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Keywords:

  • Cell wall;
  • chemical genomics;
  • endomembrane trafficking;
  • trans-Golgi network;
  • vesicle proteomics

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

The cell wall, a crucial cell compartment, is composed of a network of polysaccharides and proteins, providing structural support and protection from external stimuli. While the cell wall structure and biosynthesis have been extensively studied, very little is known about the transport of polysaccharides and other components into the developing cell wall. This review focuses on endomembrane trafficking pathways involved in cell wall deposition. Cellulose synthase complexes are assembled in the Golgi, and are transported in vesicles to the plasma membrane. Non-cellulosic polysaccharides are synthesized in the Golgi apparatus, whereas cellulose is produced by enzyme complexes at the plasma membrane. Polysaccharides and enzymes that are involved in cell wall modification and assembly are transported by distinct vesicle types to their destinations; however, the precise mechanisms involved in selection, sorting and delivery remain to be identified. The endomembrane system orchestrates the delivery of Golgi-derived and possibly endocytic vesicles carrying cell wall and cell membrane components to the newly-formed cell plate. However, the nature of these vesicles, their membrane compositions, and the timing of their delivery are largely unknown. Emerging technologies such as chemical genomics and proteomics are promising avenues to gain insight into the trafficking of cell wall components.

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[ Georgia Drakakaki (Corresponding author)]


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

Membrane trafficking from the endoplasmic reticulum (ER) through the Golgi to the plasma membrane (PM) and the apoplast is an essential delivery system for cell wall deposition. The cell wall is an organized meshwork of polysaccharides and proteins which reside in the apoplast of plant cells. Polysaccharides found in the primary cell wall include cellulose, hemicellulose, and three classes of pectic polysaccharides: homogalacturonan, rhamnogalacturonan I (RG-I), and rhamnogalacturonan II (RGII) (Mohnen 2008; Keegstra 2010; Scheller and Ulvskov 2010). The wall's cellulose components are normally assembled into microfibrils composed of 36 beta-1,4-linked glucan chains. The microfibrils are the major support elements in the primary wall. Hemicelluloses include xyloglucan (XyG), glucomannan, xylan, and mixed-linked glucans, polymers that form H-bonds to the microfibril surfaces and are thought to crosslink cellulose microfibrils (Somerville 2006; Keegstra 2010; Scheller and Ulvskov 2010). However, the extent and structural significance of the XyG-cellulose cross-linking in the dicot primary cell wall is a subject of current debate (Park and Cosgrove 2012). Cell-wall proteins (hydroxyproline- and proline-rich glycoproteins and arabinogalactan proteins) provide structure and enable modification of the cell wall in planta (reviewed by Showalter 1993). Secondary cell walls have a slightly different composition and contain lignin (Carpita 2012).

Cell walls are important for plant growth and development, which likely explains why as much as 15% of a plant's genome is devoted to cell wall biosynthesis and deposition (Carpita 2012). The wall provides protection and structural support for the plant, and deposition of new cell wall material and reorganization of the existing cell wall are required for cell growth (reviewed by Cosgrove 2005). The sugars in cell wall polysaccharides, most particularly the glucose in cellulosic glucans, can be fermented for the production of ethanol, a promising biofuel (Carpita 2012).

Excellent recent reviews address the properties of post-Golgi membrane compartments and their regulatory proteins (Park and Jurgens 2011), and discuss cell-wall biogenesis and the trafficking of cellulose synthases to or through the PM (Geisler et al. 2008; Crowell et al. 2010; Pauly and Keegstra 2010; Driouich et al. 2012). This review summarizes recent progress in understanding the delivery of cell wall materials and the regulation of post-Golgi trafficking, and additionally describes emerging technologies that are used to dissect endomembrane compartment contents and functions.

