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

Journal Article · · Plant Physiology (Bethesda)
DOI:https://doi.org/10.1104/pp.19.01550· OSTI ID:1603400
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [2];  [4];  [4];  [4]; ORCiD logo [5];  [6]; ORCiD logo [7];  [4]; ORCiD logo [8]; ORCiD logo [9]; ORCiD logo [10]; ORCiD logo [6]; ORCiD logo [5]; ORCiD logo [2]
  1. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, Department of Genetics, University of Georgia, Athens, Georgia 30602, Department of Plant Biology, University of Georgia, Athens, Georgia 30602, Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
  2. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, Department of Genetics, University of Georgia, Athens, Georgia 30602
  3. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, Department of Genetics, University of Georgia, Athens, Georgia 30602, Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
  4. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602
  5. Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium, Vlaams Instituut voor Biotechnologie, UGent Center for Plant Systems Biology, 9052 Ghent, Belgium
  6. Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin 53706, Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, Wisconsin 53726
  7. National Renewable Energy Laboratory, Golden, Colorado 80401, BioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
  8. BioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia 30602
  9. Department of Plant Biology, University of Georgia, Athens, Georgia 30602, Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, BioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia 30602
  10. Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, National Renewable Energy Laboratory, Golden, Colorado 80401, BioEnergy Science Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831

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. In this work 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.

Research Organization:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); BioEnergy Science Center (BESC) (United States); USDOE Bioenergy Research Centers (BRC) (United States). Center for Bioenergy Innovation (CBI) and Great Lakes Bioenergy Research Center (GLBRC)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; National Institute of Food and Agriculture (NIFA); National Science Foundation (NSF)
Grant/Contract Number:
AC36-08GO28308; 2015-67013-22812; IOS-1546867; IOS-09223992; DBI-0421683; WPN–ERKP695; WPN–ERKP886; SC0018409
OSTI ID:
1603400
Alternate ID(s):
OSTI ID: 1605535
Report Number(s):
NREL/JA-2700-76366; /plantphysiol/183/1/123.atom
Journal Information:
Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Vol. 183 Journal Issue: 1; ISSN 0032-0889
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 30 works
Citation information provided by
Web of Science