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4.3 Degradation of Plant Cell Walls and Membranes by Microbial Enzymes

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4.3 Degradation of Plant Cell Walls and Membranes by Microbial Enzymes 4.3 Degradation of Plant Cell Walls and Membranes by Microbial Enzymes D.F. BATEMAN and H.G. BASHAM 1. Introduction One characteristic feature of many phytopathogenic organisms is their ability to produce an array of enzymes capable of degrading the complex polysaccharides of the plant cell wall (BATEMAN and MILLAR, 1966; WOOD, 1967; ALBERSHEIM et aI., 1969; WOOD, 1973) and membrane constituents (PORTER, 1966; TSENG and BATEMAN, 1968). These enzymes usually are produced inductively. Generally, they are extracellular, highly stable and present in infected host tissues. In most plant diseases caused by microbial agents, cell walls are penetrated, tissues are colonized, and permeability of host cells is altered. A brief summary of our understanding of cell wall and membrane structure, coupled with knowledge of the enzymes capable of degrading the components of these structures, and an analysis of the association of these enzymes with diseased tissue, should enable us to make an appraisal of their involvement in pathogenesis and point the way to an objective consideration of this area of disease physiology. 2. Structural Components 2.1 Cell Wall Composition and Structure The plant cell wall is that structure surrounding the protoplast exterior to the plasmalemma. This structure may be viewed as a two-phase system--- a dispersed phase of cellulose microfibrils and a complex continuous matrix. During develop­ ment cell walls undergo conspicious changes in structure, form and function, and they exhibit dynamic, rapid changes in their various constituents (NEVINS et aI., 1968; BERLYN, 1970; NORTHCOTE, 1972). Cell walls in young tissues are composed primarily of polysaccharides and a structural protein rich in hydroxyproline (LAM­ PORT, 1970). In older tissues, walls may also contain lignin. Traditionally, the cell wall has been divided into three functional-structural regions: middle lamella, primary wall and secondary wall. Middle lamella is that region where the walls of two cells join in a tissue system. The primary wall is the first wall region formed with definite organization, and the most dynamic of the wall regions. Secondary wall is that wall portion added after cell elongation is complete. Differences between wall regions relate to chemical composition and the degree of organization; transitions from region to region are not abrupt but intergrade gradually into one another (Fig. 1). R. Heitefuss et al. (eds.), Physiological Plant Pathology © Springer-Verlag Berlin · Heidelberg 1976 4.3 Degradation of Plant Cell Walls and Membranes by Microbial Enzymes 317 Microfibrils Continuous matrix Middle Primary Secondary Lumen lamella wall wall Hemicellulose Fig. I. Distribution in the plant cell wall of the major wall consti­ Protein tuents The wall polysaccharides have historically been grouped into the pectic substan­ ces, hemicelluloses, and cellulose (NORTHCOTE, 1963). This grouping is based upon solubilities of the polysaccharide constituents rather than upon their chemical compositions. The pectic substances are composed primarily of rhamnogalacturo­ nans, galactans and arabans (ASPINALL, 1970); they are extracted with cold and hot water and solutions of chelating agents. The hemicellulosic fraction includes xylans, xyloglucans, mannans and heteropolymers of glucose, galactose and man­ nose. These substances are extracted in alkaline solutions. Cellulose is the residual wall polysaccharide remaining after the above extractions. This empirical means of wall fractionation leads to the isolation of heterogeneous mixtures of wall polysaccharides and polysaccharide fragments. The pectic substances are the primary constituents of the middle lamella and are structural elements in the primary wall (MCCLENDON, 1964; TALMADGE et a!., 1973). The major component of the pectic fraction is a high molecular weight polymer consisting of a backbone of IX-I,4-linked D-galacturonopyranose intersper­ sed with 1,2-linked rhamnopyranose. The uronic acid carboxyls may be methylated and the uronide moieties may be acetylated at positions 2 and 3. The neutral sugar polymers, consisting of lX-l,3- and lX-l,5-linked L-arabinofuranose and linear polymers of f3-1,4-linked D-galactopyranose, may serve as a bridge between the rhamnogalacturonan and the hemicellulosic wall components (TALMADGE et a!., 1973). Hemicelluloses are major constituents of the primary and secondary wall re­ gions. Functionally they link the pectic and cellulosic fractions (BAUER et a!., 318 D.F. BATEMAN and H.G. BASHAM: 1973; NORTHCOTE, 1972). Xyloglucan, a chain of fJ-1,4-linked D-glucopyranose residues with terminal branches of 1X-1,6-linked xylopyranose, is a constituent