Endomembrane Compartments and Cell Wall Biogenesis

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

Golgi: The factory manufacturing new cell wall components

The Golgi apparatus is the site of synthesis of non-cellulosic cell-wall polysaccharides other than callose (reviewed by Driouich et al. 2012). These polysaccharides are transported to the cell wall in Golgi-derived vesicles. In contrast, cellulose is produced by cellulose synthase complexes at the PM (reviewed by Somerville 2006; Driouich et al. 2012). However, the enzymes involved in producing cell wall polysaccharides are not uniformly distributed within the Golgi or compartments of the endomembrane system; different Golgi cisternae and secretion pathways are thought to have specific roles in the process. Immunogold-electron microscopy and antibodies that recognize different XyG polymer epitopes have been used to identify the sites of assembly of different XyG structural elements in the Golgi of suspension-cultured sycamore cells. The XyG backbone is synthesized only in trans cisternae, whereas the fucosylated XyG side chains were detected in the trans cisternae and the trans-Golgi network (TGN), suggesting an “assembly-line”-type of organization (Zhang and Staehelin 1992). However, in tobacco BY2 cells, the localization of a XyG polymer backbone epitope and the ectopically-expressed Arabidopsis biosynthetic enzymes XXT1 and MUR3 (involved in the addition of xylosyl and galactosyl residues, respectively, to XyG side groups) were localized in cis and medial Golgi cisternae (Chevalier et al. 2010), indicating possible differences in the location of XyG synthesis and assembly among plant species.

Pectin synthesis has been more difficult to understand because of the complexity of the polysaccharides. However, pectin backbones are synthesized in the Golgi, with side-group decorations being added in different cisternae. The synthesis of the non-esterified rhamnogalacturonan I (RGI)/homogalacturonan (HG) backbone and the methylesterification of galacturonic acid residues is thought to commence in the cis-medial Golgi and is probably completed in the medial cisternae, whereas the arabinose-containing side chains of RGI are detected only in the TGN (Zhang and Staehelin 1992). Additional studies have shown that the specific compartmentalization of pectin synthesis may differ according to cell type (Lynch and Staehelin 1992), but the precise spatiotemporal organization of these processes is unclear.

The modification continues as polysaccharides leave the Golgi. Oligosaccharide Mass Profiling (OLIMP) (Gunl et al. 2010) of Golgi-enriched and cell wall fractions of plant cells indicated that the structure of XyG showed a lower degree of substitution in the Golgi-enriched fraction than in the cell wall, suggesting that XyG side-chain addition/modification occurs along the entire secretory pathway, and possibly in the apoplast (Obel et al. 2009). Golgi morphology and the number of stacks and cisternae differ among plant species, cell types and developmental stages, which may reflect differences in the organization of the steps in cell wall polysaccharide synthesis (Staehelin et al. 1990).

Post-Golgi membrane compartments

Post-Golgi compartments include the TGN, the multi vesicular body (MVB)/prevacuolar compartment (PVC), the lytic vacuole (LV), and the storage vacuole (PSV) (Figure 1). In addition, small vesicles, such as secretory vesicles (SVs) and recycling endosomes (RE), have been identified in several studies of specific localization of proteins (Pesacreta and Lucas 1984; Dautry-Varsat 1986; Futter et al. 1996). The different SVs are structurally indistinguishable, but the fact that they contain different cargo suggests different identities (Carter et al. 2004; Jurgens 2004; Park and Jurgens 2011; Reyes et al. 2011).

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Figure 1. Simplified illustration of post-Golgi trafficking and polysaccharide deposition in a plant cell.  Many cell wall components, including proteins involved in cell wall biogenesis and polysaccharides, are synthesized in the Golgi and traffic to the plasma membrane (PM) via the trans-Golgi Network (TGN) (light blue vesicles). For example, cellulose synthase complexes (CSC; green barrels) are assembled in the Golgi and secreted to the PM, whereby cellulose biosynthesis takes place, while hemicellulose and pectins are synthesized in the Golgi and secreted to the apoplast where they are incorporated into the cell wall. CSCs are thought to recycle through the TGN/Early endosome (EE) (pink vesicles). Proteins destined for degradation travel to the vacuole via multi vesicular body/prevacuolar compartments (MVB/PVC). The MVBs (purple vesicles) are also thought to be formed through TGN maturation. This is a highly simplified representation; thus, the specific proteins and polysaccharides involved in each compartment are not indicated in detail. Dotted interior of Golgi represents cargo. RER, rough endoplasmic reticulum; SER, smooth endoplasmic reticulum; MVB/PVC, multi vesicular body/prevacuolar compartment; TGN/EE, trans-Golgi Network/Early endosome; SV, secretory vesicles; PM, plasma membrane; CSC, cellulose synthase complex.

