Phosphoinositides and cell walls (Review)
Recent studies have suggested the involvement of phosphoinositides (PIs), a class of membrane lipids, as key regulatory molecules during secretion and assembly of cell wall polymers, and even recycling processes in plants. Krishnamoorthy et al. (pp. 1049–1057) review the current state of knowledge of how PIs regulate vesicle trafficking, and their potential influence on plant cell wall architecture. They consider first how PIs are formed in plants and then examine their role in the control of vesicle trafficking. Interactions between PIs and the actin cytoskeleton and small GTPases are also discussed. Future challenges for research are suggested.
Trafficking of the cellulose synthase complex (Review)
Cellulose synthase complexes (CSCs) are assembled in the Golgi apparatus but are thought to only synthesize cellulose when localized at the plasma membrane. Hence the delivery and endocytosis of CSCs to and from the membrane are important aspects for the regulation of cellulose biosynthesis. Bashline et al. (pp. 1059–1067) review recent findings related to CSC localization and behaviour, as well as recent advances in understanding associated trafficking pathways and mechanisms. Topics such as the implications of the Golgi and trans-Golgi network in CSC assembly and trafficking, and the possible mechanisms and pathways of CSC secretion, endocytosis and recycling are also considered.
Dynamic calcium recycling by an AGP-Ca2+ oscillator (Review)
Glycomodules of cell surface arabinogalactan proteins (AGPs) bind Ca2+ stoichiometrically at pH 5, and low pH dissociates the AGP-Ca2+ capacitor and hence is the primary source of cytosolic Ca2+ waves. Lamport et al. (pp. 1069–1085) thus consider that dynamic recycling of cytosolic Ca2+ by an AGP-Ca2+ oscillator determines the Ca2+ flux and may be a crucial component in the regulation of plant growth. The link between AGPs and Ca2+-signalling includes a wide range of auxin-dependent plant processes. This solves the problem of classical AGP function at the molecular level and accounts for the wide involvement of AGPs in plant morphogenesis, including tropic and nastic movements.
Supra-molecular assembly of AGP31 in arabidopsis cell walls
AGP31 (arabinogalactan protein 31) is a remarkable cell wall protein that displays a multi-domain organization unique in Arabidopsis thaliana. Hijazi et al. (pp. 1087–1097) demonstrate that its C-terminal PAC (PRP-AGP containing Cys) domain interacts in vitro with galactans and with its own central O-glycosylated (Hyp-O-Gal/Ara-rich motifs) domain. The interaction of AGP31 with galactans (which are branches of rhamnogalacturonans I) and with itself suggests that it forms non-covalent networks in cell walls. Thus a model is proposed of of interactions of AGP31 with different cell wall components, where AGP31 participates in complex supra-molecular scaffolds. Such scaffolds could contribute to the strengthening of cell walls of quickly growing organs such as etiolated hypocotyls.
MYB46/MYB83-mediated regulation of secondary wall biosynthesis (Review)
Formation of secondary cell walls requires co-ordinated transcriptional regulation of the genes involved in the biosynthesis of cellulose, hemicellulose and lignin, and the transcription factor MYB46 (At5g12870) and its paralog MYB83 (At3g08500) have been shown to function as a master switch for the secondary wall biosynthetic program in Arabidopsis thaliana. Ko et al. (pp. 1099–1107) review our current understanding of the MYB46-mediated transcriptional regulatory network, including upstream regulators, downstream targets and negative regulators of MYB46. They conclude that because of its ability to directly regulate the biosynthesis genes for the major components, MYB46 may be useful in pathway-specific manipulation of secondary wall biosynthesis.
Cell-specific transcription and translation in root cells
A long-standing question in cellular biology is how well the transcriptome is coupled to the proteome. Rajasundaram et al. (pp. 1109–1123) assess the degree of co-ordination and divergence between these two levels of cellular organization by using cell-type specific datasets of the root transcriptome and translatome in Arabidopsis thaliana, with particular reference to cell wall biology. In agreement with previous studies in animal cells, they find that the majority of genes exhibit uncorrelated transcription and translation levels. However, components and processes are also identified that are under co-ordinated transcriptional and translational control in plant root cells, such as the development of secondary cell wall biosynthesis.
Synergism between FLA4 and ABA signalling in roots
The physiological function of fasciclin-like arabinogalactan proteins (FLAs) is largely unknown. Seifert et al. (pp. 1125–1133) study the salt-oversensitive mutant fla4 and show that externally applied abscisic acid (ABA) as well as loss of function of negative ABA regulators suppresses the fla4 phenotype. They find that fla4 shows a reduced level of ABA responsive transcripts. Synergism between ABA and FLA4 is further supported by suppression of the fla4 phenotype by chemical inhibition of ABA catabolism. The cell membrane-localized FLA4 might indirectly influence the sensitivity of cytosolic ABA signalling and thereby link cell wall biosynthesis with the stress response.
