The Plant Cell Surface

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Ilene Wiggins
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1 Journal of Integrative Plant Biology 2010, 52 (2): The Plant Cell Surface Editorial Multicellular organization and tissue construction has evolved along essentially different lines in plants and animals. Since plants do not run away, but are anchored in the soil, their tissues are more or less firm and stiff. This strength stems from the cell walls, which encase the fragile cytoplasm, and protect it. Properties of plant cell walls translate into properties of plant tissue. For instance, the cellulose microfibril angle in the different layers of walls of individual cells is a determinant of mechanical functions, which are useful to the plant itself. It also determines material properties of tissues and their potential industrial use. Indeed, plant cell walls determine the industrial value of a range of plant products including paper, timber, foodstuff, fodder, spun fibers, coatings, renewable polymers and future nanocomposites. Cell walls and their biosynthesis is a very active field of plant research. A cell wall is a product of the plant cell, which controls the composition of the wall according to specific needs: it is flexible during cell elongation, and stiff in wood cells. Whatever the final product, cell wall formation requires all parts of the production machinery of cells and is crucial for plant cell growth and therefore for plant development. Cell walls are products of developmentally regulated gene transcriptions activated by environmental cues and regulated by plant hormones and otherwise initiated signal transduction cascades. These processes control protein production and transport and their allocation to the appropriate membrane compartments, and then translocation of these compartments by action of the cytoskeleton to the right sites in the cell. This is followed by insertion of cellulose synthase complexes into the plasma membrane and exocytosis of cell wall material for which the exocyst machinery docks the Golgi compartments/vesicles. The cellulose synthase complexes produce cellulose microfibrils while many other cell wall matrix materials such as hemicelluloses and pectins are produced in Golgi compartments and assemble further inside the cell wall. If a very rigid cell wall is needed, then it is impregnated with lignin, which probably is still the least understood part of the process of cell wall formation and differentiation. doi: /j x The Role of the Cytoskeleton in Bringing the Substrate to the Forming Cell Wall In this special issue of JIPB we focus on the plant cell surface, covering not only the cell wall but also the cell cortex that functions in producing this wall. This compilation of articles is by no means covering all aspects of the process of wall production and classes of molecules making up the cell wall. For instance, there is no article on the role of cortical microtubules, which were reviewed in a rather recent issue of JIPB on the plant cytoskeleton microtubules edited by Yang and Liu (2007). However, work on the role of microtubules in cell wall deposition and cell wall texture formation is progressing fast at the moment. It shows that cellulose synthase complexes not only move along the microtubules (Paredez et al. 2006) and form a regular pattern in their absence (Paredez et al. 2006; Emons et al. 2007), but also that they are involved in their insertion into the plasma membrane (Gutierrez et al. 2009) and possibly in their recycling (Crowell et al. 2009). In summary the present knowledge of the process is as follows: cortical microtubules are not needed for cellulose synthase insertion into the plasma membrane but if present insertion occurs along them. In the same way they are not needed for making a regular cell wall texture, but if present in the cell cortex cellulose synthase complexes follow them, producing the transversely aligned cellulose microfibrils of the elongating plant cell wall. There is still a great deal to be learned about this process and its role in cell elongation. The cover image of this issue of JIPB forms part of this work (courtesy of Jelmer Lindeboom, Wageningen University). The figure shows a cell from an Arabidopsis thaliana etiolated hypocotyl expressing GFP::CESA3 in green and mcherry::tua5 in red at different time points during a photobleaching experiment. Images shown in the figure are, from left to right, 6 seconds before bleaching and 6, 98, 168 seconds after photobleaching, respectively. The square rectangle represents the photobleached region. The green dots within the rectangle represent newly inserted cellulose synthase complexes. Signaling to the Actin Cytoskeleton The actin cytoskeleton moves organelles around in the cell, and delivers Golgi bodies and their cargo for making parts C 2010 Institute of Botany, Chinese Academy of Sciences

Editorial 127 (By courtesy of Jelmer Lindeboom, Wageningen University) of the wall, to the sites of cell elongation (Miller et al. 1999; Ketelaar et al. 2003) and wall thickening (Taylor et al 2003).