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Trans-Golgi network (TGN): The hub of endomembrane trafficking

The TGN is an irregular tubulo-vesicular membrane compartment associated with a Golgi stack (Pesacreta and Lucas1984). This association with Golgi is often less tight in plant cells, and disengagement of the TGN from the Golgi can thus be observed easily in plant cells (Nebenführ et al. 1999). Rapid advances in microscopy have revealed several TGN roles, including the specific localization of many proteins at the TGN, and multiple membrane-trafficking pathways through the TGN (Samuels et al. 1995; Dettmer et al. 2006; Park and Jurgens 2011). Vesicles labeled by FM4–64, a lipophilic endosomal tracer, overlapped with the TGN marker VHA-a1-GFP, suggesting that the TGN can function as an early endosome (EE) (Dettmer et al. 2006). Recent time-lapse experiments using spinning disc confocal microscopy have supported the role of TGN as an EE by showing that the YFP-tagged, plasma membrane-localized brassinosteroid receptor BRI1 labeled endocytotic vesicles of the TGN (Viotti et al. 2010). The small molecule endosidin 1 arrests the PM proteins BRI1 and PIN2 in aggregates at the TGN labeled with the syntaxin of plants 61(SYP61), further confirming the role of TGN as an early endosome (Robert et al. 2008).

A recent proteomics analysis of the SYP61-labeled compartment showed that the SYP61-labeled TGN/EE functions in the trafficking of cell wall components (Drakakaki et al. 2012). This proteome includes several subunits of cellulose synthase complexes (CESA) and callose synthases. Given that the TGN functions as an assembly station for non-cellulosic polysaccharides (reviewed by Driouich et al. 2012), it is remarkable how this high traffic station sorts cargo to its intracellular and apoplastic destinations. In fact, several key molecular players maintain and regulate TGN/EE function, including (RAB and ADP-ribosylation factor) GTPases and SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptors) proteins (reviewed by Barfield et al. 2009; Schumacher and Krebs 2010; Park and Jurgens 2011; Thordal-Christensen et al. 2011). For example, the small GTPase RABA4b acts as an effector of phosphatidylinositol-4 kinase (PI-4K) (Preuss et al. 2006). Electron tomography showed that both RABA4b and PI-4K localize at the TGN and SVs, and indicated a potential function of the lipid kinase in regulating the size of SVs (Kang et al. 2011). The potential role of RABA4b in polysaccharide secretion was implicated by its colocalization with XyG-specific antibodies (Kang et al. 2011).

The multivesicular body/prevacuolar compartment: A starting point of protein degradation?

Proteins endocytosed into plant cells either recycle to the PM or are delivered to the vacuole for degradation. Considering that the TGN functions as an EE, endocytotic vesicles containing PM proteins destined for degradation are generally sorted at the TGN/EE to the LV through MVB/PVC. The MVB has a distinct ultrastructure, and as its name suggests it contains multiple internal lumens. Its biogenesis has been extensively studied in animals (reviewed by Piper and Katzmann 2007). Most often, ubiquitination is used as a signal for internalization and degradation. The endosomal-sorting complexes (ESCRT-0, -I, -II, and -III) detect the ubiquitinated cargo, and mediate its sorting to the MVB (reviewed by Leung et al. 2008). Interestingly, recent studies involving the localization of ESCRT components indicate that MVB maturation occurs at the TGN/EE (Scheuring et al. 2011). MVBs have been identified as the functional equivalent of late endosomes in animal cells (Tse et al. 2004). The function of MVB/PVCs in cell-wall modification and regulation has been implicated as a defense mechanism in plants under attack by pathogens (reviewed by Ding et al. 2012).

Trafficking Routes of Cell Wall Components

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

Regulators of endomembrane trafficking: Relationship between vesicle trafficking and polysaccharide deposition

