Plant Cell Walls

332 Pages·2001·20.817 MB·English

by  Nick Carpita, Mary Tierney, Malcolm Campbell (auth.), N. C. Carpita, M. Campbell, M. Tierney (eds.)

PLANT CELL WALLS
PLANT CELL WALLS
Edited by
N.C. CARPITA
Dept. Botany & Plant Pathology Purdue University, West Lafayette, IN, USA
M.CAMPBELL
Dept. Plant Sciences University of Oxford, Oxford, UK
and
M. TIERNEY
Dept. Botany University of Vermont, Burlington, VT, USA
Reprinted from Plant Molecular Biology, Volume 47 (1, 11),2001
SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.
A c.1.P. Catalogue record for this book is available from the Library of Congress
Library of Congress Catalogue-in-Publication Data
Plant cell walls / edited by Nicholas C. Carpita, Malcolm Campbell and Mary Tierney
p. cm.
lncludes bibliographical references (p.).
ISBN 978-94-010-3861-4 ISBN 978-94-010-0668-2 (eBook)
DOI 10.1007/978-94-010-0668-2
1. Plant cell walls. 1. Carpita. Nicholas C. II. Campbell, Malcolm. III. Tierney, Mary.
QK725.P5582001
571.6'82-dc21
2001046208
Printed an acid-free paper
AII Rights Reserved
@2001 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 2001
Softcover reprint of the hardcover I st edition
No part of the material protected by this copyright notice
may be reproduced Of utilized in any form or by any means,
electronic Of mechanical, including photocopying,
recording or by any information storage and retrieval
system, without written permission from the copyright
owner.
CONTENTS
Overview
Molecular biology of the plant cell wall: searching for the genes that define structure,
architecture and dynamics
N. Carpita, M. Tierney, M. Campbell 1-5
Section 1 - Cytology and metabolism
Pectin: cell biology and prospects for functional analysis
w.G.T. Willats, L. McCartney, W. Mackie, J.P. Knox 9-27
Carbon partitioning to cellulose synthesis
C.H. Haigler, M. Ivanova-Datcheva, P.S. Hogan, V.v. Salnikov, S. Hwang, K. Martin, D.P.
Delmer 29-51
Section 2 - Gene and protein structure
A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana
B. Henrissat, P.M. Coutinho, G.J. Davies 55-72
Structure function relationships of j3-D-glucan endo- and exohydrolases from higher
plants
M. Hrmova, G.B. Fincher 73-91
Section 3 - Primary wall synthesis
Molecular genetics of nucleotide sugar interconversion pathways in plants
W.-D. Reiter, G.F. Vanzin 95-113
Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating
candidates in the genomic era
R. Perrin, C. Wilkerson, K. Keegstra 115-130
Integrative approaches to determining Csi function
T.A. Richmond, C.R. Somerville 131-143
j3-D-Glycan synthases and the CesA gene family: lessons to be learned from the mixed-
linkage (1---->3), (1---->4)j3-D-glucan synthase
C.E. Vergara, N.C. Carpita 145-160
The complex structures of arabinogalactan-proteins and the journey towards under-
standing function
y. Gaspar, K.L. Johnson, K.A. McKenna, A. Bacic, C.J. Schultz 161-176
Section 4 - Growth, signaling & defense
The molecular basis of plant cell wall extension
C.P. Darley, A.M. Forrester, S.J. McQueen-Mason 179-195
WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix
C.M. Anderson, TA Wagner, M. Perret, Z.-H. He, D. He, B.D. Kohorn 197-206
Section 5 - Secondary wall synthesis
Mutations of the secondary cell wall
S.R. Turner, N. Taylor, L. Jones 209-219
Differential expression of cell-wall-related genes during the formation of tracheary
elements in the Zinnia mesophyll cell system
D. Milioni, P.-E. Sado, N.J.S tacey, C. Domingo, K. Roberts, M.C. McCann 221-238
Unravelling cell wall formation in the woody dicot stem
E.J. Mellerowicz, M. Baucher, B. Sundberg, W. Boerjan 239-274
Functional genomics and cell wall biosynthesis in loblolly pine
R. Whetten, Y.-H. Sun, Y. Zhang, R.S ederoff 275-291
Section 6 - Cell wall biotechnology
Enabling technologies for manipulating multiple genes on complex pathways
C. Halpin, A. Barakate, B.M. Askari, J.C. Abbott, M.D. Ryan 295-310
Cell wall metabolism in fruit softening and quality and its manipulation in transgenic
plants
DA Brummell, M.H. Harpster 311-340
Cover illustration
A functionally important aspect of the in muro modification of the pectic matrix is the regulation of the
degree and pattern of methyl esterification of the homogalactouronan (HG) backbone. The image shows
a junction between three tobacco stem cortical cells that have been immunolabelled with the monoclonal
antibodies LM7 (red) and PAM1 (green) and stained with the cellulose-binding reagent Calcofluor (blue).