2 Editorial 127 (By courtesy of Jelmer Lindeboom, Wageningen University) of the wall, to the sites of cell elongation (Miller et al. 1999; Ketelaar et al. 2003) and wall thickening (Taylor et al 2003). In the work by Gutierrez et al. (2009) for instance, Arabidopsis plants expressing YFP::CESA6 were treated with 1 μm latb for 4 h to disassemble the actin cytoskeleton quite severely. As a result cortical cytoplasmic streaming was slowed down, including Golgi body motility. This treatment did, however, not prevent the delivery of the CESA6 complexes to the plasma membrane. Since by this treatment the Golgi body distribution in the cell cortex, as well as CESA6 complex distribution at the plasma membrane became patchy and co-incident, the authors concluded that actin function is necessary for appropriate global dispersion of Golgi bodies and delivery of CESA6 complexes. The next obvious step is the identification and dissection of signaling cascades and networks having the cytoskeleton and its dynamics as target. In the present issue Fu (2010) discusses signaling cascades required for tip growth of pollen tubes, such as Ca 2+ -, small GTPases- and lipid-mediated signaling, which are involved in transmitting signals to actin-binding proteins. These actin-binding proteins in turn regulate the structure of the configuration of actin filaments and their turnover. The actin cytoskeleton integrates several signaling pathways at work not only in the regulation of tip cell elongation but as well in polarized diffuse, also called intercalary, plant cell growth. The Role of Exocytosis in Delivering Wall Matrix and Cellulose/Callose Producing Enzymes The exocyst, a protein complex of which the subunit genes are present in plant cells (Hala et al. 2008), and which functions in yeast and animal cells in determining the sites of exocytosis and therefore cell polarity (review for plants: Lindeboom et al.

3 128 Journal of Integrative Plant Biology Vol. 52 No ), is reviewed in the contribution by Zhang et al. (2010). This octameric vesicle tethering complex functions upstream of SNARE-mediated exocytotic vesicle fusion with the plasma membrane. These authors compare the knowledge about the exocyst in plant cells to that known from budding yeast. The Multiple Roles of Calcium Ion at the Plasma Membrane and Inside the Cell Wall Calcium is an important ion in the process of delivery and insertion of Golgi vesicles bearing wall matrix material. In addition it acts as an integral part of the cell wall, binding negative charges on pectins, and thus conveying rigidity to the flexible primary cell wall with a low cellulose microfibril content. Both these roles of the calcium ion, active in different cell compartments and at different concentrations, are reviewed in the contribution of Hepler and Winship (2010). This review on the role of calcium ion at the interface between the cell wall and the cytoplast takes the unique viewpoint of a two-way communication between cytoplasm and cell wall with calcium ion as a crucial participant and regulator. The authors mainly treat knowledge obtained from pollen tubes, but much of it is general for all plant cells. Cellulose Genes in Primary and Secondary Cell Wall Formation According to the definition chosen at the first cell wall meeting in Nijmegen in 1978, primary cell wall is the wall deposited during cell elongation, while the secondary wall is deposited after cell elongation has ceased. When working on cellulose synthase (CESA) genes, scientists found that during the primary cell wall formation in elongating cells a certain set of genes was active (Desprez et al. 2007), while during banded cellulose deposition in tracheary elements of the xylem another set of genes was required (Taylor et al. 2003). The latter were called secondary cell wall genes (Taylor et al. 2003). This definition of secondary cell wall did not match the earlier definition. Betancur et al. (2010) compare gene expression patterns associated with secondary wall synthesis in shoot trichomes of Arabidopsis and cotton, both not of the banded deposition type. They show that CESAs from either the primary or secondary (as defined by genes active in banded cellulose deposition in tracheary elements) wall clades support secondary wall thickening as defined by deposition in elongated cells. CESA genes that typically support primary wall synthesis, AtCESA1, 2, 3, 5 and 6 are active during cell expansion as well as in elongated Arabidopsis shoot trichomes. However, orthologs of CESA genes that are active during secondary wall synthesis in Arabidopsis xylem (AtCESA4, 7 and 8) are up-regulated for cotton fiber secondary wall deposition. Facts and Fiction about Cellulose Biosynthesis In their review Guerriero et al. (2010).concentrate on the facts that we really know about cellulose biosynthesis in higher plants and remind us of the many hypotheses and models that have been created during the past three decades of intensive research on cellulose synthases. The study on CESAs has been very difficult and even though plant cells make masses of the cellulose polymer all the time, its synthesis in vitro has been and still is not an easy job. As cellulose biosynthesis is one of the most important biological processes, many models based on facts have been developed but they necessarily incorporate many hypotheses that still need to be tested. While speculative models are of importance for scientific development, one must bear in mind the known knowns and the known unknowns not forgetting that there are still a lot of unknown unknowns in cellulose biosynthesis. Of these Guerriero et al. have reminded us. Cellulose Production In Vitro Cifuentes et al. (2010) describe a high-yield method for cellulose microfibril production in vitro from membranes of tobacco BY-2 suspension cultured cells. Under the best conditions tried out, use of digitonin as extraction solution in the presence of 8 mm Ca 2+ and 8 mm Mg 2+, and using 11 day old cells, up to 36% of the in vitro products were identified as cellulose whereas 64% corresponded to callose. When using maximum microfibril length produced on electron microscopy grids between 30 and 60 minutes after the start of cellulose production in vitro an elongation rate of 120 nm/min was estimated. Cellulose microfibril production at the level of groups of microfibrils could also be measured in the liquid crystal polarization microscope, but production velocity at the level of the single microfibril was not possible to determine by this method. The Ultrastructure of Xylem Formation in Poplar Kaneda et al. (2010) report on the secondary cell wall formation at the ultrastructural level in developing secondary xylem of poplar, i.e. a cell type comparable to the above-mentioned tracheary element cells with local cellulose microfibril deposition. They examined high pressure frozen/freeze substituted fibres with transmission electron microscopy at stages during fibre development. In addition the distribution of xylans and mannans in the different cell types and during tissue development was investigated with immunofluoescence and immuno-gold labeling. While xylan was deposited throughout the xylem in poplar, mannans were enriched in the S2-layers of fibres.