Secreted cell-wall components (including polysaccharides, cell-wall biosynthetic enzymes, and structural proteins) were thought to be transported from the Golgi apparatus to the PM following the default pathway, although export of wall components appears to be more complex and may involve multiple specific pathways. Non-cellulosic polysaccharides are synthesized in the Golgi apparatus and transported to the wall, although it is not yet clear specifically what these trafficking pathways are. That different cell wall components must have site-specific trafficking routes to localized areas of growth or other wall modifications is indicated by the heterogeneity of the wall polysaccharide distributions within a single cell. Examples of such heterogeneity include cell polarity and differential cell wall composition around the plasmodesmata, pit fields and intercellular spaces of parenchyma cell types (Lynch and Staehelin 1992; Orfila and Knox 2000; Willats et al. 2001; Lucas and Lee 2004; Park et al. 2011; Anderson et al. 2012). Several lines of evidence, mainly from Arabidopsis mutants, link endomembrane trafficking pathways with polysaccharide deposition. Vacuolar ATPases (V-ATPases) facilitate membrane trafficking by creating a pH gradient along the secretory pathway (Schumacher and Krebs 2010). There is evidence that cellulose content is dependent on V-ATPase activity at the TGN (Brux et al. 2008). RNA interference of TGN-localized VHA-a1 caused defects in cell wall expansion and Golgi organization that could lead to retention of CESAs in the Golgi. Similarly, the null mutants of the TGN component ECHIDNA show defects in both trafficking (including V-ATPase mislocalization) and cell elongation, furthering the connection between the TGN, V-ATPases, and cell wall deposition (Gendre et al. 2011). It is possible that apoplast acidification does not occur in the echidna mutant, and addition of the new cell wall does not proceed normally. SNARE proteins mediate vesicle fusion (Jahn and Scheller 2006) and are expected to define specific trafficking pathways such as those that are involved in cell wall polysaccharide transport and deposition. For example, mutants of the SNARE Syntaxin of Plants 122 (SYP122), exhibit polysaccharide changes as indicated by Fourier transform infrared spectroscopy (FTIR), but SYP122's role in cell wall deposition remains to be determined (Assaad et al. 2004).

Trafficking of cell wall components to the apoplast is a highly regulated process, but its regulation is not entirely understood. It has been suggested that plants have feedback mechanisms for sensing cell wall properties (for example, polymer distribution and physical characteristics), and provide modifications as needed for growth or response to environmental stimuli (Seifert and Blaukopf 2010). Regulation may occur through the partitioning of carbon into the nucleotide sugars needed for polysaccharide synthesis, or by regulating glycosyl transferases involved in polymer building (Reiter 2008). Other proteins known to perform regulatory roles include the wall associated kinases (WAKs), which are receptor-like kinases (RLKs) that likely serve as pectin receptors in cell expansion (Kohorn and Kohorn 2012), and THESEUS1 (THE1), another membrane bound (RLK) that may sense cell wall integrity (Hematy et al. 2007). Brassinosteroids are thought to play a role in cell wall regulation by ensuring homeostasis in the wall, potentially through pectins (Wolf et al. 2012).

Pathways of polysaccharide secretion

An interesting intersection between trafficking and cell wall polysaccharide synthesis was revealed by studies of the KATAMARI1 (KAM1)/MUR3 mutant. The MUR3 encodes a galactosyl transferase that adds a galactosyl residue to one of the xylosyl side-groups of a growing XyG polymer. MUR3 is allelic to KAM1, which is involved in endomembrane-actin microfilament interactions (Madson et al. 2003). The kam1/mur3 mutant has an altered endomembrane appearance (Tamura et al. 2005), whereas the lack of galactosyl transferase activity causes structural changes in XyG (Madson et al. 2003). Tamura et al. (2005) suggested that KAM1 could be involved in providing feedback from the cell wall to the cytoskeleton to control Golgi-mediated vesicle trafficking. Overall, KAM1 could provide evidence for specific actin-dependent pathways for the transport of selected polysaccharides.

Immuno-gold labeling using a pectin-specific antibody was used to show that the secretory carrier membrane protein 2 (SCAMP2) vesicles carried pectin cargo in tobacco BY-2 cells (Toyooka et al. 2009). More directly, pectin polysaccharide trafficking and deposition were observed by using copper-catalyzed click chemistry to attach a fluorophore to an alkynated fucose (Alk-Fuc) analog. A significant portion of the tagged fucose was incorporated into RG-I side branches in the cell wall of Arabidopsis root cells (Anderson et al. 2012). Polysaccharides containing this alkynated fucose analog appeared at the cell wall in uniformly-distributed punctae, probably representing sites of vesicle fusion with the PM and delivery of RG-I to the apoplast in elongating cells (Anderson et al. 2012).

