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Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.13988· OSTI ID:1459572
 [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [2];  [4];  [3];  [5];  [6]
  1. Kyoto Univ. (Japan). Research Inst. for Sustainable Humanosphere; Research Institute for Sustainable Humanosphere, Kyoto University
  2. Kyoto Univ. (Japan). Research Inst. for Sustainable Humanosphere
  3. Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
  4. Tokushima Univ., Kuramoto-cho, Tokushima (Japan). Faculty of Bioscience and Bioindustry
  5. Kyoto Univ. (Japan). Graduate School of Agriculture
  6. Kyoto Univ. (Japan). Research Inst. for Sustainable Humanosphere; Kyoto Univ. (Japan). Research Unit for Development of Global Sustainability
p-Coumaroyl ester 3-hydroxylase (C3'H) is a key enzyme involved in the biosynthesis of lignin, a phenylpropanoid polymer that is the major constituent in vascular plants’ secondary cell walls. Although the crucial role of C3'H in lignification and its manipulation to upgrade lignocellulose have been investigated in eudicots, limited information is available in monocotyledonous grass species despite their potential as biomass feedstocks. Here in this paper we address the pronounced impacts of C3'H-deficiency on the structure and properties of grass cell walls. C3'H-knockdown lines generated via RNAi-mediated gene silencing, with ~0.5% of residual expression levels, reached maturity and set seeds, whereas, in contrast, C3'H-knockout rice mutants generated via CRISPR/Cas9-mediated mutagenesis were severely dwarfed and sterile. Cell wall analysis of the mature C3'H-knockdown RNAi lines revealed that their lignins were largely enriched in p-hydroxyphenyl (H) units while substantially reduced in the normally dominant guaiacyl (G) and syringyl (S) units. Interestingly, however, the enrichment of H units was limited to being within the non-acylated lignin units, with grass-specific γ-p-coumaroylated lignin units remaining apparently unchanged. Suppression of C3'H also resulted in relative augmentation in tricin residues in lignin as well as substantial reduction in wall cross-linking ferulates. Collectively, our data demonstrate that C3'H expression is an important determinant, not only of lignin content and composition, but also of the degree of cell wall cross-linking. We also demonstrated that C3'H-suppressed rice displays enhanced biomass saccharification.
Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
Japan International Cooperation Agency; Japan Science and Technology Agency (JST); Japan Society for the Promotion of Science (JSPS); Ministry of Agriculture, Forestry and Fisheries of Japan; New Energy and Industrial Technology Development Organization (NEDO); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
FC02-07ER64494; SC0018409
OSTI ID:
1459572
Alternate ID(s):
OSTI ID: 1459711
Journal Information:
The Plant Journal, Journal Name: The Plant Journal Journal Issue: 5 Vol. 95; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (84)