PAM1 and LM7 are methylester pattern-specific antibodies and bind to unesterified and partially methyl
esterified HG respectively. In this issue, both antibodies bind to a region of cell wall that lines intercellular
spaces, but the discrete locations of LM7 and PAM1 labelling indicates that the distribution pattern of
methylesters along the HG backbone is differentially regulated within cell wall microdomains. (Courtesy
of Willats et al., Centre of Plant Sciences, Leeds, UK)
.... Plant Molecular Biology 47: 1-5,2001.
.,,, © 2001 Kluwer Academic Publishers.
Overview
Molecular biology of the plant cell wall: searching for the genes that define
structure, architecture and dynamics
Nick Carpital,*, Mary Tiemey2 and Malcolm Campbell3
1D epartment of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907-I 155, USA (* author
for correspondence; e-mail [email protected]); 2 Department of Botany, University of Vermont, Marsh Life
Building, Burlington, VT 05405, USA; 3 Department of Plant Sciences, University of Oxford, South Parks Road,
Oxford OX13RB, UK
Introduction verse genetic and molecular biological approaches,
based on discovery of homologous genes from bac
The plant cell wall is a highly organized compos teria, fungal, and animal systems, have augmented the
ite that may contain many different polysaccharides, collection of recognized wall-relevant genes consid
proteins, and aromatic substances. These complex ma erably, but the functions of many of these genes still
trices define the features of individual cells within the remain elusive.
plant body. Ultimately, the plant wall functions as the The major steps in wall biogenesis and modifica
determinant of plant morphology. The importance of tion can be divided into six specific stages: (l) the
the plant cell wall is revealed in the shear number synthesis of monomer building blocks, such as nu
of genes that are likely to be involved in cell wall cleotide sugars and monolignols, (2) the biosynthesis
biogenesis, assembly, and modification. For example, of oligomers and polysaccharides at the plasma mem
over 17% of the 25498 Arabidopsis genes have signal brane and ER-Golgi apparatus, (3) the targeting and
peptides, and over 400 proteins have been identified secretion of Golgi-derived materials, (4) the assembly
that reside in the wall (Arabidopsis Genome Initia and architectural patterning of polymers, (5) dynamic
tive, 2000). If just one-half of the proteins with signal rearrangement during cell growth and differentiation,
peptides function in the biosynthesis, assembly, and and (6) wall disassembly and catabolism of the spent
modification of the walls, then well over 2000 genes polymers. For some of these stages, such as the gener
are likely to participate in wall biogenesis during plant ation of known substrates, complete knowledge of the
development. This number is considerably larger if biochemical pathways has led to discovery of many of
all the cytosolic proteins that function in substrate the genes.encoding the enzymes involved in the catal
generation are included. Beyond this, some integral ysis. For other stages, such as wall assembly, the kinds
membrane-associated proteins, such as cellulose syn of proteins that might participate remain purely spec
thase, obviously function in cell wall biogenesis but ulative. To put into perspective the challenges of gene
do not contain signal peptides. Thus, it is likely that discovery and determination of function, we have as
some 15% of the Arabidopsis genome is dedicated to sembled articles by leading cell-wall researchers that
cell wall biogenesis and modification. Of these, only illustrate the most recent advances in this field and the
small subsets have been characterized. long road of discovery that lies ahead.