Cellulose synthase trafficking

More is known about the trafficking of the cellulose biosynthesis machinery than any other component involved in the cell wall, because yellow/green fluorescent protein (Y/GFP)-CESA fusions and their dynamic movement have been visualized directly using high-end confocal microscopy. Cellulose synthase complexes (CSCs) are composed of 36 proteins assembled into a rosette-shaped complex (Somerville 2006). There are 10 cellulose synthase (CESA) genes in Arabidopsis (Richmond 2000), and at least three (CESA1, CESA3 and CESA6) contribute to primary cell wall cellulose synthesis (Desprez et al. 2007; Persson et al. 2007; Wang et al. 2008). Interestingly, in root hair cells, a cellulose synthase-like protein, CSLD3, has been proposed as the primary cellulose synthase (Park and Cosgrove 2012). CSCs are presumably assembled in the Golgi apparatus and trafficked to the PM where they are aligned with microtubules (MT) (Paredez et al. 2006) and extrude cellulose into the apoplast.

YFP-CESA6 has been localized in the Golgi, the PM, and in vesicles trafficking between them (Paredez et al. 2006). The small subcellular compartments containing CSCs have been described as either microtubule-associated cellulose synthase compartments (MASCs) (Crowell et al. 2009), or as small CESA compartments (SmaCCs) (Gutierrez et al. 2009). It is possible that the MASCs/SmaCCs deliver the CSCs to the PM, or are responsible for their endocytosis and recycling (Crowell et al. 2009; Gutierrez et al. 2009). The localization of MASCs or SmaCCs can be altered by certain stimuli, as shown by the application of osmotic stress resulting in cortical accumulation and the tethering of the small vesicles (Crowell et al. 2009; Gutierrez et al. 2009). To date, the precise nature of the secretory vesicles that carry CESAs is unknown. Colocalization with SYP61, VHA-a1, SYP41 or SYP42 has been observed for different vesicle populations of CESAs (Crowell et al. 2009; Gutierrez et al. 2009). In a recent proteomic analysis of SYP61-isolated vesicles, several CESAs were identified, suggesting that CSCs may traffic through a SYP61-mediated pathway (Drakakaki et al. 2012). Further isolation of SmaCCs or MASCs under different conditions is necessary to identify their cargo and determine their trafficking route.

The movements of the fluorescently-tagged CESAs mark CSCs along the PM, guided by the MTs (Crowell et al. 2009; Gutierrez et al. 2009). Several excellent recent studies describe the role of cytoskeleton, and particularly the MT arrays in organizing CESAs at the cell cortex (Gutierrez et al. 2009; Crowell et al. 2010; Chan et al. 2011).

Recently, the identification of the “linker” cellulose synthase interactive protein CSI/POM2 provided insight into the CSC-MT interaction. This protein binds directly to both CESA subunits and MTs, and is critical for the co-alignment of CESA complexes with MTs (Bringmann et al. 2012; Li et al. 2012; Mei et al. 2012). Interestingly, CSI1 does not localize with Golgi-associated CSCs, indicating that CSI1 might not be required for their assembly in the Golgi (Li et al. 2012). Additional fine-tuning of our understanding of the interaction between CSI, CESAs and MTs will answer how disruption of the microtubule array influences CESA complexes, and how cellulose biosynthesis might influence MT behavior, and could reveal possible mechanisms that regulate CESA activity (Bringmann et al. 2012; Li et al. 2012).

Actin has been implicated in the trafficking of cellulose synthase complexes. Both actin filament abnormalities and cellulose deficiency occur in the ROOT HAIR DEFECTIVE3 (RHD3) gene mutant (Hu et al. 2003). Disturbance of actin in developing pollen tubes in Picea meyeri leads to altered cell wall polymer distribution (Chen et al. 2007). The use of latrunculin A to depolymerize actin filaments resulted in altered CESA-YFP Golgi localization, suggesting the involvement of actin in CESA trafficking, although complexes at the PM remained active (Gutierrez et al. 2009). Studies of xylem cellulose deposition (Wightman and Turner 2008) led to the suggestion that actin filaments are important for long-distance transport of MASCs/SmaCCs, whereas MTs maintain the complexes once they are localized at the PM (Wightman and Turner 2008; Wightman and Turner 2010). This model could hold true for primary cell wall synthesis, as mentioned above, in which the CSCs display an altered Golgi distribution after pharmacologically-induced actin disruption (Gutierrez et al. 2009). Furthermore, this model was proposed to utilize bifunctional proteins such as KAM/MUR3 (Tamura et al. 2005) to regulate actin-mediated vesicle trafficking of CESAs (Geisler et al. 2008).