Diferulate cross-links impede the enzymatic degradation of non-lignified maize walls journal June 1998
Paving the Way for Lignin Valorisation: Recent Advances in Bioengineering, Biorefining and Catalysis journal June 2016
Reductive Cleavage Method for Quantitation of Monolignols and Low-Abundance Monolignol Conjugates journal May 2018
A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures journal May 1994
Cell wall fermentation kinetics are impacted more by lignin content and ferulate cross-linking than by lignin composition journal January 2009
Down-regulation of four putative arabinoxylan feruloyl transferase genes from family PF02458 reduces ester-linked ferulate content in rice cell walls journal December 2009
Functional testing of a PF02458 homologue of putative rice arabinoxylan feruloyl transferase genes in Brachypodium distachyon journal November 2015
Regulation of CONIFERALDEHYDE 5-HYDROXYLASE expression to modulate cell wall lignin structure in rice journal April 2017
Hydroxycinnamates in lignification journal August 2009
The cinnamate/monolignol pathway journal November 2009
Catalytic activity, duplication and evolution of the CYP98 cytochrome P450 family in wheat journal November 2006
Early lignin pathway enzymes and routes to chlorogenic acid in switchgrass (Panicum virgatum L.) journal November 2013
Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice journal July 2015
Building the wall: recent advances in understanding lignin metabolism in grasses journal November 2016
Effects on Lignin Structure of Coumarate 3-Hydroxylase Downregulation in Poplar journal May 2012
Downregulation of p-Coumaroyl Quinate/Shikimate 3′-Hydroxylase (C3′H) or Cinnamate-4-hydrolylase (C4H) in Eucalyptus urophylla × Eucalyptus grandis Leads to Increased Extractability journal June 2016
WWW-query: An on-line retrieval system for biological sequence banks journal January 1996
Hot alkali-labile linkages in the walls of the forage grass Phalaris aquatica and Lolium perenne and their relation to in vitro wall digestibility journal September 2003
Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty? journal April 2013
Cell wall modifications triggered by the down-regulation of Coumarate 3-hydroxylase-1 in maize journal July 2015
The world availability of non-wood lignocellulosic biomass for the production of cellulosic ethanol and potential pretreatments for the enhancement of enzymatic saccharification journal July 2016
Quantitative Molecular Structure–Pyrolytic Energy Correlation for Hardwood Lignins journal January 2012
Occurrence of Naturally Acetylated Lignin Units journal July 2007
Syntheses of Lignin-Derived Thioacidolysis Monomers and Their Uses as Quantitation Standards journal January 2012
Derivatization Followed by Reductive Cleavage (DFRC Method), a New Method for Lignin Analysis:  Protocol for Analysis of DFRC Monomers journal July 1997
Ferulate Cross-Links Limit the Enzymatic Degradation of Synthetically Lignified Primary Walls of Maize journal July 1998
The DFRC Method for Lignin Analysis. 6. A Simple Modification for Identifying Natural Acetates on Lignins journal November 1998
Detection and Determination of p-Coumaroylated Units in Lignins journal May 1999
Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids journal January 2004
Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant journal March 2014
Whole plant cell wall characterization using solution-state 2D NMR journal August 2012
NMR studies on lignocellulose deconstructions in the digestive system of the lower termite Coptotermes formosanus Shiraki journal January 2018
Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5 journal January 2010
Upgrading of lignin-derived bio-oils by catalytic hydrodeoxygenation journal January 2014
Impact of engineered lignin composition on biomass recalcitrance and ionic liquid pretreatment efficiency journal January 2016
The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism journal April 2002
Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis journal April 2002
Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.) journal November 2005
RNAi-mediated suppression of p-coumaroyl-CoA 3'-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism journal March 2008
A polymer of caffeyl alcohol in plant seeds journal January 2012
Loss of function of cinnamyl alcohol dehydrogenase 1 leads to unconventional lignin and a temperature-sensitive growth defect in Medicago truncatula journal July 2013
CYP98A3 from Arabidopsis thaliana Is a 3′-Hydroxylase of Phenolic Esters, a Missing Link in the Phenylpropanoid Pathway journal June 2001
Identification of Grass-specific Enzyme That Acylates Monolignols with p-Coumarate journal January 2012
Effects of Coumarate 3-Hydroxylase Down-regulation on Lignin Structure journal January 2006
Clustal W and Clustal X version 2.0 journal September 2007
CRISPR-P: A Web Tool for Synthetic Single-Guide RNA Design of CRISPR-System in Plants journal September 2014
Phytozome: a comparative platform for green plant genomics journal November 2011
RiceXPro Version 3.0: expanding the informatics resource for rice transcriptome journal November 2012