4 Editorial 129 The Use of Tissue Culture in the Study of Lignification Lignin is a phenolic polymer and is abundant in cell walls of certain plant cell types. Both its structure and biosynthesis as well as the way it enters the cell wall from the cytoplasm is far from known. In plants, lignified tissues are distributed between other, non-lignified tissues, such as groups of sclerenchyma cells in between parenchyma tissue, or tracheary elements of the xylem bordering phloem cells and parenchyma ground tissue. Characterisation of native lignin in the cell wall has been difficult due to the highly cross-linked nature of the wall components. Model systems, such as plant tissue cultures with tracheary element differentiation or extracellular lignin formation, have provided useful information related to several aspects of lignin formation, e.g. the enzyme activities in the phenylpropanoid pathway and factors affecting polymerisation of monolignols. In their review Kärkönen and Koutaniemi (2010) focus on the usefulness of tissue cultures in the study of lignin structures and their biosynthesis. The Role of Peroxidase in Wall Lignification This special issue contains two articles on class III plant peroxidases (PRX). In the paper by Núňez-Flores et al. (2010) a specific PRX gene has been found to contain a gibberellic acid (GA) promoter, which explains the inhibitory effect GA has on hypocotyls and lignin development in Zinnia seedlings. The other lignin study by Fagerstedt et al. (2010) is focused on class III plant peroxidases in the polymerization of the lignin polymer in conifers and especially in Norway spruce. Indeed, it seems that these peroxidases are responsible for the activation of monolignols before their polymerization, rather than laccases of phenol oxidases (Marjamaa et al. 2006, 2007). On the whole, plants contain a large family of class III PRX genes. While there most probably is some redundancy here, it has been shown that certain PRXs are upregulated during specific events, such as lignin polymerization in tracheid cell walls, defence against fungal pathogens or formation of compression wood (Koutaniemi et al. 2007). The Role of Reactive Oxygen Species in Wall Signaling The plant cell wall is part of the apoplastic space in tissues and it is involved in signaling events between plant cells and also in early interactions between plant cells and microorganisms. Reactive oxygen species (ROS) play an important role in this signaling as reported by Nanda et al. (2010). They have recognized that the wave of ROS produced during pathogen invasion and leading to the hypersensitive reaction (HR) is missing in symbiotic interactions. This would then allow for the further interplay between the symbionts and the eventual formation of symbiosis. References Betancur L, Singh B, Rapp RA, Wendel JF, Marks MD, Roberts AW, Haigler CH (2010) Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. J. Integr. Plant Biol. 52, Cifuentes C, Bulone V, Emons AMC (2010) Biosynthesis of callose and cellulose by detergent extracts of tobacco cell membranes and quantification of the polymers synthesized in vitro. J. Integr. Plant Biol. 52, Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof Y-D, Schumacher K, Gonneau M, Höfte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, Emons AMC, Höfte H, Mulder BM (2007) Microtubules and cellulose microfibrils: how intimate is their relationship? Trends Plant Sci. 12, Fagerstedt KV, Kukkola EM, Koistinen VVT, Takahashi J, Marjamaa K (2010) Cell wall lignin is polymerised by class III secretable plant peroxidases in Norway Spruce. J. Integr. Plant Biol. 52, Fu Y (2010) The actin cytoskeleton and signaling network during pollen tube tip growth. J. Integr. Plant Biol. 52, Guerriero G, Fugelstad J, Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? J. Integr. Plant Biol. 52, Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20, Hepler PK, Winship LJ (2010) Calcium at the cell wall-cytoplast interface. J. Integr. Plant Biol. 52, Kaneda M, Rensing K, Samuels L (2001) Secondary cell wall deposition in developing secondary xylem of poplar. J. Integr. Plant Biol. 52, Koutaniemi S, Warinowski T, Kärkönen A, Alatalo E, Fossdal CG, Saranpää P, Laakso T, Fagerstedt KV, Simola LK, Paulin L, Rudd S, Teeri TH (2007) Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol. Biol. 65,

