Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1 -Knockout Poplar

• Published in: Plant physiology (Bethesda) 2020-05, Vol.183 (1), p.123-136
• Main Authors: Tsai, Chung-Jui, Xu, Peng, Xue, Liang-Jiao, Hu, Hao, Nyamdari, Batbayar, Naran, Radnaa, Zhou, Xiaohong, Goeminne, Geert, Gao, Ruili, Gjersing, Erica, Dahlen, Joseph, Pattathil, Sivakumar, Hahn, Michael G, Davis, Mark F, Ralph, John, Boerjan, Wout, Harding, Scott A
• Format: Article
• Language: English
• Subjects: 09 BIOMASS FUELS; caffeic acid; Carboxy-Lyases - genetics; Carboxy-Lyases - metabolism; Catalysis; Gene Expression Regulation, Plant; glutathione-ascorbate; Lignin - metabolism; metabolic compensation; monolignol; Plants, Genetically Modified - genetics; Plants, Genetically Modified - metabolism; Populus - metabolism; saccharification; sulfur assimilation; thiol redox; Xylem - genetics; Xylem - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.19.01550

The lignin biosynthetic pathway is highly conserved in angiosperms, yet pathway manipulations give rise to a variety of taxon-specific outcomes. Knockout of lignin-associated - : ( ) in herbaceous species mainly reduces guaiacyl (G) lignin and enhances cell wall saccharification. Here we show that CRISPR-knockout of in poplar ( × ) preferentially reduced syringyl (S) lignin, with negligible effects on biomass recalcitrance. Concordant with reduced S-lignin was downregulation of - ( ). Lignification was largely sustained by 4CL5, a low-affinity paralog of 4CL1 typically with only minor xylem expression or activity. Levels of caffeate, the preferred substrate of 4CL5, increased in line with significant upregulation of Upregulation of - - and downregulation of are consistent with preferential funneling of 4CL5 products toward G-lignin biosynthesis at the expense of S-lignin. Thus, transcriptional and metabolic adaptations to -knockout appear to have enabled 4CL5 catalysis at a level sufficient to sustain lignification. Finally, genes involved in sulfur assimilation, the glutathione-ascorbate cycle, and various antioxidant systems were upregulated in the mutants, suggesting cascading responses to perturbed thioesterification in lignin biosynthesis.