Efficiency and lignin biosynthesis: a quantitative analysis.
14/01/2018 · Amthor JS (2003) Efficiency of lignin biosynthesis: A quantitative analysis
AmthorEfficiency of lignin biosynthesis: a quantitative analysis.
Because the actual pathways used during lignin biosynthesis (among the alternative pathways considered in this analysis) are unknown, it is currently impossible to estimate the scope for improvement in the efficiency of lignin biosynthesis by changing actual pathways to more efficient pathways included in Figs –4. One exception is lignin biosynthesis via the tyrosine pathway, which is presumably limited to monocots, compared with the phenylalanine pathway (Fig. ). If use of the tyrosine pathway for lignin biosynthesis was introduced into non‐monocots, assuming that this was accomplished without detriment to the plant (e.g. through phenylalanine deficiency), lignin biosynthesis might be more efficient.
Because lignin is synthesized from monolignols rather than glucosides, alcohols must be regenerated from any monolignol glucosides formed. If required, that regeneration was assumed to occur in the apoplast by action of coniferin β‐glucosidase (EC 188.8.131.52) (e.g. ), releasing glucose (Fig. ). The same, or a similar, enzyme may regenerate both p‐coumaryl alcohol and sinapyl alcohol from their respective glucosides (if any). Transport of glucose (or one of its products) from apoplast to cytosol was assumed to occur without metabolic cost in this analysis. For example, it might be coupled to monolignol or glucoside transport to the apoplast in an antiporter. Alternatively, the hydrolysis reaction might occur in the cytosol rather than the apoplast, which would eliminate the need for glucose transport back into cytosol. If, however, glucose transport from apoplast to cytosol associated with the Fig. reaction set occurs, and is an energy‐requiring process, additional ATP (or PPi) would be required for lignin biosynthesis.
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The precise mechanism(s) of monolignol polymerization is unclear. A general notion is that monolignols are converted into free radicals that then polymerize spontaneously. During polymerization, the three monolignols may be converted to (approximately) hydroxyphenyl residues, guaiacyl residues and syringyl residues, respectively (see Table for residue characteristics). Though most evidence is circumstantial rather than direct and unequivocal, the two enzymes most often considered as catalysing the formation of the monolignol radicals are laccase(s) (EC 184.108.40.206) and peroxidase(s) (EC 1.11.1.‐) (e.g. ; ; ; ; ; ; ; ). During polymerization, the radical structure of monolignols may be retained after the linkage of an alcohol residue to a lignin polymer, causing a chain reaction or propagation of radicals (; ). In this analysis, it was assumed that 1 H atom is removed from each monolignol during polymerization, which defines the stoichiometries associated with laccase and peroxidase activities, both of which produce H2O (Fig. ). Laccase activity is more efficient than peroxidase activity because peroxidase activity requires NADH (Fig. ).
The transport of monolignol glucosides from vacuoles to the apoplast (as in gymnosperms) may be an active process and, without knowledge to the contrary, the cost of such transport was set by conjecture in this analysis to 1 ATP (forming 1 ADP and 1 Pi at the plasmalemma) per glucoside transported. For the direct transfer of monolignols to the apoplast following their biosynthesis (i.e. without glycosylation or transport into a vacuole, as in angiosperms?), the same active‐transport cost of 1 ATP per monolignol might occur. It is also possible, however, that both free monolignols and glucosides diffuse freely (i.e. without cost) down a concentration gradient from the cytosol through channels in the plasmalemma to the site of lignin polymerization within cell walls (Fig. ).
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Futile cycles of ATP production and use (e.g. ) would reduce the ‘effective’ YATP,sucrose. Whether futile cycle activity is associated with lignin biosynthesis is unknown, and is not considered in this analysis.
The monolignols p‐coumaryl alcohol, coniferyl alcohol and sinapyl alcohol are formed in the cytosol, but lignin biosynthesis occurs in the apoplast. Moreover, monolignols are unstable and toxic. In angiosperms, monolignols may be transferred to the apoplast immediately after being formed, where they participate in lignin formation. In gymnosperms, however, monolignols may be stored in stable forms, perhaps in vacuoles, before being transported to the apoplast (). In this analysis, it was assumed that any transport of stable forms of monolignols into a vacuole required energy.
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Lignin is derived mainly from three alcohol monomers: p‐coumaryl alcohol, coniferyl alcohol and sinapyl alcohol
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In contrast to the general agreement between the end result of the present analysis and the results of ), glucose requirements for lignin biosynthesis derived from the present study were considerably larger than values given by ), even after comparing results on the basis of identical monolignol residues (Table ). ) assumed that monolignol polymerization produced NADH (one per monomer residue), whereas the present analysis assumed that in the most efficient case polymerization neither produced nor consumed NADH. In less efficient, but physiologically possible and perhaps probable cases, the present analysis implied that polymerization requires input of NADH and/or ATP, which increases the overall cost of lignin biosynthesis compared with the calculations of ). The inclusion of tool maintenance costs in this analysis accounted for only a small part of the difference between the present estimates and those of ). The large differences between results of the present analysis and those of ) that occurred for guaiacyl‐ and syringyl‐based lignins (Table ) were due, in the most part, to what may have been overly efficient methoxylation reactions assumed by ). In particular, glucose requirements for lignin biosynthesis (mass per mass) declined as the number of carbon atoms per lignin residue increased in the ) analysis because they assumed that methoxylation resulted in a net production of reductant, with no ATP requirement, and the net gain in monolignol mass was greater than the increase in glucose requirement as monolignol size increased. In the present analysis, SAM regeneration required significant ATP input [eqns (S.25)–(S.28)], and the substrate requirements (their mass) for methoxylation exceeded the mass increase in monolignols resulting from methoxylation.
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According to the present analysis, when the most costly (i.e. least efficient) pathways thought to be active in plants were used, glucose requirements for lignin biosynthesis were significantly larger than glucose requirements estimated in all previously published studies (Table ). The difference between present results based on most costly pathways and previous analyses may be important because the most costly pathways included in the present analysis were derived from reaction sets that are thought to occur in plants. The most costly reaction sets considered in the present analysis might therefore be as close, or closer, to actual (as opposed to minimum potential) costs of lignin biosynthesis in plants as the most efficient reaction sets considered.
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According to the present analysis, glucose requirements for lignin biosynthesis (based on an equivalency of 2 glucose per sucrose) using the most efficient pathways thought to be associated with lignin biosynthesis were similar to glucose requirements estimated by ) (Table ). This was the case in spite of a number of improvements in the present analysis, including lower values of YATP,sucrose (or the ‘equivalent’ yield of ATP from glucose oxidation) and the use of GS/GOGAT instead of GDH to regenerate glutamate from 2‐oxoglutarate and NH3. Costs of tool maintenance (though speculative) and polymerization were included in the present analysis, but were apparently excluded from the analysis of ). The present analysis also explicitly compared substrate requirements for lignin biosynthesis via phenylalanine with tyrosine, whereas ) stated that ‘values for alternate pathways were averaged’, but did not specify whether both pathways were considered for lignin biosynthesis, or whether only the phenylalanine pathway was used.
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