Genetic and molecular basis of grass cell-wall degradability. I. Lignin–cell wall matrix interactions
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Digestion
Plant cell
Plant lignocellulose constitutes an abundant and sustainable source of polysaccharides that can be converted into biofuels. However, the enzymatic digestion of native plant cell walls is inefficient, presenting a considerable barrier to cost-effective biofuel production. In addition to the insolubility of cellulose and hemicellulose, the tight association of lignin with these polysaccharides intensifies the problem of cell wall recalcitrance. To determine the extent to which lignin influences the enzymatic digestion of cellulose, specifically in secondary walls that contain the majority of cellulose and lignin in plants, we used a model system consisting of cultured xylem cells from Zinnia elegans. Rather than using purified cell wall substrates or plant tissue, we have applied this system to study cell wall degradation because it predominantly consists of homogeneous populations of single cells exhibiting large deposits of lignocellulose. We depleted lignin in these cells by treating with an oxidative chemical or by inhibiting lignin biosynthesis, and then examined the resulting cellulose digestibility and accessibility using a fluorescent cellulose-binding probe. Following cellulase digestion, we measured a significant decrease in relative cellulose content in lignin-depleted cells, whereas cells with intact lignin remained essentially unaltered. We also observed a significant increase in probe binding after lignin depletion, indicating that decreased lignin levels improve cellulose accessibility. These results indicate that lignin depletion considerably enhances the digestibility of cellulose in the cell wall by increasing the susceptibility of cellulose to enzymatic attack. Although other wall components are likely to contribute, our quantitative study exploits cultured Zinnia xylem cells to demonstrate the dominant influence of lignin on the enzymatic digestion of the cell wall. This system is simple enough for quantitative image analysis, but realistic enough to capture the natural complexity of lignocellulose in the plant cell wall. Consequently, these cells represent a suitable model for analyzing native lignocellulose degradation.
Hemicellulose
Secondary cell wall
Digestion
Enzymatic Hydrolysis
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Studies with normal, mutant, and transgenic plants have not clearly established whether the proportion of p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units in lignin directly affects the degradability of cell walls by hydrolytic enzymes. Dehydrogenation polymer−cell wall complexes containing varying ratios of H, G, and S lignins were formed by peroxidase/H2O2-mediated polymerization of p-coumaryl, coniferyl, and sinapyl alcohols into nonlignified walls isolated from cell suspensions of maize (Zea mays L). Lignification substantially reduced the degradability of cell walls by fungal hydrolases, but degradability was not affected by lignin composition. On the basis of these results, we propose that improvements in wall degradability, previously attributed to changes in lignin composition, were in fact due to other associated changes in wall chemistry or ultrastructure. Keywords: Gramineae; Zea mays; cell wall; brown midrib; transgenic; O-methyltransferase; hydroxycinnamyl alcohols; lignin; cellulase; degradability
Guaiacol
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Secondary cell wall
Primary (astronomy)
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Because of the complexity of plant cell wall biosynthesis, the mechanisms by which lignin restrict fiber degradation are poorly understood. Many aspects of grass cell wall lignification and degradation are successfully modeled by dehydrogenation polymer‐cell wall (DHP‐CW) complexes formed with primary walls of corn Zea mays L. This system was used to assess how variations in lignin composition, structure, and cross‐linking influence the hydrolysis of cell walls by fungal enzymes. Altering the normal guaiacyl, syringyl, and p ‐hydroxyphenyl makeup of lignin did not influence cell wall degradability; each unit of lignin depressed cell wall degradability by two units. Plants with perturbed lignin biosynthesis often incorporate unusual precursors into lignin and one of these, coniferaldehyde, increased lignin hydrophobicity and further depressed degradability by up to 30%. In other studies, lignin formed by gradual “bulk” or rapid “end‐wise” polymerization of monolignols had markedly different structures but similar effects on degradability. Reductions in cell wall cross‐linking, via oxidative coupling of feruloylated xylans to lignin or nucleophilic addition of cell wall sugars to lignin quinone‐methide intermediates, increased the initial hydrolysis of cell walls by up to 46% and the extent of hydrolysis by up to 28%. Overall, these studies suggest that reductions in lignin concentration, hydrophobicity, and cross‐linking will improve the enzymatic hydrolysis and utilization of structural polysaccharides for nutritional and industrial purposes. In ongoing work, we are developing a DHP‐CW system for dicots and are investigating how cross‐linking and various acylated and unusual monolignols influence the formation of lignin and the degradation of cell walls by rumen microflora.
Depolymerization
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Grass cell wall degradability is conventionally related to the lignin content and to the ferulic-mediated cross-linking of lignins to polysaccharides. To better understand the variations in degradability, 22 maize inbred lines were subjected to image analyses of Fasga- and Mäule-stained stem sections and to chemical analyses of lignins and p-hydroxycinnamic acids. For the first time, the nearness of biochemical and histological estimates of lignin levels was established. Combination of histological and biochemical traits could explain 89% of the variations for cell wall degradability and define a maize ideotype for cell wall degradability. In addition to a reduced lignin level, such an ideotype would contain lignins richer in syringyl than in guaiacyl units and preferentially localized in the cortical region rather than in the pith. Such enrichment in syringyl units would favor wall degradability in grasses, contrary to dicots, and could be related to the fact that grass syringyl units are noticeably p-coumaroylated. This might affect the interaction capabilities of lignins and polysaccharides. Keywords: Lignin; p-hydroxycinnamic acids; cell wall enzymatic degradability; histology; brown-midrib 3; maize
Pith
Hydroxycinnamic acid
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Digestion
Plant cell
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Hemicellulose
Secondary cell wall
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This chapter examines some of the observed empirical relationships of lignin concentration and composition with cell wall digestibility. It emphasizes information regarding molecular aspects of cell wall lignification and mechanisms by which these factors may limit bacterial fermentation and enzymatic hydrolysis of forages. For the purposes of this chapter, core lignin is considered to be the phenylpropanoid polymer deposited in the cell wall from polymerization of cinnamyl alcohols during secondary wall thickening. Composition of the core lignin polymer has been discussed as a factor which influences degradability of cell wall polysaccharides. Pyrolysis is a methodology that is currently seeing increased use for analysis of lignin structure in forages. Inferences regarding relationships of lignification to cell wall degradability drawn from data such as presented in the preceding section must be made cautiously because cell wall composition data result from analysis of total plant herbage.
Phenylpropanoid
Secondary cell wall
Middle lamella
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