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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%
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