Recently, forward and reverse genetic approaches
have provided insight into the genes relevant to cell
wall metabolism. Forward genetic approaches have Visualizing gene expression
historically been hampered by technical problems as
sociated with characterization of polymer synthesis After a century's work by carbohydrate chemists and
in vitro and of higher-order architectural assembly and biochemists, we now have a fairly complete catalog
rearrangement during growth. On the other hand, re- of the major polysaccharides of the walls of higher
2
plants. The vast majority of these studies are a re ways and ultimately to cellulose via a UDP-glucose
sult of bulk chemical analysis and do not give many shuttle. Several years ago, they discovered that sucrose
ideas for the dynamic changes that occur in walls synthase, or 'SuSy', is associated with the plasma
of different tissues, different cells of the tissue, and membrane, and they presented evidence that sucrose
even within domains of a single cell wall. In situ hy may provide glucose directly to cellulose synthase.
bridization studies have been influential in beginning In their article, they present several other biochemi
to unravel cell specificity of wall-relevant gene ex cal and cellular mechanisms that might directly im
pression, and antibodies directed against wall-relevant pact cellulose synthesis from the cytosolic side of the
enzymes and specific epitopes of their substrate have plasma membrane.
afforded us a glimpse of the sub-domains of a sin
gle cell wall. Willats et al. (this issue) provide a
comprehensive summary of the complexities of pectin Genomic approaches to define wall-relevant genes
fine structure and how the use of monoclonal anti
bodies against pectin epitopes has revolutionized our Genomic approaches have provided a global view of
knowledge of their cell and wall domain specificity gene expression related to primary and secondary cell
and their dynamics during growth and development. wall synthesis. Henrissat et al. (this issue) provide a
In particular, antibodies directed against two neutral robust census of Arabidopsis glycosidases and glyco
sugar side-groups, arabinans and galactans, have re syltransferases derived from knowledge of the entire
vealed a remarkable sub-domain distribution that will Arabidopsis genome sequence. One surprise of this
now allow more refined determinations of structural census is that Arabidopsis encodes many more of
functional and dynamic relationships of these transient these enzymes than does Saccharomyces cerevisiae,
components during cell growth and development. Drosophila melanogaster or Caenorhabditis elegans.
Over 600 genes are involved in polysaccharide syn
thesis and turnover, and almost one-quarter of them
Defining pathways to synthesis (140) are involved in the turnover of pectins. One of
the major surprises that resulted from the sequenc
The selection of Arabidopsis mutants in which a cell ing of the Arabidopsis genome was the percentage of
wall sugar is over- or under-represented led to the gene families with more than 5 members (Arabidop
discovery of two genes involved in nucleotide-sugar sis Genome Initiative, 2000), and this also holds true
interconversion pathways. Reiter and Vanzin (this is for hydrolase and glycosyltransferase gene families.
sue) describe the molecular genetics of these impor In addition, 80 different hydrolase and 45 different
tant pathways for de novo substrate production and the glycosyltransferase gene families were identified, and
salvage of certain sugars after they are excised from a great many of them define families found only in
polysaccharides. The 4,6-dehydratase involved in the plants. Of these, well over half are thought to function
synthesis of GDP-L-fucose, and the C-4 epimerase within the secretory pathway or the cell wall. Repre
that interconverts UDP-Xyl and UDP-Ara represent sentative enzymes from many of these families have
just two of a minimum of 11 enzymes that function been crystallized, and their 3-dimensional structure
in the de novo pathways of nucleotide sugar synthe has been determined, so the families are beginning
sis from GDP- or UDP-Glc. Comparative genomics to be defined on the basis of their amino acid se
have given important clues on identification of the quences as well as the structure of their active sites.
remainder, and this article identified several candi Hrmova and Fincher (this issue) focus on a specific
date genes that assure that the genes that encode the subset of the hydrolase families genes from barley
entire nucleotide-interconversion pathways will be de and other cereals for which the 3-dimensional struc
duced very quickly. Another group of C-l kinases, tures are known. Through activity studies, they begin
NDP-pyrophosphorylases, and other carbohydrate to define the substrate specificities of individual fam
generating enzymes are involved in the salvage of ily members of fJ-glucan exo- and endohydrolases.
sugars back into the nucleotide-sugar pool. A gene en Through expression studies, the function of some of
coding only one of these enzymes, an arabinokinase, these hydrolases involved in the turnover of storage
has been identified. polymers and in cell growth may be inferred.