It is possible that a mechanism of CESA regulation is mediated by their recycling. It has been suggested that CESAs may be removed from the membrane to prevent expansion in conditions that are unfavorable for cell growth, such as osmotic stress (Crowell et al. 2009; Gutierrez et al. 2009). Regulated intracellular cycling was also seen in the endoglucanase KORRIGAN, which may be a cellulosic glucan-processing enzyme in the CSCs (Robert et al. 2005). Finally, a degradation mechanism has been proposed for targeting CESAs that are not properly incorporated into a complex (Taylor 2007).

A small GTPase, dynamin, which is a catalyst for membrane fusion, has been implicated in the internalization of enzymes involved in cellulose synthesis. A null mutant of a plant dynamin-related protein 1A (DRP1A), rsw9, is cellulose-deficient (Collings et al. 2008). A similar phenotype has been seen in a mutation of the rice dynamin, OsDRP1A, which is also cellulose-deficient and is a part of clathrin-dependent endocytosis (Fujimoto et al. 2010; Hirano et al. 2010). In addition, mutations in another rice dynamin OsDRP2B were affected in the production of secondary cell wall cellulose, suggesting specificity of dynamins for either primary or secondary cell walls (Xiong et al. 2010; Zhang and Zhou 2011). Further identification of the molecular components involved in plant clathrin-mediated endocytosis could pin down the role of this process in CESA recycling.

Secretion of proteins involved in cell wall modification

Cell wall enzymes involved in polysaccharide assembly and modification are secreted to the cell wall via Golgi-derived vesicles to modify polysaccharides in muro (Showalter 1993; De Caroli et al. 2011; Gunl et al. 2011; Gunl and Pauly 2011; Sampedro et al. 2012). Previously, trafficking of wall-modifying enzymes to the apoplast was thought to occur through bulk flow (Jurgens 2004), however, recent evidence indicates that multiple pathways are involved. An example of differential trafficking has been shown in a study which follows the secretion of two pectin polysaccharide-modifying proteins (a pectin methyl esterase inhibitor, PME1, and a polygalacturonase-inhibiting protein, PGIP2) in planta (De Caroli et al. 2011). The PME and the PGIP were expressed in tobacco (Nicotiana tabacum) as fluorescent protein fusions and transported to the PM and into the apoplast via separate secretion paths. Both trafficking routes were distinct from the default secretion pathway that was traced using secGFP, and were independent of the syntaxin SYP121 (De Caroli et al. 2011). Interestingly, AtPME1 was identified in the SYP61 vesicle proteome as one of the cargo molecules (Drakakaki et al. 2012). Further investigation will attempt to identify possible intersections of these pathways.

The cell plate: An excellent model to study endomembrane trafficking of cell wall components

The cell plate is a thin, membranous structure formed from Golgi-derived vesicles transported to the center of a dividing cell, requiring the trafficking of cell wall components for its maturation (Staehelin et al. 1990). The cell plate is mainly constructed by dynamic accumulation and fusion of vesicles driven from the TGN/EE under the influence of several membrane trafficking regulators, and by the dynamic rearrangement of the MT cytoskeleton (reviewed by Jurgens 2005a, 2005b and summarized in Figure 2). Interestingly, it has been proposed that endocytic material contributes to cell plate formation (Dhonukshe et al. 2006). The role of endocytosis and membrane remodeling in joining the cell plate to the parental cell wall was indicated with the identification of the adaptin-like protein TPLATE (Van Damme et al. 2011). Although sterol-dependent endocytosis restricts proteins involved in vesicle fusion at the cell plate and maintains their specificity during late cytokinesis (Boutte and Grebe 2009), the precise role of endocytic events in cell plate formation is not well understood.

