Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content
Abstract
Lignin is a phenolic heteropolymer that is deposited in secondary-thickened cell walls, where it provides mechanical strength. A recent structural characterization of cell walls from monocot species showed that the flavone tricin is part of the native lignin polymer, where it is hypothesized to initiate lignin chains. In this study, we investigated the consequences of altered tricin levels on lignin structure and cell wall recalcitrance by phenolic profiling, nuclear magnetic resonance, and saccharification assays of the naturally silenced maize (Zea mays) C2-Idf (inhibitor diffuse) mutant, defective in the CHALCONE SYNTHASE Colorless2 (C2) gene. We show that the C2-Idf mutant produces highly reduced levels of apigenin- and tricin-related flavonoids, resulting in a strongly reduced incorporation of tricin into the lignin polymer. Moreover, the lignin was enriched in β-β and β-5 units, lending support to the contention that tricin acts to initiate lignin chains and that, in the absence of tricin, more monolignol dimerization reactions occur. In addition, the C2-Idf mutation resulted in strikingly higher Klason lignin levels in the leaves. As a consequence, the leaves of C2-Idf mutants had significantly reduced saccharification efficiencies compared with those of control plants. These findings are instructive for lignin engineering strategies to improve biomass processingmore »
- Authors:
-
- Center for Plant Systems Biology, VIB (Belgium); Ghent University (Belgium). Department of Plant Biotechnology and Bioinformatics
- Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute and Department of Biological System Engineering
- Center for Plant Systems Biology, VIB (Belgium); Ghent University (Belgium). Department of Plant Biotechnology and Bioinformatics; University of Sao Paulo, Butanta, Sao Paulo (Brazil)
- Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute and Department of Biochemistry
- Univ. of Wisconsin, Madison, WI (United States). Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Department of Biological System Engineering and Department of Biochemistry
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1427679
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant Physiology (Bethesda)
- Additional Journal Information:
- Journal Name: Plant Physiology (Bethesda); Journal Volume: 173; Journal Issue: 2; Journal ID: ISSN 0032-0889
- Publisher:
- American Society of Plant Biologists
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Eloy, Nubia B., Voorend, Wannes, Lan, Wu, Saleme, Marina de Lyra Soriano, Cesarino, Igor, Vanholme, Ruben, Smith, Rebecca A., Goeminne, Geert, Pallidis, Andreas, Morreel, Kris, Nicomedes, Jose, Ralph, John, and Boerjan, Wout. Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content. United States: N. p., 2016.
Web. doi:10.1104/pp.16.01108.
Eloy, Nubia B., Voorend, Wannes, Lan, Wu, Saleme, Marina de Lyra Soriano, Cesarino, Igor, Vanholme, Ruben, Smith, Rebecca A., Goeminne, Geert, Pallidis, Andreas, Morreel, Kris, Nicomedes, Jose, Ralph, John, & Boerjan, Wout. Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content. United States. https://doi.org/10.1104/pp.16.01108
Eloy, Nubia B., Voorend, Wannes, Lan, Wu, Saleme, Marina de Lyra Soriano, Cesarino, Igor, Vanholme, Ruben, Smith, Rebecca A., Goeminne, Geert, Pallidis, Andreas, Morreel, Kris, Nicomedes, Jose, Ralph, John, and Boerjan, Wout. Fri .
"Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content". United States. https://doi.org/10.1104/pp.16.01108. https://www.osti.gov/servlets/purl/1427679.
@article{osti_1427679,
title = {Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content},
author = {Eloy, Nubia B. and Voorend, Wannes and Lan, Wu and Saleme, Marina de Lyra Soriano and Cesarino, Igor and Vanholme, Ruben and Smith, Rebecca A. and Goeminne, Geert and Pallidis, Andreas and Morreel, Kris and Nicomedes, Jose and Ralph, John and Boerjan, Wout},
abstractNote = {Lignin is a phenolic heteropolymer that is deposited in secondary-thickened cell walls, where it provides mechanical strength. A recent structural characterization of cell walls from monocot species showed that the flavone tricin is part of the native lignin polymer, where it is hypothesized to initiate lignin chains. In this study, we investigated the consequences of altered tricin levels on lignin structure and cell wall recalcitrance by phenolic profiling, nuclear magnetic resonance, and saccharification assays of the naturally silenced maize (Zea mays) C2-Idf (inhibitor diffuse) mutant, defective in the CHALCONE SYNTHASE Colorless2 (C2) gene. We show that the C2-Idf mutant produces highly reduced levels of apigenin- and tricin-related flavonoids, resulting in a strongly reduced incorporation of tricin into the lignin polymer. Moreover, the lignin was enriched in β-β and β-5 units, lending support to the contention that tricin acts to initiate lignin chains and that, in the absence of tricin, more monolignol dimerization reactions occur. In addition, the C2-Idf mutation resulted in strikingly higher Klason lignin levels in the leaves. As a consequence, the leaves of C2-Idf mutants had significantly reduced saccharification efficiencies compared with those of control plants. These findings are instructive for lignin engineering strategies to improve biomass processing and biochemical production.},