of primary cell wall. This molecule is linked covalently to the pectic fraction and by hydrogen bonds to the surface of cellulose fibrils (BAUER et aI., 1973). The xylans, consisting of fJ-l,4-1inked xylopyranose chains, are widely distributed throughout higher plants. Xylans commonly have side branches of fJ-I,3-linked arabinofuranose and 1X-1,2-linked D-glucuronopyranose (or its 4-methyl ether). The numbers and kinds of branch residues are characteristic for different plant groups. Some xylans are acetylated at carbons 2 and 3 of the xylopyranose residues (ASPINALL, 1970). Other hemicellulosic polymers include glucomannan, a heteropolysaccharide of glucopyranose and mannopyranose linked fJ-I,4, and galactoglucomannan, a glucomannan with 1,6-linked galactopyranose side branches. The glucose to man­ nose ratios in these polymers vary depending upon the source, but ratios of 1 : 3 and 1: 2 are common in coniferous and deciduous woods, respectively (ASPINALL, 1970). The mannans and galactomannans are fJ-l,4-linked mannopyranose chains, with the latter having 1,6-linked galactopyranose side branches. Both of these polymers occur in higher plants, but they do not appear to be significant as structural cell ~all constituents. Cellulose is the most abundant substance found in the plant kingdom. It exists as elementary and microfibrils and constitutes the major structural component of cell walls. In primary wall, cellulose fibrils have a more or less random orienta­ tion, but in secondary wall they occur in parallel lamellae, the different layers being oriented in different directions (MUHLETHALER, 1967). Chemically, cellulose is made up of long chains of fJ-l,4-linked D-glucopyranose. The individual chains are flat, ribbon-like molecules stabilized by hydrogen bonds between adjacent glucose residues. The glucan chains are associated with each other in fibrils through interchain hydrogen bonds between hydroxyl groups at carbon 6 and the glycosidic oxygens of adjacent chains (NORTHCOTE, 1972). Cellulose fibrils contain both cry­ stalline and amorphous regions. There is some disagreement about the diameter of these fibrils and the arrangement of the crystalline and amorphous regions within them (FREY-WYSSLING, 1969; PRESTON, 1971). One view holds that fibrils contain a crystalline core surrounded by amorphous cellulose, another holds that amorphous regions are randomly distributed within fibrils. The diameters of cellu­ lose fibrils most often quoted range from 3.5-35 nm. The occurence and function of a structural protein in cell walls has been a controversial subject (LAMPORT, 1970). Most investigators now accept the cell wall as the location of a hydroxyproline-rich glycoprotein (KEEGSTRA et aI., 1973; NORTHCOTE, 1972). This structural protein may be deposited during maturation of the primary wall (SADAVA and CHRISPEELS, 1973; SADAVA et aI., 1973). The carbohydrate components of this protein are primarily galactose and arabinose. Arabinose is glycosidically linked to the hydroxyl of the hydroxyproline moiety, and galactose is believed to be covalently linked to serine (LAMPORT et aI., 1973). A recently proposed model of primary cell walls (Fig. 2) indicates that structural protein is covalently linked to the pectic substances through the arabinogalactan fraction (KEEGSTRA et aI., 1973). Another major cell wall constituent, characteristic of woody species, is lignin (FERGUS et aI., 1969). Deposition of lignin occurs after cell wall maturation. The 4.3 Degradation of Plant Cell Walls and Membranes by Microbial Enzymes 319 Cellulose fibril & ~ \ III III ~; ~ III III III Rhamnogalacturonan: -,..1---- .....1 L Xyloglucan : III III III I L. - Linked (Arabino) Galactan: ~ 3,6 -Linked (Arabino) Galactan: Fig. 2. Proposed model of primary plant cell wall. (KEEGSTRA et aI., 1973) monomeric subunits of lignin are the oxidation products of sinapyl, coniferyl, and p-hydroxycinnamyl alcohols which condense by free radical mechanisms to form an amorphous polymer. The major intermonomer bonds between the substi­ tuted monomers in lignin include arylglycerol-p-arylether bonds, phenylcoumaran structures, and biphenyl linkages, along with several other less prevalent linkages, all in a random 3-dimensional array (FREUDENBERG, 1968). Lignin may also be covalently linked to the other polymeric wall constituents (COWLING and BROWN, 1969). The polysaccharide constituents in cell walls are quite resistant to enzymatic decomposition after the walls become lignified, since they are complexed with and masked by the lignin component (DEHORITY et al., 1962). This highly cross­ linked polymer reinforces the strength of cell walls in woody tissues. 320 D.F. BATEMAN and H.G. BASHAM: 2.2 Concepts of Membrane Composition and Structure Membranes are a major structural element of all cells. They provide a semiperme­ able barrier between the cell and
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