Haigler et at. (this issue) delve further into the Perrin et al. (this issue) outline two principal em
pathways of carbon into the nucleotide-sugar path- pirical routes to identify synthases and glycosyl trans-
)
ferases and to characterize their functions. Classical that not all CesA genes encode synthases of cellulose
means to purify and identify these enzymes relied on and underscores the need to define the function of each
biochemical schemes that were difficult at best and, synthase gene by relined biochemical techniques.
in many instances, impossible to accomplish. They
demonstrate how bioinformatics and functional ge
nomics can provide a powerful means to identify and The genomics of cell specialization
evaluate candidate genes through database searches
and 'expression profiling' by microarray analyses. In The secondary cell walls provide excellent examples
this article, they nicely review the recent advances of how cell wall modification confers specific prop
using genetic, reverse-genetic, biochemical, and het erties upon a cell to allow it to fulfill specialized
erologous expression methods that can be employed functions. Secondary cell walls are frequently a efa
10 determine the function of these families of genes. ture of cells that provide support for the plant body,
Cellulose synthase is arguably the most impor and cells involved in the transport of water and solutes
tant enzyme involved in plant cell wall biosynthe from the roots to the aerial tissues. Secondary cell
sis. Richmond and Somerville (this isssue) discuss walls allow these cells 10 resist the forces of gravity
the e normity of the cellulose synthase superfamily and/or the tensional forces associated with the tran
of Arabi(Jupsi.\· and how a powerful multidisciplinary spirational pull on a column of water. Turner et 01.
approach can be used to determine gene function (this issue) summarize how a clever mutant screen was
within this alrge superfamily. They show how cellu used 10 define genes specifically involved in cellulose
lose synthase-related functions might be deciphered synthesis and lignification during secondary cell wall
using a systematic analysis of individual cellulose syn fonnation. The mutant screen was based on the fact
thase family members. The systematic analysis melds that the inability to produce secondary cell waH com
a number of approaches. including bioinfonnatics. ponents in cells that would normally have a secondary
classical and reverse genetics coupled with chemi cell wall, like xylem cells. would cause these cells to
cal analysis of mutants, and gene expression analysis collapse. The mutants uncovered by this screen con
using microarrays and promoler::repor1er fusions. tinue to reveal much about the functjon of cellulose
The genes that arc at the core of cell wall biogen synthase family members, and mechanisms involved
esis are those thaI encode polysaccharide synlhases in the control of lignin biosynthesis.
and glycosyl transferases. Synthases are defined as As wood is essentially a collection of secondary
processive glycosyllmnsfemses that iterate linkage of cell walls, many cell-wall-relevant genes have also
mono- or disaccharide units into the backbone poly emerged from genomics research associated with
mer, whereas glycosyltransferases decorate Ihe back wood formation. For example, Mellerowicz el al.
bone with addition of specific sugars. An enormous (this isssue) have examined gene expression associ
task lies ahead to define the function of all the candi ated with xylem development in poplar. Using an
date genes that comprise this stage of wall biogene approach which fuses expressed sequence tag (EST)
sis. Twelve genes define the 'true' cellulose synthase analysis, genetic modification and microarray analy
(CesA) gene family, and 6 additional families encode sis of gene expression patterns, Mellerowicz el al.