Mixed-linkage glucan and glucuronoarabinoxylan in roots
Plant cell enlargement is unambiguously coupled to changes in cell wall architecture. Kozlova et al. (pp. 1135–1145) study the correspondence between the fine structure of cell walls and the course of the elongation process in roots of maize (Zea mays) and determine the presence of three domains of glucuronoarabinoxylan molecules: one separating cellulose microfibrils, one interacting with them, and a middle domain between the two. The middle domain is masked by mixed-linkage glucan. A model is proposed in which the mixed-linkage glucan serves as a gel-like filler of the space between the separating domain of the glucuronoarabinoxylan and the cellulose microfibrils. Space for glucan is provided along the middle domain, the proportion of which increases during cell elongation.
SNARE protein VTI13 and root hair growth in arabidopsis
Endosomal trafficking is required for polarized growth, but many of the proteins that control this process have yet to be identified. Larson et al. (pp. 1147–1159) identify VTI13 as a vesicular soluble NSF attachment receptor (SNARE) protein required for root hair growth in Arabidopsis thaliana. They demonstrate that VTI13 localizes to the vacuole membrane and the trans-Golgi network (TGN) or an early endosomal compartment, is important for TGN integrity, and is likely to play a role in the transport of cargo to the large vacuole in root hairs. They also show that VTI13 function is essential for the maintenance of cell wall organization in root hair and root epidermal cells.
PME and SBT expression in arabidopsis
In Arabidopsis thaliana, the degree of methylesterification of homogalacturonans, the main pectic constituent of the cell wall, can be modified by pectin methylesterases (PMEs) and this plays a central role in both plant development and responses to stress. Using a combination of functional genomics, biochemistry and proteomic approaches, Sénéchal et al. (pp. 1161–1175) identify a group-2 PME (PME17) that is strongly co-expressed, both spatially and temporally, with a specific subtilisin-type serine protease (SBT3.5), particularly in the roots. PME activity is modified in roots of knock-out mutants for both proteins, with consequent effects on growth. This suggests a role for SBT3.5 in the processing of PME17 in planta, and highlights a need for identifying specific PME–SBT pairs.
Rhamnogalacturonan-II in pollen tube growth (Research in Context)
Rhamnogalacturonan type-II (RG-II) is the most complex pectic polysaccharide of the plant cell wall and is necessary for strengthening. Dumont et al. (pp. 1177–1188) study pollen tubes of Arabidopsis thaliana and show the presence of specific sugars of RG-II. In addition, they analyse two T-DNA insertion lines in At3g48820 encoding a putative sialyltransferase-like protein, possibly involved in the transfer on the homogalacturonan backbone of Kdo and/or Dha, two specific sugars of RG-II. Analyses of the two heterozygous lines reveals a strong reduction in pollen germination and pollen tube growth in vitro and in vivo, suggesting that sialyltransferase-like proteins are required for proper pollen tube growth by maintaining the integrity of RG-II.
Tapetum and pollen wall ultrastructure in arabidopsis
Preserving the ultrastructure of the developing pollen cell wall presents challenges because the key cell types are embedded deep within the anther, making chemical fixation for electron microscopy difficult. Quilichini et al. (pp. 1189–1201) use a high-pressure freezing/freeze-substitution technique in order to preserve the delicate tapetum tissue and developing pollen grains during production of the complex pollen cell wall in the anther of wildtype Arabidopsis thaliana. The technique reveals the ultrastructure of tapetosomes and elaioplasts, and shows that the tapetum and middle layer of the anther remain intact into the tricellular pollen and late-uninucleate microspore stages, respectively.
Cell-wall structure and evolution in brown algae
Brown algae (Phaeophyceae) are marine organisms that are evolutionary distant from land plants and with a distinctive cell wall, the detailed organization of which is unclear. Deniaud-Bouët et al. (pp. 1203–1216) use a systematic approach to study polymer interlinks in five species of the order Fucales, and find that alginates are mostly associated with phenolic compounds while sulfated fucans are tightly associated with proteins and cellulose. They suggest that these two networks sustain distinct roles in the regulation of wall rigidity and osmotic stress responses, respectively. The emergence of this cell wall structure may have been instrumental in the acquisition of multicellularity in brown algae.