A coumaroyl-ester-3-hydroxylase Insertion Mutant Reveals the Existence of Nonredundant meta -Hydroxylation Pathways and Essential Roles for Phenolic Precursors in Cell Expansion and Plant Growth journal December 2005
GOLD HULL AND INTERNODE2 Encodes a Primarily Multifunctional Cinnamyl-Alcohol Dehydrogenase in Rice journal January 2006
Functional Characterization of Evolutionarily Divergent 4-Coumarate:Coenzyme A Ligases in Rice journal August 2011
Tricin, a Flavonoid Monomer in Monocot Lignification journal February 2015
Disrupting Flavone Synthase II Alters Lignin and Improves Biomass Digestibility journal April 2017
Highly Decorated Lignins in Leaf Tissues of the Canary Island Date Palm Phoenix canariensis journal September 2017
Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase Affects Phenylpropanoid Biosynthesis journal May 2004
Convergent Evolution of Syringyl Lignin Biosynthesis via Distinct Pathways in the Lycophyte Selaginella and Flowering Plants journal April 2010
A Systems Biology View of Responses to Lignin Biosynthesis Perturbations in Arabidopsis journal September 2012
Coexistence but Independent Biosynthesis of Catechyl and Guaiacyl/Syringyl Lignin Polymers in Seed Coats journal July 2013
Metabolic engineering of novel lignin in biomass crops journal October 2012
Suppression of a single BAHD gene in Setaria viridis causes large, stable decreases in cell wall feruloylation and increases biomass digestibility journal January 2018
Ferulic acid: a key component in grass lignocellulose recalcitrance to hydrolysis journal November 2014
Genetic engineering of grass cell wall polysaccharides for biorefining journal June 2017
p -Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon journal February 2014
Identification and suppression of the p‐ coumaroyl CoA:hydroxycinnamyl alcohol transferase in Zea mays L. journal May 2014
Tricin-lignins: occurrence and quantitation of tricin in relation to phylogeny journal November 2016
Monolignol ferulate conjugates are naturally incorporated into plant lignins journal October 2016
Feedstocks for Lignocellulosic Biofuels journal August 2010
Lignin Valorization: Improving Lignin Processing in the Biorefinery journal May 2014
Lignin Biosynthesis journal June 2003
The Cytochrome P450 Homepage journal October 2009
Down-regulation of p-coumaroyl quinate/shikimate 3′-hydroxylase (C3′H) and cinnamate 4-hydroxylase (C4H) genes in the lignin biosynthetic pathway of Eucalyptus urophylla × E. grandis leads to improved sugar release journal August 2015
The impact of alterations in lignin deposition on cellulose organization of the plant cell wall journal June 2016
Suppression of CINNAMOYL-CoA REDUCTASE increases the level of monolignol ferulates incorporated into maize lignins journal May 2017
Preparative Thioacidolysis of Spruce Lignin: Isolation and Identification of Main Monomeric Products journal January 1986
Can Lignin Be Accurately Measured? journal January 2005
Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens journal May 2016
Grass Cell Walls: A Story of Cross-Linking journal January 2017
Occurrence of guaiacyl/p-hydroxyphenyl lignin in Arabidopsis thaliana T87 cells journal January 2011
Rapid analysis of transgenic rice straw using near-infrared spectroscopy journal January 2012
Microscale thioacidolysis method for the rapid analysis of ^|^#946;-O-4 substructures in lignin journal January 2012
Characterization of 5-Hydroxyconiferaldehyde O-Methyltransferase in Oryza sativa journal January 2013
CAD2 deficiency causes both brown midrib and gold hull and internode phenotypes in Oryza sativa L. cv. Nipponbare journal January 2013
MYB-mediated upregulation of lignin biosynthesis in Oryza sativa towards biomass refinery journal January 2017
High-throughput determination of thioglycolic acid lignin from rice journal January 2009

Cited By (10)

4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase journal April 2019
OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls journal August 2019
Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice journal November 2019
Expression of Eucalyptus globulus LACCASE48 Restores Lignin Content of Arabidopsis thaliana lac17 Mutant journal November 2019
Recruitment of specific flavonoid B‐ring hydroxylases for two independent biosynthesis pathways of flavone‐derived metabolites in grasses journal April 2019
Lignin characterization of rice CONIFERALDEHYDE 5-HYDROXYLASE loss-of-function mutants generated with the CRISPR/Cas9 system journal December 2018
Os MYB 108 loss‐of‐function enriches p ‐coumaroylated and tricin lignin units in rice cell walls journal April 2019
Comparative evaluations of lignocellulose reactivity and usability in transgenic rice plants with altered lignin composition journal February 2019
Stacking of a low-lignin trait with an increased guaiacyl and 5-hydroxyguaiacyl unit trait leads to additive and synergistic effects on saccharification efficiency in Arabidopsis thaliana journal September 2018
Low Lignin Mutants and Reduction of Lignin Content in Grasses for Increased Utilisation of Lignocellulose journal May 2019

Figures / Tables (7)


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