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"Albersheim, Peter"
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RHAMNOGALACTURONAN II: Structure and Function of a Borate Cross-Linked Cell Wall Pectic Polysaccharide
Rhamnogalacturonan II (RG-II) is a structurally complex pectic polysaccharide that was first identified in 1978 as a quantitatively minor component of suspension-cultured sycamore cell walls. Subsequent studies have shown that RG-II is present in the primary walls of angiosperms, gymnosperms, lycophytes, and pteridophytes and that its glycosyl sequence is conserved in all vascular plants examined to date. This is remarkable because RG-II is composed of at least 12 different glycosyl residues linked together by more than 20 different glycosidic linkages. However, only a few of the genes and proteins required for RG-II biosynthesis have been identified. The demonstration that RG-II exists in primary walls as a dimer that is covalently cross-linked by a borate diester was a major advance in our understanding of the structure and function of this pectic polysaccharide. Dimer formation results in the cross-linking of the two homogalacturonan chains upon which the RG-II molecules are constructed and is required for the formation of a three-dimensional pectic network in muro. This network contributes to the mechanical properties of the primary wall and is required for normal plant growth and development. Indeed, changes in wall properties that result from decreased borate cross-linking of pectin may lead to many of the symptoms associated with boron deficiency in plants. [PUBLICATION ABSTRACT]
Journal Article
Occurrence of the Primary Cell Wall Polysaccharide Rhamnogalacturonan II in Pteridophytes, Lycophytes, and Bryophytes. Implications for the Evolution of Vascular Plants
Borate ester cross-linking of the cell wall pectic polysaccharide rhamnogalacturonan II (RG-II) is required for the growth and development of angiosperms and gymnosperms. Here, we report that the amounts of borate cross-linked RG-II present in the sporophyte primary walls of members of the most primitive extant vascular plant groups (Lycopsida, Filicopsida, Equisetopsida, and Psilopsida) are comparable with the amounts of RG-II in the primary walls of angiosperms. By contrast, the gametophyte generation of members of the avascular bryophytes (Bryopsida, Hepaticopsida, and Anthocerotopsida) have primary walls that contain small amounts (approximately 1% of the amounts of RG-II present in angiosperm walls) of an RG-II-like polysaccharide. The glycosyl sequence of RG-II is conserved in vascular plants, but these RG-IIs are not identical because the non-reducing L-rhamnosyl residue present on the aceric acid-containing side chain of RG-II of all previously studied plants is replaced by a 3-O-methyl rhamnosyl residue in the RG-IIs isolated from Lycopodium tristachyum, Ceratopteris thalictroides, Platycerium bifurcatum, and Psilotum nudum. Our data indicate that the amount of RG-II incorporated into the walls of plants increased during the evolution of vascular plants from their bryophyte-like ancestors. Thus, the acquisition of a boron-dependent growth habit may be correlated with the ability of vascular plants to maintain upright growth and to form lignified secondary walls. The conserved structures of pteridophyte, lycophyte, and angiosperm RG-IIs suggests that the genes and proteins responsible for the biosynthesis of this polysaccharide appeared early in land plant evolution and that RG-II has a fundamental role in wall structure.
Journal Article
Detection of Expansin Proteins and Activity during Tomato Fruit Ontogeny
Expansins are plant proteins that have the capacity to induce extension in isolated cell walls and are thought to mediate pH-dependent cell expansion. J. K. C. Rose, H. H. Lee, and A. B. Bennett ([1997] Proc Natl Acad Sci USA 94: 5955-5960) reported the identification of an expansin gene (LeExp1) that is specifically expressed in ripening tomato (Lycopersicon esculentum) fruit where cell wall disassembly, but not cell expansion, is prominent. Expansin expression during fruit ontogeny was examined using antibodies raised to recombinant LeExp1 or a cell elongation-related expansin from cucumber (CsExp1). The LeExp1 antiserum detected expansins in extracts from ripe, but not preripe tomato fruit, in agreement with the pattern of LeExp1 mRNA accumulation. In contrast, antibodies to CsExp1 cross-reacted with expansins in early fruit development and the onset of ripening, but not at a later ripening stage. These data suggest that ripening-related and expansion-related expansin proteins have distinct antigenic epitopes despite overall high sequence identity. Expansin proteins were detected in a range of fruit species and showed considerable variation in abundance; however, appreciable levels of expansin were not present in fruit of the rin or Nr tomato mutants that exhibit delayed and reduced softening. LeExp1 protein accumulation was ethylene-regulated and matched the previously described expression of mRNA, suggesting that expression is not regulated at the level of translation. We report the first detection of expansin activity in several stages of fruit development and while characteristic creep activity was detected in young and developing tomato fruit and in ripe pear, avocado, and pepper, creep activity in ripe tomato showed qualitative differences, suggesting both hydrolytic and expansin activities.
Journal Article
Requirement of Borate Cross-Linking of Cell Wall Rhamnogalacturonan II for Arabidopsis Growth
Turgor-driven plant cell growth depends on wall structure. Two allelic L-fucose-deficient Arabidopsis thaliana mutants (mur1-1 and 1-2) are dwarfed and their rosette leaves do not grow normally. mur1 leaf cell walls contain normal amounts of the cell wall pectic polysaccharide rhamnogalacturonan II (RG-II), but only half exists as a borate cross-linked dimer. The altered structure of mur1 RG-II reduces the rate of formation and stability of this cross-link. Exogenous aqueous borate rescues the defect. The reduced cross-linking of RG-II in dwarf mur1 plants indicates that plant growth depends on wall pectic polysaccharide organization.