Cell wall biosynthesis in charophyte green algae (Research in Context)
Charophyte green algae (CGA) are the closest living relatives to land plants, and the cell wall was possibly a defining structure that enabled the green algal ancestor to colonize land. Mikkelsen et al. (pp. 1217–1236) provide genetic evidence that many of the most important core cell wall polysaccharides have their evolutionary origins in CGA, including cellulose, mannan, xyloglucan, xylan and pectin, as well as arabinonogalactan proteins (AGPs). Moreover, they provide the first evidence that all cellulose synthase-like genes present in early-divergent land plants were already present in CGA, implying that some features of land plant cell walls evolved prior to the transition to land, rather than having evolved as a result of selection pressures inherent in this transition.
Cortical cytoskeleton and wall dynamics in a green alga
The site of cell division in plant cells is often marked or ‘predicted’ by a cortical band of microtubules called the pre-prophase band (PPB). Ochs et al. (pp. 1237–1249) study cell expansion in the unicellular charophyte green alga, Penium margaritaceum, and find a cortical cytoskeletal band of microtubules and actin filaments at the cell isthmus. Like a pre-prophase band, this marks the future site of cell division and also serves as the focal point of cell wall deposition during ‘bi-directional’ cell expansion. The study demonstrates that a cortical cytoskeletal aggregate like the PPB appears in early divergent green plants such as charophytes.
Seed coat polysaccharide production (Review)
During seed coat differentiation the epidermal cells of certain species accumulate polysaccharides either to reinforce cell walls, or for release during seed imbibition to form sticky mucilage. North et al. (pp. 1251–1263) review the recent exploitation of these cells as a model system for the study of polysaccharide metabolism and properties, particularly in the model plant Arabidopsis thaliana. The potential for intra- and interspecies natural variation in these polysaccharides as a resource to extend the use of this model and to improve our knowledge of seed mucilage ecophysiological function is examined.
Variation of cell wall properties in Miscanthus
Miscanthus represents one of the most promising dedicated lignocellulosic bioenergy crops. A key trait for biomass conversion to biofuels and biomaterials is cell wall quality. Costa et al. (pp. 1265–1277) present data on cell wall compositional changes as a function of development and tissue type across 25 selected Miscanthus genotypes. They report compositional differences between stem and leaf samples to be predominantly associated with structural carbohydrates, while lignin content does not correlate with ethanol production from leaf biomass. Overall, leaf tissue contributes significantly to total above-ground biomass at all developmental stages. These factors highlight the importance of examining leaf and stem biomass composition separately in order to infer gene–trait associations relating to cell wall quality of lignocellulosic biomass.
Cell wall profiling of wine and table grapes
Table grapes are bred for crunchy texture and physical appearance, whereas wine grapes have been selected for small size and concentrated flavour and aroma. Moore et al. (pp. 1279–1294) apply cell wall profiling tools to characterize a table grape cultivar, ‘Crimson Seedless’, versus a wine grape, ‘Cabernet Sauvignon’, with respect to changes at three ripening stages: green berry touch stage, véraison and full-ripe berries. They identify pectic-β-(1,4)-galactans, extensins and arabinogalactan-proteins as polymers that differentiate the different phenological stages. Whilst the general pattern of changes is highly conserved in both cultivars, elevated levels of pectin epitopes are detected in the ‘Crimson Seedless’ samples. They conclude that genetic developmental programming has a strong influence on the cell wall changes occurring in ripening Vitis vinifera grape berries.
Fern cell wall composition and functional specialization
Fern gametophytes and sporophytes are free-living and show many morphological and physiological differences. Eeckhout et al. (pp. 1295–1307) combine glycan microarray analysis with in situ immunolabelling in order to compare the presence and distribution of glycan epitopes between both generations in the fern model system Ceratopteris richardii ‘C-Fern’. They find pectic homogalacturonan, mannan and xyloglucan present in gametophytic and sporophytic tissues, while xylans and pectic galactans are only detected in the sporophyte. Rhizoids and root hairs show a similar arabinogalactan protein and xyloglucan epitope distribution. The results indicate that cell wall composition largely reflects functional specialization rather than genetic origin.
Xyloglucan endotransglucosylase/hydrolases in rice
Although xyloglucans are ubiquitous in land plants, they are less abundant in Poales than in eudicotyledons. However, the xyloglucan endotransglucosylase/hydrolase (XTH) gene family in rice (Oryza sativa) is comparable in size to that of the eudicotyledon Arabidopsis thaliana. Hara et al. (pp. 1309–1318) study the function of three representative rice XTHs and find all have xyloglucan endohydrolase (XEH) activity and one has both XEH and xyloglucan endotransglycosylase activities. Phenotypic analysis of transgenic lines with altered expression of a rice XTH suggests that XTHs play redundant roles in rice growth.
