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

Erica Gjersing, Mark Davis, Chung-Jui Tsai, Peng Xu, Liang-Jiao Xue, Hao Hu, Batbayar Nyamdari, Radnaa Naran, Xiaohong Zhou, Geert Goeminne, Ruili Gao, Joseph Dahlen, Sivakumar Pattathil, Michael Hahn, John Ralph, Wout Boerjan, Scott Harding

Research output: Contribution to journalArticlepeer-review

36 Scopus Citations

Abstract

The lignin biosynthetic pathway is highly conserved in angiosperms, yet pathway manipulations give rise to a variety of taxonspecific outcomes. Knockout of lignin-associated 4-coumarate:CoA ligases (4CLs) in herbaceous species mainly reduces guaiacyl (G) lignin and enhances cell wall saccharification. Here we show that CRISPR-knockout of 4CL1 in poplar (Populus tremula 3 alba) preferentially reduced syringyl (S) lignin, with negligible effects on biomass recalcitrance. Concordant with reduced S-lignin was downregulation of ferulate 5-hydroxylases (F5Hs). 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 caffeoyl shikimate esterase1. Upregulation of caffeoyl-CoA O-methyltransferase1 and downregulation of F5Hs are consistent with preferential funneling of 4CL5 products toward G-lignin biosynthesis at the expense of S-lignin. Thus, transcriptional and metabolic adaptations to 4CL1-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.

Original languageAmerican English
Pages (from-to)123-136
Number of pages14
JournalPlant Physiology
Volume183
Issue number5
DOIs
StatePublished - 2020

Bibliographical note

Publisher Copyright:
Copyright © 2020 American Society of Plant Biologists. All rights reserved.

NREL Publication Number

  • NREL/JA-2700-76366

Keywords

  • caffeic acid
  • glutathione-ascorbate
  • metabolic compensation
  • monolignol
  • saccharification
  • sulfur assimilation
  • thiol redox

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