Journal Article
Molecular Cloning and Characterization of Glucanase Inhibitor Proteins: Coevolution of a Counterdefense Mechanism by Plant Pathogens
A characteristic plant response to microbial attack is the production of endo-β-1,3-glucanases, which are thought to play an important role in plant defense, either directly, through the degradation of β-1,3/1,6-glucans in the pathogen cell wall, or indirectly, by releasing oligosaccharide elicitors that induce additional plant defenses. We report the sequencing and characterization of a class of proteins, termed glucanase inhibitor proteins (GIPs), that are secreted by the oomycete Phytophthora sojae, a pathogen of soybean, and that specifically inhibit the endoglucanase activity of their plant host. GIPs are homologous with the trypsin class of Ser proteases but are proteolytically nonfunctional because one or more residues of the essential catalytic triad is absent. However, specific structural features are conserved that are characteristic of protein-protein interactions, suggesting a mechanism of action that has not been described previously in plant pathogen studies. We also report the identification of two soybean endoglucanases: EGaseA, which acts as a high-affinity ligand for GIP1; and EGaseB, with which GIP1 does not show any association. In vitro, GIP1 inhibits the EGaseA-mediated release of elicitor-active glucan oligosaccharides from P. sojae cell walls. Furthermore, GIPs and soybean endoglucanases interact in vivo during pathogenesis in soybean roots. GIPs represent a novel counterdefensive weapon used by plant pathogens to suppress a plant defense response and potentially function as important pathogenicity determinants.
Journal Article
Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves
The cell-wall polysaccharides of Arabidopsis thaliana leaves have been isolated, purified, and characterized. The primary cell walls of all higher plants that have been studied contain cellulose, the three pectic polysaccharides homogalacturonan, rhamnogalacturonan I, and rhamnogalacturonan II, the two hemicelluloses xyloglucan and glucuronoarabinoxylan, and structural glycoproteins. The cell walls of Arabidopsis leaves contain each of these components and no others that we could detect, and these cell walls are remarkable in that they are particularly rich in phosphate buffer-soluble polysaccharides (34% of the wall). The pectic polysaccharides of the purified cell walls consist of rhamnogalacturonan I (11%), rhamnogalacturonan II (8%), and homogalacturonan (23%). Xyloglucan (XG) accounts for 20% of the wall, and the oligosaccharide fragments generated from XG by endoglucanase consist of the typical subunits of other higher plant XGs. Glucuronoarabinoxylan (4%), cellulose (14%), and protein (14%) account for the remainder of the wall. Except for the phosphate buffer-soluble pectic polysaccharides, the polysaccharides of Arabidopsis leaf cell walls occur in proportions similar to those of other plants. The structures of the Arabidopsis cell-wall polysaccharides are typical of those of many other plants
Journal Article
Inhibition of 2,4-dichlorophenoxyacetic acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide
Xyloglucan, isolated from the soluble extracellular polysaccharides of suspension-cultured sycamore (Acer pseudoplatanus) cells, was digested with an endo-β-1,4-glucanase purified from the culture fluid of Trichoderma viride. A nonasaccharide-rich Bio-Gel P-2 fraction of this digest inhibited 2,4-dichlorophenoxyacetic-acid-stimulated elongation of etiolated pea stem segments. The inhibitory activity of this oligosaccharide fraction exhibited a well-defined concentration optimum between 10-2 and 10-1 micrograms per milliliter. Another fraction of the same xyloglucan digest, rich in a structurally related heptasaccharide, did not, at similar concentrations, significantly inhibit the elongation.
Journal Article
Developmental and tissue-specific structural alterations of the cell-wall polysaccharides of Arabidopsis thaliana roots
The plant cell wall is a dynamic structure that plays important roles in growth and development and in the interactions of plants with their environment and other organisms. We have used monoclonal antibodies that recognize different carbohydrate epitopes present in plant cell-wall polysaccharides to locate these epitopes in roots of developing Arabidopsis thaliana seedlings. An epitope in the pectic polysaccharide rhamnogalacturonan I is observed in the walls of epidermal and cortical cells in mature parts of the root. This epitope is inserted into the walls in a developmentally regulated manner. Initially, the epitope is observed in atrichoblasts and later appears in trichoblasts and simultaneously in cortical cells. A terminal alpha-fucosyl-containing epitope is present in almost all of the cell walls in the root. An arabinosylated (1 leads to 6)-beta-galactan epitope is also found in all of the cell walls of the root with the exception of lateral root-cap cell walls. It is striking that these three polysaccharide epitopes are not uniformly distributed (or accessible) within the walls of a given cell, nor are these epitopes distributed equally across the two walls laid down by adjacent cells. Our results further suggest that the biosynthesis and differentiation of primary cell walls in plants are precisely regulated in a temporal, spatial, and developmental manner.
Journal Article
Changes in the structure of xyloglucan during cell elongation
Xyloglucans were isolated by sequential extraction of the cell walls of pea (Pisum sativum L. cv. Alaska) with a xyloglucan-specific endoglucanase and KOH. The xyloglucan content and xyloglucan-oligosaccharide composition were determined for fractions obtained from the elongating and non-elongating segments of pea stems grown in the light and in darkness. The results were consistent with the hypothesis that regulated growth of the cell wall depends on xyloglucan metabolism. Furthermore, the characterization of xyloglucan extracted from leaves of light-grown pea plants indicates that xyloglucan metabolism is tissue specific. Changes in xyloglucan subunit structure observed in elongating stems are consistent with the in muro realization of a metabolic pathway that was previously proposed solely on the basis of the in vitro activities of plant glycosyl hydrolases.
Journal Article