4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase
Abstract
Lignin biosynthesis is evolutionarily conserved among higher plants and features a critical 3-hydroxylation reaction involving phenolic esters. Yet, increasing evidence questions the involvement of a single pathway to lignin formation in vascular plants. In this work we describe an enzyme catalyzing the direct 3-hydroxylation of 4-coumarate to caffeate in lignin biosynthesis as a bifunctional peroxidase that oxidizes both ascorbate and 4-coumarate at comparable rates. A combination of biochemical and genetic evidence in the model plants Brachypodium distachyon and Arabidopsis thaliana supports a role for this coumarate 3-hydroxylase (C3H) in the early steps of lignin biosynthesis. The subsequent efficient O-methylation of caffeate to ferulate in grasses is substantiated by in vivo biochemical assays. Our results identify C3H as the only non-membrane bound hydroxylase in the lignin pathway and revise the currently accepted models of lignin biosynthesis, suggesting new gene targets to improve forage and bioenergy crops.
- Authors:
-
[1];
[2];
[3];
[3];
[1]
- Univ. of North Texas, Denton, TX (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of North Texas, Denton, TX (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1545188
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Barros, Jaime, Escamilla-Trevino, Luis, Song, Luhua, Rao, Xiaolan, Serrani-Yarce, Juan Carlos, Palacios, Maite Docampo, Engle, Nancy, Choudhury, Feroza K., Tschaplinski, Timothy J., Venables, Barney J., Mittler, Ron, and Dixon, Richard A. 4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase. United States: N. p., 2019.
Web. doi:10.1038/s41467-019-10082-7.
Barros, Jaime, Escamilla-Trevino, Luis, Song, Luhua, Rao, Xiaolan, Serrani-Yarce, Juan Carlos, Palacios, Maite Docampo, Engle, Nancy, Choudhury, Feroza K., Tschaplinski, Timothy J., Venables, Barney J., Mittler, Ron, & Dixon, Richard A. 4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase. United States. https://doi.org/10.1038/s41467-019-10082-7
Barros, Jaime, Escamilla-Trevino, Luis, Song, Luhua, Rao, Xiaolan, Serrani-Yarce, Juan Carlos, Palacios, Maite Docampo, Engle, Nancy, Choudhury, Feroza K., Tschaplinski, Timothy J., Venables, Barney J., Mittler, Ron, and Dixon, Richard A. Tue .
"4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase". United States. https://doi.org/10.1038/s41467-019-10082-7. https://www.osti.gov/servlets/purl/1545188.
@article{osti_1545188,
title = {4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase},
author = {Barros, Jaime and Escamilla-Trevino, Luis and Song, Luhua and Rao, Xiaolan and Serrani-Yarce, Juan Carlos and Palacios, Maite Docampo and Engle, Nancy and Choudhury, Feroza K. and Tschaplinski, Timothy J. and Venables, Barney J. and Mittler, Ron and Dixon, Richard A.},
abstractNote = {Lignin biosynthesis is evolutionarily conserved among higher plants and features a critical 3-hydroxylation reaction involving phenolic esters. Yet, increasing evidence questions the involvement of a single pathway to lignin formation in vascular plants. In this work we describe an enzyme catalyzing the direct 3-hydroxylation of 4-coumarate to caffeate in lignin biosynthesis as a bifunctional peroxidase that oxidizes both ascorbate and 4-coumarate at comparable rates. A combination of biochemical and genetic evidence in the model plants Brachypodium distachyon and Arabidopsis thaliana supports a role for this coumarate 3-hydroxylase (C3H) in the early steps of lignin biosynthesis. The subsequent efficient O-methylation of caffeate to ferulate in grasses is substantiated by in vivo biochemical assays. Our results identify C3H as the only non-membrane bound hydroxylase in the lignin pathway and revise the currently accepted models of lignin biosynthesis, suggesting new gene targets to improve forage and bioenergy crops.},
doi = {10.1038/s41467-019-10082-7},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {Tue Apr 30 00:00:00 EDT 2019},
month = {Tue Apr 30 00:00:00 EDT 2019}
}
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The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes
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Understanding functional diversity and substrate specificity in haem peroxidases: what can we learn from ascorbate peroxidase?
journal, January 2003
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The action of o-dihydric phenols in the hydroxylation of p-coumaric acid by a phenolase from leaves of spinach beet (Beta vulgaris L.)
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Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice
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Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS
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Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis
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Ascorbate Peroxidase 1 Plays a Key Role in the Response of Arabidopsis thaliana to Stress Combination
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Rapid Accumulation of Glutathione During Light Stress in Arabidopsis
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Purification and Characterization of Pea Cytosolic Ascorbate Peroxidase
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Stress-Induced Phenylpropanoid Metabolism.
journal, July 1995
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The origin and evolution of lignin biosynthesis: Tansley review
journal, June 2010
- Weng, Jing-Ke; Chapple, Clint
- New Phytologist, Vol. 187, Issue 2
Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon
journal, June 2017
- Sibout, Richard; Proost, Sebastian; Hansen, Bjoern Oest
- New Phytologist, Vol. 215, Issue 3
Downregulation of p‐ COUMAROYL ESTER 3‐ HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification
journal, July 2018
- Takeda, Yuri; Tobimatsu, Yuki; Karlen, Steven D.
- The Plant Journal, Vol. 95, Issue 5
Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis
journal, August 2013
- Vanholme, R.; Cesarino, I.; Rataj, K.
- Science, Vol. 341, Issue 6150
Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014
- Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
- Science, Vol. 344, Issue 6185, p. 1246843-1246843
Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012
- Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
- Biotechnology for Biofuels, Vol. 5, Issue 1
A 13C isotope labeling method for the measurement of lignin metabolic flux in Arabidopsis stems
journal, June 2018
- Wang, Peng; Guo, Longyun; Jaini, Rohit
- Plant Methods, Vol. 14, Issue 1
Dynamic changes in transcriptome and cell wall composition underlying brassinosteroid-mediated lignification of switchgrass suspension cells
journal, November 2017
- Rao, Xiaolan; Shen, Hui; Pattathil, Sivakumar
- Biotechnology for Biofuels, Vol. 10, Issue 1
Generation and Characterization of the Western Regional Research Center Brachypodium T-DNA Insertional Mutant Collection
journal, September 2012
- Bragg, Jennifer N.; Wu, Jiajie; Gordon, Sean P.
- PLoS ONE, Vol. 7, Issue 9
Gene Knockout Study Reveals That Cytosolic Ascorbate Peroxidase 2(OsAPX2) Plays a Critical Role in Growth and Reproduction in Rice under Drought, Salt and Cold Stresses
journal, February 2013
- Zhang, Zhiguo; Zhang, Quian; Wu, Jinxia
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PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus
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Biotechnological Potential of LSD1, EDS1, and PAD4 in the Improvement of Crops and Industrial Plants
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