Diversification of Lignin Supramolecular Structure during the Evolution of Plants

Abstract

The 3D macromolecular structure (supramolecular structure, SMS) of lignin in different morphological regions of the cell wall is widely diverse in many respects: (1) type and frequency of monomer (p-hydroxyphenyl (H)-, guaiacyl(G)- and syringyl (S)-propane) units, (2) type and frequency of interunit bonds, (3) shape, size, and (4) linkages between lignin and polysaccharides. This diversity is found also in different kinds of cells of different plant species. The causes of the complicated heterogeneity of lignin SMS can be understood reasonably well from the viewpoints of evolutionary biology and polymer chemistry: “ontogenesis recapitulates phylogenesis”, and growing of lignin SMS is controlled by the supply of monolignols and polymerization conditions provided by previously deposited polysaccharides. The first land plants emerged with lignified vascular tissue having excellent capabilities in conduction of aqueous material and mechanical support of the plant stem and branches. Lignin playd a multifunctional role in making the tracheid wall hydrophobic and mechanically strong, and very defensive against biodegradative microbes by formation of structurally heterogeneous SMS. A cluster of globular HG lignin consisting of condensed oligolignols effectively protects weak β-O-4' bonds located inside the lignin SMS from biodegradation by exogenous enzymes or other active agents. For Pterido-phyta and gymnosperms, the first dominant vascular plants with HG lignin, this resulted in longevity of huge plants and slow alternation of generations around the Carboniferous period. Changes of the environment on earth promoted the evolution of angiosperms in which multifunctional tracheids differentiated into conduction-specialized vessels and support-specialized fibers. The excessively strong defense function of HG lignin became moderate in less condensed SG lignin, and the weakened defense rendered cell walls of angiosperms biodegradable easily after plant death to provide space for growing of young plnts and frequent alternation of generations. Lignin in Gramineae containing ester-bonded ferulic and p-coumaric acids is highly biodegradable. Thus, angiosperms with lignin of appropriate defense function evolved by the ready adaptability to environmental change on earth through frequent gene conversion. Additional factors promoting evolution of lignin structure are proposed. © 2013, The Japan Wood Research Society. All rights reserved.