, of course they were made of the same old stuffI mean
conceptually different. Let me try to explain. Much of the plant body
(and in large plants the bulk of it) is comprised of cell wall
material. It forms a tough yet extensible extracellular matrix of
polysaccharides for young and growing cells (the primary cell wall),
and a strong, thicker, and sometimes lignin-impregnated structure in
secondary tissues (the secondary cell wall). The composition,
architecture, and mechanical properties of these walls are ideally
suited to the functions they perform, and so for many years plant
biologists have been asking the same obvious yet important questions
about cell walls: What are the structures of the key cell wall
polymers? How are they made and deposited? How do they function in cell growth and differentiation? What is the relationship between
extracellular events in the wall and intracellular events? How is all
this regulated? In 1975, the main tools available for tackling these
questions were still biochemistry and electron microscopy, and the
conceptual picture of the wall that emerged from these approaches was
understandably structural and static. Nevertheless, the broad framework
was available for describing the three main classes of structural
polysaccharides in the wall (cellulose, pectin, and the so-called
hemicelluloses or cross-linking glycans), the proteins and lignin, and
influential models already existed suggesting how they might all be put
together (7). The problem was that most of this work started
with large preparations of purified cell walls, commonly from
whole-plant organs or from cell cultures, and this was hard to relate
back to the obvious fact that the plant body itself contains numerous different cell types, most with clearly distinguishable cell walls. The
biggest single shift in the next 25 years was to be from the chemistry
of isolated and homogenized cell walls to an appreciation of the
subtle, changing, functional complexity of individual walls around
individual cells within the plant; in other words, a conceptual shift
toward understanding walls in their cellular context. I shall chart
this shift by looking at six areas where the cellular context has
extended and changed our understanding of cell wall biology. In many
cases, it is not surprising that these conceptual shifts have been
driven by technical innovations in microscopies, spectroscopies, model
systems, and molecular genetics, as well as by valuable lessons learned
from bacterial, animal, and fungal systems.
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THE INCREASING COMPLEXITY OF WALL POLYMERS |
Both classes of polymer in the primary wall, polysaccharide and
protein, have been shown to harbor remarkable complexity. A combination
of chemical and physical techniques that include HPLC, gas
chromatography-mass spectrometry, and NMR, coupled with isotope
labeling, linkage analysis, and the use of pure degradative enzymes
with defined specificity, have slowly revealed the remarkable chemical
heterogeneity of polysaccharides such as xyloglucan and the baroque
complexity of the pectic polysaccharide rhamnogalacturonan II. The
groups associated with Fons Voragen (Wageningen, The Netherlands) and
Peter Albersheim (Athens, GA) have made major contributions in this
area, the latter group exploiting the use of uniform cell suspension
cultures (7). There was also a growing appreciation that the cell walls
of the grasses differed in several important respects from those of
other flowering plants, particularly in the non-cellulosic
polysaccharides. This was highlighted by Bruce Stone's work at LaTrobe
(Australia) and by Nick Carpita's work at Purdue (West Lafayette, IN;
3). There has been a similar growth in our understanding of the
families of cell wall proteins. After Derek T.A. Lamport, working in
Don Northcote's lab (Cambridge, UK), identified the unusual
amino acid hydroxy-Pro in cell wall proteins, both polypeptide
sequencing and gene cloning have allowed large families of wall
proteins to be classified, both with and without this unusual amino
acid. These now include Pro-rich proteins, Gly-rich proteins, and
arabinogalactan proteins. It is sad that less progress has been made in
attributing secure biological functions to these polymers (17),
although functional genomics approaches in Arabidopsis should soon
change this situation.
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THE IMPORTANCE OF WALL ARCHITECTURE |
The mechanical and functional properties of the cell wall are
defined by its detailed molecular architecture as a fiber composite (17). Our current picture of wall architecture has been transformed in
the last 20 years by the information provided by high-resolution electron microscopy and the use of polymer-specific probes in particular specific antibodies.
Electron microscopy has a distinguished history in wall research, and
high resolution images of replicas (10) led to a new spate of model
building based on structure rather than the biochemistry that had
underpinned older models (7). A consensus emerged that walls were built
of two independent networks, cross-linked cellulose microfibrils and
cross-linked pectin, each with distinct physical and mechanical
properties (3). The nature of the cross-links in both cases has been
slow to emerge but most contributions here have come from Stephen
Fry's (Edinsburgh University, Scotland) thorough biochemical approach
(18). The relative contributions of each network to the mechanical
properties of the wall have been greatly clarified by the
exploitation of a beautiful in vitro system that uses Acetobacter
xylinum as a source of cellulose microfibrils to mimic the
self-assembly of the higher plant cell wall (19).
Complexity has been mapped onto this simple model through the use of
antibodies. Over the last 10 years we have learned that not only do the
walls of different cells have different compositions, but that
different wall polymers may be concentrated in different wall layers,
and even that different domains or facets of a single cell wall may
have very different compositions. This is true, not only for wall
polysaccharides (8), but also for wall-associated proteins (14). This
insight has focussed attention on the relationship between activities
within the cell, in particular the cytoskeleton and targeted secretion,
and the ordered structure of the wall outside; in other words, on cell
biology (Fig. 1).
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Figure 1.
A section through part of a potato tuber stained
with calcofluor (blue) to show the cellulose in the cell walls,
together with the monoclonal antibody LM5 (red) that reveals the
nonuniform distribution of 1,4-galactan in the walls. (Photo courtesy
of Max Bush and Grant Calder [John Innes Centre].)