30 more cellulose synthase-like (Csl) genes, Of the are developing a 'genetic roadmap' 10 secondary cell
12 CesAs, only three have actually been confirmed wall formation. Whetten el al. (this issue) also com
biochemically, defined through selection of mutants bined EST analysis with microarray assessment of
lacking their function and rescue of wild-type cel transcript accumulation to develop an understanding
lulose synthesis by complementation. Vergara a nd of wood formation in loblolly pine. The findings of
Carpita (this issue) provide a phylogenetic comparison these two groups point 10 the power of using trees
of the CesA genes from two grass species. rice and 10 develop a comprehensive picture of secondary cell
maize. with those of Arabidopsis and two additional wall formation in the context of xylem development.
dicotyledonous species. From analysis of the amino Future studies which make interspecific comparisons
acid sequences of what was originally thought to be a of this process (between pine and poplar, for exam
hypervariablc region, they discovered that this region ple) should create a picture of the general mechanisms
was not really variable but contained family-specific underpinning secondary cell wall formation.
combinations of motifs that probably function in catal One of the few model systems to study the pre
ysis or processivity. Their work raises the possibility cise development of a single cell type ill vitro is that
4
of the transdifferentiation of Zinnia mesophyll cells spatially with respect to their neighbors, plant devel
into tracheary elements. Milioni et al. (this issue) opment relies on discrete and coordinate changes in
optimized the time-course of trans-differentiation to the cell wall to direct the final shape of each cell
48 h to permit selection of time-points for comparative that, ultimately, defines the morphology of the en
gene expression studies. They exploited a powerful tire plant body. All living cells contain also cell wall
AFLP-cDNA approach to document the dynamic ex molecules that affect patterns of development, mark
pression of over 600 genes involved in signaling, wall a cell's position within the plant, or participate in
polymer synthesis and degradation, lignification, and cell-cell and wall-nucleus communication. Another
programmed cell death in this system. The Zinnia sys surprise that emerged from the analysis of the Ara
tem is a powerful tool with which to uncover candidate hidopsis genome is the relative richness of the protein
genes involved in cell wall formation in planta. kinase gene families, a great many of which reside
in the plasma membrane with external facing recep
tor domains (Arabidopsis Genome Initiative, 2000).
How are polymers secreted and assembled into a Anderson et al. (this issue) explored a unique group
cell-specific architecture? of plasma membrane-associated protein kinases called
WAKs. At least some of the WAKs appear to be
Gaspar et al. (this issue) present an in-depth analysis directly associated with pectins and glycine-rich pro
of the gene families that comprise the arabinogalactan teins within the wall. Through this interaction, WAKs
proteins (AG-Ps). The precise function of these pro may function in a range of cellular processes, from
teoglycans is still unknown, but they are associated cell growth and cell anchoring to resistance against
with several developmental events, such as differ pathogens. They undoubtedly represent the tip of the
entiation, cell-cell recognition, embryogenesis, and iceberg with respect to understanding how and what
programmed cell death. They discovered several years messages plant cells communicate.
ago that some of the AG-Ps contain glycosylphos
phatidylinositol anchoring domains, the so-called
'GPI anchors'. Because this structural feature is as Remodeling the wall for plant improvement
sociated with signaling in animal cells, its presence
indicates a potentially new function for AG-Ps. Their A major practical goal of plant cell wall research is
review presents models of proteoglycan function in to generate plants with genetically defined variation
animals and yeast that may shed light on special in composition and architecture to permit assessment
functions of AG-Ps in plants. of modifications on wall properties and plant develop
While specific knowledge of the proteins involved ment. As the range of products produced by transgenic
in assembly and rearrangement during growth are plants continues to broaden, plant cell walls have now
some of the least understood, the xyloglucan en become key targets for plant improvement. Exam
dotransglycosylases and and i'l-expansins, have ples include the modification of pectin-cross-linking
(Y-
greatly modified long-held views about how plant or cell-cell adhesion to increase shelf-life of fruits and
growth regulators controlled growth-related wall ex vegetables, the enhancement of dietary fiber contents
pansion. Darley et al.'s article (this issue) summarizes of cereals, the improvement of yield and quality of
how these two enzymes might function coordinately fibers, and the relative allocation of carbon to wall
during wall expansion and addresses an equally impor biomass for use as biofuels. The reviews that comprise
tant question that heretofore has rarely been broached: this special issue highlight a few of the advances in the
how does the growth stop? identification of the relevant genes and gene products
that are being or could be manipulated to alter cell
wall structures in our crop plants and trees. Brummell
The cell wall is more than an extensible box and Harpster (this issue) review many of the potential
enzymes and proteins that are potential determinants
The six stages of wall development might reasonably of wall softening and swelling that accompany some
be used to classify the fundamental structural elements types of fruit ripening, such as tomato. They explain
of the wall, but they are far from a comprehensive how antisense inhibition and over-expression has been
set of genes whose products function in the plant's used to dissect the temporal requirements involved in
'extracellular matrix'. Because plant cells are fixed wall depolymerization during fruit ripening.
