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Title: OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls

Abstract

Lignin is a phenylpropanoid polymer produced in the secondary cell walls of vascular plants. Although most eudicot and gymnosperm species generate lignins solely via polymerization of p-hydroxycinnamyl alcohols (monolignols), grasses additionally use a flavone, tricin, as a natural lignin monomer to generate tricin-incorporated lignin polymers in cell walls. We previously found that disruption of a rice 5- HYDROXYCONIFERALDEHYDE O-METHYLTRANSFERASE (OsCAldOMT1) reduced extractable tricin-type metabolites in rice vegetative tissues. This same enzyme has also been implicated in the biosynthesis of sinapyl alcohol, a monolignol that constitutes syringyl lignin polymer units. Here, we further demonstrate through in-depth cell wall structural analyses that OsCAldOMT1-deficient rice plants produce altered lignins largely depleted in both syringyl and tricin units. We also show that recombinant OsCAldOMT1 displayed comparable substrate specificities towards both 5-hydroxyconiferaldehyde and selgin intermediates in the monolignol and tricin biosynthetic pathways, respectively. These data establish OsCAldOMT1 as a bifunctional O-methyltransferase predominantly involved in the two parallel metabolic pathways both dedicated to the biosynthesis of tricin-lignins in rice cell walls. Given that cell wall digestibility was greatly enhanced in the OsCAldOMT1-deficient rice plants, genetic manipulation of CAldOMTs conserved in grasses may serve as a potent strategy to improve biorefinery applications of grass biomass.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [2]; ORCiD logo [2];  [3]; ORCiD logo [2]; ORCiD logo [2];  [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [2]
  1. Kyoto Univ. (Japan); The Univ. of Hong Kong, Pokfuloam (Hong Kong)
  2. Kyoto Univ. (Japan)
  3. Univ. of Wisconsin, Madison, WI (United States); École polytechnique Fédérale, Lausanne (Switzerland)
  4. Kyoto Univ. (Japan). Graduate School of Agriculture
  5. Univ. of Wisconsin, Madison, WI (United States)
  6. The Univ. of Hong Kong, Pokfuloam (Hong Kong)
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
[DASH/FBAS (Research Institute for Sustainable Humanosphere, Kyoto University) and the NMR spectrometer at JURC (Institute for Chemical Research, Kyoto University)]
OSTI Identifier:
1579356
Grant/Contract Number:  
[SC0018409; FC02-07ER64494]
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
[ Journal Volume: 9; Journal Issue: 1]; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Lam, Pui Ying, Tobimatsu, Yuki, Matsumoto, Naoyuki, Suzuki, Shiro, Lan, Wu, Takeda, Yuri, Yamamura, Masaomi, Sakamoto, Masahiro, Ralph, John, Lo, Clive, and Umezawa, Toshiaki. OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls. United States: N. p., 2019. Web. doi:10.1038/s41598-019-47957-0.
Lam, Pui Ying, Tobimatsu, Yuki, Matsumoto, Naoyuki, Suzuki, Shiro, Lan, Wu, Takeda, Yuri, Yamamura, Masaomi, Sakamoto, Masahiro, Ralph, John, Lo, Clive, & Umezawa, Toshiaki. OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls. United States. doi:10.1038/s41598-019-47957-0.
Lam, Pui Ying, Tobimatsu, Yuki, Matsumoto, Naoyuki, Suzuki, Shiro, Lan, Wu, Takeda, Yuri, Yamamura, Masaomi, Sakamoto, Masahiro, Ralph, John, Lo, Clive, and Umezawa, Toshiaki. Mon . "OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls". United States. doi:10.1038/s41598-019-47957-0. https://www.osti.gov/servlets/purl/1579356.
@article{osti_1579356,
title = {OsCAldOMT1 is a bifunctional O-methyltransferase involved in the biosynthesis of tricin-lignins in rice cell walls},
author = {Lam, Pui Ying and Tobimatsu, Yuki and Matsumoto, Naoyuki and Suzuki, Shiro and Lan, Wu and Takeda, Yuri and Yamamura, Masaomi and Sakamoto, Masahiro and Ralph, John and Lo, Clive and Umezawa, Toshiaki},
abstractNote = {Lignin is a phenylpropanoid polymer produced in the secondary cell walls of vascular plants. Although most eudicot and gymnosperm species generate lignins solely via polymerization of p-hydroxycinnamyl alcohols (monolignols), grasses additionally use a flavone, tricin, as a natural lignin monomer to generate tricin-incorporated lignin polymers in cell walls. We previously found that disruption of a rice 5-HYDROXYCONIFERALDEHYDE O-METHYLTRANSFERASE (OsCAldOMT1) reduced extractable tricin-type metabolites in rice vegetative tissues. This same enzyme has also been implicated in the biosynthesis of sinapyl alcohol, a monolignol that constitutes syringyl lignin polymer units. Here, we further demonstrate through in-depth cell wall structural analyses that OsCAldOMT1-deficient rice plants produce altered lignins largely depleted in both syringyl and tricin units. We also show that recombinant OsCAldOMT1 displayed comparable substrate specificities towards both 5-hydroxyconiferaldehyde and selgin intermediates in the monolignol and tricin biosynthetic pathways, respectively. These data establish OsCAldOMT1 as a bifunctional O-methyltransferase predominantly involved in the two parallel metabolic pathways both dedicated to the biosynthesis of tricin-lignins in rice cell walls. Given that cell wall digestibility was greatly enhanced in the OsCAldOMT1-deficient rice plants, genetic manipulation of CAldOMTs conserved in grasses may serve as a potent strategy to improve biorefinery applications of grass biomass.},
doi = {10.1038/s41598-019-47957-0},
journal = {Scientific Reports},
number = [1],
volume = [9],
place = {United States},
year = {2019},
month = {8}
}

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