Possible mechanisms for the generation of phenyl glycoside‐type lignin–carbohydrate linkages in lignification with monolignol glucosides

• Published in: The Plant journal : for cell and molecular biology 2020-09, Vol.104 (1), p.156-170
• Main Authors: Miyagawa, Yasuyuki, Tobimatsu, Yuki, Lam, Pui Ying, Mizukami, Takahito, Sakurai, Sayaka, Kamitakahara, Hiroshi, Takano, Toshiyuki
• Format: Article
• Language: English
• Subjects: Acacia - metabolism; Acacia mangium; Addition polymerization; Bamboo; Biomimetics; Carbohydrate Metabolism; Carbohydrates; cell wall; Cell Wall - metabolism; Cell walls; Coherence; Eucalyptus; Eucalyptus - metabolism; Eucalyptus camaldulensis; Glucosidase; Glucosides; Glucosides - metabolism; Glycosides; Glycosides - metabolism; Hardwoods; Intermediates; Lignin; Lignin - metabolism; lignin–carbohydrate complex; lignin–carbohydrate linkage; Linkages; Metabolic Networks and Pathways; monolignol glucoside; NMR; Nuclear magnetic resonance; Peroxidase; phenyl glycoside; Phyllostachys edulis; Pine trees; Pinus taeda; Pinus taeda - metabolism; Poaceae - metabolism; Polymerization; Polymers; Poplar; Populus - metabolism; Populus euramericana; Prepolymers; Quantum phenomena; Quinones; Structural analysis
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14913

SUMMARY The existence and formation of covalent lignin–carbohydrate (LC) linkages in plant cell walls has long been a matter of debate in terms of their roles in cell wall development and biomass use. Of the various putative LC linkages proposed to date, evidence of the native existence and formation mechanism of phenyl glycoside (PG)‐type LC linkages in planta is particularly scarce. The present study aimed to explore previously overlooked mechanisms for the formation of PG‐type LC linkages through the incorporation of monolignol glucosides, which are possible lignin precursors, into lignin polymers during lignification. Peroxidase‐catalyzed lignin polymerization of coniferyl alcohol in the presence of coniferin and syringin in vitro resulted in the generation of PG‐type LC linkages in synthetic lignin polymers, possibly via nucleophilic addition onto quinone methide (QM) intermediates formed during polymerization. Biomimetic lignin polymerization of coniferin via the β‐glucosidase/peroxidase system also resulted in the generation of PG‐type as well as alkyl glycoside‐type LC linkages. This occurred via non‐enzymatic QM‐involving reactions and also via enzymatic transglycosylations involving β‐glucosidase, which was demonstrated by in‐depth structural analysis of the synthetic lignins by two‐dimensional NMR. We collected heteronuclear single‐quantum coherence (HSQC) NMR for native cell wall fractions prepared from pine (Pinus taeda), eucalyptus (Eucalyptus camaldulensis), acacia (Acacia mangium), poplar (Populus × eurarnericana) and bamboo (Phyllostachys edulis) wood samples, which exhibited correlations, albeit at low levels, that were well matched with those of the PG‐type LC linkages in synthetic lignins incorporating monolignol glucosides. Overall, our results provide a molecular basis for feasible mechanisms for the generation of PG‐type LC linkages from monolignol glucosides and further substantiates their existence in planta. Significance Statement Biomimetic lignin polymerization with monolignol glucosides, which are possible lignin precursors, produces synthetic lignin polymers containing phenyl glycoside‐type lignin–carbohydrate linkages. Comparisons of NMR spectra of native cell wall fractions and synthetic lignins incorporating monolignol glucosides support the in planta occurrence of such LC linkages arising from monolignol glucosides.