doi = {10.1104/pp.16.01108},
journal = {Plant Physiology (Bethesda)},
number = 2,
volume = 173,
place = {United States},
year = {Fri Dec 09 00:00:00 EST 2016},
month = {Fri Dec 09 00:00:00 EST 2016}
}
Web of Science
Works referencing / citing this record:
The lignin toolbox of the model grass Setaria viridis
journal, June 2019
- Ferreira, Sávio Siqueira; Simões, Marcella Siqueira; Carvalho, Gabriel Garon
- Plant Molecular Biology, Vol. 101, Issue 3
Deposition of lignin in four species of Saccharum
journal, April 2019
- Llerena, Juan Pablo Portilla; Figueiredo, Raquel; Brito, Michael dos Santos
- Scientific Reports, Vol. 9, Issue 1
Phenolic cross-links: building and de-constructing the plant cell wall
journal, January 2020
- Mnich, Ewelina; Bjarnholt, Nanna; Eudes, Aymerick
- Natural Product Reports
PbrMYB169 positively regulates lignification of stone cells in pear fruit
journal, January 2019
- Xue, Cheng; Yao, Jia-Long; Xue, Yong-Song
- Journal of Experimental Botany, Vol. 70, Issue 6
Chalcone synthase is ubiquitinated and degraded via interactions with a RING-H2 protein in petals of Paeonia ‘He Xie’
journal, May 2019
- Gu, Zhaoyu; Men, Siqi; Zhu, Jin
- Journal of Experimental Botany, Vol. 70, Issue 18
Lignin biosynthesis: old roads revisited and new roads explored
journal, December 2019
- Dixon, Richard A.; Barros, Jaime
- Open Biology, Vol. 9, Issue 12
Recruitment of specific flavonoid B‐ring hydroxylases for two independent biosynthesis pathways of flavone‐derived metabolites in grasses
journal, April 2019
- Lam, Pui Ying; Lui, Andy C. W.; Yamamura, Masaomi
- New Phytologist, Vol. 223, Issue 1
Lignin from hydrothermally pretreated grass biomass retards enzymatic cellulose degradation by acting as a physical barrier rather than by inducing nonproductive adsorption of enzymes
journal, April 2018
- Djajadi, Demi T.; Jensen, Mads M.; Oliveira, Marlene
- Biotechnology for Biofuels, Vol. 11, Issue 1
Mutation of 4-coumarate: coenzyme A ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants
journal, April 2019
- Xiong, Wangdan; Wu, Zhenying; Liu, Yuchen
- Biotechnology for Biofuels, Vol. 12, Issue 1
SbCOMT (Bmr12) is involved in the biosynthesis of tricin-lignin in sorghum
journal, June 2017
- Eudes, Aymerick; Dutta, Tanmoy; Deng, Kai
- PLOS ONE, Vol. 12, Issue 6
Color for Life: Biosynthesis and Distribution of Phenolic Compounds in Pepper (Capsicum annuum)
text, January 2019
- Carvalho Lemos, Virginia; Reimer, Julia Jessica; Wormit, Alexandra
- RWTH Aachen University
Isolation and Characterization of Three Chalcone Synthase Genes in Pecan (Carya illinoinensis)
journal, June 2019
- Zhang,
- Biomolecules, Vol. 9, Issue 6
Lignins: Biosynthesis and Biological Functions in Plants
journal, January 2018
- Liu, Qingquan; Luo, Le; Zheng, Luqing
- International Journal of Molecular Sciences, Vol. 19, Issue 2
Elucidating Tricin-Lignin Structures: Assigning Correlations in HSQC Spectra of Monocot Lignins
journal, August 2018
- Lan, Wu; Yue, Fengxia; Rencoret, Jorge
- Polymers, Vol. 10, Issue 8
Color for Life: Biosynthesis and Distribution of Phenolic Compounds in Pepper (Capsicum annuum)
journal, April 2019
- Carvalho Lemos,
- Agriculture, Vol. 9, Issue 4
Deposition of lignin in four species of Saccharum
journal, April 2019
- Llerena, Juan Pablo Portilla; Figueiredo, Raquel; Brito, Michael dos Santos
- Scientific Reports, Vol. 9, Issue 1
Lignin biosynthesis: old roads revisited and new roads explored
journal, December 2019
- Dixon, Richard A.; Barros, Jaime
- Open Biology, Vol. 9, Issue 12
Hydroxystilbene Glucosides Are Incorporated into Norway Spruce Bark Lignin
journal, April 2019
- Rencoret, Jorge; Neiva, Duarte; Marques, Gisela
- Plant Physiology, Vol. 180, Issue 3
Lignin from hydrothermally pretreated grass biomass retards enzymatic cellulose degradation by acting as a physical barrier rather than by inducing nonproductive adsorption of enzymes
journal, April 2018
- Djajadi, Demi T.; Jensen, Mads M.; Oliveira, Marlene
- Biotechnology for Biofuels, Vol. 11, Issue 1
SbCOMT (Bmr12) is involved in the biosynthesis of tricin-lignin in sorghum
journal, June 2017
- Eudes, Aymerick; Dutta, Tanmoy; Deng, Kai
- PLOS ONE, Vol. 12, Issue 6
Lignins: Biosynthesis and Biological Functions in Plants
journal, January 2018
- Liu, Qingquan; Luo, Le; Zheng, Luqing
- International Journal of Molecular Sciences, Vol. 19, Issue 2
Elucidating Tricin-Lignin Structures: Assigning Correlations in HSQC Spectra of Monocot Lignins
journal, August 2018
- Lan, Wu; Yue, Fengxia; Rencoret, Jorge
- Polymers, Vol. 10, Issue 8
Comprehensive tissue-specific transcriptome profiling of pineapple (Ananas comosus) and building an eFP-browser for further study
journal, December 2018
- Mao, Qi; Chen, Chengjie; Xie, Tao
- PeerJ, Vol. 6