Macromolecular lignin replication: A mechanistic working hypothesis

At the time of the first realization that the last step in lignin biosynthesis involves lignol radical coupling, it was difficult to envisage how such a process could be regiospecifically controlled. It was thus natural to expect that lignin macromolecules should have random primary structures. This has now been the prevailing assumption for almost fifty years, but of its correctness there has been no clear proof. Rather there have been occasional but insistent indications that lignins cannot just be products of random monolignol dehydropolymerization. Thus the present article seeks to apprehend the mechanistic implications of a situation where lignin primary structure would be determined by the sequence of interunit linkages along each biopolymer chain. The ramifications of a simple working hypothesis, that macromolecular lignin replication might occur directly through a template polymerization mechanism, are explored in detail. The manner in which the fidelity of the process could be maintained, through specific π-orbital interactions between the lignol radical precursors and characteristic substructures in the pre-existing lignin macromolecules, is explicitly described. The consequences of template polymerization are shown to be consistent with the absence of both optical activity and crystallinity in macromolecular lignin domains. It is proposed that the inherent primary structures of lignins are encoded in contiguous ‘dirigent’ arrays of lignol radical coupling sites distributed along individual polypeptide chains within lignifying plant cell walls. This revised version was published online in June 2006 with corrections to the Cover Date.