5 130 Journal of Integrative Plant Biology Vol. 52 No Lindeboom JJ, Mulder BM, Vos JW, Ketelaar MJ, Emons AMC (2008) Cellulose microfibril deposition: coordinated activity at the plant plasma membrane. J. Microsc. 231, Kärkönen A, Koutaniemi S (2010) Lignin biosynthesis studies in plant tissue cultures. J. Integr. Plant Biol. 52, Ketelaar MJ, Ruijter NCA de, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15, Marjamaa K, Hilden K, Kukkola E, Lehtonen M, Holkeri H, Haapaniemi P, Koutaniemi S, Teeri TH, Fagerstedt K, Lundell T (2006) Cloning, characterization and localisation of three novel class III peroxidases in lignifying xylem of Norway spruce (Picea abies). Plant Mol. Biol. 61, Marjamaa K, Kukkola EM, Fagerstedt KV (2007) Lignification in development. Int. J. Plant Dev. Biol. 1, Miller DD, Ruijter NCA de, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochitooligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J. 17, Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J. Integr. Plant Biol. 52, Núñez-Flores MJL, Gutiérrez J, Gómez-Ros LV, Uzal EN, Sottomayo M, Barceló AR(2010) Downregulation of the basic peroxidase isoenzyme from Zinnia elegans by gibberellic acid. J. Integr. Plant Biol. 52, Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. USA 100, Yang Z, Liu B (2007) Celebrating plant cells: a special issue on plant cell biology. J. Integr. Plant Biol. 49, Zhang Y, Liu CM, Emons AMC, Ketelaar T (2010) The plant exocyst. J. Integr. Plant Biol. 52, Anne-Mie C. Emons The Editor of this Special Issue Plant Cell Biology Droevendaalsesteeg 1 Wageningen University 6708 PB Wageningen The Netherlands Kurt V. Fagerstedt The Editor of this Special Issue Plant Biology PO Box 65 FI Helsinki University Finland

13-3. Synthesis-Secretory pathway: Sort lumenal proteins, Secrete proteins, Sort membrane proteins

13-3. Synthesis-Secretory pathway: Sort lumenal proteins, Secrete proteins, Sort membrane proteins Molecular sorting: specific budding, vesicular transport, fusion 1. Why is this important? A. Form and