Influence of extraction conditions on citrus pectins
Pectin is used as a gelling, thickening and emulsifying agent in a wide range of applications, and current industrial extraction processes are based on fruit peel, a waste product from the juicing industry. Kaya et al. (pp. 1319–1326) examine how pectin components vary in relation to the plant source (orange, lemon, lime, grapefruit) and consider the influence of extraction conditions on the chemical and macromolecular characteristics of pectin samples. They find that structural, and hence macromolecular, variations within the different citrus pectin samples are mainly related to their rhamnogalacturonan I contents and integrity, and, to a lesser extent, to the length of their homogalacturonan domains.
Structural variation of RGII in wine (Research in Context)
Rhamnogalacturonan II (RGII) is a structurally complex pectic sub-domain composed of more than 12 different sugars and 20 different linkages distributed in five side chains along a homogalacturonan backbone. Buffetto et al. (pp. 1327–1337) study RGII from wine (Vitis vinifera, ‘Merlot’) and determine several modifications to its structure. Some of these, such as dearabinosylation and deacetylation, are shown to be the consequence of acid treatment, whilst others, such as methyl-esterification, methyl-etherification and oxidation, reflect natural diversity. A range of RGII structures exhibiting specific physico-chemical properties are thus shown to co-exist in wine.
Receptor-like kinases and maintenance of cell wall integrity (Review)
Plant cell walls are exposed to a wide range of stress stimuli that have to be detected by a suitable receptor in order to induce specific reactions appropriate to the organ affected and the developmental state of the plant. Engelsdorf and Hamann (pp. 1339–1347) review recent developments in our knowledge on plant cell wall integrity maintenance with a specific focus on possible signal elicitors and receptors. Recent evidence implicates receptor-like kinases (RLKs) in the regulatory networks associated with plant cell wall-related stress, and hence potential functions of RLKs in cell wall integrity maintenance are discussed.
Regulation of stress-induced callose biosynthesis (Viewpoint)
Deposition of callose, a (1,3)-β-glucan cell wall polymer, is involved in several fundamental biological process, but despite its importance detailed knowledge about the regulation of its biosynthesis in plants is rather limited. Ellinger and Voigt (pp. 1349–1358) summarize data from 10 years of research, focussing on callose deposition in response to pathogen attack in the model plant Arabidopsis thaliana. They consider that growing evidence has been found that the timing of callose deposition in the multilayered system of plant defence responses could be the key parameter for optimal effectiveness. This timing seems to be achieved through co-ordinated transport and formation of the callose synthase complex.
Arabinogalactan proteins in parasitic plant haustoria
The hyaline body, a central parenchymatous tissue found in the haustoria of some parasitic plants, is hypothesized to process nutrients abstracted from the host. Pielach et al. (pp. 1359–1373) carry out the first cell wall-focussed immunocytochemical study of hyaline bodies using three hemiparasites of semi-natural grasslands: Rhinanthus minor, Odontites vernus and Melampyrum pratense. Their results show extensive paramural and intercellular modifications and the presence of large intercellular globules suggestive of storage functions. All of these structures are extremely rich in arabinogalactan proteins (AGPs), a class of hyperglycosylated proteins, which may participate in nutrient transfer and metabolism in the hyaline bodies.
Nano-structural changes in pectins during fruit softening (Review)
Textural changes during fruit ripening are mainly due to the dissolution of the middle lamella, and pectins, a major component of fruit cell walls, are extensively modified during this process. Paniagua et al. (pp. 1375–1383) discuss the main features of pectin disassembly during fruit ripening and review the nano-structural characterization of pectins and its relationship with texture and postharvest fruit shelf life, as determined by atomic force microscopy (AFM). Most AFM studies show a reduction in the length of individual pectin chains and in the frequency of aggregates during ripening. Pectins covalently bound to the cell wall appear to be the most affected. They conclude that AFM studies can provide valuable insights into the relationships between pectins and fruit ripening.
A surface-spread AGP with a lysine-rich subdomain
Certain membrane-associated arabinogalactan-proteins (AGPs) with lysine-rich subdomains participate in plant growth, development and resistance to stress. Zhou et al. (pp. 1385–1397) observe one such AGP labelled with EGFP (LeAGP1-EGFP) in a living leaf cell of Arabidopsis thaliana using confocal microscopy and on inert chips using atomic force microscopy. They find that in the selected cell type it can form aligned perimembrane bands, and viewed at high resolution on the artificial substrates it can form arcs, rings, clusters and lacy sheets. It can form composite rings of larger size when the AGP-specific Yariv reagent is added. The nano-behavior of LeAGP1-EGFP on artificial substrates should be useful, in combination with other biophysical data, in developing ideas about the assembly of this regulatory glycoprotein at the surface of the cell membrane.