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Figure 2. Cytokinesis in plant cells.  During cytokinesis, the cell plate, a plant-specific compartment, is formed at the center of cells to facilitate the separation of the two new daughter cells. Vast secretion with the assistance of endocytosis provides membrane property and the required components for new cell wall construction. Cell plate formation is a dynamic process which includes vesicle trafficking, fusion and fission. RABA2/3-labeled vesicles are highly accumulated at the center of the cell plate formation process. Vesicles labeled by KNOLLE are localized at the cell plate during all the steps of cell plate formation. Fusion and fission of vesicles accumulated at the center of the cell (STEP I) result in tubular-vesicular membrane structures (STEP II). During this step, callose (green hexagons) contributes to the expansion of membrane structures (STEP III). These expansions continue in order to form a sheet-like membrane structure that eventually becomes the new cell wall, which includes cellulose and xyloglucan (red and blue hexagons) (STEP IV). A recent study detected SCAMP2 localization at the cell plate (Toyooka et al. 2009), indicating the contribution of pectin (yellow hexagons) carrying vesicles during cell plate formation.

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Several regulators of membrane trafficking, including RAB-GTPase and SNARE proteins, are involved in cell plate formation (Chow et al. 2008). The Q-SNARE protein KNOLLE accumulates at the cell plate at the early stages of its formation (Lauber et al. 1997). Reichardt et al. (2011) showed that selective rescue of the knolle mutant was achieved by another Q-SNARE PEN1, but not by SYP113, suggesting the specific utilization of SNARE proteins during cytokinesis. The R-SNARE VAMP771 is also first detected at the cell plate at an early stage of cytokinesis (Zhang et al. 2011). Similarly, the GTPase RABA2A localizes at the cell plate throughout the entire cell plate maturation process, whereas raba2/3 mutants show cytokinesis defects, demonstrating the importance of RABA2A in cell plate formation (Chow et al. 2008; Geisler et al. 2008).

Delivery of cell wall materials to the cell plate has been studied through diverse approaches, including electron microscopy combined with the use of polysaccharide-specific antibodies. The current model of cell plate maturation suggests that callose provides a framework for the deposition of other polysaccharides (Samuels et al. 1995). Recently, a new inhibitor of cell plate formation and callose deposition, Endosidin 7 (ES7), was identified, resulting in incomplete cell plates and providing a useful tool to study the deposition of callose and other polysaccharides during cell plate maturation (Drakakaki et al. 2011). Beta-glucosyl Yariv (beta-GlcY), a known inhibitor of arabinogalactan proteins (AGP), was recently used to demonstrate the potential involvement of AGPs in cell plate positioning (Yu and Zhao 2012).

SCAMP2 localizes in secretory vesicles that accumulate at the cell plate in the early stages of its formation (Toyooka et al. 2009). Interestingly, SCAMP2 vesicles carry pectins, suggesting that SCAMP2 plays a role in delivering this polysaccharide during cell plate maturation. However, how SACMP2 vesicles can traffic cell wall material to both the PM and the cell plate is unclear. A possible explanation is that SNARE proteins other than SCAMP might define the different population of vesicles. Careful observation of the ES7 inhibitory mechanism, and specifically identification of the proteins targeted by ES7, might provide insight into the roles of callose, pectins and other polysaccharides during cell plate formation.

Emerging techniques to study endomembrane trafficking and cell wall deposition

Pinpointing the specific functions of the compartments and the distinct vesicle types involved in trafficking to the plasma membrane is tremendously challenging given their similar physicochemical properties and the overall complexity of the endomembrane system. More important, the dynamic nature of trafficking makes identification of the cargo moving in different vesicles particularly challenging. The emerging technologies of chemical genomics, organelle proteomics, cell wall analysis using OLIMP, the use of polysaccharide antibodies and tagged substrates, and the use of fluorescent tagged screens in combination with next-generation sequencing are promising avenues for dissecting several aspects of cell wall biosynthesis and polysaccharide transport (Obel et al. 2009; Drakakaki et al. 2011; Anderson et al. 2012; Avci et al. 2012; Drakakaki et al. 2012; Nikolovski et al. 2012; Parsons et al. 2012a; Sparkes and Brandizzi 2012).