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THE WALL OF THE SINGLE CELL |
Local variation in wall thickness and composition is now seen as
an integral part of a cell's differentiation process in relation to
its cellular neighbors. This extends from the birth of the wall during
cytokinesis, through cell expansion to local thickening (collenchyma,
xylem, vessel elements, and epidermal cells), and wall dissolution
(vessel elements and sieve tube elements). The dynamic nature of the
wall during the life of a cell is well illustrated by the appearance
and rearrangements of the plasmodesmata that penetrate the wall and
provide cytoplasmic connectivity between cells.
The use of monoclonal antibodies, notably by Mike Hahn (Athens, GA),
Andrew Staehilin (Boulder, CA), J. Paul Knox (Leeds, UK), and Roger I. Pennell (Ceres Inc., CA), has been crucial in enabling us to appreciate
just how complex and dynamic the plant extracellular matrix can be (8, 14).
Cell suspension cultures offer ready access to the primary cell walls
of a single cell type (7) and the single greatest contribution to our
understanding of secondary cell walls is also likely to come from a
single cell model for tracheary element differentiation, derived from
Zinnia elegans mesophyll cells (4).
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THE BIOSYNTHESIS, DEPOSITION, AND GROWTH OF THE WALL |
Although the precursors for wall polymer biosynthesis were
identified long ago, the biosynthetic enzymes, the glycosyl
transferases, that used them remained doggedly resistant to discovery
until only about 5 years ago. Cellulose, long known to be made at the plasma membrane by large "protein machines" called rosettes (12), is now known to be made in plants by enzymes that have some homology to
their bacterial counterparts (13). It emerges that the cellulose synthase and cellulose synthase-like gene families are enormous and are
now the focus of a major research effort. Related genes are being
uncovered, and those encoding enzymes that make matrix polysaccharides
also are being revealed.
The ordered deposition of cellulose microfibrils has long been known to
involve the plant cytoskeleton. Although a straightforward causal
effect, from microtubule orientation to cellulose orientation, probably
operates in some cases (9), the situation is far from simple (1), and
the cellular context suggests that extensive cross talk exists between
the extracellular matrix and the cytoskeleton (16, 20). Microinjection
of fluorescent analogs and the use of green fluorescent protein-tagged
proteins, coupled with confocal microscopy, have vastly increased our
understanding of cytoskeletal dynamics in plant cells (6), and this is
likely to expand into time-resolved studies of the wall itself.
Along with wall deposition have come some initial steps in clarifying
how the wall architecture of growing cells is remodeled during the
incorporation of new material. Several new enzymes have been
characterized, including cut-and-paste enzymes for remodeling cross-linking xyloglucan, as well as enzymes that appear to regulate both the yield threshold of the wall and its extensibility (11). A
comprehensive and synthetic picture of the molecular basis of wall
extension and its cellular controls remains a major problem for
the future. Recent progress in this field is reviewed in this issue in
an article by Dan Cosgrove (Pennsylvania State University).
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THE IMPACT OF MOLECULAR GENETICS |
Partly because wall polysaccharides are not themselves direct gene
products, and partly because screens were hard to devise, the power of
the tools of molecular genetics has been slower to impinge on the wall
field than on many others. It's now clear from expressed sequence tag
and cDNA databases and the Arabidopsis genome project that at least
1,000 genes are involved in making, assembling, and remodeling the cell
wall and endowing it with particular properties; however, functional
analysis of most of them remains a project for the future. Forward
genetic screens have now begun to generate mutants with altered walls,
largely as a result of the initiatives of Chris Somerville's group
(Carnegie Institute, Stanford, CA; 15) and Richard Williamson's
group (Canberra, Australia). The cloning of the genes involved
in several characterized cell wall mutants is the first notable step in
this field, and it's likely that analysis of insertional mutants and
mutants in sensitized backgrounds will move the field along
quickly. Gene sequencing projects have highlighted the large size of
many families of wall-related genes; for example, pectin-mobilizing enzymes.
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THE WALL TALKS BACK |
In this necessarily brief account I have placed emphasis on the
cellular context of the wall. Nowhere is that more obviously important
than in the slow realization that the wall, far from being inert and
silent stuff outside the cell, is instead intimately involved in
extensive conversations with the cell, sometimes even with a managerial
tone! The plant cell senses numerous signals through the wall via its
connections to integral plasma membrane proteins. Turgor, osmosensing,
mechanical stresses, and strains all are mediated through the wall, and
I have already mentioned the wall's talk back to the cytoskeleton (16, 20). In addition, the wall seems to have homeostatic properties because
there are many cases now where the lowering of one wall component
appears to be compensated for by the rise in another. Two examples
suffice to show how the wall has emerged as a repository for important signals or instructions to the cell within. These signals can act
during the course of normal development to influence local cell fate
decisions, as was elegantly shown by Berger et al. (2), or they
can act in response to external events such as pathogen attack. In the
latter case, small fragments of structural wall polysaccharides, when
released by degradative enzymes, act back as signaling ligands to alert
the cell to mount a defense response (5).
The last 25 years have seen a progressive shift in our perception of
the wall toward a structure that is unique to the cell within, locally
deposited and remodeled, dynamic and developmentally regulated,
complex, and able to respond not only to cellular events, but to
influence them in return. This is a great platform for the boom time
that functional genomics and the new cell biology promise.
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ACKNOWLEDGMENTS |
My own work over this period has been supported by the
Biotechnology and Biological Science Research Council. Special thanks to Maureen McCann for her sane and stimulating input to many of the
ideas expressed here.
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FOOTNOTES |
*
E-mail keith.roberts{at}bbsrc.ac.uk; fax
44-1603-450019.
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© 2001 American Society of Plant Physiologists
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TOP
INTRODUCTION
THE INCREASING COMPLEXITY OF...