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

Abstract

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 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 x 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.

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [4];  [5];  [2];  [6];  [1]; ORCiD logo [5];  [4];  [3];  [2]
  1. University of Georgia; Oak Ridge National Laboratory
  2. University of Georgia
  3. Ghent University; VIB Center for Plant Systems Biology
  4. University of Wisconsin
  5. National Renewable Energy Laboratory (NREL), Golden, CO (United States)
  6. Oak Ridge National Laboratory; University of Georgia
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1605535
Report Number(s):
NREL/JA-2700-76366
DOE Contract Number:  
AC36-08GO28308
Resource Type:
Journal Article
Journal Name:
Plant Physiology
Additional Journal Information:
Journal Name: Plant Physiology
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; caffeic acid; monolignol; saccharification; thiol redox; glutathione-ascorbate; sulfur assimilation; metabolic compensation

Citation Formats

Tsai, Chung-Jui, Xu, Peng, Xue, Liang-Jiao, Hu, Hao, Nyamdari, Batbayar, Naran, Radnaa, Zhou, Xiaohong, Goeminne, Geert, Gao, Ruili, Gjersing, Erica L, Dahlen, Joseph, Pattathil, Sivakumar, Hahn, Michael G., Davis, Mark F, Ralph, John, Boerjan, Wout A., and Harding, Scott A. Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1-Knockout Poplar. United States: N. p., 2020. Web. doi:10.1104/pp.19.01550.
Tsai, Chung-Jui, Xu, Peng, Xue, Liang-Jiao, Hu, Hao, Nyamdari, Batbayar, Naran, Radnaa, Zhou, Xiaohong, Goeminne, Geert, Gao, Ruili, Gjersing, Erica L, Dahlen, Joseph, Pattathil, Sivakumar, Hahn, Michael G., Davis, Mark F, Ralph, John, Boerjan, Wout A., & Harding, Scott A. Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1-Knockout Poplar. United States. doi:10.1104/pp.19.01550.
Tsai, Chung-Jui, Xu, Peng, Xue, Liang-Jiao, Hu, Hao, Nyamdari, Batbayar, Naran, Radnaa, Zhou, Xiaohong, Goeminne, Geert, Gao, Ruili, Gjersing, Erica L, Dahlen, Joseph, Pattathil, Sivakumar, Hahn, Michael G., Davis, Mark F, Ralph, John, Boerjan, Wout A., and Harding, Scott A. Fri . "Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1-Knockout Poplar". United States. doi:10.1104/pp.19.01550.
@article{osti_1605535,
title = {Compensatory Guaiacyl Lignin Biosynthesis at the Expense of Syringyl Lignin in 4CL1-Knockout Poplar},
author = {Tsai, Chung-Jui and Xu, Peng and Xue, Liang-Jiao and Hu, Hao and Nyamdari, Batbayar and Naran, Radnaa and Zhou, Xiaohong and Goeminne, Geert and Gao, Ruili and Gjersing, Erica L and Dahlen, Joseph and Pattathil, Sivakumar and Hahn, Michael G. and Davis, Mark F and Ralph, John and Boerjan, Wout A. and Harding, Scott A.},
abstractNote = {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 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 x 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.},
doi = {10.1104/pp.19.01550},
journal = {Plant Physiology},
number = ,
volume = ,
place = {United States},
year = {2020},
month = {3}
}