Chemical genomics has been used to modify the activity of proteins or pathways rapidly, reversibly, and conditionally, overcoming difficulties caused by gene lethality and redundancy, issues that too often disrupt experimental approaches that depend on mutations (Hicks and Raikhel 2012). This approach has provided insight into disease responses, hormone signaling, and cell wall metabolism, and is emerging as a powerful tool for unraveling redundant networks (Hicks and Raikhel 2012). An exhaustive confocal microscopy-based screen has been carried out recently that identified a library of compounds affecting endomembrane trafficking in vivo (Drakakaki et al. 2011). This screen discovered the aforementioned small molecule ES7, which can be used to study cell plate maturation (Drakakaki et al. 2011). These chemicals provide invaluable tools to dissect mechanisms underlying the trafficking and deposition of cell wall components, both to the cell plate and the apoplast.

Plant organelles such as the Golgi apparatus or TGN-specific vesicles can be isolated and analyzed in their natural state so that their constituent proteins can be identified (Parsons et al. 2012a; 2012b). In addition, immunoisolation can be used to separate vesicles having specific surface-exposed target proteins on their membranes. This approach was used to isolate vesicles displaying SYP61 (Drakakaki et al. 2012). The proteome of the isolated SYP61 vesicles was characterized, providing additional information about their cargo. Interestingly, components of the cellulose biosynthesis machinery (for example, CESA3 and CESA6) and other proteins involved in cell wall development were also identified in the SYP61 vesicle proteome, suggesting that SYP61 vesicles are involved in the trafficking of cell wall components (Drakakaki et al. 2012). Co-localization experiments validated the results with proteins including ECHIDNA (Gendre et al. 2011), in which mutants show perturbed cell elongation and cell wall deficiencies, overall emphasizing the role of SYP61 vesicles in the trafficking of cell wall biosynthetic machinery.

Taken together, small molecules can lead to the dissection of complex vesicle trafficking pathways, while vesicle isolation can highlight novel forms of cargo trafficking.

Other means of elucidating cell wall deposition include using antibodies to visualize specific epitopes of cell wall polysaccharides when they are in transit as well as after they have been assembled into the wall structure (Avci et al. 2012), or the micro analysis of polysaccharides in isolated organelles (Obel et al. 2009). Additionally, image-based screening of mutants using subcellular fluorescence markers can reveal the hidden subcellular trafficking machinery (Sparkes and Brandizzi 2012).

Future Perspectives

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

Extensive studies of plant endomembrane trafficking have been assisted by recent developments in microscopy and genetics. Important roles of several key players in post-Golgi trafficking, as well as the detailed structures and functions of subcellular compartments, have been demonstrated (reviewed by Park and Jurgens 2011). However, the trafficking mechanisms that regulate the deposition of cell wall polysaccharides and structural proteins, and their assembly into a functional cell wall, remain largely unknown.

Evidence accumulated from a number of studies has demonstrated the role of the TGN and specific vesicles, but many questions remain unanswered. Does the TGN contain one or many types of vesicles? How do vesicles compartmentalize, and what are their membrane and lipid compositions? For example, vesicles labeled by the GTPases RABA2 are localized at the TGN in interphase cells, and co-localize with TGN markers such as VHA-a1. However, during cytokinesis, RABA2 and RABA3 localize at the cell plate, marking a secretory compartment specific for cell plate formation (Chow et al. 2008), suggesting that the TGN includes a heterogeneous vesicle population, or at least a population whose functions shift with the cell cycle. In addition, do secretory vesicles carry CESAs as well as other cell wall-related proteins together with wall polysaccharides? Furthermore, how is the timing of polysaccharide deposition regulated during cell plate maturation, and how is it coordinated with cell wall assembly? In particular, how is cell wall assembly coordinated when some wall components are built in the Golgi, and others at the PM-apoplast interface?

Emerging technologies such as vesicle isolation and proteomics are beginning to unravel the identities of specific cargo and small molecules, and can help in the dissection of specific pathways. These approaches, in combination with polysaccharide tracking using cell biological, immunological and biochemical methods, can help fill the gaps in our knowledge of the trafficking of cell wall components.

(Co-Editor: Jianping Hu)

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Endomembrane Compartments and Cell Wall Biogenesis
  5. Trafficking Routes of Cell Wall Components
  6. Future Perspectives
  7. Acknowledgements
  8. References

We would like to thank Dr. John Labavitch for his critical reading of this manuscript. We apologize to our colleagues whose work we were not able to include in this review due to length limitations. This work was supported by UC Davis start up funds, and a Hellman fellowship to G.D. N.W. was supported by a Plant Sciences GSR and the CREATE-IGERT NSF DGE-0653984 grant.

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