Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification
Abstract
Summary 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 of secondary cell walls in vascular plants. 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 we address the pronounced impacts of C3 ′ H deficiency on the structure and properties of grass cell walls. C3 ′ H ‐knockdown lines generated via RNA interference ( RNA i)‐mediated gene silencing, with about 0.5% of the residual expression levels, reached maturity and set seeds. 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 RNA i lines revealed that their lignins were largely enriched in p ‐hydroxyphenyl (H) units while being substantially reduced in the normally dominant guaiacyl (G) and syringyl (S) units. Interestingly, however, the enrichment of H units was limited to within the non‐acylated lignin units, with grass‐specific γ‐ p ‐coumaroylated lignin units remaining apparently unchanged. Suppression of C3 ′ H also resultedmore »
- Authors:
-
[1];
- Kyoto Univ. (Japan). Research Inst. for Sustainable Humanosphere
- Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Tokushima Univ., Kuramoto-cho, Tokushima (Japan). Faculty of Bioscience and Bioindustry
- Kyoto Univ. (Japan). Graduate School of Agriculture
- Kyoto Univ. (Japan). Research Inst. for Sustainable Humanosphere; Kyoto Univ. (Japan). Research Unit for Development of Global Sustainability
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Japan Science and Technology Agency (JST); Japan International Cooperation Agency; Ministry of Agriculture, Forestry and Fisheries of Japan; Japan Society for the Promotion of Science (JSPS); New Energy and Industrial Technology Development Organization (NEDO)
- OSTI Identifier:
- 1459572
- Alternate Identifier(s):
- OSTI ID: 1459711
- Grant/Contract Number:
- SC0018409; FC02-07ER64494; DE‐FC02‐07ER64494; DE‐SC0018409
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Volume: 95; Journal Issue: 5; Journal ID: ISSN 0960-7412
- Publisher:
- Society for Experimental Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; lignin; grass; Oryza sativa; RNAi; CRISPR/Cas9; saccharification; p-coumarate; ferulate; NMR; DFRC
Citation Formats
Takeda, Yuri, Tobimatsu, Yuki, Karlen, Steven D., Koshiba, Taichi, Suzuki, Shiro, Yamamura, Masaomi, Murakami, Shinya, Mukai, Mai, Hattori, Takefumi, Osakabe, Keishi, Ralph, John, Sakamoto, Masahiro, and Umezawa, Toshiaki. Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification. United States: N. p., 2018.
Web. doi:10.1111/tpj.13988.
Takeda, Yuri, Tobimatsu, Yuki, Karlen, Steven D., Koshiba, Taichi, Suzuki, Shiro, Yamamura, Masaomi, Murakami, Shinya, Mukai, Mai, Hattori, Takefumi, Osakabe, Keishi, Ralph, John, Sakamoto, Masahiro, & Umezawa, Toshiaki. Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification. United States. https://doi.org/10.1111/tpj.13988
Takeda, Yuri, Tobimatsu, Yuki, Karlen, Steven D., Koshiba, Taichi, Suzuki, Shiro, Yamamura, Masaomi, Murakami, Shinya, Mukai, Mai, Hattori, Takefumi, Osakabe, Keishi, Ralph, John, Sakamoto, Masahiro, and Umezawa, Toshiaki. Mon .
"Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification". United States. https://doi.org/10.1111/tpj.13988. https://www.osti.gov/servlets/purl/1459572.
@article{osti_1459572,
title = {Downregulation of p-COUMAROYL ESTER 3-HYDROXYLASE in rice leads to altered cell wall structures and improves biomass saccharification},
author = {Takeda, Yuri and Tobimatsu, Yuki and Karlen, Steven D. and Koshiba, Taichi and Suzuki, Shiro and Yamamura, Masaomi and Murakami, Shinya and Mukai, Mai and Hattori, Takefumi and Osakabe, Keishi and Ralph, John and Sakamoto, Masahiro and Umezawa, Toshiaki},
abstractNote = {Summary 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 of secondary cell walls in vascular plants. 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 we address the pronounced impacts of C3 ′ H deficiency on the structure and properties of grass cell walls. C3 ′ H ‐knockdown lines generated via RNA interference ( RNA i)‐mediated gene silencing, with about 0.5% of the residual expression levels, reached maturity and set seeds. 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 RNA i lines revealed that their lignins were largely enriched in p ‐hydroxyphenyl (H) units while being substantially reduced in the normally dominant guaiacyl (G) and syringyl (S) units. Interestingly, however, the enrichment of H units was limited to 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 a 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.},
doi = {10.1111/tpj.13988},
journal = {The Plant Journal},
number = 5,
volume = 95,
place = {United States},
year = {Mon Jun 11 00:00:00 EDT 2018},
month = {Mon Jun 11 00:00:00 EDT 2018}
}
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Figures / Tables:
Table 1: Growth characteristics of wild-type (WT) and OsC3ˊH1-knockdown (OsC3ˊH1-KD-a and OsC3ˊH1-KD-b) rice plants.
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Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice
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- Martin, Andri Fadillah; Tobimatsu, Yuki; Kusumi, Ryosuke
- Scientific Reports, Vol. 9, Issue 1
Comparative evaluations of lignocellulose reactivity and usability in transgenic rice plants with altered lignin composition
journal, February 2019
- Takeda, Yuri; Tobimatsu, Yuki; Yamamura, Masaomi
- Journal of Wood Science, Vol. 65, Issue 1
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
- de Vries, Lisanne; Vanholme, Ruben; Van Acker, Rebecca
- Biotechnology for Biofuels, Vol. 11, Issue 1
4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase
journal, April 2019
- Barros, Jaime; Escamilla-Trevino, Luis; Song, Luhua
- Nature Communications, Vol. 10, Issue 1
OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls
journal, August 2019
- Lam, Pui Ying; Tobimatsu, Yuki; Matsumoto, Naoyuki
- Scientific Reports, Vol. 9, Issue 1
Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice
journal, November 2019
- Martin, Andri Fadillah; Tobimatsu, Yuki; Kusumi, Ryosuke
- Scientific Reports, Vol. 9, Issue 1
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