5
With the advent of biotechnology, agricultural for which database comparisons provide putative func
researchers are investigating particular enzymes in tion, but only about 1000 genes have been assigned a
volved in cell wall metabolism in the hope of pro function by direct experimental evidence (Somerville
ducing crops with desired characteristics by enhancing and Dangl, 2000). This year, an ambitious new initia
commercially valuable traits, such as fiber produc tive was launched with a goal to know the function of
tion in flax, cotton, ramie and sisal, or abolishing every Arabidopsis gene by the year 2010 (Chory et aI.,
costly ones, such as lignification in some plant tis 2000).
sues. For example, the pulp and paper industry and The research ofthe 2010 Program is expected to ra
the livestock industry each would benefit by selective diate from the perspective of the gene but, as cell-wall
reduction the lignin content in their respective sources biologists are acutely aware, the cell wall is, literally
of raw material. Reducing lignin content would reduce and figuratively, the farthest cellular structure from the
organochlorine wastes and cut costs tremendously for gene. The reason for this is that the wall is an amalgam
the paper industry, which currently uses chemical ex of a great number of molecules that are synthesized
tractions to purify cellulose from wood. Halpin et al. by an as yet unknown cellular machinery, encoded
(this issue) describe their novel approaches to deter by genes that are far from being fully characterized.
mine which biosynthetic steps are both necessary and Hence, the scientific problems to be solved extend
sufficient to alter lignin content and composition for beyond expression arrays and three-dimensional pro
desired end uses. In one approach, they have devel tein structures. To achieve the goal of understanding
oped a novel system which uses the self-cleaving 2A the function of every wall-relevant gene will require
peptide from the hoof-and-mouth virus to simultane new biochemical and cellular methodologies to paral
ously express two individual proteins under the control lel and even exceed the advances in gene and protein
of one promoter. While this system is quite useful technologies that are embodied by the 2010 Program.
for the simultaneous analysis of multiple biosynthetic The Arabidopsis genome has become a spring
steps in the lignin biosynthetic pathway, it is also board for comparative genetics with the genomes of
likely to be broadly applicable to the analysis of many many other plant species, including our important crop
proteins, beyond those involved in cell wall biogen plants. Although Arabidopsis has proven itself to be a
esis. This is an excellent example of how science superior model plant for genetic studies, many other
designed to cope with the problems associated with species are far more suitable for cellular and biochem
cell wall analysis it likely to be of benefit to all plant ical studies that will unveil gene function. The articles
scientists. constituting this issue not only illustrate the enormous
progress that has been made in identifying the wealth
of wall-related genes but they also point to future
Cell-wall functional genomics in the coming directions and how far we have to go.
decade
The completion of the Arabidopsis genome sequence References
culminates the first century of genetics research since
the rediscovery of Mendel's experiments. Now that we Arabidopsis Genome Initiative. 2000. Analysis of the genome se
quence of the flowering plant Arabidopsis thaliana. Nature 408:
have a complete inventory of the genes sufficient to
796-815.
make a higher plant, what will be the next step for
Chory, J., Ecker, J.R., Briggs, S., Caboche, M., Coruzzi, G., el al.
cell-wall biologists? We estimate that about 15% of 2000. Functional genomics and the virtual plant. A blueprint for
the genome is connected in some way with the biogen understanding how plants are built and how to improve them.
Plant Physiol. 123: 423-425.
esis, rearrangement, and turnover of a cell wall. About
Somerville, C. and Dangl, J. 2000. Plant biology in 2010. Science
45% of the genome encodes proteins for which no
290: 2077-2078.
known function can be deduced. The remaining 55%