4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase

Jaime Barros; Luis Escamilla-Trevino; Luhua Song; Xiaolan Rao; Juan Carlos Serrani-Yarce; Maite Docampo Palacios; Nancy Engle; Feroza K. Choudhury; Timothy J. Tschaplinski; Barney J. Venables; Ron Mittler; Richard A. Dixon

doi:10.1038/s41467-019-10082-7

4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase

Jaime Barros, Luis Escamilla-Trevino, Luhua Song, Xiaolan Rao, Juan Carlos Serrani-Yarce, Maite Docampo Palacios, Nancy Engle, Feroza K. Choudhury, Timothy J. Tschaplinski, Barney J. Venables, Ron Mittler, Richard A. Dixon

Research output: Contribution to journal › Article › peer-review

173 Scopus citations

Abstract

Lignin biosynthesis is evolutionarily conserved among higher plants and features a critical 3-hydroxylation reaction involving phenolic esters. However, increasing evidence questions the involvement of a single pathway to lignin formation in vascular plants. Here 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.

Original language	English
Article number	1994
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-10082-7
State	Published - Dec 1 2019

Funding

We thank Chan Man Ha for help with genetic crossing experiments, Xiaoqiang Wang and Mina Aziz for advice on protein molecular modeling, Meredith Lauren Yeary for help in metabolomic data extraction, and the BioAnalytical Facility at the University of North Texas for support with mass spectrometry analyses. We gratefully acknowledge funding from the University of North Texas and the BioEnergy Science Center and the Center for Bioenergy Innovation (Oak Ridge National Laboratory), US Department of Energy (DOE) Bioenergy Research Centers supported by the Office of Biological and Environmental Research in the DOE Office of Science. This manuscript has been coauthored by UT-Battelle, LLC under Contract No. DE-AC05–00OR22725 with the U.S. Department of Energy. J.B. is also indebted to the Barrie Foundation and the Spanish National Science Foundation for postdoctoral training fellowships.

Funders	Funder number
Barrie Foundation
BioEnergy Science Center
DOE Office of Science
Office of Biological and Environmental Research
Spanish National Science Foundation
US Department of Energy
UT-Battelle, LLC
U.S. Department of Energy
Oak Ridge National Laboratory
University of North Texas

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Barros, J., Escamilla-Trevino, L., Song, L., Rao, X., Serrani-Yarce, J. C., Palacios, M. D., Engle, N., Choudhury, F. K., Tschaplinski, T. J., Venables, B. J., Mittler, R., & Dixon, R. A. (2019). 4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase. Nature Communications, 10(1), Article 1994. https://doi.org/10.1038/s41467-019-10082-7

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abstract = "Lignin biosynthesis is evolutionarily conserved among higher plants and features a critical 3-hydroxylation reaction involving phenolic esters. However, increasing evidence questions the involvement of a single pathway to lignin formation in vascular plants. Here 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.",

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AB - Lignin biosynthesis is evolutionarily conserved among higher plants and features a critical 3-hydroxylation reaction involving phenolic esters. However, increasing evidence questions the involvement of a single pathway to lignin formation in vascular plants. Here 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.

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4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase

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